Non‐coding RNAs in plant stress responses: molecular insights and agricultural applications

Abstract

Non‐coding RNAs (ncRNAs) have emerged as crucial regulators in plant responses to environmental stress, orchestrating complex networks that finetune gene expression under both abiotic and biotic challenges. To elucidate this intricate ncRNA crosstalk, this review comprehensively summarizes recent advances in understanding the mechanisms of key regulatory ncRNAs including microRNAs (miRNAs), long non‐coding RNAs (lncRNAs), circular RNAs (circRNAs), tRNA derived fragments (tRFs) and small interfering RNAs (siRNAs) in mediating plant adaptations to stress conditions. We discuss molecular insights into how these ncRNAs modulate stress signalling pathways, control hormonal responses and interact through elaborate crosstalk mechanisms. We also emphasize emerging biotechnological strategies that leverage both innate and artificial ncRNAs as well as potential approaches for finetuning ncRNA levels to engineer stress‐resilient crops. Collectively, continued advances in high‐throughput sequencing, functional genomics and computational modelling will deepen our understanding of ncRNA network mediated stress responses, ultimately guiding the design of robust climate‐resilient crops.

Full text

Turn on search term navigation

Introduction

Environmental adversities including biotic (e.g. fungus, bacteria, virus, pests) and abiotic (e.g. extreme temperature, drought, salinity) stresses significantly hamper crop performance, causing substantial losses in agricultural and economic output (Kim et al., 2019). The ever-intensifying climate change incurred by global warming exacerbates the problem, leading to more frequent and intense environmental anomalies, such as unseasonal temperature fluctuations, drought and flooding events (Anderegg et al., 2020; Hassani et al., 2020; Steg, 2018), outbreaks of pest and pathogen diseases (Hódar et al., 2012; Trebicki, 2020) as well as deteriorating soil conditions that expose crops to nutrient deficiencies, high salinity and excessive environmental pollutants (e.g. heavy metal, pesticide, herbicide) (Zandalinas et al., 2021). Facing these complex and multifactorial challenges, there is an urgent need in acquiring knowledge for a better understanding of plant–environment interactions at the molecular levels to develop effective strategies for plant genetic engineering producing stress-resilient crops.

Non-coding RNAs (ncRNAs) are a diverse class of RNA molecules transcribed from DNA that do not encode proteins. Despite the lack of protein-coding potential, ncRNAs play pivotal roles in RNA splicing, editing and gene silencing mechanisms and are integral to various cellular processes, including chromatin remodelling, transcriptional regulation and post-transcriptional modifications (Gomes et al., 2013). The ncRNAs are classified into structural ncRNAs and regulatory ncRNAs based on their function and origins. While the well-documented structural ncRNAs such as transfer RNA (tRNAs), ribosomal RNA (rRNAs), small nuclear RNA (snRNAs) and small nucleolar RNAs (snoRNAs) are essential for basic cellular functions, they are generally less directly involved in stress signalling pathways. The regulatory RNAs are further classified into two subclasses based on their size, the long non-coding RNAs (lncRNAs) that exceed 200 nucleotides (nt) and the small RNAs (sRNAs) that range from 18 to 30 nt such as microRNAs (miRNAs) and small interfering RNAs (siRNAs) (Waititu et al., 2020). More recently, a unique subclass of ncRNA with a closed-loop structure identified as circular RNAs (circRNAs) was found to be ubiquitously present in eukaryote species (Zhang et al., 2020d). Over the past decade, numerous studies have elucidated the functions and mechanisms of ncRNAs in plants, underscoring their pivotal roles in regulating plant development and environmental adaptation. These findings highlight the potential of ncRNAs as targets for genetic manipulation for desired plant phenotypes.

In this review, we highlight the milestone discoveries and recent developments in our understanding of plant ncRNAs in relation to stress adaptations. Given the importance of ncRNAs in plant species and the considerable attention that ncRNA research has garnered, several review papers have been published recently (Cao et al., 2024; Yadav et al., 2024). Although these review articles provide a broad overview of the diverse classes of ncRNAs and their general roles in modulating plant responses to environmental stresses, they often fall short of offering a comprehensive list of specific examples that detail the mechanisms within each ncRNA category, which are essential for elucidating the intricate fine-tuning networks and crosstalk among ncRNAs in plant stress regulation. Here, we aimed to provide an in-depth, high-level overview of the well-characterized regulatory ncRNAs in plants. We systematically and comprehensively summarize their functions and mechanisms in mediating plant adaptations to various stress conditions. We also discuss key aspects of the complex crosstalk networks between ncRNAs that govern plant stress responses based on the abundant information we gathered from up-to-date studies. Furthermore, we explore the potential applications of ncRNAs by integrating synthetic biotechnology approaches to address complex trait modifications in diverse agricultural systems.

Biogenesis and functions of regulatory ncRNAs

miRNAs

MicroRNAs (miRNAs) (Figure 1a) are highly conserved small endogenous non-coding RNAs found in diverse eukaryotic species that are typically 18–24 nucleotides (Ambros, 2011). The biogenesis of miRNAs starts with the transcription of miR genes into primary RNA transcripts (pri-miRNAs) by RNA polymerase II (Pol II), forming a stem-loop structure (Reinhart et al., 2002). Subsequently, the pri-miRNA is processed into a miRNA/miRNA duplex by DICER-LIKE 1 (DCL1) in association with HYPONASTIC LEAVES 1 (HYL1) and SERRATE (SE), then methylated at the 3′-end by HEN1 and transported into the cytoplasm by HASTY (HST1). The duplex is subsequently loaded onto the Argonaute 1 (AGO1) protein, forming the RNA-induced silencing complex (RISC) in the cytoplasm. Within this complex, the non-functional passenger strand of the miRNA is degraded, while the functional guide strand is retained. This guide strand directs RISC to target mRNA for degradation based on sequence complementarity, regulating the target gene expression through transcription inhibition (Pagano et al., 2021). Additionally, miRNA can regulate gene expression through translation inhibition by binding to 5′ UTR to prevent ribosome recruitment (Eulalio et al., 2008).

[IMAGE OMITTED. SEE PDF]

siRNAs

siRNAs (Figure 1b) are grouped into trans-acting siRNAs (ta-siRNA), cis-acting siRNAs (ca-siRNAs), heterochromatic siRNAs (hc-siRNA), natural antisense siRNAs (nat-siRNAs) and phased siRNAs (phasiRNAs) based on their origins (Mallory and Vaucheret, 2006; Zhang et al., 2012). Among which, hc-siRNA are transcribed mainly by Pol IV-associated RNA polymerase activities, which incorporate with AGO4/6 protein to form RISC that can direct the DNA methylation activity of DNA methyltransferase 2 (DRM2) at Pol V-transcribed loci (Zhan and Meyers, 2023), ultimately influencing gene expression at pre-transcription level. The generation of phasiRNA relies on the miRNA target transcripts. The primary mRNA fragment after being cleaved by miRNA/AGO1 is stabilized by SUPPRESSOR OF GENE SILENCING3 (SGS3) before filling in the complementary strand to form dsRNA by RNA-dependent RNA polymerase 6 (RDR6). The dsRNA is subsequently processed into phasiRNA by DCL4/5, methylated by HEN1, then incorporated into AGO1 to function as RISCs (Zhan and Meyers, 2023). Similarly, the biogenesis of ta-siRNA starts from Pol II-transcribed TAS loci that are first cleaved by AGO7, then stabilized by SGS3 and converted into dsRNA by RDR6. DCL2/4 dices the dsRNA into the 21-nt ta-siRNAs, which are methylated by HEN1 and loaded into AGO1 to silence targets. The nat-siRNAs are produced when overlapping sense–antisense transcript pairs form dsRNAs, which are then processed into the 21–24-nt nat-siRNAs by RDR2/6 and DCL1/3 to be loaded into AGO1/2 to silence the overlapping transcripts. The ca-siRNAs are derived from bidirectional transcription at repetitive or transposon-rich loci. Pol IV and RDR2 generate the precursor, DCL3 then processes it into the 24-nt ca-siRNAs and AGO4/6 loads them to direct DRM2-mediated methylation at the very loci they came from (Cao et al., 2024).

lncRNAs

Long non-coding RNAs (lncRNAs) (Figure 1c) are RNA transcripts exceeding 200 nucleotides in length that lack a discernible open reading frame (ORF) (St. Laurent et al., 2015). They are categorized based on their genomic localization as long intergenic lncRNAs (lincRNAs), intronic ncRNAs (incRNAs), natural antisense transcripts (NATs), bidirectional lncRNAs (BI-lncRNAs) and overlapping lncRNAs (OT-lncRNAs) (Mattick and Rinn, 2015). The majority of lncRNAs are transcribed by Pol II, as well as Pol I and Pol III (Mattick et al., 2023). In plant systems, two additional polymerases, Pol IV and Pol V, have been identified as key players in the synthesis of lncRNAs, particularly those involved in recognizing and silencing transposable elements (Wierzbicki et al., 2021).

lncRNAs can serve as precursors for miRNA and siRNA in the nucleus for downstream transcriptional inhibition (Bouba et al., 2019), and they can also modulate chromatin structure and epigenetic landscapes to influence gene expression. For example, lncRNA APOLO (AUXIN-REGULATED PROMOTER LOOP) facilitates target recognition through sequence complementarity and R-loop formation. This interaction enables APOLO to decoy protein complexes and reconfigure three-dimensional chromatin architecture, ultimately fine-tuning the transcription level of associated genes (Ariel et al., 2020). lncRNAs were also found to have crucial functions in the cytoplasm, such as lncRNA-protein interaction to promote protein stability and subcellular localization (Zhao et al., 2024) and mRNA translational regulation through cis or trans mechanisms (Chen et al., 2020b). In addition, lncRNA can act as endogenous target mimics that sequester mature miRNA to regulate the activity of miRNA-mediated target repression (Meng et al., 2021).

circRNAs

Circular RNAs (circRNAs) (Figure 1d) are endogenous single-stranded RNAs with a distinct close-loop structure, which has been found to be ubiquitously present in eukaryotes and prokaryote species (Wilusz and Sharp, 2013). Circular RNAs form covalently closed loops without 5′ caps or 3′ tails, which makes them inherently resistant to exonuclease-mediated degradation (Jeck et al., 2013). circRNAs are classified into exonic circRNAs, intronic circRNAs, intergenic circRNAs and UTR circRNAs based on their origins in the genome (Ye et al., 2017). circRNAs are produced through two main mechanisms. In one process called backsplicing, circRNA is formed by looping downstream 5′ splice site of a pre-mRNA with an upstream 3′ splice site. In another process, circRNA is formed by lariat RNAs. When lariat RNAs undergo 3′ exonucleolytic degradation, they remove extra sequences and leave behind an intronic circular RNA that features a unique 2′,5′-phosphodiester bond (Liu et al., 2023a).

CircRNAs perform diverse functions, including acting as miRNA sponges to prevent miRNAs from degrading their target mRNAs, interacting with RNA-binding proteins (RBPs) to influence their stability, activity and localization, and serving as molecular scaffolds to facilitate interactions between proteins or between proteins and nucleic acids. Additionally, circRNAs can bind directly to mRNAs or DNA to stabilize transcripts and regulate gene expression. Some circRNAs also contain internal ribosome entry sites (IRES), which allows IRES or m⁶A-mediated translation (Liu et al., 2023a).

tRFs

Transfer RNA-derived fragments (tRFs) (Figure 1e) are highly heterogeneous and are emerging as important regulatory molecules with diverse roles in gene regulation (Magee and Rigoutsos, 2020). tRNAs transcribed by RNA polymerase III serve as precursors for tRF-5s and tRF-3s after maturation by 5′ and 3′ trimming and the addition of the CCA tail at the 3′ end. Subsequently, 5′-tRFs, 3′-tRFs, and internal tRNA fragments (i-tRFs) are generated by cleavage within the D- and L-loops of the mature tRNA, which are 15–28 nt in length. Longer tRFs are generated from cleavage in the A-loop, which contains an anticodon loop, resulting in 5′ and 3′ tRNA halves that range from 30 to 40 nt in length (Panstruga, 2024). tRFs can regulate translation by binding to mRNA molecules, either enhancing or inhibiting protein synthesis. They can also modulate gene expression through Argonaute-mediated RNA silencing and influence alternative splicing length (Panstruga, 2024). Additionally, they are transported via extracellular vesicles, supporting intercellular and interspecies communication, which is demonstrated to play crucial symbiotic role between soybean roots and microbes that involved in nodule initiation and development (Ren et al., 2019).

miRNAs in plant stress responses

Plant miRNAs have emerged as pivotal regulators of plant responses to a wide array of environmental challenges, including abiotic stresses (such as drought, salinity, extreme temperatures and nutrient deficiencies) and biotic stresses (such as pathogen and pest attacks). They are arguably the most important class of non-coding RNAs in this context, given their direct role in post-transcriptional regulation, while many other ncRNAs play auxiliary roles that fine-tune miRNA function. In the following sections, we highlight the most extensively characterized plant miRNAs (Table 1) and discuss their functions under abiotic stress (Tables 2–4) and biotic stress (Table 5) across different plant species.

Table 1 Overview of the targets and functions of the most characterized miRNAs in plants to date, as summarized in this review

miRNA	Target gene(s)	Functions of the target genes	Reference
miR156	SPL (squamosa promoter-binding protein-like)	Phase transition; branching; anthocyanin biosynthesis; stress tolerance	Kantar et al. (2011), Visentin et al. (2020)
miR159	MYB (myeloblastosis) transcription factors	ABA signalling; stomatal regulation; osmo protectant accumulation	Pieczynski et al. (2013), Reyes and Chua (2007)
miR160	ARF (auxin response factor) genes	Auxin response; root architecture; growth–defence balance	Barrera-Figueroa et al. (2011), Chang et al. (2020)
miR164	NAC (NAM, ATAF, CUC) transcription factors	Root development; senescence; stress responses	Fang et al. (2014), Peng et al. (2022)
miR166	HD-ZIP III (homeodomain-leucine zipper III) transcription factors	Leaf polarity; vascular patterning; meristem maintenance	Jatan et al. (2019)
miR167	ARF (auxin response factor) genes	Flower/seed development; lateral root formation; stress adaptation	Jodder et al. (2017), Singroha et al. (2021)
miR168	AGO1 (argonaute1) gene	RNA silencing machinery; Global miRNA regulation; Biotic/abiotic stress	Li et al. (2012)
miR169	NF-YA subunits (nuclear factor Y, subunit A)	ABA-dependent gene expression; stomatal function; early stress responses	Chen et al. (2024b), Li et al. (2008)
miR171	SCL (Scarecrow-Like) transcription factors	Shoot, root, nodule development	Um et al. (2022)
miR319	TCP (teosinte branched1/cycloidea/PCF)	Leaf morphology; flower development; wax/lignin biosynthesis	Ren et al. (2022), Zhou et al. (2013)
miR393	TIR1/AFB (transport inhibitor1/auxin SIGNALLING F-BOX); LecRLKs (Lectin RLKs)	Auxin perception; root architecture; immune signalling	Xia et al. (2012)
miR395	APS (ATP sulfurylase) and SULTR (Sulfate Transporter) genes	Sulfur assimilation; sulfate transport; stress modulation	Bhardwaj et al. (2024), Jagadeeswaran et al. (2014)
miR396	GRF (growth-regulating factor) transcription factors	Cell proliferation; leaf/organ size; growth–defence trade-offs	Fracasso et al. (2021), Liu et al. (2017a)
miR398	CSD/CCS (copper/zinc superoxide dismutase/ copper chaperone)	ROS detoxification; copper homeostasis; stress tolerance	Lu et al. (2010)
miR399	PHO2 (phosphate2) and SPX domain proteins	Phosphate homeostasis; Pi transporter abundance; ion balance	Baek et al. (2016), Liu et al. (2024)
miR408	Plantacyanins, LAC (laccase) genes, cupredoxins	Copper binding; lignin/cuticle biosynthesis; oxidative stress control	Akgul and Aydinoglu (2025), Bai et al. (2018)
miR444	MIKCC-type MADS box genes	Root architecture; virus/pathogen defence; development	Feng et al. (2023), Wang et al. (2016)
miR528	Ascorbate oxidase, MAX2 (F-box) genes, copper-binding proteins	ROS regulation; strigolactone signalling; plant architecture	Balyan et al. (2023), Yuan et al. (2015)
miR530	SPL (squamosa promoter-binding protein-like)	Panicle branching; yield traits; disease resistance	Hu et al. (2023), Li et al. (2021b)
miR535	SPL (Squamosa Promoter-Binding Protein-Like)	Seed/flower development; stress tolerance; yield components	Yue et al. (2020), Zhang et al. (2022b)
miR827	SPX-MFS (SPX-major facility superfamily), WRKY	Pi transport; transcriptional regulation; stress signalling	Chen et al. (2024a), Hackenberg et al. (2013)
miR1432	Calcium signalling genes ACA (Ca²⁺-ATPase), CaML (calmodulin)	Calcium homeostasis; stress adaptation; growth–defence balance	Dai et al. (2024), Jia et al. (2021)

Table 2 Summary of the positive or negative impacts of various miRNAs on species-specific plant responses to abiotic stresses, including drought, salt, heat and cold

miRNA	Regulation	Drought	Salt	Heat	Cold
miR156	Positive	Barley¹, wheat¹, soybean², Populus³, peach⁴, switchgrass⁵, Brachypodium⁶, alfalfa⁷, tomato⁸, maize⁹, apple¹⁰, Arabidopsis¹⁰	Arabidopsis¹², sugarcane¹³, chickpea¹⁴, radish¹⁵, Medicago truncatula¹⁶, alfalfa¹⁷	Alfalfa^18,19	Rice²⁰
Negative	Rice²¹	Maize²², cotton²³, Solanum ²⁴, wheat²⁵	–	Apple¹⁰
miR159	Positive	Arabidopsis²⁶, maize²⁷, wheat²⁷, barley²⁷, tomato²⁸, poplar¹¹	Soybean³⁰, artichoke³¹	–	Maize³⁴
Negative	Potato²⁹	Sugar beet³²	Rice³³	–
miR160	Positive	Cowpea³⁵, ginkgo³⁶, potato³⁷, apple³⁸	Peanut³⁹, soybean⁴⁰, maize⁴¹	Arabidopsis⁴²	–
Negative	–	–	Cotton⁴³	–
miR164	Positive	Poplar⁴⁴	Poplar⁴⁴	Arabidopsis⁴⁹	–
Negative	Malaysian rice⁴⁶, wheat⁴⁷, apple⁴⁸	Wheat⁴⁷, maize⁴⁵	–	Tea⁵⁰, tomato⁵¹
miR166	Positive	Medicago⁵², chickpea⁵³	Potato⁵⁶, broomcorn⁵⁷	Wheat⁶⁰	Tomato⁶¹
Negative	Tea⁵⁴, maize⁵⁵	Switchgrass⁵⁸, pearl⁵⁹	–	–
miR167	Positive	Arabidopsis⁶², maize⁶²	Tamarisk⁶⁵, cotton⁶⁶, rice⁶⁷	–	–
Negative	Tomato⁶³, wheat⁶⁴	Maize⁶⁸, tomato⁶⁹	Tomato⁶⁹	Wheat⁷⁰
miR168	Positive	Arabidopsis⁷¹, Ipomoea⁷²	Ipomoea⁷²	–	Arabidopsis and Wheat⁷⁴
Negative	Maize⁷³	Maize⁷³	–	–
miR169	Positive	Arabidopsis⁷⁵, tomato⁷⁶, turfgrass⁷⁷	Rice⁸⁰, turfgrass⁷⁷	Arabidopsis⁸¹, tomato⁸¹	–
Negative	Maize⁷⁸, soybean⁷⁹	Maize⁷⁸	–	–
miR171	Positive	Arabidopsis⁸², rice⁸³, mulberry⁸⁴, potato⁸⁵	Arabidopsis⁸², mulberry⁸⁴	Arabidopsis⁸²	–
Negative	–	–	–	–
miR319	Positive	Turfgrass⁸⁶, wild alfalfa⁸⁷, sweet potato⁸⁸	Turfgrass⁸⁶, bean⁸⁹, poplar⁹⁰, switchgrass⁹¹	Tomato⁹²	Rice⁹³, sugarcane⁹⁴, cassava⁹⁴
Negative	–	–
miR393	Positive	Arabidopsis⁹⁵, turfgrass⁹⁶	Arabidopsis⁹⁹, tobacco¹⁰⁰, wheat¹⁰¹, turfgrass⁹⁶	Turfgrass⁹⁶	Switchgrass¹⁰², banana¹⁰³
Negative	Rice⁹⁷, barley⁹⁸	Rice⁹⁴	–	–
miR396	Positive	Tobacco¹⁰⁴	Turfgrass¹⁰⁸, tomato¹⁰⁹	Artichoke¹¹⁰	Artichoke¹¹⁰
Negative	Tomato¹⁰⁴, soybean¹⁰⁵, pitaya¹⁰⁶, tree peony¹⁰⁷	–	–	–
miR398	Positive	–	–	–	–
Negative	Tomato¹¹¹, cotton¹¹², rice¹¹³	Arabidopsis¹¹⁴, poplar¹¹⁵, tomato¹¹⁶	Arabidopsis¹¹⁷	Chrysanthemum¹¹⁸, wheat¹¹⁹
miR399	Positive	Grapevine¹²⁰	Arabidopsis¹²¹	–	Wheat¹²²
Negative	Arabidopsis¹²¹	–	–	–
miR408	Positive	Ryegrass¹²³, chickpea¹²⁴	Arabidopsis¹²⁷, tobacco¹²⁸		Arabidopsis¹³², rice¹³³
Negative	Arabidopsis¹²⁵, rice¹²⁶	Rice¹²⁹, wheat¹³⁰, maize¹³¹	–	–
miR528	Positive	–	Rice¹³⁴, turfgrass¹³⁵	–	–
Negative	–	–	–	–
miR827	Positive	Barley¹³⁶, potato¹³⁷	–	–	–
Negative	–	–	–	–
miR1432	Positive	–	–	–	–
Negative	Barley¹³⁸, rice¹³⁹	Rice¹³⁹	–	Rice¹³⁹

miRNA in abiotic stress

Abiotic stresses including drought, salinity and extreme temperatures are among the most important factors significantly impacting agriculture production. The roles miRNAs play in orchestrating plant responses to various abiotic stress conditions have been extensively explored in model plants and many crop species. An overview of the major discoveries from these efforts as detailed in this section and summarized in Table 2 provides critical information for the development of effective novel molecular strategies facilitating plant adaptation to adverse environments.

miRNA in drought stress

miR156

miR156 has been identified as a key regulator induced by drought through an endogenous strigolactone (SL) pathway, contributing to SL-induced drought tolerance via an ABA-dependent pathway (Korek and Marzec, 2023). Up-regulation of miR156 under drought stress has been documented in several plant species, including barley (Hordeum vulgare) (Kantar et al., 2011), wild emmer wheat (Triticum dicoccoides) (Kantar et al., 2011), soybean (Glycine max) (Li et al., 2011b), Populus euphratica (Li et al., 2011a), peach (Prunus persica) (Eldem et al., 2012), switchgrass (Panicum virgatum) (Sun et al., 2012), Brachypodium distachyon (Bertolini et al., 2013), alfalfa (Medicago sativa) (Arshad et al., 2017a), tomato (Solanum lycopersicum) (Visentin et al., 2020), maize (Zea mays) (Tang et al., 2022a) and apple (Malus domestica) (Chen et al., 2023a).

Notably, miR156 expression in apple calli and Arabidopsis thaliana is linked to drought tolerance through flavonoid accumulation and enhanced reactive oxygen species (ROS) scavenging (Chen et al., 2023a). However, miR156 was found to be inhibited under drought conditions in rice (Oryza sativa) (Zhou et al., 2010). Functional studies on miR156 have demonstrated its potential in improving drought tolerance. In tomato, overexpression of miR156 led to lower stomatal conductance, enhancing drought tolerance (Visentin et al., 2020). In alfalfa, moderate levels of miR156 expression enhanced drought tolerance through the regulation of SPL13 and WD40-1, which fine-tuned DFR expression, enhanced anthocyanin biosynthesis and regulated various developmental processes (Feyissa et al., 2019). Moreover, miR156 enriches proteins under drought stress that are involved in antioxidant activity, ABA signalling, stomatal motion and secondary metabolite biosynthesis (Puri et al., 2023).

miR159

In Arabidopsis thaliana, miR159 levels increase in response to ABA treatment and drought (Reyes and Chua, 2007). Similar drought response has also been observed in maize (Zea mays), wheat (Triticum aestivum) and barley (Hordeum vulgare), suggesting that higher levels of miR159 may confer greater drought tolerance (Zhang, 2015).

In potato (Solanum tuberosum), the down-regulation of CBP80 decreases miR159 levels, leading to the up-regulation of its target genes, MYB33 and MYB101. This enhances drought stress tolerance by improving ABA sensitivity and promoting structural adaptations, indicating that miR159 negatively regulates drought tolerance in potato (Pieczynski et al., 2013). In tomato (Solanum lycopersicum), sly-miR159 has been shown to play a role in drought stress adaptation by targeting the SlMYB33 transcription factor. This regulation correlates with the accumulation of osmo-protective compounds, such as proline and putrescine, enhancing plant drought tolerance (López-Galiano et al., 2019). In poplar (Populus euphratica), miR159a expression is significantly increased following drought treatment. Overexpression of miR159a reduces stomatal open area, thereby improving water-use efficiency. Additionally, it enhances reactive oxygen species (ROS) scavenging capacity, which reduces membrane damage under drought stress (Fu et al., 2023).

miR160

miR160a/b has been found to be strongly up-regulated during drought stress in two cowpeas (Vigna unguiculata) genotypes, suggesting its positive involvement in plant stress response pathways (Barrera-Figueroa et al., 2011). In ginkgo (Ginkgo biloba), miR160a plays a role in drought stress tolerance by decreasing the expression of auxin response factors (ARFs) and participating in the indole-3-acetic acid (IAA) signalling pathway (Chang et al., 2020). In potato (Solanum tuberosum), overexpression of miR160a-5p suppresses its target gene ARF16. This suppression alters physiological and biochemical traits, reduces hydrogen peroxide (H₂O₂) accumulation and increases proline levels, particularly under drought stress, contributing to improved stress tolerance (Şanlı and Öztürk Gökçe, 2021). In apple (Malus domestica), overexpression of Mdm-miR160 or MdHYL1 and suppression of MdARF17 improved drought tolerance. Conversely, suppression of Mdm-miR160 or MdHYL1 and overexpression of MdARF17 resulted in greater drought sensitivity, highlighting the positive regulatory role of miR160 in drought tolerance mechanisms (Shen et al., 2022).

miR164

In rice (Oryza sativa), overexpression of miR164-targeted NAC genes (OMTN1- OMTN6) reduces plant drought tolerance during the reproductive stage. This finding underscores the potential positive regulatory role of miR164 in plant drought resistance (Fang et al., 2014). In desert poplar (Populus euphratica), the miR164-PeNAC regulatory module has been demonstrated to influence lateral root development and stem elongation, ultimately enhancing drought performance (Lu et al., 2017).

Conversely, in the Malaysian rice variety MR303, reduced expression of miR164b under drought conditions leads to increased accumulation of NAM1, a NAC family transcription factor. This suggests a negative regulatory role of miR164 in drought tolerance, with NAM1 potentially contributing to enhanced stress resistance (Xin et al., 2023). In wheat (Triticum aestivum), overexpression of TaNAC14 promotes root growth and enhances drought tolerance. However, tae-miR164, which targets TaNAC14, inhibits root development and reduces tolerance to drought and salinity by suppressing TaNAC14 expression. This highlights the negative role of miR164 in drought tolerance in wheat (Chi et al., 2023). Similarly, in wild apple (Malus sieversii) and cultivated apple (Malus domestica), miR164g expression is suppressed under drought stress, allowing up-regulation of its target transcription factor MsNAC022. MsNAC022 enhances drought tolerance by increasing reactive oxygen species (ROS) scavenging enzyme activity such as MsPOD (Peng et al., 2022).

miR166

In the legume (Medicago truncatula), miR166a was found to be up-regulated under drought stress, suggesting a positive regulatory role in drought responses (Wang et al., 2011b). Similarly, drought also stimulates miR166 expression in the chickpea (Cicer arietinum L.) roots inoculated with the plant growth-promoting rhizobacteria (PGPR) Pseudomonas putida strain RA, indicating a potential role miR166 plays in enhancing drought tolerance via PGPR-mediated mechanisms (Jatan et al., 2019).

On the other hand, miR166 has also been found to negatively regulate plant responses to drought stress. In tea plants (Camellia sinensis), miR166 is down-regulated under drought stress that leads to the up-regulation of its target genes ATHB-14-like and ATHB-15-like, the two key players in plant drought response, suggesting that miR166 down-regulation contributes to improved drought tolerance in tea plants (Guo et al., 2017). MiR166 as a negative regulator for plant drought stress response was further confirmed in maize (Zea mays). Transgenic maize plants with inactivated miR166 through short tandem target mimicry exhibited enhanced drought resistance (Kouhi et al., 2020).

miR166 could also be tissue-specific in regulating drought stress. In barley (Hordeum vulgare), Hvu-miR166 is down-regulated in leaf tissues but up-regulated in root tissues, indicating its distinct roles in contributing to barley's overall drought response (Kantar et al., 2011). Similarly, in safflower (Carthamus tinctorius), miR166 is significantly down-regulated in leaf tissues, with the lowest expression observed 48 h after stress exposure. In root tissues, miR166 expression initially increases, and then declines 12 h after drought stress. This differential expression pattern of miR166 in safflower suggests a tissue-specific gene regulation mechanisms in miR166-mediated plant drought stress responses (Kouhi et al., 2020).

miR167

miR167 is critical in regulating plant responses to drought stress through an ABA-independent pathway by targeting auxin response factors (ARFs), specifically ARF6 and ARF8. These ARFs are integral to auxin signalling, which governs various developmental and stress-response processes. Although miR167 was up-regulated in Arabidopsis thaliana and maize (Zea mays) under drought stress, suggesting its role in positively regulating plant drought stress responses (Singroha et al., 2021), it was found that in tomato (Solanum lycopersicum), drought stress resulted in reduced expression of miR167a (Jodder et al., 2017) hinting at its negative regulatory role responding to drought stress. In addition, in wheat (Triticum aestivum), reduced expression of miR167 under drought stress led to stomatal closure and increased leaf water content (Fileccia et al., 2019), supporting the negative regulatory role of miR167 in plant drought stress responses observed in tomato. These findings reveal the diverse, context-dependent roles of miR167 in plant drought responses, mediated through its regulation of auxin signalling pathways.

miR168

miR168 has been implicated in regulating drought stress responses in plants, primarily through its interaction with Argonaute 1 (AGO1). In Arabidopsis, drought conditions lead to elevated miR168a transcription, suggesting that miR168 plays a role in plant adaptive response to drought stress by modulating AGO1 levels (Li et al., 2012). This is also true in a drought-tolerant Convolvulaceae species, Ipomoea campanulata, where miR168 expression was found to be up-regulated under drought stress, indicating a potential positive role of miR168 in drought response (Ghorecha et al., 2017).

However, in maize (Zea mays), most members of the miR168 family were down-regulated under drought stress across four maize inbred lines. This down-regulation suggests that miR168 may negatively regulate drought stress responses in maize (Wang et al., 2014c), which indicates complex regulation mechanisms of miR168 under drought stress depending on the plant species and context.

miR169

miR169 is a key regulator of plant responses to drought stress, functioning through the modulation of nuclear factor Y subunits (NF-YA) and other stress-related genes. While it exhibits positive regulation in some species, its role can be negative or context-dependent in others, highlighting its diverse regulatory functions across plant species.

In Arabidopsis (Arabidopsis thaliana), miR169 is induced by drought stress, pointing to its involvement in drought adaptation through the regulation of stress-responsive genes (Li et al., 2008). Similarly, in rice (Oryza sativa), miR169g is induced by drought via a dehydration-responsive element (DRE), where it targets a CCAAT-box binding transcription factor that regulates multiple stress-related genes, further supporting its role as a positive regulator in drought responses (Zhao et al., 2009).

In tomato (Solanum lycopersicum), miR169 accumulation also increases under drought stress. Targets of Sly-miR169 include SlNF-YA1/2/3 and SlMRP1, which are down-regulated during stress conditions. This regulation suggests that miR169 positively influences drought tolerance in tomato by modulating auxin transport and stress-related pathways (Zhang et al., 2011c). In creeping bentgrass (Agrostis stolonifera L.), miR169 targets AsNFYA genes and acts as a positive regulator of drought tolerance. This regulation is achieved by minimizing stomata formation and enhancing antioxidant activity, thus reducing water loss and oxidative damage under drought conditions (Chen et al., 2024b).

However, contrasting roles of miR169 are observed in other species. In maize (Zea mays), zma-miR169 is significantly down-regulated under drought stress simulated by polyethylene glycol (PEG) treatment. This down-regulation suggests that miR169 negatively regulates drought tolerance in maize, as its suppression might allow increased expression of NF-YA genes critical for drought responses (Luan et al., 2015). Similarly, in soybean (Glycine max), miR169 targets GmNFYA3, a positive regulator of drought tolerance. The down-regulation of miR169 under stress permits the up-regulation of GmNFYA3, enhancing drought adaptation. This indicates a negative role of miR169 in regulating drought stress in soybean (Ni et al., 2013).

miR171

miR171 was found to positively regulate drought stress in most documented plant species. In Arabidopsis (Arabidopsis thaliana), miR171 is induced under drought conditions, suggesting its involvement in plant adaptive drought response (Liu et al., 2008). In rice (Oryza sativa), the expression of miR171 during drought stress is stage-dependent, with higher expression observed during the tillering stage and lower expression during the reproductive stage (Zhou et al., 2010). Later, it was demonstrated in rice that Osa-miR171f targets SCL6-I and SCL6-II, which are involved in shoot branching and flag leaf morphology (Um et al., 2022). Overexpression of osa-miR171f (osa-miR171f-OE) enhances drought tolerance through up-regulation of flavonoid biosynthesis genes in osa-miR171f-OE plants (Um et al., 2022). In mulberry (Morus notabilis), most mno-miR171 family members, except mno-miR171h, are significantly up-regulated under drought stress. This up-regulation highlights their positive role in drought stress responses (Sun et al., 2022). Similar expression pattern has also been observed in potato (Solanum tuberosum), where stu-miR171a, stu-miR171b, and stu-miR171c were all induced under drought stress, highlighting the positive regulatory roles miR171 play in plant drought stress response (Hwang et al., 2011).

miR319

miR319 plays a significant positive role in regulating drought tolerance across plant species by targeting TCP (teosinte branched1/cycloidea/PCF) transcription factors. In creeping bentgrass (Agrostis stolonifera), overexpression of Osa-miR319a leads to the down-regulation of putative target genes, including AsPCF5, AsPCF6, AsPCF8, and AsTCP14. This results in increased production of leaf wax, which mitigates water loss under drought stress, demonstrating a positive regulatory role in drought tolerance (Zhou et al., 2013). In wild alfalfa (Medicago ruthenica), the miR319-TCP4 regulatory module is suggested to act as a homeostasis factor that balances growth and stress adaptation under drought conditions. This dual role highlights the involvement of miR319 in maintaining a trade-off between development and drought tolerance (Guo et al., 2021). In sweet potato (Ipomoea batatas), overexpression of IbmiR319a enhances drought resistance by modulating leaf and petiole structure, as well as lignin biosynthesis. These changes contribute to reduced water loss, underscoring the role miR319 plays in structural adaptations to drought stress (Ren et al., 2022).

miR393

The effect of miR393 regulation on auxin and ABA pathways on drought tolerance is highly context-dependent, with contrasting outcomes depending on the species and specific stress conditions. In Arabidopsis thaliana, miR393 plays a pivotal role in the ABA-mediated inhibition of lateral root proliferation under drought stress. By targeting auxin receptors TIR1 and AFB2, miR393 optimizes root architecture to improve water acquisition, highlighting its positive regulatory role in drought tolerance (Chen et al., 2012). In creeping bentgrass (Agrostis stolonifera L.), overexpression of Osa-miR393a is associated with reduced stomatal density and denser cuticles, leading to decreased water loss and enhanced drought tolerance (Zhao et al., 2019).

On the other hand, miR393 negatively regulates drought in other species. In rice (Oryza sativa), OsmiR393 targets OsTIR1 and OsAFB2, homologues of auxin receptor genes in Arabidopsis. Overexpression of OsmiR393 reduces auxin signalling and negatively regulates drought tolerance, suggesting a complex and context-dependent role in stress responses (Xia et al., 2012). In barley (Hordeum vulgare), miR393 exhibits a dual role in regulating stomatal development and drought tolerance. Overexpression of miR393 increases stomatal density, leading to reduced drought tolerance due to impaired ABA biosynthesis and increased oxidative stress. In contrast, knockdown of miR393 enhances drought tolerance, suggesting a fine-tuned regulatory balance is required for optimal drought adaptation (Yuan et al., 2019b).

miR396

miR396 primarily functions as a negative drought regulator in most documented plant species. In tomato (Solanum lycopersicum), miR396 down-regulation triggers synergistic molecular and morphological adaptations that enhance water use efficiency, indicating that miR396 may negatively regulate drought stress responses (Fracasso et al., 2021). In soybean (Glycine max), pre-miR396a/i/b/d/g/k/e/h are up-regulated in leaves but down-regulated in roots under low water potential. Overexpression of miR396a/b/c/i in Arabidopsis thaliana seedlings resulted in lower survival rates compared to wild-type plants after rewatering under soil drying conditions. These results suggest that miR396 acts as a negative regulator of drought tolerance in soybeans (Liu et al., 2017a). In Pitaya (Hylocereus polyrhizus), hpo-miR396b is down-regulated during drought stress, correlating with the up-regulation of its target gene HpGRF6. This suggests that miR396 negatively regulates drought tolerance in Pitaya (Li et al., 2019a). In tree peony (Paeonia ostii), ptc-miR396g-5p expression decreases under drought conditions, correlating with increased expression of its target STAT transcription factor. This further supports the role of miR396 as a negative regulator of drought tolerance in this species (Guo et al., 2022).

Interestingly, contrasting results have been observed in tobacco expressing tomato miR396, where overexpression of Sp-miR396a-5p in tobacco (Nicotiana tabacum) enhanced tolerance to drought stress, suggesting that miR396's role in drought regulation may be species- and context-dependent (Chen et al., 2015a).

miR398

In tomato (Solanum lycopersicum) (Luan et al., 2014) and cotton (Gossypium hirsutum) (Xie et al., 2015), miR398 is down-regulated under drought stress, while miR398 is up-regulated in wild emmer wheat (Triticum turgidum ssp. dicoccoides) (Kantar et al., 2011) and peanut (Arachis hypogaea) (Park and Grabau, 2017), indicating a divergent role in drought responses in these species. Interestingly, in switchgrass (Panicum virgatum) (Hivrale et al., 2016), miR398 levels remain unaltered under drought conditions, highlighting species-specific regulatory mechanisms (Li et al., 2022).

In rice (Oryza sativa), overexpression of Os-miR398 in transgenic plants leads to reduced expression of its target genes, CSD1 and CSD2. This reduction impairs antioxidant capacity, making transgenic rice plants more sensitive to drought stress. These findings suggest that miR398 negatively regulates drought tolerance in rice by interfering with the plant's ability to mitigate oxidative damage (Lu et al., 2010).

miR399

miR399 is known for targeting genes involved in phosphate homeostasis and stress adaptations. In grapevine (Vitis vinifera), promoter regions of Vvi-MIR399 contain cis-elements associated with drought and hormonal responses, including elements responsive to gibberellic acid (GA), abscisic acid (ABA), methyl jasmonate (MeJA) and salicylic acid (SA). Overexpression of Vvi-MIR399e and Vvi-MIR399f in Arabidopsis thaliana enhanced drought tolerance, suggesting that miR399 positively regulates drought stress in grapevine (Liu et al., 2024).

Interestingly, overexpression of At-miR399f in Arabidopsis thaliana leads to hypersensitivity to drought stress (Baek et al., 2016), showing a controverse result. This indicates that heterologous expression of miR399 transcript from different species may not consistently affect drought stress tolerance.

miR408

miR408 plays a complex and species-dependent role in regulating plant responses to drought stress. In perennial ryegrass (Lolium perenne L.), transgenic plants expressing Os-miR408 exhibited improved drought tolerance characterized by better membrane stability and reduced lipid peroxidation, indicating reduced oxidative damage. These findings suggest that miR408 acts as a positive regulator of drought tolerance in ryegrass (Hang et al., 2021). In chickpea (Cicer arietinum), overexpression of miR408 enhanced drought tolerance by repressing the expression of PLANTACYANIN, a copper-binding protein targeted by miR408. This repression coincided with increased expression of stress-related transcription factors, including DREB2A, DREB1A and Rd17/29A, highlighting miR408's role as a positive regulator of drought responses in chickpea (Hajyzadeh et al., 2015).

In Arabidopsis thaliana, miR408 expression was up-regulated under drought conditions, leading to the down-regulation of its target genes, including cupredoxin, PLC and LAC3. However, overexpression of miR408 increased drought sensitivity, as indicated by higher death rates and reduced height under stress. Conversely, knockout mutants of miR408 showed decreased death rates and better growth under drought conditions, suggesting that miR408 acts as a negative regulator of drought tolerance in Arabidopsis (Ma et al., 2015). Recent findings further reveal that miR408's target, PLANTACYANIN (PCY), promotes reactive oxygen species (ROS) accumulation in guard cells, leading to stomatal closure and reduced photosynthetic gas exchange, which enhances drought resistance. These findings solidify the role of miR408 as a negative regulator of drought stress in Arabidopsis (Yang et al., 2024). In rice (Oryza sativa), overexpression of miR408 decreased drought tolerance. Plants overexpressing miR408 exhibited lower survival rates and higher water loss rates after recovery from drought stress, indicating a detrimental effect of miR408 on drought resistance in rice (Sun et al., 2018).

miR528

Little insight was given regarding the relationship between miR528 and plant drought defence. One study in rice (Oryza sativa) shows that miR528 targets OsD3, which encodes the F-BOX/LRR-REPEAT MAX2 homologue, a key component of the strigolactone signalling pathway critical for regulating plant architecture. Under drought stress, miR528 is differentially expressed: it is down-regulated in the inflorescence and roots but up-regulated in the flag leaf. Overexpression of miR528 in rice mimics traits of the OsD3 mutant, including increased tillering and altered root architecture (Balyan et al., 2023). These observations suggest that miR528 modulates plant morphology and drought defence in a tissue-specific manner, which warrants further investigations.

miR535

miR535 is another miRNA that has been largely overlooked across the diverse range of plant species regarding drought stress. In rice (Oryza sativa), OsmiR535 expression is induced under drought stress. However, CRISPR/Cas9 knockout of OsmiR535 results in enhanced tolerance to salt stress, suggesting that OsmiR535 negatively regulates stress tolerance. While its induction under drought stress implies involvement in stress signalling pathways, the improved stress resilience in knockout plants indicates that OsmiR535 may act as a suppressor of drought stress adaptation (Yue et al., 2020).

miR827

In barley (Hordeum vulgare), constitutive expression of Hv-miR827 enhances drought tolerance by improving whole-plant water use efficiency and recovery under severe drought conditions. However, this drought tolerance comes at the cost of growth inhibition, suggesting a trade-off between stress tolerance and growth in barley (Ferdous et al., 2017b). In potato (Solanum tuberosum), stu-miR827 targets the transcription factor StWRKY48. Suppressing stu-miR827 in transgenic potato lines leads to increased stomatal density, which reduces drought resistance. These findings indicate that miR827 positively regulates drought tolerance by repressing StWRKY48, thus preventing excessive water loss and enhancing plant resilience under drought stress (Yang et al., 2022). The studies demonstrate that miR827 plays a significant role in regulating drought tolerance by modulating water use efficiency, stomatal development, and transcriptional regulation of stress-associated genes.

miR1432

miR1432 has been demonstrated to have a negative regulatory effect under drought stress. In barley (Hordeum vulgare), a homologue of Osa-miR1432 was significantly down-regulated under drought stress, suggesting that miR1432 negatively regulates drought stress (Ferdous et al., 2017a). In rice (Oryza sativa), miR1432 targets the P-type IIB Ca²⁺ ATPase gene OsACA6, a key player in maintaining calcium homeostasis during stress. Overexpression of miR1432 suppresses OsACA6, leading to impaired calcium signalling and worsened drought tolerance (Dai et al., 2024). Additionally, miR1432 also targets OsCaML2, an EF-hand calcium-binding protein involved in calcium-mediated signalling under drought stress. Mutation or suppression of MIR1432 improves drought tolerance by preventing the down-regulation of OsCaML2, whereas overexpression of a miR1432-resistant form of OsCaML2 (OEmCaML2) enhances drought tolerance (Luo et al., 2024). These findings establish miR1432 as a negative regulator of drought tolerance in rice by disrupting calcium signalling pathways.

miRNA in salt stress

miR156

miR156 is up-regulated under salt stress in several plant species, including Arabidopsis thaliana (Liu et al., 2008), sugarcane (Saccharum spontaneum) (Bottino et al., 2013), chickpea (Cicer arietinum) (Kohli et al., 2014), radish (Raphanus sativus) (Sun et al., 2015), Medicago truncatula (Cao et al., 2018) and rice (Oryza sativa) (Aycan et al., 2023). In alfalfa (Medicago sativa), miR156 up-regulation under severe salt stress enhances the expression of stress-related transcription factors such as ERF, ZFP, AP2, WRKY and bZIP, contributing to improved salt tolerance (Arshad et al., 2017b). Conversely, miR156 is down-regulated under salt stress in maize (Zea mays) (Shinde et al., 2020), cotton (Gossypium hirsutum) (Wang et al., 2013b), Solanum linnaeanum (Zhuang et al., 2014) and wheat (Triticum aestivum) (Zeeshan et al., 2021). These findings demonstrate that miR156 exhibits contrasting regulatory roles in salt stress tolerance across species.

miR159

miR159 is involved in plant responses to salt stress, with its role varying across species. In soybean (Glycine max), all six MIR159 genes (MIR159a–MIR159f) were up-regulated under salt stress. This indicates a broad role for miR159 in salt stress tolerance mechanisms, potentially through ion homeostasis and root-specific adaptations (Li et al., 2023). In artichoke (Cynara cardunculus), miR159 expression increased following saline solution treatment, suggesting a positive role in plant response to salt stress (Islam et al., 2022). In sugar beet (Beta vulgaris L.), miR159 was down-regulated within 16 h of NaCl treatment, indicating a potentially contrasting role in salt stress responses compared to other species (Zhang et al., 2024).

miR160

miR160 plays a critical role in regulating salt stress tolerance across plant species by targeting auxin response factors (ARFs). In peanut (Arachis hypogaea L.), miR160 targets the ARF gene Arahy.7DXUOK. Overexpression of miR160 in transgenic plants enhances salt tolerance by degrading the transcript of the target gene, as revealed by RNA-seq analysis (Tang et al., 2022b). In soybean (Glycine max), the miR160a–GmARF16–GmMYC2 regulatory module improves salt tolerance by cleaving GmARF16, which otherwise activates GmMYC2. GmMYC2 acts as a transcription factor that suppresses proline biosynthesis, reducing salinity tolerance. By suppressing GmMYC2, miR160 promotes proline accumulation, enhancing salt stress adaptation (Wang et al., 2024). In maize (Zea mays), bio-priming with Bacillus spp significantly induced miR160d transcript levels under salt stress. This suggests that miR160 contributes to salt stress tolerance in maize, potentially through microbial interactions and stress signalling (Aydinoglu et al., 2023).

miR164

miR164 plays a key regulatory role in plant responses to salt stress by targeting NAC transcription factors and influencing root development and plant architecture. In poplar (Populus euphratica), the miR164-PeNAC regulatory module influences lateral root development and stem elongation, resulting in improved performance under salt stress. This suggests a positive role for miR164 in salt tolerance in this species (Lu et al., 2017).

However, in wheat (Triticum aestivum), tae-miR164 targets TaNAC14, a NAC transcription factor that promotes root development and enhances salinity tolerance. This indicates that miR164 plays a negative role in salt stress adaptation in wheat (Chi et al., 2023). Similarly, in maize (Zea mays), zma-miR164a expression decreases under salt stress, leading to the up-regulation of its target genes GRMZM2G114850 (a NAC transcription factor) and GRMZM2G008819 (an electron carrier protein). The NAC transcription factor enhances salt stress tolerance by regulating downstream stress-responsive genes, highlighting the critical role of miR164 down-regulation in improving salt tolerance in maize. This indicates that miR164 has a role that varies across species, acting as a positive or negative regulator depending on the context.

miR166

The regulatory effects of miR166 in plant salinity response vary between positive and negative roles depending on the species and context. In potatoes (Solanum tuberosum), miR166 was induced under salinity stress conditions. Network modelling based on Arabidopsis thaliana revealed that the induction of miR166 likely modulates the expression of target genes involved in developmental and stress-response pathways, suggesting that miR166 enhances salinity tolerance in potatoes (Kitazumi et al., 2015). Similarly, in broomcorn (Sorghum bicolor), up-regulation of miR166 in roots and leaves under salinity stress suggests that miR166 plays a positive role in salinity adaptation by modulating stress-responsive pathways (Sharma et al., 2020).

In contrast, high-throughput sequencing in switchgrass (Panicum virgatum) reported that miR166 was down-regulated upon salinity treatment. This down-regulation correlated with salinity stress mitigation, indicating a distinct mechanism where miR166 suppression improves stress tolerance (Xie et al., 2014). Additionally, in pearl millet (Pennisetum glaucum), miR166 was one of the most significantly down-regulated microRNA families under salinity stress. This suggests that miR166 may negatively regulate salt stress responses in this species (Shinde et al., 2020).

miR167

miR167 is a key regulator of salinity stress responses in plants by targeting auxin response factors to modulate developmental and stress-related pathways. In the tamarisk tree (Tamarix chinensis), tch-miR167 targets TcARF6, a transcription factor with a glutamine-rich region that is critical for the salt stress response. Under salt stress, tch-miR167 expression increases, leading to the down-regulation of TcARF6 and likely contributing to salinity adaptation in tamarisk (Ye et al., 2020). In cotton (Gossypium hirsutum), miR167 expression is up-regulated in salt-tolerant cultivars compared to salt-sensitive ones, suggesting its involvement in enhancing salt tolerance (Yin et al., 2012). Similarly, in rice (Oryza sativa L.), miR167 is specifically and significantly expressed in the shoot and root tissues of seedlings from the salt-tolerant Doc Phung (DP) cultivar, indicating its positive role in regulating salt stress responses in rice (Nguyen et al., 2023).

In contrast, miR167 plays a negative role in salt tolerance in other species. In maize (Zea mays), the down-regulation of miR167 at the early stages of salt stress in salt-tolerant lines leads to the accumulation of ARF transcription factors, which regulate root and stem development to enhance biomass production and mitigate salt stress damage (Shinde et al., 2020). In tomato (Solanum lycopersicum), salt stress reduces miR167a expression, further supporting its negative regulatory role in this species (Jodder et al., 2017).

miR169

miR169 is a key player in salinity stress responses through its regulation of NF-YA transcription factors. In rice (Oryza sativa), miR-169n/o is salt-responsive and selectively cleaves an NF-YA transcription factor gene, contributing to transcriptional regulation under salt stress conditions. This highlights the role of miR169 in modulating stress-responsive gene networks in rice (Zhao et al., 2009). In creeping bentgrass (Agrostis stolonifera L.), miR169 targets AsNFYA genes and acts as a positive regulator under salt stress. It maintains ion homeostasis by regulating ion-channel genes and reduces oxidative damage through elevated antioxidant pathways, enhancing plant resilience to salinity (Chen et al., 2024b). In maize (Zea mays), miR169 exhibits a dynamic response to salt stress. Zma-miR169 is up-regulated during short-term exposure to NaCl and down-regulated during long-term exposure, reflecting the expression changes of ZmNF-YA. This suggests a regulatory role in balancing stress adaptation over time (Luan et al., 2015). Additionally, the ZmmiR169q/ZmNF-YA8 module was identified as a key regulator of maize root development under salt stress, underscoring its importance in maintaining root architecture and stress resilience (Xing et al., 2023).

miR171

In Arabidopsis thaliana, miR171 is induced under high salinity conditions, suggesting its involvement in modulating stress-responsive pathways to enhance salt tolerance (Liu et al., 2008). Similarly, in mulberry (Morus notabilis), most members of the mno-miR171 family, except mno-miR171h, are significantly up-regulated under salt stress. This indicates that mno-miR171 family plays a positive role in salinity stress responses (Sun et al., 2022). However, experimental validation and the exact mechanism of miR171 in regulating salt stress require further investigations.

miR319

miR319 positively regulates salinity stress responses across diverse plant species by targeting TCP transcription factors. In creeping bentgrass (Agrostis stolonifera), overexpression of Osa-miR319a leads to reduced sodium uptake, thereby improving salinity tolerance in transgenic plants (Zhou et al., 2013). In common bean (Phaseolus vulgaris), the miR319-targeted gene Pvul-TCP-1 is down-regulated in roots under salt stress. This underscores its role in modulating salt stress responses through root-specific regulatory mechanisms (İlhan et al., 2018). In poplar (Populus spp.), overexpression of miR319a confers enhanced salt tolerance, while miR319a-MIMIC plants with reduced miR319a activity exhibit salt sensitivity. miR319a-overexpressing plants exhibit reduced cambium cell layers, wider xylem with increased vessel and fibre numbers and lumen area, and thinner cell walls, facilitating ion transport and enhancing salinity adaptation (Cheng et al., 2024). In switchgrass (Panicum virgatum), miR319 regulates PvPCF5, which fine-tunes ethylene synthesis. This regulatory pathway enhances salt tolerance, indicating the role of miR319 in modulating hormonal responses to salinity stress (Liu et al., 2019).

miR390

miR390 is another regulator of plant salinity stress responses, acting primarily through its interaction with auxin response factors (ARFs). In poplar (Populus spp.), miR390 expression is strongly induced by salt stress in roots. miR390 targets ARF3.1, ARF3.2 and ARF4, which are significantly down-regulated under salt stress and further suppressed in miR390-overexpressing lines. Overexpression of miR390 promotes primary root growth and enhances salt tolerance, while knockdown of miR390 (via short tandem target mimic) inhibits root elongation and reduces salt resistance. This suggests that miR390 positively regulates salt stress tolerance in poplar by promoting adaptive root architecture (He et al., 2018). In Jerusalem artichoke (Helianthus tuberosus L.), miR390 expression is induced under moderate salt stress, with the miR390-TAS3-ARF module positively regulating salt tolerance. This highlights the conserved role of miR390 in modulating stress adaptation through ARF signalling in this species as well (Wen et al., 2020).

In contrast, in cotton (Gossypium hirsutum), miR390 negatively regulates salt stress tolerance. Its target, GhCEPR2, was identified as a critical gene in the salt stress response. Overexpression of GhCEPR2 in both Arabidopsis thaliana and cotton enhanced salt tolerance, which was associated with increased proline content and decreased malondialdehyde (MDA) levels, reducing lipid peroxidation and oxidative damage. This indicates that suppression of miR390 improves salt resistance in cotton (Chu et al., 2022).

miR393

miR393 regulates salt stress tolerance by modulating auxin signalling pathways. In Arabidopsis thaliana, salt stress induces miR393 expression, triggering stabilization of Aux/IAA repressors and repressing TIR1/AFB2-mediated auxin signalling. Mutants lacking miR393ab showed enhanced lateral root growth and length during salinity stress but exhibited increased ROS levels and reduced ascorbate peroxidase (APX) activity compared to wild-type plants (Iglesias et al., 2014). Overexpression of a miR393-resistant TIR1 gene (mTIR1) enhanced salt tolerance by circumventing miR393-mediated repression, leading to improved germination rates, reduced water loss, preserved chlorophyll content, delayed senescence and reduced mortality under salt stress (Chen et al., 2015b). In tobacco (Nicotiana tabacum), overexpression of AtmiR393a from Arabidopsis conferred enhanced salt tolerance, as transgenic lines exhibited reduced sensitivity to NaCl stress during seedling growth (Feng et al., 2010). In wheat (Triticum aestivum), miR393 expression was significantly induced by salt stress, suggesting its role in plant response to salinity (Wang et al., 2014a). In creeping bentgrass (Agrostis stolonifera L.), overexpression of Osa-miR393a improved salt tolerance by increasing potassium uptake, which aids in ionic balance under salinity stress (Zhao et al., 2019).

The overwhelmingly positive influence of miR393 in salt stress ceased in the study of rice (Oryza sativa), where transgenic plants overexpressing osa-MIR393 exhibited increased sensitivity to salt and alkali stress compared to wild-type plants, indicating a negative regulatory role of miR393 in salinity tolerance (Gao et al., 2011).

miR396

miR396 plays a significant role in plant salinity stress responses by targeting Growth-Regulating Factors (GRFs) and modulating physiological and molecular traits critical for stress adaptation. In creeping bentgrass (Agrostis stolonifera), overexpression of Osa-miR396c improved salt tolerance. Transgenic plants exhibited better water retention, higher chlorophyll content, improved cell membrane integrity, and enhanced Na⁺ exclusion during high salinity exposure. Four potential miR396 target genes, likely members of the GRF transcription factor family, were up-regulated in response to salt stress, highlighting their involvement in regulating plant growth and stress responses (Yuan et al., 2019a). In tomato (Solanum lycopersicum), overexpression of Sp-miR396a-5p in tobacco (Nicotiana tabacum) increased salt tolerance, further supporting the conserved role of miR396 in enhancing salinity adaptation across species (Chen et al., 2015a).

miR398

miR398 plays a negative role in salinity stress responses by regulating antioxidant enzymes such as Cu/Zn superoxide dismutase (CSD), ascorbate peroxidase (APX) and catalase (CAT). In Arabidopsis thaliana, miR398 is steadily suppressed under salt stress, allowing for the up-regulation of its target genes involved in oxidative stress responses. This suggests that miR398 negatively regulates salt stress tolerance by limiting the expression of key antioxidant enzymes (Jia et al., 2009b). Similarly, in poplar (Populus spp.), miR398 expression levels decline during prolonged salt stress exposure, indicating that its suppression supports improved salt stress tolerance (Jia et al., 2009b). In tomato (Solanum lycopersicum), overexpression of sly-miR398b in transgenic plants resulted in reduced plant growth, including decreased shoot and root biomass, shorter plant height and higher accumulation of superoxide radicals. This led to severe oxidative damage due to the down-regulation of antioxidant enzymes such as CSD, APX, and CAT. These findings confirm that miR398 overexpression is detrimental under salt stress and that its suppression is necessary to enhance salinity tolerance (He et al., 2021).

miR399

miR399 plays a critical role in modulating phosphate homeostasis and salinity tolerance in Arabidopsis thaliana by regulating the PHO2 pathway and phosphate transporter genes. Under salt stress, elevated miR399 levels significantly enhance the expression of phosphate transporters PHT1;4 and PHT1;9, promoting PO₂ translocation from roots to shoots. This ensures adequate phosphate availability in aerial tissues, supporting essential physiological processes and enabling better adaptation to salinity stress (Pegler et al., 2020). Additionally, overexpression of miR399f in Arabidopsis enhances tolerance to both salt stress and exogenous ABA, further demonstrating the positive regulatory role of miR399 in salinity adaptation (Baek et al., 2016).

miR408

miR408 regulates salinity stress responses by modulating oxidative stress, ion homeostasis, and lignin biosynthesis through its targets, such as cupredoxin, LAC3, and plastocyanin-like proteins. Its regulatory role is highly species-specific, acting as either a positive or negative regulator of salt stress tolerance. In Arabidopsis thaliana, miR408 targets cupredoxin and LAC3. Transgenic plants with elevated miR408 expression exhibit reduced oxidative stress, increased root length (main and lateral), and up-regulated expression of CSD1 and CSD2. These changes enhance salt tolerance by mitigating oxidative damage and improving root architecture (Ma et al., 2015). In Nicotiana benthamiana, salt stress significantly induces miR408 expression. Transgenic tobacco plants overexpressing Sm-MIR408 show improved seed germination under salinity stress, with increased activity of NbSOD (superoxide dismutase), NbPOD (peroxidase), and NbCAT (catalase). This results in lower ROS levels and reduced oxidative damage, highlighting miR408's positive regulatory role (Guo et al., 2018).

In contrast, in rice (Oryza sativa), miR408 expression is down-regulated under salinity stress, while its target genes, such as helicase DSHCT and plastocyanin-like, are up-regulated. This suggests that miR408 negatively regulates salt stress adaptation in rice by suppressing these genes (Macovei and Tuteja, 2012). In wheat (Triticum aestivum), TaCLP1 (a chemocyanin-like protein and plantacyanin) is a target of tae-miR408. Overexpression of TaCLP1 in Schizosaccharomyces pombe (yeast) enhances cell growth under high salinity, indicating that miR408 negatively regulates salt stress tolerance by suppressing TaCLP1 (Feng et al., 2013). In maize (Zea mays), salt stress suppresses miR408 expression. Transgenic maize overexpressing MIR408b is hypersensitive to salt stress, characterized by increased net Na⁺ efflux, redistribution of Na⁺ to the intercellular space, reduced lignin accumulation and fewer cells in vascular bundles under salinity. Conversely, knockout of miR408 or overexpression of ZmLAC9 enhances salt tolerance, indicating a negative regulatory role of miR408 in maize (Qin et al., 2023).

miR528

miR528 positively regulates salt tolerance. In rice (Oryza sativa), miR528 positively regulates salt tolerance by down-regulating the gene encoding l-ascorbate oxidase (AO). Overexpression of miR528 enhances rice salt tolerance, while its knockdown compromises tolerance. The miR528-AO module improves salinity adaptation by increasing abscisic acid (ABA) and ascorbic acid levels, which reduce ROS accumulation and oxidative damage (Wang et al., 2021b). In creeping bentgrass (Agrostis stolonifera), AsAAO (ascorbic acid oxidase) and COPPER ION BINDING PROTEIN1 were identified as putative targets of miR528. Constitutive expression of rice miR528 in creeping bentgrass enhanced salt tolerance by improving potassium (K⁺) homeostasis and elevating antioxidant activity, contributing to ionic balance and reduced oxidative stress under salinity stress (Yuan et al., 2015).

miR535

miR535 was found to primarily have a negative effect on salt stress tolerance. In rice (Oryza sativa), the expression of OsmiR535 is induced under salt stress, but CRISPR/Cas9 knockout of OsmiR535 enhances tolerance to salt stress, indicating that OsmiR535 negatively regulates the response to salt stress (Yue et al., 2020). A similar regulatory role was found in switchgrass. In switchgrass (Panicum virgatum L.), inoculation with Azorhizobium caulinodans ORS571 promotes plant growth and increases tolerance to salinity stress. Interestingly, following inoculation, miR535 levels were decreased, further suggesting that miR535 negatively regulates plant salt stress response (Chen et al., 2023b).

miR1432

Experimental validation was done in rice (Oryza sativa), where miR1432 targets the P-type IIB Ca²⁺ ATPase gene OsACA6. Overexpression of miR1432 suppresses OsACA6, which is critical for maintaining calcium homeostasis during stress, leading to reduced salt tolerance (Dai et al., 2024).

miRNA in cold stress

miR156

miR156 plays a diverse role in cold stress tolerance. In apple (Malus domestica), overexpression of miR156 decreased cold tolerance, as evidenced by increased H₂O₂ content and reduced catalase (CAT) and peroxidase (POD) activities under cold stress (Shen et al., 2023). Conversely, in Arabidopsis thaliana, overexpression of its target SPL9 enhances freezing tolerance by up-regulating C-repeat binding factor 2 (CBF2) (Zhao et al., 2022). In rice (Oryza sativa), miR156 indirectly enhances cold stress tolerance by activating stress-responsive genes, including OsLEA3, OsRab16A and OsDREB2A through the transcription factor OsMYB2 (Zhou and Tang, 2019).

miR159

miR159 in maize (Zea mays) has been shown to modulate plant growth and development under chilling stress by targeting transcription factors such as GAMYB, likely contributing to improved cold stress adaptation (Božić et al., 2024).

miR160

miR160-ARF module in maize is implicated in regulating transcription factors and redox homeostasis during chilling stress, although its precise mechanisms remain to be elucidated (Aydinoglu, 2020).

miR164

miR164 has been identified as a key player in regulating cold tolerance in tea plants (Camellia sinensis), where decreased expression of csn-miR164a leads to the up-regulation of CsNAC1, which promotes cold-responsive genes such as CsCBFs. Silencing csn-miR164a enhances cold tolerance in tea plants, whereas its overexpression impairs stress adaptation in Arabidopsis (Li et al., 2024). In tomato (Solanum lycopersicum), the Sl-miR164a/b-5p-NAM3 module negatively regulates cold tolerance by suppressing SlNAM3. Overexpression of SlNAM3 improves cold tolerance by enhancing photosynthetic efficiency and reducing oxidative damage under cold stress (Dong et al., 2022).

miR166

In tomato (Solanum lycopersicum), Sly-miR166 targets HD-ZIP III genes and its higher expression correlates with enhanced cold stress responses (Valiollahi et al., 2014).

miR167

In wheat (Triticum aestivum), miR167 regulates the auxin-signalling pathway and developmental responses to cold stress. Certain miR167 members, such as tae-miR167d and tae-miR167c, are down-regulated during cold stress, suggesting a negative regulatory role (Tang et al., 2012b).

miR168

miR168 is up-regulated during cold stress in both wheat and Arabidopsis, indicating its positive role in cold stress adaptation (Gupta et al., 2014; Liu et al., 2008).

miR319

miR319 is a well-characterized positive regulator of cold stress tolerance in rice, sugarcane (Saccharum officinarum), and cassava (Manihot esculenta). In rice, overexpression of miR319 enhances cold tolerance by targeting TCP transcription factors such as OsPCF5, OsPCF6, OsPCF8 and OsTCP21, improving ROS scavenging (Schommer et al., 2012; Wang et al., 2014b; Yang et al., 2013). Similar regulatory mechanisms are observed in sugarcane and cassava, where miR319 is up-regulated under cold stress and down-regulates TCP targets, enhancing stress tolerance (Lei et al., 2017; Thiebaut et al., 2012).

miR393

In switchgrass (Panicum virgatum), overexpression of osa-miR393a enhances cold tolerance by up-regulating cold-responsive genes such as PvCOR47, PvICE1 and PvRAV1 while reducing oxidative stress (Liu et al., 2017b). Similarly, miR393-mediated phasiRNAs in banana (Musa spp.) are enriched under cold stress, further supporting its role in stress adaptation (Zhu et al., 2019a).

miR395

In grape (Vitis vinifera), miR395 regulates sulfur metabolism, influencing the synthesis of antioxidant compounds critical for cold stress responses. Its regulation appears to negatively impact cold tolerance by increasing oxidative stress during cold exposure (Ghabooli et al., 2019).

miR396

In Jerusalem artichoke, up-regulation of htu-MIR396 under cold stress alters GRF and WRKY transcription factors, enhancing stress tolerance in specific tissues (Ding et al., 2024). Similarly, Overexpression of tomato Sp-miR396a-5p in tobacco increased tolerance to cold stress (Chen et al., 2015a).

miR398

miR398 plays a crucial role in cold tolerance by modulating antioxidant systems. In chrysanthemum, CdICE1 suppresses miR398, enabling the up-regulation of CSD1 and CSD2, which mitigate oxidative stress, indicating miR398 is a negative cold stress regulator (Chen et al., 2013). In wheat, lncRNAs (lncR9A, lncR117, lncR616) act as competing endogenous RNAs (ceRNAs) to sequester miR398, indirectly enhancing CSD1 expression and cold tolerance, further implicating miR398 is negatively regulating cold stress (Lu et al., 2020b).

miR399

miR399 is up-regulated during cold stress in wheat (Triticum aestivum), preventing degradation of TaICE1 and enhancing freezing tolerance (Peng et al., 2021).

miR408

In Arabidopsis, miR408 improves cold tolerance by enhancing antioxidant gene expression, including CSD1 and CSD2 (Ma et al., 2015). Rice and maize also show improved cold tolerance and stress adaptation with miR408 overexpression, which modulates antioxidant systems and growth-related pathways (Akgul and Aydinoglu, 2025; Sun et al., 2018).

miR528

miR528 is another key regulator, OsmiR528 enhancing cold tolerance in Arabidopsis by repressing rice homologue OsMYB30 and activating stress-response genes (Tang and Thompson, 2019). In banana, miR528 down-regulation under cold stress leads to excessive ROS accumulation and peel browning, revealing its potential positive regulatory role in cold stress tolerance (Zhu et al., 2020). Interestingly, the miR156c-MaSPL4 module in banana inhibit miR528 level to modulate cold stress adaptation (Kong et al., 2025), illustrating a complex interplay between these miRNAs.

miR535

In rice (Oryza sativa), OsmiR535 plays a negative regulatory role in cold stress responses. It targets three SPL genes (OsSPL14, OsSPL11 and OsSPL4), and its expression is induced by cold stress. Overexpression of OsmiR535 suppresses core components of the CBF-mediated cold signalling pathway, including OsCBF1, OsCBF2 and OsCBF3. This suppression leads to inhibited early seedling growth under cold stress, aggravated cold-induced cell death, and increased accumulation of reactive oxygen species (ROS). As a result, rice plants overexpressing OsmiR535 are more sensitive to cold stress (Sun et al., 2020a).

miR1432

In rice (Oryza sativa), miR1432 negatively impacts cold stress tolerance by targeting the P-type IIB Ca²⁺ ATPase gene OsACA6. Overexpression of miR1432 suppresses OsACA6, a gene critical for maintaining calcium homeostasis during stress. This suppression disrupts calcium signalling, which is essential for stress adaptation, ultimately leading to worsened cold tolerance (Dai et al., 2024).

miRNA in heat stress

miR156

The role of miR156 in heat stress tolerance has been demonstrated in alfalfa (Medicago sativa), where overexpression of miR156 and down-regulation of its target SPL13 enhance heat stress tolerance by improving physiological responses, as well as increasing anthocyanin and chlorophyll accumulation (Matthews et al., 2019). miR156-overexpressing alfalfa plants also exhibited higher antioxidant and proline levels under heat stress, further contributing to their improved tolerance (Arshad et al., 2020).

miR159

In rice (Oryza sativa), overexpression of miR159 resulted in increased sensitivity to heat stress, highlighting its negative regulatory role (Wang et al., 2012).

miR160

In Arabidopsis thaliana, miR160 suppresses ARF10/16/17 to regulate heat shock protein (HSP) gene expression, positively influencing thermotolerance. Transgenic Arabidopsis plants overexpressing miR160 showed enhanced heat tolerance, while inhibition of miR160 resulted in reduced heat tolerance (Li et al., 2014; Lin et al., 2018). Additionally, in tomato (Solanum lycopersicum), the miR160-ARF17 module regulates the transition from post-meiotic to mature pollen under heat stress, suggesting a positive role in heat stress tolerance (Keller et al., 2020). However, in cotton (Gossypium hirsutum), miR160 overexpression increased sensitivity to heat stress by decreasing ARF10/17 mRNA levels, leading to indehiscent anthers due to disrupted auxin responses during sporogenous cell proliferation (Chen et al., 2020a; Ding et al., 2017).

miR164

miR164 has been identified as a positive regulator of heat tolerance in Arabidopsis. Transgenic plants overexpressing miR164 displayed improved heat tolerance compared to wild-type plants, whereas miR164 mutants exhibited heat-sensitive phenotypes. These effects were associated with altered chlorophyll a/b ratios, reduced H₂O₂ accumulation, and changes in heat shock protein expression (Tsai et al., 2023).

miR166

In wheat (Triticum aestivum), eight miRNAs, including tae-miR166, were reported to be up-regulated under heat stress, suggesting their positive roles in heat stress responses (Xin et al., 2010).

miR167

In tomato, heat stress caused reduced expression of miR167a, indicating its negative regulatory role in heat tolerance (Jodder et al., 2017).

miR168

In flowering Chinese cabbage (Brassica rapa), miR168 was up-regulated during heat stress, pointing to its potential positive regulatory role (Ahmed et al., 2019).

miR169

The regulation of miR169 during heat stress has been studied in both Arabidopsis and tomato. Heat Stress Transcription Factors (HSFs) bind to miR169, and silencing HSFs reduces miR169 levels, leading to decreased heat tolerance through increased expression of NF-YA target genes. Elevated miR169 under heat stress represses NF-YA post-transcriptionally, alleviating the suppression of HSFA7, a heat stress effector, thus indicating miR169's positive role in thermotolerance (Rao et al., 2022).

miR171

miR171 expression was up-regulated in the leaves of Arabidopsis under heat stress, suggesting its involvement in heat stress responses (Mahale et al., 2014).

miR319

miR319 plays a crucial role in heat stress tolerance across species. In tomato, overexpression of sha-miR319d enhanced heat tolerance by increasing the activities of superoxide dismutase (SOD) and catalase (CAT) (Shi et al., 2019).

miR393

In creeping bentgrass (Agrostis stolonifera), overexpression of osa-miR393a increased the expression of small heat-shock proteins, providing cellular protection against heat damage (Zhao et al., 2019).

miR396

In Jerusalem artichoke (Helianthus tuberosus), htu-MIR396 was up-regulated under 42°C heat stress, inducing the expression of GRF transcription factors (HtGRF4/6/10/12/13) in leaves and HtSCL33 in roots while repressing HtWRKY40 in leaves, which contributed to heat stress adaptation (Ding et al., 2024).

miR398

miR398 also positively regulates heat stress tolerance. In Arabidopsis, transgenic plants overexpressing miR398-resistant forms of CSD1, CSD2 or CCS1 exhibited reduced heat tolerance due to decreased activities of heat-stress transcription factors and heat-shock proteins. This indicates that miR398 is critical for maintaining proper thermotolerance through its regulation of heat stress-responsive genes (Guan et al., 2013).

miRNA in UV-B radiation stress

miRNAs also play significant roles in mediating plant responses to UV-B radiation, often regulating oxidative stress, antioxidative capacity and stress tolerance mechanisms.

miR156 has been found to accumulate under UV-B radiation in Arabidopsis thaliana through an age-dependent pathway, suggesting its involvement in UV stress responses (Dotto et al., 2018). Similarly, miR160 has been identified as UV-responsive under UV-B radiation in Arabidopsis and Populus tremula (Jia et al., 2009a; Zhou et al., 2007).

In perennial ryegrass (Lolium perenne), overexpression of OsmiR164a (OE164) resulted in greater UV-B sensitivity compared to wild-type and miR164-suppressed (MIM164) plants. This increased sensitivity was associated with more leaf scorching, higher electrolyte leakage and lower relative water content. These effects were linked to reduced antioxidative capacity and anthocyanin accumulation under UV-B stress, emphasizing the negative regulatory role of miR164 in UV-B tolerance (Xu et al., 2024).

UV-B radiation also up-regulates miR166 expression in multiple species, including Arabidopsis, rice (Oryza sativa), Populus and Prunus, suggesting a conserved role for this miRNA in UV-B stress responses (Jia et al., 2009a). Similarly, miR167 expression is increased under UV-B radiation in Populus tremula, further supporting its involvement in mitigating UV stress effects (Jia et al., 2009a). In Arabidopsis thaliana, miR169 is up-regulated by UV-B radiation, indicating its potential regulatory role in the UV-B stress response (Zhou et al., 2007).

In wheat (Triticum aestivum), miR171 is induced by UV-B radiation, highlighting its positive role in regulating UV responses (Wang et al., 2013a). Interestingly, miR398 is also up-regulated under UV-B radiation, where accumulation of detrimental ROS is expected (Jia et al., 2009a). This suggests miR398 has a distinct regulatory mechanism involved in UV-specific stress responses.

miRNA in nutrient deficiency

miRNAs are involved in nutrient deficiency, such as nitrogen, phosphorus, potassium and sulfur shortages. Here, we summarize how these miRNAs regulate nutrient uptake under different deficiency conditions (Table 3).

Table 3 Summary of the positive or negative impacts of various miRNAs on species-specific plant responses to nutrient deficiency including nitrogen, phosphorus, potassium and sulfur deficiency

Deficiency	miRNA	Regulation	Species	Reference
Nitrogen	miR169	Negative	Arabidopsis thaliana	Rao et al. (2022)
miR396	Rice (Oryza sativa)	Liu et al. (2017a)
miR171	Positive	Arabidopsis thaliana	Liu et al. (2008)
miR528	Creeping bentgrass (Agrostis stolonifera)	Yuan et al. (2015)
miR393	Arabidopsis thaliana	Chen et al. (2012)
Phosphorus	miR159e	Negative	Soybean (Glycine max)	Li et al. (2023)
miR528	Maize (Zea mays)	Balyan et al. (2023)
miR156	Positive	Soybean (Glycine max)	Li et al. (2011b)
miR399	Arabidopsis thaliana	Baek et al. (2016)
miR399	Rapeseed (Brassica napus)	Du et al. (2023)
miR399	Rice (Oryza sativa)	Hu et al. (2015)
miR408	Wheat (Triticum aestivum)	Xin et al. (2010)
miR827	Rice (Oryza sativa)	Lin et al. (2010)
miR827	Barley (Hordeum vulgare)	Ferdous et al. (2017a)
miR827	Maize (Zea mays)	Ferdous et al. (2017b)
miR160	Common bean (Phaseolus vulgaris)	Valdés-López et al. (2010)
Potassium	miR1432	Negative	Barley (Hordeum vulgare)	Ferdous et al. (2017a)
miR160a	Positive	Banana (Musa acuminata)	Cheng et al. (2019)
miR168	Tomato (Solanum lycopersicum)	Liu et al. (2020a)
Sulfur	miR395	Positive	Arabidopsis thaliana	Bhardwaj et al. (2024)

miRNA in phosphorus (P) deficiency

In soybean (Glycine max), miR156 overexpression enhances tolerance to P deficiency by negatively regulating four SPL genes, including AtSPL4/5/6/15 (Lu et al., 2023). Overexpression of miR159e in soybean reduces phosphorus content in leaves, indicating its negative role in P absorption and transport (Li et al., 2023). miR160 is differentially regulated under P deficiency in common bean (Phaseolus vulgaris), with changes observed across various organs to help the plant cope with nutrient stress (Valdés-López et al., 2010). In Arabidopsis thaliana, elevated miR399 levels reduce PHO2 transcript abundance, leading to enhanced activity of Pi transporters like PHT1;4, improving P translocation and tolerance under P-deficient conditions (Pegler et al., 2021).

Similarly, in rapeseed (Brassica napus), overexpression of Bna-miR399c increases root length and biomass under low P conditions, improving Pi acquisition and accumulation (Du et al., 2023). In rice (Oryza sativa), miR399 down-regulates LTN1, increasing concentrations of Fe, K, Na and Ca under P-deficient conditions (Hu et al., 2015). miR408 is induced under Pi starvation in wheat (Triticum aestivum), where it regulates the phosphate transporter gene NtPT2, improving Pi uptake and acquisition (Bai et al., 2018). In maize (Zea mays), the ZmmiR528-ZmLac3 regulatory module is critical for root growth under low P conditions. Overexpression of miR528 impairs root growth and Pi uptake, indicating a negative role, whereas overexpressing its target ZmLac3 enhances Pi deficiency tolerance (Pei et al., 2024). miR827 plays a positive role in regulating Pi homeostasis across species. In rice, it targets OsSPX-MFS1 and OsSPX-MFS2, promoting Pi uptake under deficient conditions (Lin et al., 2010). In barley (Hordeum vulgare), miR827 targets SPX-domain-containing genes to regulate P-responsive pathways (Hackenberg et al., 2013). In maize, lncRNA767 assists miR827 in targeting key Pi transporter components, further enhancing Pi starvation tolerance (Chen et al., 2024a).

miRNA in nitrogen (N) deficiency

miR160 regulates root system architecture through auxin signalling to enhance lateral and adventitious root (LR/AR) development under N-deficient conditions in Arabidopsis, cotton, and Brassica napus (Magwanga et al., 2019). In Arabidopsis, miR169 is strongly down-regulated under N starvation, allowing NFYA family members to enhance N uptake and stress resilience (Zhao et al., 2011). In Arabidopsis, miR171 is induced upon N starvation, suppressing SCL6-II/III/IV to enhance primary root system development, highlighting its positive role in N starvation tolerance (Liang et al., 2012). In rice, knockout of miR396e and miR396f increases biomass and yield under N-deficient conditions, indicating that miR396 negatively regulates N stress (Zhang et al., 2020a). In creeping bentgrass (Agrostis stolonifera), miR528 positively regulates N-deficient stress by increasing N accumulation, chlorophyll synthesis and antioxidant activity (Yuan et al., 2015). In Arabidopsis, miR393/AFB3 was found to be a unique nitrate-responsive regulatory mechanism, It modulates root system architecture through auxin signalling, allowing plants to adapt root growth to external nitrate availability and internal nitrogen status, both miR393-overexpression and AFB3 mutation increased the primary root length in seedlings under nitrogen deficient conditions (Vidal et al., 2010).

miRNA in potassium (K) deficiency

In banana (Musa acuminata), miR160a and its target MaARF18-like-2 mediate low K⁺ responses by regulating Ca²⁺ signalling, ion transport and ROS-associated genes (Tang et al., 2025). In tomato (Solanum lycopersicum), miR168 suppresses SlAGO1A, enhancing root growth, leaf development and K⁺ content under K-deficiency stress (Liu et al., 2020a). In barley (Hordeum vulgare), miR1432 is down-regulated under K-deficiency, indicating its negative role in regulating stress tolerance via Ca²⁺ signalling pathways (Zeng et al., 2019).

miRNA in sulfur (S) deficiency

miR395 plays a distinct and crucial role in regulating S homeostasis. In Arabidopsis thaliana, miR395 was induced under sulfate-deficient conditions (Bhardwaj et al., 2024). It targets a low-affinity sulfate transporter gene AST68 and ATP sulfurylase genes APS1, APS3, and APS4 to regulate sulfate uptake under S deprivation (Jagadeeswaran et al., 2014). Similarly, up-regulation of miR395 was observed in rice under sulfate deficiency conditions, and overexpression of OsamiR395h in Tabacco resulted in cleavage of sulfate transporter gene NtaSULTR2, leading to disrupted sulfate homeostasis (Yuan et al., 2016).

miRNA in pollutant stress

miRNAs have also been implicated in modulating plant tolerance to various pollutants, including cadmium, chromium, aluminium, phenanthrene, copper, sulfur dioxide and arsenite, by targeting key genes involved in stress response pathways (Table 4).

Table 4 Summary of miRNAs involved in plant pollutant responses

Pollutant	Regulation	miRNA	Species	Reference
Aluminium (Al)	Positive	miR393	Barley (Hordeum vulgare)	Bai et al. (2017)
miR390	Flax (Linum usitatissimum)	Dmitriev et al. (2017)
miR319	Flax (Linum usitatissimum)
miR393	Flax (Linum usitatissimum)
Arsenite [As (III)]	Negative	miR528	Rice (Oryza sativa)	Liu et al. (2015)
miR408	Arabidopsis thaliana	Kumar et al. (2023)
Cadmium (Cd)	Negative	miR160	Cabbage (Brassica napus)	Huang et al. (2010)
miR535	Rice (Oryza sativa)	Yue et al. (2023)
miR398	Tomato (Solanum lycopersicum)	Yan et al. (2023a)
miR390	Rice (Oryza sativa)	Ding et al. (2016)
Positive	miR395	Cabbage (Brassica napus)	Zhang et al. (2013)
miR156	Arabidopsis thaliana	Zhang et al. (2020b)
miR166	Rice (Oryza sativa)	Ding et al. (2018)
Chromium (Cr)	Negative	miR160	Rice (Oryza sativa)	Dubey et al. (2020)
Positive	miR166	Rice (Oryza sativa)
miR171	Rice (Oryza sativa)
Copper (Cu)	Negative	miR398	Grapevine (Vitis vinifera)	Leng et al. (2017)
miR398	Hickory (Carya cathayensis)	Sun et al. (2020c)
miR408	Wheat (Triticum aestivum)	Feng et al. (2013)
Phenanthrene	Negative	miR398	Wheat (Triticum aestivum)	Li et al. (2020)
Positive	miR164	Wheat (Triticum aestivum)	Li et al. (2021a)
Sulfur Dioxide (SO₂)	Positive	miR398	Arabidopsis thaliana	Li et al. (2017a)
miR395	Arabidopsis thaliana

miRNA in cadmium (Cd) stress

MicroRNAs play diverse roles in regulating Cd stress tolerance. miR156 enhances Cd stress tolerance in Arabidopsis thaliana by modulating ROS levels and the expression of cadmium uptake and transport genes (Zhang et al., 2020b). Conversely, miR160 is transcriptionally down-regulated under Cd stress in cabbage (Brassica napus), which leads to increased auxin levels. This auxin boost promotes adventitious and lateral root development, aiding in Cd tolerance (Huang et al., 2010).

In rice (Oryza sativa), miR166 regulates Cd toxicity by targeting OsHB4. Silencing OsHB4 improves Cd tolerance, while overexpression increases Cd accumulation in leaves and grains, highlighting the miR166-OsHB4 module as a key pathway for mitigating Cd toxicity (Ding et al., 2018). miR390 is down-regulated under Cd stress in rice, and its overexpression results in reduced Cd tolerance and increased Cd accumulation, further emphasizing its role as a negative regulator of Cd stress (Ding et al., 2016). In cabbage (Brassica napus), miR395 enhances Cd tolerance by reducing oxidative stress, increasing chlorophyll and glutathione levels and up-regulating key Cd-responsive genes like BnPCS1 and Sultr1;1 (Zhang et al., 2013).

In tomato (Solanum lycopersicum), miR398 is down-regulated under Cd stress, and its overexpression results in greater susceptibility, with increased oxidative damage and growth inhibition under Cd stress (Yan et al., 2023a). Finally, miR535 in rice targets SPL7, a regulator of Nramp5, which controls Cd uptake. Overexpression of miR535 increases Cd sensitivity and accumulation, while its knockout reduces Cd uptake and improves tolerance (Yue et al., 2023).

miRNA in chromium (Cr) stress

Under Cr stress, miR160 in rice is down-regulated, leading to auxin-mediated root development, which enhances tolerance (Dubey et al., 2020). In the meantime, miR166 and miR171 are up-regulated in rice in response to Cr stress (Dubey et al., 2020), highlighting distinctive roles of miRNAs in response to Cr stress.

miRNA in aluminium (Al) stress

MicroRNAs such as miR390, miR319 and miR393 play roles in aluminium stress regulation. In flax (Linum usitatissimum), miR390 and miR319 are significantly up-regulated under Al stress, enhancing root tolerance by targeting TAS3, which reduces ARF-mediated auxin responses and decreases Al accumulation in roots (Dmitriev et al., 2017). In resistant cultivars of flax, miR393 is up-regulated under Al stress, mitigating root elongation inhibition and ROS-induced cell death (Dmitriev et al., 2017). Similarly, in barley (Hordeum vulgare), overexpression of miR393 improves Al tolerance by counteracting root elongation inhibition and reducing oxidative damage, while knockdown transgenics display increased sensitivity to Al (Bai et al., 2017).

miRNA in phenanthrene stress

In wheat (Triticum aestivum), miR164 is up-regulated under phenanthrene stress, suppressing NAC1 and reducing adventitious root formation. This response helps mitigate damage caused by ROS generation and lipid peroxidation (Li et al., 2021a). In wheat roots, phenanthrene exposure impairs the conversion of pri-miR398 to pre-miR398, resulting in decreased levels of mature miR398. This reduction in miR398 alleviates its gene-silencing effect on CSD1, which mitigates phenanthrene-induced oxidative stress by boosting superoxide dismutase (SOD) activity and enhancing plant tolerance (Li et al., 2020), demonstrating negative regulatory role of miR398.

miRNA in copper (Cu) stress

The role of miR398 in Cu stress varies across species. In hickory (Carya cathayensis), miR398 targets CSD1, CSD2, CSD3, and COX5b.1. Overexpression of miR398 reduces CSD activity, weakening Cu stress tolerance (Sun et al., 2020c). In grapevine (Vitis vinifera), miR398 inhibition under Cu stress increases CSD1 and CSD2 expression, improving Cu tolerance by reducing ROS levels and enhancing SOD activity (Leng et al., 2017). In wheat, miR408 targets TaCLP1, a gene linked to cell growth under Cu²⁺ stress. Overexpression of TaCLP1 suggests that miR408 plays a negative role in Cu stress tolerance (Feng et al., 2013).

miRNA in sulfur dioxide (SO₂) stress

In Arabidopsis thaliana, miR395 and miR398 are up-regulated under SO₂ stress, down-regulating its targets, including APS3, APS4 and SULTR2;1. This results in increased glutathione levels, enhanced antioxidative capacity and improved SO₂ tolerance (Li et al., 2017a).

miRNA in arsenite [As(III)] stress

In Arabidopsis thaliana, miR408 targets GSTU25, a gene involved in sulfur assimilation and detoxification. Overexpression of miR408 increases sensitivity to arsenite stress, while knockout mutants developed using CRISPR/Cas9 show enhanced tolerance (Kumar et al., 2023). Similarly, in rice, overexpression of miR528 increases arsenite sensitivity by altering antioxidant activity and amino acid metabolism, highlighting its negative regulatory role (Liu et al., 2015).

miRNA in biotic stress

miRNAs have long been observed as essential regulators in biotic defence. They modulate target gene expression to dynamically orchestrate defence signalling pathways and fine-tune plant immune responses against a broad spectrum of pathogens including bacteria, fungi and viruses and pests, playing multifaceted roles across different plant species (Table 5).

Table 5 miRNAs involved in plant biotic stress responses

miRNA	Regulation	Plant	Pathogen/Pest	Reference
miR1432	Negative	Rice (Oryza sativa)	Magnaporthe oryzae (blast fungus)	Li et al. (2021c)
Positive	Wheat (Triticum aestivum)	Stripe rust (Puccinia striiformis)	Feng et al. (2016)
Rice (Oryza sativa)	Xanthomonas oryzae (bacterial blight)	Jia et al. (2021)
miR156	Negative	Rice (Oryza sativa)	Brown planthopper (Nilaparvata lugens)	Ge et al. (2018)
Loblolly pine (Pinus taeda)	Cronartium quercuum f. sp. fusiforme (fungus)	Lu et al. (2007)
Wheat (Triticum aestivum)	Powdery mildew (Blumeria graminis)	Xin et al. (2010)
Positive	Arabidopsis (Arabidopsis thaliana)	Tobacco mosaic virus (TMV-Cg)	Tagami et al. (2007)
Tobacco (Nicotiana tabacum)	Tobamoviridae (viruses)	Bazzini et al. (2007)
miR159	Negative	Tobacco (Nicotiana tabacum)	Phytophthora species (oomycete)	Zheng et al. (2020)
Arabidopsis (Arabidopsis thaliana)	Root-knot nematodes (RKN)	Medina et al. (2017)
Positive	Cotton (Gossypium hirsutum)	Verticillium dahliae (fungus)	Zhang et al. (2016)
Arabidopsis (Arabidopsis thaliana)
miR160	Positive	Cassava (Manihot esculenta)	Colletotrichum gloeosporioides (fungus)	Pinweha et al. (2015)
Banana (Musa acuminata)	Fusarium oxysporum (fungus)	Cheng et al. (2019)
Potato (Solanum tuberosum)	Phytophthora infestans (oomycete)	Natarajan et al. (2018)
Arabidopsis (Arabidopsis thaliana)	Pseudomonas syringae pv. tomato (bacterium)	Xue and Yi (2018)
miR164	Negative	Arabidopsis (Arabidopsis thaliana)	General pathogen defence	Gupta et al. (2020)
Positive	Poplar (Populus tomentosa)	Leaf black spot (Marssonina brunnea)	Chen et al. (2021)
Wheat (Triticum aestivum)	Stripe rust (Puccinia striiformis)	Feng et al. (2014)
Cotton (Gossypium hirsutum)	Verticillium dahliae (fungus)	Hu et al. (2020)
miR166	Negative	Soybean (Glycine max)	Asian soybean rust (Phakopsora pachyrhizi)	Kulcheski et al. (2011)
Positive	Populus (Populus trichocarpa)	Botryosphaeria dothidea (bacterial stem canker)	Zhao et al. (2012)
Persicaria minor	Fusarium oxysporum (fungus)	Samad et al. (2017)
Mungbean (Vigna radiata)	Mungbean Yellow Mosaic India Virus	Kundu et al. (2017)
Wheat (Triticum aestivum)	Powdery mildew (Erysiphe graminis)	Xin et al. (2010)
miR167	Negative	Rice (Oryza sativa)	Magnaporthe oryzae (rice blast fungus)	Zhang et al. (2020c)
Positive	Arabidopsis (Arabidopsis thaliana)	Pseudomonas syringae (bacterium)	Caruana et al. (2020)
Soybean (Glycine max)	Soybean mosaic virus (SMV)	Yin et al. (2013)
miR168	Positive	Chinese crabapple (Malus hupehensis)	Botryosphaeria dothidea (fungus)	Yu et al. (2017)
Arabidopsis (Arabidopsis thaliana)	Fusarium oxysporum (fungal elicitors)	Baldrich et al. (2014)
miR169	Negative	Maize (Zea mays)	Bipolaris maydis (fungus)	Xie et al. (2024)
Positive	Turfgrass (Agrostis stolonifera)	General pathogen defence	Chen et al. (2024b)
miR171	Positive	Sweet orange (Citrus sinensis)	Citrus psorosis virus (CPsV)	Reyes et al. (2016)
Kenaf (Hibiscus cannabinus)	Hibiscus chlorotic ringspot virus	Gao et al. (2013)
Lotus japonicus (Lotus japonicus)	Rhizobial bacteria (nodules)	De Luis et al. (2012)
Rice (Oryza sativa)	Rice stripe virus (RSV)	Tong et al. (2017)
miR319	Positive	Tomato (Solanum lycopersicum)	Root-knot nematodes (Meloidogyne spp.)	Zhao et al. (2015)
miR390	Negative	Apple (Malus × domestica)	Alternaria alternata apple pathotype (AAAP)	Qin et al. (2021)
Tobacco (Nicotiana attenuata)	Manduca sexta (herbivore)	Pradhan et al. (2021)
Positive	Apple (Malus × domestica)	Colletotrichum gloeosporioides (fungus)	Shi et al. (2022)
miR393	Negative	Arabidopsis (Arabidopsis thaliana)	Botrytis cinerea (fungus)	Djami-Tchatchou and Dubery (2019)
Positive	Cassava (Manihot esculenta)	Colletotrichum gloeosporioides (fungus)	Pinweha et al. (2015)
Arabidopsis (Arabidopsis thaliana)	Pseudomonas syringae pv. tomato (bacterium)	Zhang et al. (2011b)
miR395	Negative	Apple (Malus × domestica)	Alternaria alternata	Zhang et al. (2017)
miR396	Negative	Tomato (Solanum lycopersicum)	Phytophthora nicotianae (oomycete)	Chen et al. (2015a)
Alfalfa (Medicago sativa)	Spodoptera litura (insect herbivore)	Yan et al. (2023b)
miR398	Positive	Wheat (Triticum aestivum)	Fusarium culmorum (fungus)	Salamon et al. (2021)
Rice (Oryza sativa)	Magnaporthe oryzae (fungus)	Li et al. (2019b)
Negative	Brachypodium distachyon	Bamboo mosaic virus (BaMV)	Lin et al. (2022)
Tomato (Solanum lycopersicum)	Botrytis cinerea (fungus)	Liu et al. (2023b)
Barley (Hordeum vulgare)	Powdery mildew (Blumeria graminis)	Xu et al. (2014)
Common bean (Phaseolus vulgaris)	Sclerotinia sclerotiorum (fungus)	Naya et al. (2014)
Maize (Zea mays)	General pathogen defence	Gandham et al. (2024)
miR408	Negative	Soybean (Glycine max)	Soybean cyst nematode (Heterodera glycines)	Feng et al. (2022)
Wheat (Triticum aestivum)	Stripe rust (Puccinia striiformis)	Feng et al. (2013)
miR444	Negative	Rice (Oryza sativa)	Rhizoctonia solani (sheath blight)	Feng et al. (2023)
Positive	Rice (Oryza sativa)	Rice stripe virus (RSV)	Wang et al. (2016)
miR528	Negative	Rice (Oryza sativa)	Rice stripe virus (RSV)	Yao et al. (2019)
miR530	Negative	Rice (Oryza sativa)	Magnaporthe oryzae (blast fungus)	Li et al. (2021b)
Maize (Zea mays)	Northern leaf blight (Setosphaeria turcica)	Wu et al. (2014)
Cotton (Gossypium hirsutum)	Verticillium dahliae (fungus)	Hu et al. (2023)
miR535	Negative	Rice (Oryza sativa)	Magnaporthe oryzae (blast fungus)	Zhang et al. (2022b)
miR827	Positive	Tobacco (Nicotiana tabacum)	Chilli veinal mottle virus (ChiVMV)	Tang et al. (2024)
Negative	Arabidopsis (Arabidopsis thaliana)	Cyst nematode infection	Hewezi et al. (2016)
Rice (Oryza sativa)	Magnaporthe oryzae (blast fungus)	Bundó et al. (2024)
Grapevine (Vitis quinquangularis)	General pathogen defence	Luo et al. (2024)

miR156

The expression level of miR156 has been observed to increase in various plant-virus interactions. For example, tobacco (Nicotiana tabacum) exhibits elevated miR156 levels when infected with members of the Tobamoviridae, Potyviridae, and Potexviridae families (Bazzini et al., 2007). Similarly, Arabidopsis (Arabidopsis thaliana) shows increased miR156 expression in response to infection by tobacco mosaic virus (TMV-Cg), turnip yellow mosaic virus (TYMV) and turnip mosaic virus (TuMV) (Chen et al., 2004; Kasschau et al., 2003; Tagami et al., 2007). In rice (Oryza sativa), infection with pathogens has also been associated with elevated miR156 expression (Zhang et al., 2020c). miR156 has been shown to play a role in regulating plant defence mechanisms. In rice (Oryza sativa), it negatively regulates resistance to brown planthopper by enhancing the biosynthesis of jasmonic acid (JA) and jasmonoyl-isoleucine (Ge et al., 2018).

In contrast, a repression of miR156 has been reported in other plant-pathogen interactions. For instance, in galled loblolly pine (Pinus taeda) infected with the fungus Cronartium quercuum f. sp. fusiforme in its stem, miR156 expression is significantly down-regulated (Lu et al., 2007). Similarly, wheat (Triticum aestivum) infected with powdery mildew also exhibits markedly decreased miR156 expression (Xin et al., 2010).

miR159

It has been shown that cotton (Gossypium hirsutum) and Arabidopsis (Arabidopsis thaliana) accumulate elevated levels of miR159 in response to the fungus Verticillium dahliae. In this interaction, miR159 is exported into the fungal hyphae, where it targets the gene encoding isotrichodermin C-15 hydroxylase (HiC-15), a critical enzyme for hyphal growth (Zhang et al., 2016). Additionally, miR159 accumulates to higher levels in Arabidopsis (Arabidopsis thaliana) root galls that form in response to root-knot nematodes (RKN). Functional evidence for the involvement of the miR159-GAMYB pathway in this process comes from studies on an Arabidopsis mir159abc triple mutant, which exhibits greater resistance to RKN infection (Medina et al., 2017). In tomato (Solanum lycopersicum), the regulatory function of sly-miR159 is stress-specific, suggesting its potential role in distinct signalling pathways for different stress responses, including mechanical damage caused by pests (López-Galiano et al., 2019). In tobacco (Nicotiana tabacum), inhibition of miR159 activates GAMYB, resulting in strong defence responses against Phytophthora infection. However, such defence activation is not observed in Arabidopsis (Arabidopsis thaliana) or rice (Oryza sativa), indicating species-specific functional differences or additional regulatory requirements for triggering defence responses (Zheng et al., 2020).

miR160

Bacterial and fungal pathogen exposure has been shown to induce miR160 expression and down-regulate auxin response factors (ARFs), thereby generating defence responses in multiple plant species. In Arabidopsis (Arabidopsis thaliana), miR160 is induced in response to Pseudomonas syringae pv. tomato (Pst DC3000) and Botrytis cinerea infections (Xue and Yi, 2018; Zhang et al., 2011a). Similarly, in banana (Musa acuminata), miR160 is up-regulated in response to Fusarium oxysporum infection (Cheng et al., 2019), and in cassava (Manihot esculenta), miR160 induction occurs during infection with Colletotrichum gloeosporioides (Pinweha et al., 2015). Additionally, miR160 has been found to play a crucial role in local defence and systemic acquired resistance during potato (Solanum tuberosum) interaction with Phytophthora infestans. This regulatory role involves balancing the antagonistic cross-talk between auxin-mediated growth and salicylic acid-mediated defence responses (Natarajan et al., 2018).

miR164

In wheat (Triticum aestivum), tae-miR164 and its target gene TaNAC21/22, a NAC transcription factor from the NAM subfamily, have been identified as key regulators of the plant response to stripe rust. During stripe rust infection, tae-miR164 and TaNAC21/22 exhibit contrasting expression patterns, with tae-miR164 suppressing TaNAC21/22 to enhance resistance (Feng et al., 2014), which is a similar miR164-NAC regulatory module that has been uncovered as a critical player in the defence response of Chinese white poplar (Populus tomentosa) to the leaf black spot fungus Marssonina brunnea (Chen et al., 2021). In cotton (Gossypium hirsutum), the ghr-miR164-GhNAC100 regulatory module plays a pivotal role in resistance to Verticillium dahliae. Overexpression of ghr-miR164 or knockdown of GhNAC100 enhances disease resistance, demonstrating that the ghr-miR164-GhNAC100 module positively regulates Verticillium resistance (Hu et al., 2020).

Interestingly, miR164 serve as a negative biotic stress regulator in Arabidopsis (Arabidopsis thaliana), where down-regulation of ath-miR164c under combined stress conditions leads to increased AtP5CS1 expression and proline accumulation, which enhances pathogen resistance (Gupta et al., 2020).

miR166

In Persicaria minor, an aromatic plant of Malaysia, miR166 targets the HD-ZIP III transcription factor family, which is involved in the production of secondary metabolites that help defend against Fusarium oxysporum infection (Samad et al., 2017). In Populus trichocarpa (black cottonwood), miR166 is up-regulated in the stem bark in response to infection with poplar bacterial stem canker (Botryosphaeria dothidea), suggesting a positive defensive role for miR166 in the plant response to this pathogen (Zhao et al., 2012). In wheat (Triticum aestivum), infection with powdery mildew (Erysiphe graminis) alters miR166 expression. Specifically, miR166d is highly up-regulated, while miR166a maintains basal expression levels, indicating a positive defensive mechanism against the pathogen (Xin et al., 2010). In mungbean (Vigna radiata), miR166 expression is up-regulated in a resistant pattern at later stages of Mungbean Yellow Mosaic India Virus (MYMIV) infection, targeting bZIP transcription factors (Kundu et al., 2017). However, in soybean (Glycine max), miR166a-5p and miR166f are down-regulated in susceptible plants upon infection with Phakopsora pachyrhizi, the causative agent of Asian soybean rust, highlighting a contrasting role for miR166 in pathogen susceptibility (Kulcheski et al., 2011).

miR167

The expression of miR167 shows diverse regulation in response to biotic stress across different plant species. Viral infections, such as Hibiscus chlorosis ringspot virus (Gao et al., 2013), Cucumber mosaic virus (CMV) and Tomato aspergillosis virus (TAV) (Feng et al., 2009), have been reported to increase miR167 expression. Similarly, fungal or viral infections in tomato (Solanum lycopersicum) activate miR167a, suggesting its involvement in stress responses (Jodder et al., 2017). In contrast, cyst nematodes (Hewezi et al., 2008) and root-knot nematodes (RKN) (Pan et al., 2019) induce significant down-regulation of miR167. Interestingly, under wheat rust stress, miR167 expression initially increases but is later down-regulated, reflecting a dynamic regulatory pattern (Gupta et al., 2012).

The regulatory roles of miR167 have been demonstrated through its targeting of auxin response factors (ARFs). In Solanaceae plants, miR167 modulates the expression of IAR3, leading to alterations in auxin homeostasis and enhanced pathogen defence (D'Ippolito et al., 2016). In soybean (Glycine max), miR167 targets ARFs to reduce the negative impact of Soybean mosaic virus (SMV) infection on plant growth (Yin et al., 2013). In Arabidopsis (Arabidopsis thaliana), miR167a targets ARF6 and ARF8, resulting in relatively closed leaf stomata to restrict the entry of Pseudomonas syringae, thereby contributing to pathogen defence (Caruana et al., 2020). However, in rice (Oryza sativa), knockdown of osa-miR167d promotes the expression of defence- and cell death-related genes (KS4, PAL, NAC4, PR1a, PBZ1 and PR10b), increases jasmonic acid (JA) content and enhances immunity to Magnaporthe oryzae. These findings indicate a negative regulatory role of miR167 in defence against Magnaporthe oryzae (Zhang et al., 2020c).

miR168

In Arabidopsis (Arabidopsis thaliana), miR168 is induced by fungal infection caused by fungal elicitors such as Fusarium oxysporum. This suggests that the miR168-ARGONAUTE1 (AGO1) module may act as a positive regulator during fungal infection (Baldrich et al., 2014). In Chinese crabapple (Malus hupehensis), miR168 and its target MhAGO1 play a critical role in regulating resistance to Botryosphaeria dothidea. This regulatory module reduces reactive oxygen species (ROS) production and promotes salicylic acid (SA)-mediated defence responses, thereby delaying symptom development and inhibiting pathogen growth (Yu et al., 2017).

miR169

In maize (Zea mays), zma-miR169s has been identified as a negative regulator of defence against Bipolaris maydis. During B. maydis infection, the expression levels of zma-miR169s and its precursor are significantly repressed. Furthermore, CRISPR/Cas9 mutants of zma-miR169s exhibit enhanced resistance to B. maydis (Xie et al., 2024). However, in creeping bentgrass (Agrostis stolonifera L.), RNA-Seq analysis of miR169 transgenic plants suggests that miR169 positively regulates biotic stress responses (Chen et al., 2024b).

miR171

In rice (Oryza sativa), overexpression of osa-miR171b reduces susceptibility to rice stripe virus (RSV) and alleviates viral symptoms, highlighting its role as a positive regulator of viral resistance (Tong et al., 2017). Similarly, in kenaf (Hibiscus cannabinus), Hibiscus chlorotic ringspot virus infection up-regulates miR171 while its target gene SCL1 is down-regulated, suggesting a positive regulatory role of miR171 in defence against this viral pathogen (Gao et al., 2013). In the meantime, miR171 appears to have a more complex regulatory role in sweet orange (Citrus sinensis) during Citrus psorosis virus (CPsV) infection, miR171 is down-regulated due to interactions between the viral 24 K protein and pre-miR171a in the nucleus, resulting in the up-regulation of targets such as Scarecrow-like 6. This interaction suggests that miR171 may contribute to CPsV defence in sweet orange but inhibited due to viral counter defence (Reyes et al., 2016). Beyond viral infections, miR171 is also implicated in bacterial interactions. In Lotus japonicus, Lja-miR171c expression is elevated in infected nodules compared to healthy ones, indicating its potential involvement in bacterial infection and nodule development (De Luis et al., 2012).

miR390

In apple (Malus × domestica), mdm-miR390a negatively regulates disease resistance by targeting and suppressing the expression of MdRPK2 and MdLRR8, two genes associated with pathogen recognition and resistance. Overexpression of mdm-miR390a in apple and tobacco (Nicotiana tabacum) enhances susceptibility to Alternaria alternata apple pathotype (AAAP) infection. In contrast, overexpression of MdRPK2 or MdLRR8 improves resistance, but co-expression with mdm-miR390a diminishes this resistance, confirming its counteractive role in pathogen defence. This highlights the negative regulatory role of miR390 in pathogen infection (Qin et al., 2021). Similarly, in tobacco (Nicotiana attenuata), miR390 is induced during herbivory, resulting in the down-regulation of ARF4. Overexpression of Na-miR390 reduces auxin accumulation and leads to decreased capsule production when attacked by Manduca sexta herbivores. This suggests that miR390 negatively regulates biotic stress responses by reducing capsule protection during herbivore attacks (Pradhan et al., 2021).

However, the role of miR390 is not universally negative. Transgenic apple plants (‘GL-3’) overexpressing MIR390b show reduced fungal damage to leaves and fruit following Colletotrichum gloeosporioides infection. This increased resistance is associated with enhanced superoxide dismutase (SOD) and peroxidase (POD) activity, which mitigates oxidative stress. These findings suggest a more complex regulatory mechanism for miR390 that depends on the specific type of pathogen invasion (Shi et al., 2022).

miR319

In tomato (Solanum lycopersicum), miR319 targets TCP4 gene, which enhances jasmonic acid biosynthesis genes and regulates endogenous jasmonic levels in leaves, promoting overall systemic root-knot nematode resistance (Zhao et al., 2015).

miR393

The miR393 family plays a pivotal role in regulating plant immunity and balancing defence responses against pathogens. In Arabidopsis thaliana, the AGO2-miR393b-MEMB12 module is critical for antibacterial immunity by promoting PR1 exocytosis. Meanwhile, miR393 also contributes to immunity via AGO1 by modulating auxin signalling (Zhang et al., 2011b). Acting as a regulatory node, miR393 represses auxin signalling to fine-tune metabolic and signalling pathways, enhancing resistance to biotrophic pathogens while stabilizing the salicylic acid (SA)-mediated immune response. However, this defensive strategy comes with a trade-off, as it increases susceptibility to necrotrophic pathogens due to resource reallocation (Robert-Seilaniantz et al., 2011). Additionally, miR393 is involved in the regulation of innate immune responses in Arabidopsis during the perception of bacterial lipopolysaccharide (LPS). LPS recognition involves lectin-domain receptor-like kinases (LecRLKs), which function as surveillance proteins. Overexpression of miR393 suppresses LecRLK expression, while repression of miR393 induces it, highlighting potential negative regulatory role of miR393 in LPS-mediated defence (Djami-Tchatchou and Dubery, 2019). In cassava (Manihot esculenta), miR393 exhibits a differential regulatory role in the resistance to Colletotrichum gloeosporioides depending on plant genotype. In the sensitive cultivar Hanatee, miR393 expression is significantly decreased during infection, whereas in the resistant cultivar Huay Bong 60, miR393 expression increases, indicating its positive role in regulating pathogen defence mechanisms (Pinweha et al., 2015).

miR395

In apple (Malus×domestica), Md-miR395 targets MdWRKY26, a critical regulator of defence-related gene. Overexpression of Md-miR395 reduces the expression level of MdWRKYN1 and MdWRKY26 and results in the increased plant susceptibility towards Alternaria alternata f. sp. mali infection, indicating the negative regulatory role of miR395 in leaf spot defence (Zhang et al., 2017).

miR396

In alfalfa (Medicago sativa), miR396 expression is significantly up-regulated during wounding treatments against Spodoptera litura larvae. However, overexpression of MIM396, which sequesters miR396, enhances resistance to larvae. This improved resistance is associated with higher lignin content, enhanced biosynthesis of low-molecular weight flavonoids and glucosinolates, suggesting that miR396 negatively regulates defence responses to herbivory (Yan et al., 2023b). Similarly, in tomato (Solanum lycopersicum), overexpression of Sp-miR396a-5p leads to increased susceptibility to Phytophthora nicotianae infection, further confirming the negative regulatory role of miR396 in biotic stress responses (Chen et al., 2015a).

miR398

The miR398 family plays much diverse and context-dependent roles in plant responses to biotic stresses, influencing oxidative stress regulation and immune responses across species. In rice (Oryza sativa), miR398 enhances immunity against the rice blast fungus (Magnaporthe oryzae) by targeting key genes involved in oxidative stress regulation, including CSD1, CSD2, SODX (superoxide dismutase X) and CCSD (copper chaperone for superoxide dismutase). This regulation affects superoxide dismutase (SOD) activity and hydrogen peroxide (H₂O₂) levels, which are critical for pathogen defence (Li et al., 2019b). Similarly, in wheat (Triticum aestivum), miR398 expression increases during early responses to Fusarium culmorum inoculation, suggesting its positive role in stress regulation (Salamon et al., 2021).

In contrast, miR398 can have negative effects on defence responses in other plants. In barley (Hordeum vulgare), the resistance gene Mla suppresses hvu-miR398 to ensure adequate HvSOD1 accumulation, which facilitates the oxidative burst and enhances defence against powdery mildew fungus, highlighting miR398's negative regulatory role in stress response (Xu et al., 2014). Similarly, in maize (Zea mays), miR398 targets SKIP5 (SKP1-interacting partner 5), which is critical for protein turnover during stress and immunity, suggesting that miR398 may hinder resistance to biotic stresses (Gandham et al., 2024).

In tomato (Solanum lycopersicum), miR398 plays complex roles depending on the stressor. During Potato spindle tuber viroid (PSTVd) infection, miR398 is significantly induced, reducing the expression of SOD1, SOD2 and CCS1. This impairs the plant's ability to detoxify reactive oxygen species (ROS), but the resulting excessive ROS triggers lethal systemic necrosis, potentially as part of the plant defence strategy (Suzuki et al., 2019). However, in response to Botrytis cinerea by tomato, sly-miR398b levels are significantly reduced in infected leaves. Overexpression of sly-miR398b suppresses critical MeJA-responsive defence genes, weakening jasmonate-mediated immunity (Liu et al., 2023b).

In other species, miR398 also displays contrasting roles. In common bean (Phaseolus vulgaris), miR398b is down-regulated during fungal infection by Sclerotinia sclerotiorum, leading to the up-regulation of CSD1 and Nod19. This regulation helps mitigate oxidative stress caused by the fungal attack (Naya et al., 2014). Conversely, in Brachypodium distachyon and Nicotiana benthamiana, Bamboo mosaic virus (BaMV) infection increases miR398 levels. However, this up-regulation does not counteract the virus but instead promotes virus infection symptoms by increasing ROS levels (Lin et al., 2022).

miR408

In wheat (Triticum aestivum), TaCLP1, a target gene of tae-miR408, plays a crucial role in resistance to stripe rust. Silencing of TaCLP1 reduces resistance to stripe rust, indicating that tae-miR408 negatively regulates defence against this pathogen (Feng et al., 2013). Similarly, in soybean (Glycine max), gma-miR408 expression is highly up-regulated during soybean cyst nematode (SCN) migration and syncytium formation. Overexpression of gma-miR408 decreases soybean resistance to SCN by reducing reactive oxygen species (ROS) accumulation, which is essential for effective defence responses. Conversely, silencing gma-miR408 enhances resistance to SCN by increasing ROS accumulation (Feng et al., 2022), thereby highlighting the negative role of miR408 in pathogen defences.

miR444

The miR444 family plays a multifaceted role in regulating biotic stress responses in rice (Oryza sativa), balancing resistance mechanisms through distinct signalling pathways. miR444 targets three MIKCC-type MADS box genes: OsMADS23, OsMADS27a and OsMADS57. During Rice stripe virus (RSV) infection, miR444 expression is up-regulated. Overexpression of miR444 enhances resistance to RSV by increasing the expression of OsRDR1 (RNA-dependent RNA polymerase 1). This is facilitated by the suppression of the repressive activity of OsMADS23, OsMADS27a and OsMADS57 on OsRDR1 transcription, leading to effective antiviral responses (Wang et al., 2016).

In contrast, osa-miR444b.2 acts as a negative regulator of plant resistance to Rhizoctonia solani, the causal agent of rice sheath blight. It influences ethylene (ET) and auxin (IAA) signalling pathways, thereby compromising resistance. This highlights the complexity of miR444's role in regulating biotic stress, with its effects varying based on the specific pathogen and regulatory context (Feng et al., 2023).

miR528

In rice (Oryza sativa), SPL9 directly binds to specific motifs in the promoter region of miR528 and activates its transcription. Increased miR528 expression lowers Ascorbic Oxidase mRNA levels, compromising rice defence against Rice stripe virus (RSV), indicating that miR528 functions as a negative regulator of biotic stress (Yao et al., 2019). Additionally, during viral infection, miR528 becomes preferentially bound by cleavage-defective AGO18 complexes. This sequestration reduces the functional availability of miR528, resulting in increased Ascorbic Oxidase activity, which boosts antiviral defences (Wu et al., 2017).

miR530

The miR530 family has been identified as a negative regulator of plant growth and defence responses across several species. In maize (Zea mays), miR530 is down-regulated during Northern leaf blight infection, indicating that it negatively regulates blight response. The reduced expression of miR530 during infection is likely part of a defence mechanism to enhance resistance (Wu et al., 2014). In rice (Oryza sativa), miR530 negatively regulates the transcription factor gene OsSPL3, which is involved in blast disease responses. Blocking miR530 increases the levels of OsSPL14, leading to enhanced resistance to blast disease, improved yield, and better maturity in rice plants. This indicates that miR530 plays a dual role in negatively regulating both growth and blast disease resistance (Li et al., 2021b). In cotton (Gossypium hirsutum), ghr-miR530 has been identified as a key miRNA involved in the distant response to Verticillium dahliae infection in roots. ghr-miR530 directly cleaves GhSAP6 mRNA during post-transcriptional regulation. Silencing ghr-miR530 enhances resistance to V. dahliae, while its overexpression reduces resistance. Similarly, knockdown of GhSAP6, the target of ghr-miR530, decreases resistance, likely due to the down-regulation of salicylic acid (SA)-related genes such as GhNPR1 and GhPR1. These findings suggest that ghr-miR530 negatively regulates V. dahliae infection by suppressing the SA signalling pathway (Hu et al., 2023).

miR535

In rice (Oryza sativa), miR535 negatively regulates rice immunity against Magnaporthe oryzae, the causal agent of rice blast disease. Osa-miR535 targets OsSPL4, and overexpression of Osa-miR535 significantly reduces the accumulation of SPL4TBS-YFP, a fusion protein containing the OsSPL4 target sequence, thereby suppressing rice immunity. Conversely, overexpression of OsSPL4 (OXSPL4) enhances plant resistance to rice blast fungus. This resistance is associated with increased hydrogen peroxide (H₂O₂) accumulation, indicative of an activated immune response (Zhang et al., 2022b).

miR827

miR827 exhibits negative regulatory role in many species. In rice (Oryza sativa), miR827 targets OsSPX-MFS1 and OsSPX-MFS2, which encode vacuolar phosphate (Pi) transporters. Overexpression of MIR827 disrupts Pi homeostasis, leading to increased plant susceptibility to Magnaporthe oryzae infection. Conversely, CRISPR/Cas9 knockout of MIR827 results in plant resistance to M. oryzae, highlighting the negative regulatory role of miR827 in biotic stress responses in rice (Bundó et al., 2024). In Arabidopsis thaliana, nematode-induced activation of the miR827-nitrogen limitation adaptation (NLA) module within the syncytium suppresses plant immune responses, enabling nematode infection and disease establishment. This suggests that miR827 negatively regulates biotic stress by facilitating pathogen colonization (Hewezi et al., 2016). In grapevine (Vitis quinquangularis), miR827a negatively regulates VqMYB14, a key transcription factor gene involved in stilbene synthesis, which is crucial for defence metabolite production. By reducing stilbene levels, miR827a weakens the plant basal immunity, potentially increasing vulnerability to pathogens (Luo et al., 2024).

miR827 may also play a positive role in pathogen defences. In tobacco (Nicotiana tabacum), miR827 is up-regulated in Chilli veinal mottle virus (ChiVMV)-infected recovery tissue. Overexpression of miR827 improves plant resistance to ChiVMV infection in Nicotiana benthamiana, while interference with miR827 increases susceptibility. FBPase was identified as a target of miR827 in N. benthamiana, and transient overexpression of FBPase increases susceptibility to ChiVMV infection. These findings indicate that miR827 positively regulates plant resistance to ChiVMV by suppressing FBPase expression (Tang et al., 2024).

miR1432

miR1432 has multifaceted role in pathogen defence, where its function varies depending on the host and invading pathogen species. In rice (Oryza sativa), overexpression of miR1432 compromises plant resistance to blast disease caused by Magnaporthe oryzae. miR1432 targets and suppresses LOC_Os03g59790, which encodes OsEFH1, an EF-hand family protein involved in defence. Overexpression of OsEFH1 enhances blast disease resistance but reduces yield, suggesting that miR1432 fine-tunes OsEFH1 expression to balance blast disease resistance with plant growth (Li et al., 2021c). miR1432 can have positive role in pathogen defence in rice, overexpression of osa-miR1432 enhances rice resistance to Xanthomonas oryzae pv. oryzae (Xoo), and as expected, overexpression of OsCaML2, a target of osa-miR1432, compromises resistance to Xoo, solidifying the positive role of miR1432 in Xoo defence. (Jia et al., 2021). In wheat (Triticum aestivum), tae-miR1432 is highly expressed during infection with Puccinia striiformis f. sp. tritici (Pst), the causal agent of stripe rust, suggesting a potential positive role for tae-miR1432 in regulating plant pathogen defence (Feng et al., 2016).

lncRNAs in plant stress responses

Long non-coding RNAs (lncRNAs) are emerging as versatile regulators that play crucial roles in how plants adapt to a wide range of stress conditions. Across different species, lncRNAs have been found to modulate gene expression through diverse mechanisms such as co-expression with stress-responsive mRNAs or acting as molecular sponges for miRNAs. Recent advances in high-throughput sequencing have led to an overwhelming deposition of lncRNA data that underscores the dynamic responsiveness of lncRNAs to a wide array of stress conditions (Patra et al., 2023). In this section, we summarize some of the highlighted lncRNAs (Table 6.) from studies that have been characterized by their unique roles in response to stress conditions.

Table 6 Summary of the highlighted lncRNAs involved in plant stress responses, detailing their regulatory mechanisms and species of origin

Stress	lncRNA	Mechanism	Species	Reference
Drought	XLOC_063105	Co-express with ethylene signalling pathway genes	Cotton (Gossypium hirsutum)	Lu et al. (2016)
XLOC_115463
lncRNA_tomato_467	Co-expressed with a K⁺ channel gene	Tomato (Solanum lycopersicum)	Eom et al. (2019)
Salt	lncRNA973	Promote Na⁺/K⁺ homeostasis and antioxidant acitivty	Cotton (Gossypium hirsutum)	Zhang et al. (2019)
npc48	Target mimic of miR164	Arabidopsis (Arabidopsis thaliana)	Ben Amor et al. (2009)
MtCIR2	Repress ABA catabolic gene CYP707A2	Medicago truncatula	Sun et al. (2025)
lncRNA13472	Target mimic of miR169	Sweet sorghum (Sorghum bicolor)	Sun et al. (2020b)
Cold	lincRNA340	Target mimic of miR169	Cassava (Manihot esculenta)	Li et al. (2017b)
lncNAT159	Target mimic of miR164
MtCBF	Co-express with CBF gene	Medicago truncatula	Zhao et al. (2020)
Heat	TCONS_00031790	Target mimic of miR9748	Cucumber (Cucumis sativus)	He et al. (2020)
TCONS_00014332
TCONS_00014717
TCONS_00005674
MSTRG.32907	Stress-related TF regulation	Maize (Zea mays)	Lv et al. (2019)
MSTRG.35709
MSTRG.44074
MSTRG.37268
Biotic	lncRNA48734	Target mimic of miR156	Tomato (Solanum lycopersicum)	Yang et al. (2020)
lncRNA44664	Target mimic of miR396
slylnc1077	Target mimic of miR399	Tomato (Solanum lycopersicum)	Wang et al. (2015)
slylnc0195	Target mimic of miR166
MSTRG18363	Target mimic of miR1918	Tomato (Solanum lycopersicum)	Zhou et al. (2021)
ELENA1	Mediate binding of MED19a subunit	Arabidopsis thaliana	Panstruga (2024)
TCONS_00021785	Target mimic of miR319	Paulownia tomentosa	Fan et al. (2018)
ALEX1	Promotes ARF3 homodimerization	Rice (Oryza sativa)	Lei et al. (2025)
TalnRNA5	Precursor for miR2004	Wheat (Triticum aestivum)	Xin et al. (2011)
TapmlnRNA19	Precursor for miR2004
TahlnRNA27	Precursor for miR2010
GhlncLOX3	Co-express with lipoxygenases promote JA biosythesis	Cotton (Gossypium hirsutum)	Wang et al. (2021a)
lncRNA809	Promote MmNAC17 expression	Malus micromalus	Du et al. (2025)

lncRNAs in drought stress

In cotton, the expression pattern of 10 820 high-confidence lncRNAs were changed significantly under drought stress and re-watering conditions. Among those, many intronic lncRNAs tend to mirror the expression of nearby protein-coding genes, suggesting they might regulate these adjacent genes, and lncRNAs XLOC_063105 and XLOC_115463 were predicted to be positively involved in regulating genes related to the ethylene signalling pathway that is crucial for drought stress response (Lu et al., 2016). In Brassica juncea, a significant number of lncRNAs were found to co-express with mRNAs that are linked to antioxidant defence (superoxide dismutase, peroxidase and glutathione S-transferase) and transcriptional factors (MIKC-MADS, NAC and MYB) under drought stress. Interestingly, they were also predicted as endogenous target mimics (eTMs) or as direct targets of miRNAs (miR156, miR159, miR172, miR319 and miR399) that were involved in stress regulations (Bhatia et al., 2020). In tomato, 244 of the identified lncRNAs were predicted to be eTMs of 92 tomato miRNAs under drought stress. In addition, lncRNA_tomato_467 was co-expressed with a K⁺ channel genes, potentially affecting stomatal regulation to prevent water loss (Eom et al., 2019).

lncRNAs in salt stress

In cotton, lncRNA973 is expressed at low levels under normal conditions, but its expression is significantly up-regulated upon salt treatment. Functional analyses using overexpression in Arabidopsis and gene silencing (VIGS) in cotton revealed that higher levels of lncRNA973 enhance salt tolerance. Overexpression lines showed salt stress response, while knockdown plants exhibited wilting, increased oxidative damage, and disrupted Na⁺/K⁺ homeostasis. Moreover, lncRNA973 was demonstrated to modulate the expression of several salt stress-responsive genes, including those involved in ROS detoxification (SOD, CAT, POD), ion transport (e.g. NHX7), osmolyte biosynthesis (P5CS) and key transcription factors (MYB5, WRKY46, NAC29, ERF62). It may also interact with the miR399-PHO2 module in cotton, further influencing stress responses (Zhang et al., 2019). In Arabidopsis, overexpression of npc48 led to altered plant morphology and is linked to a dramatic reduction in miR164 level (Ben Amor et al., 2009). Since miR164 targets the NAC gene that positively regulates salt stress (Shan et al., 2020), it is possible that npc48 is a positive salt stress regulator. In salt-tolerant sweet sorghum (M-81E line), 5 differentially expressed lncRNAs were detected that were possibly related to salt stress. Most interestingly, one of the competitive endogenous RNA, lncRNA13472, may compete with a gene encoding a proton pump subunit for binding to sbi-MIR169b, thereby modulating the stability and expression of its mRNAs to enhance salt tolerance (Sun et al., 2020b). In Medicago truncatula, MtCIR2 is up-regulated and functions as a negative regulator of seed germination during salt stress. MtCIR2 suppresses the expression of the ABA catabolic gene CYP707A2, leading to increased endogenous ABA levels, while simultaneously inhibiting GA biosynthetic genes (GA20ox1, GA20ox2 and GA20ox5) to lower GA concentrations. This shift creates a higher ABA/GA ratio that disrupts both ABA and GA signalling pathways ultimately resulting in enhanced sensitivity of seed germination to salt stress (Sun et al., 2025).

lncRNAs in cold stress

In cassava, 318 lncRNAs showed significant changes under cold stress. Intergenic lncRNAs, including lincRNA419, lincRNA207 and lincRNA234, are up-regulated under cold stress, highlighting their potential role in the stress response. Additionally, some of the differentially expressed lncRNAs act as precursors for miRNAs, such as miR156g, miR160d, miR166h, miR167g and miR169d, which are known to influence cold stress responses. Moreover, other lncRNAs were predicted to function as eTMs, with lncNAT159 predicted to sequester miR164 and lincRNA340 proposed to sequester miR169 (Li et al., 2017b). In Medicago truncatula, 983 cold-responsive lncRNAs in leaves and 1288 in roots were identified. One of the intergenic lncRNA, MtCIR1, which originated from a cluster of CBF/DREB1 genes on chromosome 6, was found to be rapidly up-regulated upon exposure to cold within 2 h. The rapid expression of MtCIR1 precedes the subsequent induction of the neighbouring MtCBF genes, indicating it co-expresses with the cold tolerance CBF gene to boost cold stress defence (Zhao et al., 2020).

lncRNAs in heat stress

In cucumber (Cucumis sativus L.), 108 lncRNAs showed differential expression patterns under high-temperature stress. Many of these lncRNAs are implicated in the stress response through two main mechanisms, either by co-expression with neighbouring mRNAs that are enriched in stress-related functions such as defence response and signal transduction or acting as eTMs. four lncRNAs (TCONS_00031790, TCONS_00014332, TCONS_00014717 and TCONS_00005674) were predicted to bind miR9748. This interaction likely modulates the expression of key mRNAs for proteins involved in plant hormone signal transduction (e.g. auxin-responsive protein IAA16, protein TIFY 9-like and ethylene response sensor 1) (He et al., 2020). In maize, reconstructing co-expression networks of lncRNA and transposable elements under heat stress revealed that lncRNA MSTRG.32907, MSTRG.35709, MSTRG.44074 and MSTRG.37268 are highly interconnected with key transcription factors such as TCP and NAC, which are known to mediate stress response (Lv et al., 2019).

lncRNAs in biotic stress

In tomato, differentially expressed lncRNAs under root-knot nematode (Sneb821) infection were analysed and two lncRNAs were functionally validated for their roles in stress response. lncRNA44664 was found to interact with the miR396a/GRF module by sponging miR396 to increase the expression of GRFs to enhance root-knot nematode resistance. In addition, lncRNA48734 regulates the miR156d/SPL pathway by sponging miR156 to increase SPL expression, leading to lowered H₂O₂ accumulation to fine tune ROS mediated pathogen defence response (Yang et al., 2020). A genome-wide analysis of tomato lncRNAs in response to TYLCV infection found that 529 lncRNAs were differentially expressed. Notably, lylnc0049 and slylnc0761 are significantly up-regulated in infected plants, and functional tests (VIGS) indicated that altering their levels affects virus accumulation, implicating them in the defence response. Additionally, several lncRNAs act as eTMs, where slylnc0195 functions as a decoy for miR166, which normally targets class III HD-Zip transcription factors known to play roles in plant development and stress responses. Similarly, slylnc1077 appears to act as an eTM for miR399. These interactions suggest that tomato lncRNAs contribute to TYLCV resistance by fine-tuning miRNA-mediated regulatory networks that control stress and developmental pathways (Wang et al., 2015). Six lncRNAs were commonly up-regulated when infected with Botrytis cinerea. Among these, MSTRG18363 was highlighted due to its increased expression and its critical role in mediating stress responses. MSTRG18363 acts as eTMs to sequester miR1918, which normally represses the expression of the defence-related gene SlATL20 (a RING-H2 finger protein). By binding miR1918, MSTRG18363 prevents it from down-regulating SlATL20, thereby enhancing the plant induced systemic resistance against the pathogen (Zhou et al., 2021). In Arabidopsis, lncRNA ELENA1 was significantly induced by the bacterial pathogen Pseudomonas syringae pv. tomato DC3000. Overexpression of ELENA1 enhances the expression of key defence genes such as PR1/2, leading to superior pathogen resistance. ELENA1 works by binding to the MED19a subunit as a mediator complex, which facilitates the enrichment of MED19a on the PR1 promoter, resulting in boosted PR1 transcription during the immune response. In response to Fusarium oxysporum infection, lncNAT at the At1g13609 locus was significantly more induced than its corresponding sense transcript, suggesting that these antisense RNAs might be induced independently rather than simply reflecting co-regulated transcription. In addition, 20 novel lincRNAs were identified, and knocking them down led to increased disease susceptibility, indicating that these lincRNAs likely contribute positively to antifungal defence (Zhu et al., 2014). In Paulownia tomentosa, 112 lncRNAs were differentially expressed when infected with phytoplasma (witches' broom disease), some of these lncRNAs appear to act as miRNA (miR156, miR160, and miR171) precursors while others function as targets or target mimics. One of the lncRNA, TCONS_00021785, was predicted to be eTMs for the ptmiR319 family, which in turn up-regulates the expression of TCP transcription factors to boost defence response (Fan et al., 2018). In rice, a key lncRNA (ALEX1) is induced upon bacterial infection (Xoo). ALEX1 localizes mainly to the nucleus and directly interacts with ARF3 by binding to its intrinsically disordered middle region, leading to the inhibition of solid-like ARF3 condensates and promotes ARF3 homodimerization. This functional phase change of ARF3 enables it to more effectively repress the transcription of the target genes like JAZ13, which in turn modulates the jasmonic acid signalling pathway and enhances rice resistance to bacterial pathogens (Lei et al., 2025). In wheat, 125 lncRNAs were responsive for the infection of powdery mildew. The lncRNA transcript TalnRNA5 and TapmlnRNA19 were predicted to be the precursor for miR2004 and TahlnRNA27 for Ta-miR2010, suggesting that lncRNA regulates stress responses via miRNA pathways (Xin et al., 2011). In cotton, two NAT lncRNAs (GhANX2 and GhRLP7) are identified to play key roles in defence against Verticillium dahlia. Repressing GhlncNAT-ANX2 and GhlncNAT-RLP7 leads to increased levels of lipoxygenases (LOX1 and LOX2) that are involved in jasmonic acid signalling, resulting in enhanced resistance to Verticillium dahlia infection (Zhang et al., 2018). In addition, 4277 lncRNAs were differentially expressed in the cotton root during Verticillium dahlia infection, with over 95% of the lncRNAs functioning as mRNA co-expression pairs. Notably, a subset of these lncRNAs appears to be closely linked to jasmonic acid biosynthesis. The GhlncLOX3 is significantly up-regulated following infection and is predicted to regulate GhLOX3, a lipoxygenase gene involved in jasmonic acid synthesis. Functional assays using virus-induced gene silencing (VIGS) showed that silencing GhlncLOX3 led to decreased expression of GhLOX3 associated with lower jasmonic acid level and increased disease susceptibility (Wang et al., 2021a). In Malus micromalus, sorbitol acts as an upstream signal that increases the expression of a key long non-coding RNA, lncRNA809, under fungal pathogen Alternaria alternata infection. lncRNA809 positively regulates the transcription factor MmNAC17 which binds directly to the promoters of critical flavonoid biosynthesis genes (MmF3H and MmLAR), resulting in the accumulation of catechin, boosting pathogen defence (Du et al., 2025).

circRNAs in plant stress responses

Recent studies have highlighted the pivotal roles of circular RNAs (circRNAs) in mediating plant responses to a variety of biotic and abiotic stresses across multiple species.

In Arabidopsis, it was reported circR194 and circR4022 are involved in the response to Pseudomonas syringae infection, while circR11208 is associated with the response to Botrytis cinerea. Moreover, both circR4022 and circR11208 are crucial to salt stress tolerance (Wang et al., 2022). Bioinformatic analyses have revealed that circRNAs are differentially expressed under pathogen challenges in other crops as well. In cotton, infection with the fungus causing Verticillium wilt leads to distinct circRNA expression profiles (Xiang et al., 2018), and in maize, infection by Maize Iranian mosaic virus (MIMV) triggers differential circRNA expression (Xiang et al., 2018). In grapevines, circRNAs also mediate responses to abiotic stress. It was identified that a circRNA derived from the ATP sulfurylase 1 (Vv-ATS1) gene, Vv-circATS1, is up-regulated under cold stress. Functional analyses demonstrated that overexpression of Vv-circATS1 in Arabidopsis enhances cold tolerance, potentially by acting as a miRNA sponge for a wide range of miRNAs (Gao et al., 2019). In contrast, another grapevine circRNA, Vv-circPTCD1, derived from the second exon of the PTCD1 gene, is induced by salt and drought stress. Overexpressing Vv-circPTCD1 in Arabidopsis significantly increased sensitivity to heat, salt and drought, suggesting that the functional outcomes of circRNAs may be species-dependent and require validation of potential outcomes (Ren et al., 2023). In tomato, circRNAs have been shown to play critical roles during both abiotic and biotic stress responses. Several circRNAs were found to act as sponges for 24 miRNAs during cold stress. These circRNAs are involved in antioxidant pathways, cell wall degradation, membrane lipid peroxidation, energy metabolism and stress-responsive transcription factors such as CBF and WRKY (Zuo et al., 2016). Additionally, circRNA45 and circRNA47 were shown to be induced and sequester miR477-3p upon infection with Phytophthora infestans, leading to an increased expression of receptor-like kinase 2 (RLK2) to triger elevated activation of plant defence mechanisms (Hong et al., 2020). In cucumbers, circRNAs were reported to mediate signal transduction and ion homeostasis to facilitate adaptation under salt stress (Zhu et al., 2019b). Similarly, in soybean, circRNAs are differentially expressed under Pi starvation, where they are implicated in modulating redox activity and signal transduction processes (Lv et al., 2020). In moso bamboo, a novel circRNA (PeSca_6:12316320|12 372 905) was identified to sponge miR156, which in turn regulates a serine carboxypeptidase gene important for nitrogen metabolism (Zhu et al., 2023).

The circRNAs that have been reported in plant so far primarily function as miRNA sponges, and their roles appear to be species dependent. Although significant advances have been made in identifying plant circRNAs, much remains unknown about their other functions, including their potential roles in protein scaffolding and IRES/m^6A-driven translation, which is well-studied in animals (Kristensen et al., 2022). In-depth functional analyses are also required to elucidate the complex regulatory networks of circRNAs and their interactions with downstream pathways and other non-coding RNAs. A better understanding of these mechanisms will be crucial for applying circRNAs in plant trait modification.

tRFs in plant stress responses

tRFs are responsive in various stress conditions. In rice, the 5′ tRF Arg^CCT was induced by cold but suppressed by salt treatment. In Arabidopsis, the 5′ tRF Arg^CCT and 5′ tRF Arg^TCG were induced by drought (Zhu et al., 2018) and the 5′ tRF Asp^GTC and 5′ tRF Gly^TCC were induced by Pi Starvation in root (Hsieh et al., 2009). Upon UV-C irradiation in Arabidopsis, specific groups of 5′ tRF fragments were significantly up-regulated, including 5′ tRF Gly^GCC, 5′ tRF Gly^TCC, 5′ tRF Pro^TGG and 5′ tRF Val^AAC, indicating their potential positive roles in UV stress regulation. Similarly, the 5′ tRF fragment derived from tRNA Gly^GCC was notably increased under drought, cold or salt stresses, while there was a general decrease in both nuclear and plastid 3′ tRF levels across various tRNAs (Cognat et al., 2017). In Chinese cabbage (Brassica rapa), a unique subset of 5′ tRFs was identified from the chloroplast genome and found to be significantly down-regulated during heat stress, indicating their potential role in heat stress (Wang et al., 2011a).

While studies have highlighted the stress-responsive nature of tRFs (Table 7), their precise downstream functions and underlying mechanisms remain largely enigmatic. Further research is needed to elucidate their target interactions, signalling pathways and the broader implications of their dynamic regulation to offer innovative strategies for improving plant resilience.

Table 7 Overview of tRNA-derived fragments (tRFs) involved in plant stress responses

Type	tRNA	Stress	Regulation	Species	Reference
Arg^CCT	5′ tRF	Cold	UP	Rice	Alves et al. (2017)
Arg^CCT	5′ tRF	Salt	DOWN
Arg^CCT	5′ tRF	Drought	UP	Arabidopsis
Arg^TCG
Gly^TCC	5′ tRF	Pi starvation	UP	Arabidopsis	Hsieh et al. (2009)
Asp^GTC
Gly^TCC	5′ tRF	UV-C	UP	Arabidopsis	Cognat et al. (2017)
Gly^GCC
Pro^TGG
Val^AAC
Chloroplast tRFs	5′ tRF	Heat	DOWN	Chinese cabbage	Wang et al. (2011a)
Gly^GCC	5′ tRF	Drought, cold, salt	UP	Arabidopsis	Alves et al. (2017)
Nuclear and plastid tRFs	3′ tRF	DOWN

siRNAs in plant stress responses

Small interfering RNAs (siRNAs) are pivotal regulators of plant stress responses, governing both abiotic and biotic stress adaptations. By mediating post-transcriptional gene silencing and RNA-directed DNA methylation, siRNAs modulate the expression of key stress-related genes, including transcription factors and hormone signalling components. Under abiotic stress challenges, siRNAs fine-tune stress-inducible pathways, optimizing plant growth and survival in adverse environments. During biotic stress, they actively silence genes linked to susceptibility, bolstering plant defences against pathogens and pests. Moreover, siRNAs contribute to stress ‘memory’, priming plants for faster, more robust reactions upon repeated exposures. Understanding these multifaceted siRNA networks holds significant promise for developing crops with enhanced resilience to diverse stresses.

siRNAs in drought stress

siRNAs have emerged as key regulators of drought stress responses across diverse plant species. In Hordeum vulgare, siRNAs targeting HvCKX2.1 (cytokinin oxidase 2.1) modulate cytokinin degradation, ultimately influencing germination and shoot emergence via cytokinin riboside accumulation (Surdonja et al., 2017). During drought at the immature grain stage, H. vulgare produces more 24 nt siRNAs and shows elevated DNA methylation in the HvCKX2.1 promoter region, underscoring a potential epigenetic mechanism for drought adaptation (Surdonja et al., 2017). Similarly, in H. vulgare and Triticum aestivum, 24 nt phasiRNAs accumulate prior to meiosis, likely interacting with AGO6 to preserve male fertility under water-limited conditions (Bélanger et al., 2020). Bruguiera gymnorrhiza further illustrates siRNA-mediated drought resilience through TAS3-derived ta-siRNAs (Bélanger et al., 2020). Moreover, in Craterostigma plantagineum, a drought-induced siRNA appears to enhance desiccation tolerance by triggering ABA induction (Hilbricht et al., 2008). Collectively, these findings highlight the critical role of siRNAs in orchestrating plant responses to water scarcity.

siRNAs in salt stress

siRNAs also play a pivotal role in plant adaptation to high-salinity environments. In Arabidopsis thaliana, a natural antisense siRNA (nat-siRNA) arises from overlapping SRO5 and P5CDH transcripts, mediating osmoprotection under salt stress. Specifically, a 24 nt siRNA corresponding to SRO5 targets P5CDH for degradation, increasing proline levels and bolstering salt tolerance (Borsani et al., 2005). Although reduced P5CDH activity can elevate toxic P5C, the mitochondrial SRO5 protein helps mitigate this toxicity. Together, the SRO5–P5CDH nat-siRNA system forms a regulatory loop that modulates ROS production and governs the broader salt stress responses in plants (Borsani et al., 2005).

siRNAs in heat stress

In Triticum aestivum (wheat), siRNA expression patterns shift dynamically in response to extreme temperature fluctuations. Four specific siRNAs demonstrate varied expression profiles under cold and heat stress. For instance, siRNA005047_0654_1904 is induced by cold but suppressed under heat, salinity and drought. Similarly, siRNA080621_1340_0098 is up-regulated during cold stress yet down-regulated under high temperatures. By contrast, siRNA002061_0636_3054 and siRNA007927_0100_2975.1 both show reduced expression under heat, salinity, and drought (Yao et al., 2010). These findings highlight how siRNAs orchestrate complex regulatory networks, enabling wheat to adapt at the molecular level to temperature extremes.

siRNAs in biotic stress

siRNAs play a pivotal role in protecting plants from a variety of biotic stressors. In Arabidopsis thaliana, infection by the nematode Heterodera schachtii triggers a marked increase in several siRNAs (siRNA9, siRNA41 and siRNA46). Additionally, the natural antisense siRNA nat-siRNAATGB2 has been linked to effector-triggered immunity (ETI) by silencing PPRL family genes, which act as negative regulators of ETI (Katiyar-Agarwal et al., 2006). By down-regulating these suppressors, siRNAs enhance plant immune response, reinforcing resistance to pathogen invasion.

The earliest endogenous siRNA associated with biotic stress was nat-siRNA/ATGB2, which fine-tunes effector-triggered immunity (ETI)—a pivotal layer of plant defence (Khraiwesh et al., 2012). Besides degrading pathogen-derived genetic material, nat-siRNA/ATGB2 influences the expression of resistance (R) genes, thereby broadening plant protection against bacteria, viruses and fungi (Ding et al., 2024; Khraiwesh et al., 2012). This targeted regulation helps avoid immune hyperactivation in the absence of pathogens, conserving energy and preventing deleterious autoimmunity. Upon pathogen detection, however, nat-siRNA/ATGB2 rapidly shifts plant responses to a heightened defence state, reinforcing R-gene activity and enhancing overall immune robustness (Ding et al., 2024). Through this dual role—maintaining immune homeostasis and amplifying defence—siRNA-mediated pathways serve as key molecular switches in plant immunity.

The miRNA–phasiRNA pathway is pivotal for regulating plant disease resistance, particularly by modulating nucleotide-binding site leucine-rich repeat (NBS-LRR) proteins (Jyothsna and Alagu, 2022). In parasitic interactions, Cuscuta spp. accumulate 22-nt miRNAs that target host transcripts, influencing secondary phasiRNA production and thereby adapting plant defences (Shahid et al., 2018). Key components of this pathway include AGO7, which is essential for generating TAS3-derived ta-siRNAs linked to symbiosis with rhizobia in Lotus japonicus; importantly, ago7 mutants exhibit heightened susceptibility to fungal infections (Ellendorff et al., 2009). Pathogen invasion often reprograms miRNAs and phasiRNAs to regulate NLR genes critical for immune responses, with AGO1—typically associated with 21- and 22-nt miRNAs—being instrumental in pathogen-triggered immunity (PTI); indeed, ago1 mutants display compromised resistance to bacterial pathogens (Li et al., 2010). Moreover, RNA-dependent RNA polymerase RDR6 supports secondary siRNA generation, as OsRDR6 mutants in rice show increased necrosis upon infection by Xanthomonas oryzae pv. oryzae, underscoring its vital role in bacterial defence.

RNA interference (RNAi) offers a precise, sustainable tool for crop protection against viral pathogens and other pests (Septiani et al., 2025). In squash and melon, for instance, lipid-encapsulated synthetic siRNAs confer antifungal resistance against Botrytis cinerea (Bakhat et al., 2025). However, much of the antiviral response in plants derives from virus-derived siRNAs (vsiRNAs), which originate from double-stranded RNA intermediates in RNA viruses or from bidirectional transcription of circular DNA viruses (Guo et al., 2019). Dicer-like (DCL) proteins process these dsRNAs into 21–24 nt primary siRNAs, and RNA-dependent RNA polymerases (RDRs) can amplify them into secondary siRNAs (Brodersen and Voinnet, 2006). The 21 nt siRNAs generated by DCL4 are particularly important for post-transcriptional gene silencing (PTGS), guiding Argonaute (AGO) complexes to target and degrade viral RNAs (Garcia-Ruiz et al., 2010). Beyond directly cleaving viral genomes, vsiRNAs can reprogram host gene expression to bolster immune responses; for example, Tomato yellow leaf curl virus (TYLCV) vsiRNAs silence SlLNR1—a key antiviral defence gene—while Wheat yellow mosaic virus (WYMV)–derived vsiRNAs enhance broad-spectrum resistance in wheat by repressing TaAAED1, thereby promoting reactive oxygen species (ROS) accumulation (Liu et al., 2021). Another subset, virus-activated siRNAs (vasiRNAs), which emerge from host exons in a DCL4- and RDR1-dependent manner, further underscores the intricate interplay between viral infection and the host RNA silencing machinery (Cao et al., 2014). Notably, plant small RNAs, including vsiRNAs, can migrate through plasmodesmata and phloem, and in some cases even cross species boundaries, amplifying their protective scope (Wang and Dean, 2020). In tobacco, for instance, nat-miR6019 specifically cleaves the N gene that confers resistance against Tobacco mosaic virus (TMV), demonstrating the adaptability of RNAi in pathogen defence (Li et al., 2012). Moreover, under pathogen-free conditions, certain NLR and PRR genes remain under the surveillance of 22 nt miRNAs and secondary phasiRNAs, preventing autoimmunity and conserving resources. Collectively, these insights highlight the multifaceted and essential role of siRNA pathways in safeguarding plants against viral threats—and by extension, a wide array of biotic stresses.

siRNAs in other stresses

Hypoxia stress

In Arabidopsis thaliana, TAS1-, TAS2- and TAS3-derived ta-siRNAs show increased accumulation under low-oxygen conditions. This up-regulation is tightly linked to miR-173 and miR-390, which target members of the pentatricopeptide repeat (PPR) protein family (Moldovan et al., 2010). PPR proteins, integral to RNA processing, can suppress mitochondrial cytochromes and respiratory pathways, thereby bolstering plant tolerance to hypoxic environments (Moldovan et al., 2010). These findings underscore the complex interplay of ta-siRNAs, miRNAs and PPR proteins in managing hypoxia stress.

Wounding and oxidative stress

In Ipomoea batatas, wounding triggers the accumulation of miR828 in leaves, leading to the production of phasiRNAs from its targets IbMYB and IbTLD. These phasiRNAs act in cis, reinforcing the silencing of their own source transcripts and driving lignin and hydrogen peroxide (H₂O₂) accumulation (Liu et al., 2020b). Elevated lignin and H₂O₂ enhance structural integrity and oxidative defences, respectively, thereby increasing resilience to mechanical damage and environmental stresses.

Cross talks between ncRNAs under stress conditions

ncRNAs have revealed themselves as master regulators in plant stress responses. Their ability to communicate across various layers of gene regulation establishes a finely tuned and dynamic adaptation to environmental challenges (Figure 2). By compiling a vast array of studies, we can highlight not only the individual roles of these ncRNAs but also their synergistic interactions with one another. For example, lncRNAs and circRNAs can operate as miRNA sponges, which sequester miRNAs that negatively regulate stress resistance trait to ensure the expression of key stress-responsive genes. In tomato, lncRNAs have been shown to bind and inhibit stress-associated miRNAs (e.g. miR396, miR156) which regulate transcription factors implicated in pathogen and drought resistance (Yang et al., 2020). Likewise, circRNAs in grapevine under salinity or cold conditions can sequester miRNAs that would otherwise suppress ion-transport or antioxidant genes (Gao et al., 2019). Such sponging events are part of the fine-tuning mechanism for optimizing the expression of stress resistance genes, providing a multi-layered control over stress adaptations.

[IMAGE OMITTED. SEE PDF]

Additionally, miRNA synergizes with siRNA for target suppression, such is seen in Ipomoea batatas, where degradation of IbMYB and IbTLD leads to the formation of their respective phasiRNAs, and the reinforcement of the silencing effect promotes lignin and H₂O₂ accumulation in response to wounding (Liu et al., 2020). lncRNA can intercept this process through functioning as eTMs, as is seen in tomato, ncRNA44664 sponges miR396, preventing GRF cleavage into phasiRNAs, thereby altering the final phasiRNA pool that influences root-knot nematode defence (Yang et al., 2020).

Moreover, these ncRNAs often converge on shared RNAi components (e.g. DCL, RDR, AGO), effectively creating competition or synergy for the same molecular machinery. A strong wave of miRNA expression triggered by drought can increase the pool of AGO1-bound complexes, thereby shifting how other siRNAs or circRNA-bound miRNAs access to AGO proteins. Such molecular bottlenecks can alter the ultimate balance of gene silencing events under combined or sequential stresses, which is a hallmark of the intricate, dynamic crosstalk shaping plant stress resistance trait.

The unified view emerging from these findings is that ncRNAs do far more than just the regulation of the isolated targets. They function in layered networks, with each class (miRNAs, siRNAs, lncRNAs, circRNAs and tRFs) feeding into or counteracting the others to create flexible, context-dependent regulatory modules. By integrating diverse research findings, we can better understand how these molecular regulators work in concert to modulate plant growth, development, and stress resilience, paving the way for innovative strategies in sustainable crop improvement.

Trade-off effects of ncRNA on plant traits

While ncRNAs are master regulators in fine-tuning plants for environmental adaptation, some of them often improve plant tolerance to one stress at the cost of compromising different aspects of plant development or plant performance under other stressful conditions. For example, constitutive overexpression of miR156 in alfalfa enhances drought resilience by boosting anthocyanin biosynthesis and antioxidant capacity, yet these transgenic lines exhibit delayed flowering and reduced shoot biomass (Feyissa et al., 2019). Likewise, creeping bentgrass plants engineered to express high levels of miR169 show reduced stomatal density and stronger ROS scavenging under drought, but display stunted leaf expansion and lower photosynthetic rates under normal conditions (Chen et al., 2024b). A similar trade-off has been observed with miR827 in barley. Elevated Hv-miR827 improves plant water-use efficiency and salt tolerance under severe drought, yet simultaneously suppresses both root and shoot development, indicating that investment in stress adaptation diverts energy from biomass accumulation (Ferdous et al., 2017b). These cases demonstrate that manipulating a single ncRNA can shift resource allocation towards stress defence while compromising growth or the other way around. Such antagonistic effects underscore the need for precise, context-dependent control of ncRNA expression to balance plant growth and resilience. Thus, we will review the current development of biotechnology approaches and propose several solutions to mitigate the trade-off effect in the following section.

Non-coding RNA-based biotechnological approaches for crop improvement

Biotic and abiotic stresses such as drought, salinity, extreme temperatures, and heavy metal toxicity are increasingly challenging due to their rising frequency and detrimental effects on plant growth, yield and produce quality (Zhang et al., 2022a). Plants have evolved intricate mechanisms to perceive and respond to these environmental changes, with ncRNAs playing pivotal early regulatory roles in mitigating stress impacts (Yadav et al., 2024). This review has comprehensively summarized the functions of non-coding RNAs, highlighting their complex involvement in multiple stress responses through both positive and negative regulatory mechanisms. To tailor crops with desired traits for specific environmental conditions, a multifaceted biotechnological approach is required to develop optimal transgenic varieties. Here, we outline several promising application strategies that have demonstrated utility in achieving these goals.

Constitutive up- or down-regulation of ncRNA gene expression

Non-coding RNAs play diverse regulatory roles in various aspects of environmental adaptation. Numerous studies summarized in this review have demonstrated that overexpression of ncRNAs using constitutive promoters, such as the Cauliflower Mosaic Virus 35S (CaMV35S) (Odell et al., 1985) and ubiquitin (Ubi) (Christensen and Quail, 1996) promoters, effectively enhances their regulatory functions. This approach is particularly valuable when an ncRNA exhibits multiple positive regulatory roles beneficial for agricultural applications.

However, for ncRNAs that primarily function as negative regulators of stress resistance (e.g. miR398, miR530, miR1432), down-regulation strategies are required. CRISPR-based knockout techniques have been successfully employed to knock ncRNA genes that negatively influence target traits (Bundó et al., 2024; Lyu et al., 2023), thereby mitigating their adverse effects on plant stress responses. Additionally, the application of stem-loop target mimicry (STTM) provides a robust method for sequestering and down-regulating miRNAs at the cellular level, enabling fine-tuned regulation of gene expression networks (Tang et al., 2012a).

Inducible or synthetic promoter for controlled ncRNA gene expression

Although overexpression and knockout strategies are effective methods for manipulating ncRNA expression levels to achieve desired traits, most ncRNAs summarized in this review exhibit diverse regulatory roles across different environmental adaptations. A single ncRNA may positively enhance a specific stress response while simultaneously negatively impacting another, rendering simple overexpression or knockout approaches unsuitable for comprehensive trait improvement. In efforts to harness ncRNA for enhanced crop performance, strategies that fine-tune the expression ncRNAs are essential.

A complementary strategy utilizing inducible promoter can be combined into an integrated platform to balance ncRNA overexpression and knockdown construct (Figure 3a). For example, miR169 was shown to positively regulate stress resistance while negatively impacting growth in creeping bentgrass (Chen et al., 2024b), in order to improve stress tolerance while promoting plant growth, a stress-inducible promoter such as the SaAsr1 gene promoter from the halophyte Spartina alterniflora (Sengupta et al., 2022) can be used to drive the expression of miR169. This approach boosts miR169 levels under stressful conditions, while maintaining a basal expression level under normal conditions to avoid adverse effects on growth. In the meantime, a stress-inhibiting promoter, such as the ZmPP2C26 gene promoter from maize (Lu et al., 2020a), can be employed to direct the expression of a miR169 target mimic, thereby under normal conditions, elevated levels of the mimic can enhance growth by inhibiting miR169 activity. Under stress conditions, the mimic construct would be suppressed due to the inactivation of the stress-inhibited promoter, ensuring that innate miR169 and its overexpression cassette function effectively to mediate stress responses. This strategy is not only applicable to manipulating individual ncRNA, but also feasible to create artificial module to fine-tune regulatory dynamics within multiple ncRNAs to achieve ideal environment adaptation traits.

[IMAGE OMITTED. SEE PDF]

Furthermore, advances in synthetic biology may facilitate the design of synthetic promoters that incorporate core promoter elements with specific synthetic motifs, allowing for precise control of promoter strength and environmental responsiveness (Cai et al., 2020; Liu and Stewart, 2016). However, the successful implementation of these strategies will require careful calibration of promoter strength to achieve optimal levels of the specific ncRNA being utilized.

Artificial ncRNA for fine-tuned target gene expression

Modulating the expression of endogenous ncRNAs has been shown to effectively influence plant environmental adaptations. However, due to the complexity of regulatory networks, the alteration of endogenous ncRNA may lead to pleiotropic effects, potentially disrupting multiple critical pathways (Chorostecki et al., 2023). In addition, the redundancy among ncRNAs target genes can mask the effects of any single-ncRNA manipulation (Gao et al., 2020). Thus, the recent advance in the synthetic approach to designing artificial ncRNAs is crucial in developing transgenic plants because it enables precise control over gene expression (low or high) and minimizes undesirable off-target effects.

Artificially designing and synthesizing miRNA (short hairpin miRNA) and siRNA has been attempted in the past due to its great potential in developing gene-silencing techniques (Carbonell et al., 2014; Niemeier et al., 2010). More recently, advancements in artificial microRNA (amiRNA) technology have demonstrated that gene silencing can be achieved through minimal precursor designs, significantly reducing the size of traditional miRNA constructs while maintaining high efficiency (Cisneros et al., 2023). This study identified an 89-nucleotide minimal precursor, derived from AtMIR390a, that produces accurately processed amiRNAs and induces effective gene silencing in plants. Furthermore, the amiRNAs were designed with high specificity to their respective targets by computationally optimizing the amiRNA duplex to maximize complementarity while minimizing off-target effects, demonstrating an efficient and selective gene silencing approach using synthetic ncRNA.

Streamlined strategy for multiple ncRNA manipulation

Gene pyramiding has been demonstrated to be an effective strategy to boost desirable benefits of multiple candidate genes while compensating for undesirable effect to synergistically impact overall performance of the target crops (Zhao et al., 2024). The same strategy can be used to manipulate multiple ncRNA expression by integrating several synthetic ncRNAs into one genetic construct, either with different expression cassettes or a single expression cassette, to simultaneously regulate multiple target genes involved in stress responses, growth or development. This multiplexing approach allows for a coordinated modulation of various biological pathways, enabling plants to more effectively manage complex environmental challenges (Rajput et al., 2023). The redundancy inherent in stacking ncRNAs not only provides a backup mechanism if one component is less effective but can also lead to synergistic effects where the combined regulatory influence is greater than the sum of its parts (Figure 3b). In our work in creeping bentgrass, a gene pyramiding strategy that stacks multiple miRNAs (miR319, miR393, miR396 and miR528) with a minimal precursor design has been demonstrated to be highly effective. This approach not only generated transgenic grass with total sterility for gene containment purposes but also successfully incorporated a suite of stress resistance traits without imposing any penalty on growth.

Future perspectives

Non-coding RNAs have emerged as pivotal regulators in plant stress responses, orchestrating complex networks that fine-tune gene expression and modulate environmental adaptations. Research on ncRNAs has provided pieces of the overwhelmingly complex puzzle of their regulatory networks. Although miRNAs and lncRNAs are the most extensively studied due to their more essential roles in transcriptional and translational regulation, studies on circRNAs and tRFs are also indispensable to fully understand the nuanced dynamics of these networks.

Looking ahead, advances in high-throughput sequencing and synthetic biology will further unravel the intricate regulatory mechanisms of ncRNAs. The possible deployment of machine learning algorithms can help predict and identify potential relationships among ncRNAs within dynamic patterns. Additionally, the development of precise gene-editing tools and artificial ncRNA constructs offers exciting opportunities to engineer crops with enhanced resilience and productivity under ever-changing environmental conditions. Continued research in this field promises to pave the way for sustainable agricultural practices and the development of next-generation transgenic varieties that are better equipped to cope with the challenges of climate change and environmental stress.

Acknowledgements

This work was supported by Biotechnology Risk Assessment Grant Program competitive grants nos. 2019-33522-30102, 2021-33522-35342 and 2024-33522-43691 from the USDA National Institute of Food and Agriculture. The work is also partially supported by the National Science Foundation under Grant No. 2005030 through a LSAMP Bridge to Doctorate fellowship for R.W. Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Conflict of interest

The authors declare no conflict of interests.

Author contributions

H.L. and X.C. conceptualized the work. X.C. drafted the manuscript. Z.C. and R.W. participated in the discussion and literature review. X.C. and H.L. revised the paper. All authors read and approved the final manuscript.

Data availability statement

No datasets were generated or used for this review paper.

References

Ahmed, W., Xia, Y., Zhang, H., Li, R., Bai, G., Siddique, K.H.M. and Guo, P. (2019) Identification of conserved and novel miRNAs responsive to heat stress in flowering Chinese cabbage using high‐throughput sequencing. Sci. Rep. 9, 14922.

Akgul, B. and Aydinoglu, F. (2025) Evaluation of zma‐miR408 and its target genes function on maize (Zea mays) leaf growth response to cold stress by VIGS‐based STTM approach. Gene 938, 149161.

Alves, C.S., Vicentini, R., Duarte, G.T., Pinoti, V.F., Vincentz, M. and Nogueira, F.T.S. (2017) Genome‐wide identification and characterization of tRNA‐derived RNA fragments in land plants. Plant Mol. Biol. 93, 35–48.

Ambros, V. (2011) MicroRNAs and developmental timing. Curr. Opin. Genet. Dev. 21, 511–517.

Anderegg, W.R.L., Trugman, A.T., Badgley, G., Anderson, C.M., Bartuska, A., Ciais, P., Cullenward, D. et al. (2020) Climate‐driven risks to the climate mitigation potential of forests. Science 368, eaaz7005.

Ariel, F., Lucero, L., Christ, A., Mammarella, M.F., Jegu, T., Veluchamy, A., Mariappan, K. et al. (2020) R‐loop mediated trans action of the APOLO long noncoding RNA. Mol. Cell 77, 1055–1065.e4.

Arshad, M., Feyissa, B.A., Amyot, L., Aung, B. and Hannoufa, A. (2017a) MicroRNA156 improves drought stress tolerance in alfalfa (Medicago sativa) by silencing SPL13. Plant Sci. 258, 122–136.

Arshad, M., Gruber, M.Y., Wall, K. and Hannoufa, A. (2017b) An insight into microRNA156 role in salinity stress responses of Alfalfa. Front. Plant Sci. 8, 356. https://doi.org/10.3389/fpls.2017.00356

Arshad, M., Puri, A., Simkovich, A.J., Renaud, J., Gruber, M.Y., Marsolais, F. and Hannoufa, A. (2020) Label‐free quantitative proteomic analysis of alfalfa in response to microRNA156 under high temperature. BMC Genomics 21, 758.

Aycan, M., Nahar, L., Baslam, M. and Mitsui, T. (2023) B‐type response regulator hst1 controls salinity tolerance in rice by regulating transcription factors and antioxidant mechanisms. Plant Physiol. Biochem. 196, 542–555.

Aydinoglu, F. (2020) Elucidating the regulatory roles of microRNAs in maize (Zea mays L.) leaf growth response to chilling stress. Planta 251, 38.

Aydinoglu, F., Kahriman, T.Y. and Balci, H. (2023) Seed bio‐priming enhanced salt stress tolerance of maize (Zea mays L.) seedlings by regulating the antioxidant system and miRNA expression. 3 Biotech 13, 378.

Baek, D., Chun, H.J., Kang, S., Shin, G., Park, S.J., Hong, H., Kim, C. et al. (2016) A role for Arabidopsis miR399f in salt, drought, and ABA signaling. Mol. Cells 39, 111–118.

Bai, B., Bian, H., Zeng, Z., Hou, N., Shi, B., Wang, J., Zhu, M. et al. (2017) miR393‐Mediated Auxin Signaling Regulation is Involved in Root Elongation Inhibition in Response to Toxic Aluminum Stress in Barley. Plant Cell Physiol. 58, 426–439.

Bai, Q., Wang, X., Chen, X., Shi, G., Liu, Z., Guo, C. and Xiao, K. (2018) Wheat miRNA TaemiR408 acts as an essential mediator in plant tolerance to Pi deprivation and salt stress via modulating stress‐associated physiological processes. Front. Plant Sci. 9, 499. https://doi.org/10.3389/fpls.2018.00499

Bakhat, N., Jiménez‐Sánchez, A., Ruiz‐Jiménez, L., Padilla‐Roji, I., Velasco, L., Pérez‐García, A. and Fernández‐Ortuño, D. (2025) Fungal effector genes involved in the suppression of chitin signaling as novel targets for the control of powdery mildew disease via a nontransgenic RNA interference approach. Pest Manag. Sci. https://doi.org/10.1002/ps.8660

Baldrich, P., Kakar, K., Siré, C., Moreno, A.B., Berger, A., García‐Chapa, M., López‐Moya, J.J. et al. (2014) Small RNA profiling reveals regulation of Arabidopsis miR168 and heterochromatic siRNA415 in response to fungal elicitors. BMC Genomics 15, 1083.

Balyan, S., Sharma, D., Kansal, S., Panwar, V., Jajo, R., Chithung, T.A. and Raghuvanshi, S. (2023) Monocot‐specific miR528 act as the post‐transcriptional regulator of strigolactone signaling via Dwarf 3 in rice. bioRxiv. https://doi.org/10.1101/2023.11.06.565764

Barrera‐Figueroa, B.E., Gao, L., Diop, N.N., Wu, Z., Ehlers, J.D., Roberts, P.A., Close, T.J. et al. (2011) Identification and comparative analysis of drought‐associated microRNAs in two cowpea genotypes. BMC Plant Biol. 11, 127.

Bazzini, A.A., Hopp, H.E., Beachy, R.N. and Asurmendi, S. (2007) Infection and coaccumulation of tobacco mosaic virus proteins alter microRNA levels, correlating with symptom and plant development. Proc. Natl. Acad. Sci. USA 104, 12157–12162.

Bélanger, S., Pokhrel, S., Czymmek, K. and Meyers, B.C. (2020) Premeiotic, 24‐nucleotide reproductive phasiRNAs are abundant in anthers of wheat and barley but not rice and maize. Plant Physiol. 184, 1407–1423.

Ben Amor, B., Wirth, S., Merchan, F., Laporte, P., d'Aubenton‐Carafa, Y., Hirsch, J., Maizel, A. et al. (2009) Novel long non‐protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res. 19, 57–69.

Bertolini, E., Verelst, W., Horner, D.S., Gianfranceschi, L., Piccolo, V., Inzé, D., Pè, M.E. et al. (2013) Addressing the role of microRNAs in reprogramming leaf growth during drought stress in Brachypodium distachyon. Mol. Plant 6, 423–443.

Bhardwaj, E., Pokhriyal, E., Jain, A., Lal, M., Khari, M., Jalan, K. and Das, S. (2024) The non‐canonically organized members of MIR395 gene family in Brassica juncea are associated with developmentally regulated, sulfate‐stress responsive bidirectional promoters that exhibit orientation‐dependent differential transcriptional activity. Plant Sci. 348, 112214.

Bhatia, G., Singh, A., Verma, D., Sharma, S. and Singh, K. (2020) Genome‐wide investigation of regulatory roles of lncRNAs in response to heat and drought stress in Brassica juncea (Indian mustard). Environ. Exp. Bot. 171, 103922.

Borsani, O., Zhu, J., Verslues, P.E., Sunkar, R. and Zhu, J.‐K. (2005) Endogenous siRNAs derived from a pair of natural cis‐antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123, 1279–1291.

Bottino, M.C., Rosario, S., Grativol, C., Thiebaut, F., Rojas, C.A., Farrineli, L., Hemerly, A.S. et al. (2013) High‐throughput sequencing of small RNA transcriptome reveals salt stress regulated MicroRNAs in sugarcane. PLoS One 8, e59423.

Bouba, I., Kang, Q., Luan, Y.‐S. and Meng, J. (2019) Predicting miRNA‐lncRNA interactions and recognizing their regulatory roles in stress response of plants. Math. Biosci. 312, 67–76.

Božić, M., Ignjatović Micić, D., Delić, N. and Nikolić, A. (2024) Maize miRNAs and their putative target genes involved in chilling stress response in 5‐day old seedlings. BMC Genomics 25, 479.

Brodersen, P. and Voinnet, O. (2006) The diversity of RNA silencing pathways in plants. Trends Genet. 22, 268–280.

Bundó, M., Val‐Torregrosa, B., Martín‐Cardoso, H., Ribaya, M., Campos‐Soriano, L., Bach‐Pages, M., Chiou, T.‐J. et al. (2024) Silencing Osa‐miR827 via CRISPR/Cas9 protects rice against the blast fungus Magnaporthe oryzae. Plant Mol. Biol. 114, 105.

Cai, Y.‐M., Kallam, K., Tidd, H., Gendarini, G., Salzman, A. and Patron, N.J. (2020) Rational design of minimal synthetic promoters for plants. Nucleic Acids Res. 48, 11845–11856.

Cao, C., Long, R., Zhang, T., Kang, J., Wang, Z., Wang, P., Sun, H. et al. (2018) Genome‐wide identification of microRNAs in response to salt/alkali stress in Medicago truncatula through high‐throughput sequencing. Int. J. Mol. Sci. 19, 4076.

Cao, M., Du, P., Wang, X., Yu, Y.Q., Qiu, Y.H., Li, W., Gal‐On, A. et al. (2014) Virus infection triggers widespread silencing of host genes by a distinct class of endogenous siRNAs in Arabidopsis. Proc. Natl. Acad. Sci. USA 111, 14613–14618.

Cao, W., Yang, L., Zhuang, M., Lv, H., Wang, Y., Zhang, Y. and Ji, J. (2024) Plant non‐coding RNAs: The new frontier for the regulation of plant development and adaptation to stress. Plant Physiol. Biochem. 208, 108435.

Carbonell, A., Takeda, A., Fahlgren, N., Johnson, S.C., Cuperus, J.T. and Carrington, J.C. (2014) New generation of artificial MicroRNA and synthetic trans‐acting small interfering RNA vectors for efficient gene silencing in Arabidopsis. Plant Physiol. 165, 15–29.

Caruana, J.C., Dhar, N. and Raina, R. (2020) Overexpression of Arabidopsis microRNA167 induces salicylic acid‐dependent defense against Pseudomonas syringae through the regulation of its targets ARF6 and ARF8. Plant Direct 4, e00270.

Chang, B., Ma, K., Lu, Z., Lu, J., Cui, J., Wang, L. and Jin, B. (2020) Physiological, transcriptomic, and metabolic responses of Ginkgo biloba L. to drought, salt, and heat stresses. Biomolecules 10, 1635.

Chen, G., Wang, Y., Liu, X., Duan, S., Jiang, S., Zhu, J., Zhang, Y. et al. (2023a) The MdmiR156n regulates drought tolerance and flavonoid synthesis in apple calli and Arabidopsis. Int. J. Mol. Sci. 24, 6049.

Chen, H., Li, Z. and Xiong, L. (2012) A plant microRNA regulates the adaptation of roots to drought stress. FEBS Lett. 586, 1742–1747.

Chen, J., Li, W.X., Xie, D., Peng, J.R. and Ding, S.W. (2004) Viral virulence protein suppresses RNA silencing–mediated defense but upregulates the role of Microrna in host gene expression[W]. Plant Cell 16, 1302–1313.

Chen, J., Pan, A., He, S., Su, P., Yuan, X., Zhu, S. and Liu, Z. (2020a) Different MicroRNA families involved in regulating high temperature stress response during cotton (Gossypium hirsutum L.) anther development. Int. J. Mol. Sci. 21, 1280.

Chen, L., He, J., Wang, X., Zhang, S., Pan, J., Peng, J., Mo, B. et al. (2024a) miR827 orchestrates the regulation of SPX‐MFS1 and SPX‐MFS5 with the assistance of lncRNA767 to enhance phosphate starvation tolerance and maize development. Plant Biotechnol. J. 22, 3489–3504.

Chen, L., Luan, Y. and Zhai, J. (2015a) Sp‐miR396a‐5p acts as a stress‐responsive genes regulator by conferring tolerance to abiotic stresses and susceptibility to Phytophthora nicotianae infection in transgenic tobacco. Plant Cell Rep. 34, 2013–2025.

Chen, L., Zhu, Q.‐H. and Kaufmann, K. (2020b) Long non‐coding RNAs in plants: Emerging modulators of gene activity in development and stress responses. Planta 252, 92.

Chen, P., Wei, Q., Yao, Y., Wei, J., Qiu, L., Zhang, B. and Liu, H. (2023b) Inoculation with Azorhizobium caulinodans ORS571 enhances plant growth and salt tolerance of switchgrass (Panicum virgatum L.) seedlings. Biotechnol. Biofuels Bioproducts 16, 35.

Chen, S., Wu, J., Zhang, Y., Zhao, Y., Xu, W., Li, Y. and Xie, J. (2021) Genome‐wide analysis of coding and non‐coding RNA reveals a conserved miR164–NAC–mRNA regulatory pathway for disease defense in populus. Front. Genet. 12, 668940. https://doi.org/10.3389/fgene.2021.668940

Chen, X., Chen, Z., Fiorentino, A., Kuess, M., Tharayil, N., Kumar, R., Leonard, E. et al. (2024b) MicroRNA169 integrates multiple factors to modulate plant growth and abiotic stress responses. Plant Biotechnol. J. 22, 2541–2557.

Chen, Y., Jiang, J., Song, A., Chen, S., Shan, H., Luo, H., Gu, C. et al. (2013) Ambient temperature enhanced freezing tolerance of Chrysanthemum dichrum CdICE1Arabidopsis via miR398. BMC Biol. 11, 121.

Chen, Z., Hu, L., Han, N., Hu, J., Yang, Y., Xiang, T., Zhang, X. et al. (2015b) Overexpression of a miR393‐resistant form of transport inhibitor response protein 1 (mTIR1) enhances salt tolerance by increased osmoregulation and Na+ exclusion in Arabidopsis thaliana. Plant Cell Physiol. 56, 73–83.

Cheng, C., Liu, F., Sun, X., Tian, N., Mensah, R.A., Li, D. and Lai, Z. (2019) Identification of Fusarium oxysporum f. Sp. Cubense tropical race 4 (Foc TR4) responsive miRNAs in banana root. Sci. Rep. 9, 13682.

Cheng, Y., Wang, Q., Yang, L., Li, Q. and Yan, X. (2024) MiR319a‐mediated salt stress response in poplar. Hort. Res. 11, uhae157.

Chi, Q., Du, L., Ma, W., Niu, R., Wu, B., Guo, L., Ma, M. et al. (2023) The miR164‐TaNAC14 module regulates root development and abiotic‐stress tolerance in wheat seedlings. J. Integr. Agric. 22, 981–998.

Chorostecki, U., Bologna, N.G. and Ariel, F. (2023) The plant noncoding transcriptome: a versatile environmental sensor. EMBO J. 42, e114400.

Christensen, A.H. and Quail, P.H. (1996) Ubiquitin promoter‐based vectors for high‐level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res. 5, 213–218.

Chu, Y., Bai, W., Wang, P., Li, F., Zhan, J. and Ge, X. (2022) The mir390‐GhCEPR2 module confers salt tolerance in cotton and Arabidopsis. Ind. Crop Prod. 190, 115865.

Cisneros, A.E., Martín‐García, T., Primc, A., Kuziuta, W., Sánchez‐Vicente, J., Aragonés, V., Daròs, J.‐A. et al. (2023) Transgene‐free, virus‐based gene silencing in plants by artificial microRNAs derived from minimal precursors. Nucleic Acids Res. 51, 10719–10736.

Cognat, V., Morelle, G., Megel, C., Lalande, S., Molinier, J., Vincent, T., Small, I. et al. (2017) The nuclear and organellar tRNA‐derived RNA fragment population in Arabidopsis thaliana is highly dynamic. Nucleic Acids Res. 45, 3460–3472.

Dai, Y., Feng, X., Liu, Z., Wang, M., Zhou, Y., Cui, L., Wei, X. et al. (2024) miR1432 negatively regulates cold tolerance by targeting OsACAs. Plant Cell Environ. 47, 5443–5456.

De Luis, A., Markmann, K., Cognat, V., Holt, D.B., Charpentier, M., Parniske, M., Stougaard, J. et al. (2012) Two MicroRNAs linked to nodule infection and nitrogen‐fixing ability in the legume Lotus japonicus. Plant Physiol. 160, 2137–2154.

Ding, B., Yue, Y., Chen, X., Long, X. and Zhou, Z. (2024) Identification and expression analysis of miR396 and its target genes in Jerusalem artichoke under temperature stress. Gene 893, 147908.

Ding, Y., Gong, S., Wang, Y., Wang, F., Bao, H., Sun, J., Cai, C. et al. (2018) MicroRNA166 modulates cadmium tolerance and accumulation in rice. Plant Physiol. 177, 1691–1703.

Ding, Y., Ma, Y., Liu, N., Xu, J., Hu, Q., Li, Y., Wu, Y. et al. (2017) Micro RNA s involved in auxin signalling modulate male sterility under high‐temperature stress in cotton (Gossypium hirsutum). Plant J. 91, 977–994.

Ding, Y., Ye, Y., Jiang, Z., Wang, Y. and Zhu, C. (2016) MicroRNA390 is involved in cadmium tolerance and accumulation in rice. Front. Plant Sci. 7, 235. https://doi.org/10.3389/fpls.2016.00235

D'Ippolito, S., Vankova, R., Joosten, M.H.A.J., Casalongué, C.A. and Fiol, D.F. (2016) Knocking down expression of the auxin‐amidohydrolase IAR3 alters defense responses in Solanaceae family plants. Plant Sci. 253, 31–39.

Djami‐Tchatchou, A.T. and Dubery, I.A. (2019) miR393 regulation of lectin receptor‐like kinases associated with LPS perception in Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 513, 88–92.

Dmitriev, A.A., Kudryavtseva, A.V., Bolsheva, N.L., Zyablitsin, A.V., Rozhmina, T.A., Kishlyan, N.V., Krasnov, G.S. et al. (2017). miR319, miR390, and miR393 are involved in aluminum response in Flax (Linum usitatissimum L.). Biomed. Res. Int. 2017, 4975146.

Dong, Y., Tang, M., Huang, Z., Song, J., Xu, J., Ahammed, G.J., Yu, J. et al. (2022) The miR164a‐NAM3 module confers cold tolerance by inducing ethylene production in tomato. Plant J. 111, 440–456.

Dotto, M., Gómez, M.S., Soto, M.S. and Casati, P. (2018) UV‐B radiation delays flowering time through changes in the PRC2 complex activity and miR156 levels in Arabidopsis thaliana. Plant Cell Environ. 41, 1394–1406.

Du, K., Yang, Y., Li, J., Wang, M., Jiang, J., Wu, J., Fang, Y. et al. (2023) Functional analysis of Bna‐miR399c‐PHO2 regulatory module involved in phosphorus stress in Brassica napus. Life 13, 310.

Du, T., Meng, D., Cao, H., Lian, Y., Wu, R., Liu, T., Wang, T. et al. (2025) Sorbitol induces flavonoid accumulation as a secondary signal via the nanoencapsulated SPc/lncRNA809‐MmNAC17 module against Alternaria alternata in Malus micromalus. Molecular Horticulture 5, 5.

Dubey, S., Saxena, S., Chauhan, A.S., Mathur, P., Rani, V. and Chakrabaroty, D. (2020) Identification and expression analysis of conserved microRNAs during short and prolonged chromium stress in rice (Oryza sativa). Environ. Sci. Pollut. Res. 27, 380–390.

Eldem, V., Çelikkol Akçay, U., Ozhuner, E., Bakır, Y., Uranbey, S. and Unver, T. (2012) Genome‐wide identification of miRNAs responsive to drought in peach (Prunus persica) by high‐throughput deep sequencing. PLoS One 7, e50298.

Ellendorff, U., Fradin, E.F., De Jonge, R. and Thomma, B.P.H.J. (2009) RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J. Exp. Bot. 60, 591–602.

Eom, S.H., Lee, H.J., Lee, J.H., Wi, S.H., Kim, S.K. and Hyun, T.K. (2019) Identification and functional prediction of drought‐responsive long non‐coding RNA in tomato. Agronomy 9, 629.

Eulalio, A., Huntzinger, E. and Izaurralde, E. (2008) Getting to the root of miRNA‐mediated gene silencing. Cell 132, 9–14.

Fan, G., Cao, Y. and Wang, Z. (2018) Regulation of long noncoding RNAs responsive to phytoplasma infection in Paulownia tomentosa. International Journal of Genomics 2018, 3174352.

Fang, Y., Xie, K. and Xiong, L. (2014) Conserved miR164‐targeted NAC genes negatively regulate drought resistance in rice. J. Exp. Bot. 65, 2119–2135.

Feng, H., Duan, X., Zhang, Q., Li, X., Wang, B., Huang, L., Wang, X. et al. (2014) The target gene of tae‐miR164, a novel NAC transcription factor from the NAM subfamily, negatively regulates resistance of wheat to stripe rust. Mol. Plant Pathol. 15, 284–296.

Feng, H., Wang, T., Feng, C., Zhang, Q., Zhang, X., Huang, L., Wang, X. et al. (2016) Identification of microRNAs and their corresponding targets involved in the susceptibility interaction of wheat response to Puccinia striiformis f. Sp. Tritici. Physiol. Plant. 157, 95–107.

Feng, H., Zhang, Q., Wang, Q., Wang, X., Liu, J., Li, M., Huang, L. et al. (2013) Target of tae‐miR408, a chemocyanin‐like protein gene (TaCLP1), plays positive roles in wheat response to high‐salinity, heavy cupric stress and stripe rust. Plant Mol. Biol. 83, 433–443.

Feng, J., Wang, K., Liu, X., Chen, S. and Chen, J. (2009) The quantification of tomato microRNAs response to viral infection by stem‐loop real‐time RT‐PCR. Gene 437, 14–21.

Feng, T., Zhang, Z.‐Y., Gao, P., Feng, Z.‐M., Zuo, S.‐M. and Ouyang, S.‐Q. (2023) Suppression of rice Osa‐miR444.2 improves the resistance to sheath blight in rice mediating through the phytohormone pathway. Int. J. Mol. Sci. 24, 3653.

Feng, X.‐M., You, C.‐X., Qiao, Y., Mao, K. and Hao, Y.‐J. (2010) Ectopic overexpression of Arabidopsis AtmiR393a gene changes auxin sensitivity and enhances salt resistance in tobacco. Acta Physiologiae Plantarum 32, 997–1003.

Feng, Y., Qi, N., Lei, P., Wang, Y., Xuan, Y., Liu, X., Fan, H. et al. (2022) Gma‐miR408 enhances soybean cyst nematode susceptibility by suppressing reactive oxygen species accumulation. Int. J. Mol. Sci. 23, 14022.

Ferdous, J., Sanchez‐Ferrero, J.C., Langridge, P., Milne, L., Chowdhury, J., Brien, C. and Tricker, P.J. (2017a) Differential expression of microRNAs and potential targets under drought stress in barley. Plant Cell Environ. 40, 11–24.

Ferdous, J., Whitford, R., Nguyen, M., Brien, C., Langridge, P. and Tricker, P.J. (2017b) Drought‐inducible expression of Hv‐miR827 enhances drought tolerance in transgenic barley. Funct. Integr. Genomics 17, 279–292.

Feyissa, B.A., Arshad, M., Gruber, M.Y., Kohalmi, S.E. and Hannoufa, A. (2019) The interplay between miR156/SPL13 and DFR/WD40–1 regulate drought tolerance in alfalfa. BMC Plant Biol. 19, 434.

Fileccia, V., Ingraffia, R., Amato, G., Giambalvo, D. and Martinelli, F. (2019) Identification of microRNAS differentially regulated by water deficit in relation to mycorrhizal treatment in wheat. Mol. Biol. Rep. 46, 5163–5174.

Fracasso, A., Vallino, M., Staropoli, A., Vinale, F., Amaducci, S. and Carra, A. (2021) Increased water use efficiency in miR396‐downregulated tomato plants. Plant Sci. 303, 110729.

Fu, T., Wang, C., Yang, Y., Yang, X., Wang, J., Zhang, L., Wang, Z. et al. (2023) Function identification of miR159a, a positive regulator during poplar resistance to drought stress. Horticulture Res. 10, uhad221.

Gandham, P., Rajasekaran, K., Sickler, C., Mohan, H., Gilbert, M. and Baisakh, N. (2024) MicroRNA (miRNA) profiling of maize genotypes with differential response to Aspergillus flavus implies zma‐miR156–squamosa promoter binding protein (SBP) and zma‐miR398/zma‐miR394–F‐box combinations involved in resistance mechanisms. Stress Biol. 4, 26.

Gao, F., Cai, Y., Kapranov, P. and Xu, D. (2020) Reverse‐genetics studies of lncRNAs—What we have learnt and paths forward. Genome Biol. 21, 93.

Gao, P., Bai, X., Yang, L., Lv, D., Pan, X., Li, Y., Cai, H. et al. (2011) osa‐MIR393: A salinity‐ and alkaline stress‐related microRNA gene. Mol. Biol. Rep. 38, 237–242.

Gao, R., Wan, Z.Y. and Wong, S.‐M. (2013) Plant growth retardation and conserved miRNAs are correlated to Hibiscus chlorotic ringspot virus infection. PLoS One 8, e85476.

Gao, Z., Li, J., Luo, M., Li, H., Chen, Q., Wang, L., Song, S. et al. (2019) Characterization and cloning of grape circular RNAs identified the cold resistance‐related Vv‐circATS1. Plant Physiol. 180, 966–985.

Garcia‐Ruiz, H., Takeda, A., Chapman, E.J., Sullivan, C.M., Fahlgren, N., Brempelis, K.J. and Carrington, J.C. (2010) Arabidopsis RNA‐dependent RNA polymerases and dicer‐like proteins in antiviral defense and small interfering RNA biogenesis during Turnip mosaic virus infection. Plant Cell 22, 481–496.

Ge, Y., Han, J., Zhou, G., Xu, Y., Ding, Y., Shi, M., Guo, C. et al. (2018) Silencing of miR156 confers enhanced resistance to brown planthopper in rice. Planta 248, 813–826.

Ghabooli, M., Beheshti Rooy, S.S., Mohseni Fard, E. and Karimi, R. (2019) miR395 is involved in response to cold stress and modulation of sulfate and phosphate deficiency in Grape (Vitis vinifera). J. Plant Mol. Breed. 7, 56–66.

Ghorecha, V., Zheng, Y., Liu, L., Sunkar, R. and Krishnayya, N.S.R. (2017) MicroRNA dynamics in a wild and cultivated species of Convolvulaceae exposed to drought stress. Physiol. Mol. Biol. Plants 23, 291–300.

Gomes, A.Q., Nolasco, S. and Soares, H. (2013) Non‐coding RNAs: multi‐tasking molecules in the cell. Int. J. Mol. Sci. 14, 16010–16039.

Guan, Q., Lu, X., Zeng, H., Zhang, Y. and Zhu, J. (2013) Heat stress induction of mi398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J. 74, 840–851.

Guo, L., Shen, J., Zhang, C., Guo, Q., Liang, H. and Hou, X. (2022) Characterization and bioinformatics analysis of ptc‐miR396g‐5p in response to drought stress of Paeonia ostii. Non‐Coding RNA Res. 7, 150–158.

Guo, M., Li, H., Zhu, L., Wu, Z., Li, J. and Li, Z. (2021) Genome‐wide identification of microRNAs associated with osmotic stress and elucidation of the role of miR319 in Medicago ruthenica seedlings. Plant Physiol. Biochem. 168, 53–61.

Guo, X., Niu, J. and Cao, X. (2018) Heterologous expression of Salvia miltiorrhiza MicroRNA408 enhances tolerance to salt stress in Nicotiana benthamiana. Int. J. Mol. Sci. 19, 3985.

Guo, Y., Zhao, S., Zhu, C., Chang, X., Yue, C., Wang, Z., Lin, Y. et al. (2017) Identification of drought‐responsive miRNAs and physiological characterization of tea plant (Camellia sinensis L.) under drought stress. BMC Plant Biol. 17, 211.

Guo, Z., Li, Y. and Ding, S.W. (2019) Small RNA‐based antimicrobial immunity. Nat. Rev. Immunol. 19, 31–44.

Gupta, A., Patil, M., Qamar, A. and Senthil‐Kumar, M. (2020) Ath‐miR164c influences plant responses to the combined stress of drought and bacterial infection by regulating proline metabolism. Environ. Exp. Bot. 172, 103998.

Gupta, O.P., Meena, N.L., Sharma, I. and Sharma, P. (2014) Differential regulation of microRNAs in response to osmotic, salt and cold stresses in wheat. Mol. Biol. Rep. 41, 4623–4629.

Gupta, O.P., Permar, V., Koundal, V., Singh, U.D. and Praveen, S. (2012) MicroRNA regulated defense responses in Triticum aestivum L. during Puccinia graminis f.sp. Tritici infection. Mol. Biol. Rep. 39, 817–824.

Hackenberg, M., Shi, B.‐J., Gustafson, P. and Langridge, P. (2013) Characterization of phosphorus‐regulated miR399 and miR827 and their isomirs in barley under phosphorus‐sufficient and phosphorus‐deficient conditions. BMC Plant Biol. 13, 214.

Hajyzadeh, M., Turktas, M., Khawar, K.M. and Unver, T. (2015) miR408 overexpression causes increased drought tolerance in chickpea. Gene 555, 186–193.

Hang, N., Shi, T., Liu, Y., Ye, W., Taier, G., Sun, Y., Wang, K. et al. (2021) Overexpression of Os‐microRNA408 enhances drought tolerance in perennial ryegrass. Physiol. Plant. 172, 733–747.

Hassani, A., Azapagic, A. and Shokri, N. (2020) Predicting long‐term dynamics of soil salinity and sodicity on a global scale. Proc. Natl. Acad. Sci. 117, 33017–33027.

He, F., Xu, C., Fu, X., Shen, Y., Guo, L., Leng, M. and Luo, K. (2018) The MicroRNA390/TRANS‐ACTING SHORT INTERFERING RNA3 module mediates lateral root growth under salt stress via the auxin pathway. Plant Physiol. 177, 775–791.

He, X., Guo, S., Wang, Y., Wang, L., Shu, S. and Sun, J. (2020) Systematic identification and analysis of heat‐stress‐responsive lncRNAs, circRNAs and miRNAs with associated co‐expression and ceRNA networks in cucumber (Cucumis sativus L.). Physiol. Plant. 168, 736–754.

He, Y., Zhou, J., Hu, Y., Fang, C., Yu, Y., Yang, J., Zhu, B. et al. (2021) Overexpression of sly‐miR398b increased salt sensitivity likely via regulating antioxidant system and photosynthesis in tomato. Environ. Exp. Bot. 181, 104273.

Hewezi, T., Howe, P., Maier, T.R. and Baum, T.J. (2008) Arabidopsis small RNAs and their targets during cyst nematode parasitism. Mol. Plant Microbe Interact. 21, 1622–1634.

Hewezi, T., Piya, S., Qi, M., Balasubramaniam, M., Rice, J.H. and Baum, T.J. (2016) Arabidopsis miR827 mediates post‐transcriptional gene silencing of its ubiquitin E3 ligase target gene in the syncytium of the cyst nematode Heterodera schachtii to enhance susceptibility. Plant J. 88, 179–192.

Hilbricht, T., Varotto, S., Sgaramella, V., Bartels, D., Salamini, F. and Furini, A. (2008) Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytol. 179, 877–887.

Hivrale, V., Zheng, Y., Puli, C.O.R., Jagadeeswaran, G., Gowdu, K., Kakani, V.G., Barakat, A. et al. (2016) Characterization of drought‐ and heat‐responsive microRNAs in switchgrass. Plant Sci. 242, 214–223.

Hódar, J.A., Zamora, R. and Cayuela, L. (2012) Climate change and the incidence of a forest pest in Mediterranean ecosystems: can the North Atlantic Oscillation be used as a predictor? Clim. Change 113, 699–711.

Hong, Y.‐H., Meng, J., Zhang, M. and Luan, Y.‐S. (2020) Identification of tomato circular RNAs responsive to Phytophthora infestans. Gene 746, 144652.

Hsieh, L.‐C., Lin, S.‐I., Shih, A.C.‐C., Chen, J.‐W., Lin, W.‐Y., Tseng, C.‐Y., Li, W.‐H. et al. (2009) Uncovering small RNA‐mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol. 151, 2120–2132.

Hu, B., Wang, W., Deng, K., Li, H., Zhang, Z., Zhang, L. and Chu, C. (2015) MicroRNA399 is involved in multiple nutrient starvation responses in rice. Front. Plant Sci. 6, 188.

Hu, G., Lei, Y., Liu, J., Hao, M., Zhang, Z., Tang, Y., Chen, A. et al. (2020) The ghr‐miR164 and GhNAC100 modulate cotton plant resistance against Verticillium dahlia. Plant Sci. 293, 110438.

Hu, G., Wang, B., Jia, P., Wu, P., Lu, C., Xu, Y., Shi, L. et al. (2023) The cotton miR530‐SAP6 module activated by systemic acquired resistance mediates plant defense against Verticillium dahliae. Plant Sci. 330, 111647.

Huang, S.Q., Xiang, A.L., Che, L.L., Chen, S., Li, H., Song, J.B. and Yang, Z.M. (2010) A set of miRNAs from Brassica napus in response to sulphate deficiency and cadmium stress: S deficiency‐ and Cd‐regulated miRNAs from B. napus. Plant Biotechnol. J. 8, 887–899.

Hwang, E.‐W., Shin, S.‐J., Yu, B.‐K., Byun, M.‐O. and Kwon, H.‐B. (2011) miR171 family members are involved in drought response in Solanum tuberosum. J. Plant Biol. 54, 43–48.

Iglesias, M.J., Terrile, M.C., Windels, D., Lombardo, M.C., Bartoli, C.G., Vazquez, F., Estelle, M. et al. (2014) MiR393 regulation of auxin signaling and redox‐related components during acclimation to salinity in Arabidopsis. PLoS One 9, e107678.

İlhan, E., Büyük, İ. and İnal, B. (2018) Transcriptome – Scale characterization of salt responsive bean TCP transcription factors. Gene 642, 64–73.

Islam, W., Waheed, A., Naveed, H. and Zeng, F. (2022) MicroRNAs mediated plant responses to salt stress. Cells 11, 2806.

Jagadeeswaran, G., Li, Y.‐F. and Sunkar, R. (2014) Redox signaling mediates the expression of a sulfate‐deprivation‐inducible microRNA395 in Arabidopsis. Plant J. 77, 85–96.

Jatan, R., Tiwari, S., Asif, M.H. and Lata, C. (2019) Genome‐wide profiling reveals extensive alterations in Pseudomonas putida‐mediated miRNAs expression during drought stress in chickpea (Cicer arietinum L.). Environ. Exp. Bot. 157, 217–227.

Jeck, W.R., Sorrentino, J.A., Wang, K., Slevin, M.K., Burd, C.E., Liu, J., Marzluff, W.F. et al. (2013) Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19, 141–157.

Jia, X., Ren, L., Chen, Q.‐J., Li, R. and Tang, G. (2009a) UV‐B‐responsive microRNAs in Populus tremula. J. Plant Physiol. 166, 2046–2057.

Jia, X., Wang, W.‐X., Ren, L., Chen, Q.‐J., Mendu, V., Willcut, B., Dinkins, R. et al. (2009b) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol. Biol. 71, 51–59.

Jia, Y., Li, Q., Li, Y., Zhai, W., Jiang, G. and Li, C. (2021) Inducible enrichment of Osa‐miR1432 confers rice bacterial blight resistance through suppressing OsCaML2. Int. J. Mol. Sci. 22, 11367.

Jodder, J., Das, R., Sarkar, D., Bhattacharjee, P. and Kundu, P. (2017) Distinct transcriptional and processing regulations control miR167a level in tomato during stress. RNA Biol. 15, 130–143.

Jyothsna, S. and Alagu, M. (2022) Role of phasiRNAs in plant‐pathogen interactions: Molecular perspectives and bioinformatics tools. Physiol. Mol. Biol. Plants 28, 947–961.

Kantar, M., Lucas, S.J. and Budak, H. (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233, 471–484.

Kasschau, K.D., Xie, Z., Allen, E., Llave, C., Chapman, E.J., Krizan, K.A. and Carrington, J.C. (2003) P1/HC‐Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev. Cell 4, 205–217.

Katiyar‐Agarwal, S., Morgan, R., Dahlbeck, D., Borsani, O., Villegas, A., Zhu, J.‐K., Staskawicz, B.J. et al. (2006) A pathogen‐inducible endogenous siRNA in plant immunity. Proc. Natl. Acad. Sci. USA 103, 18002–18007.

Keller, M., Schleiff, E. and Simm, S. (2020) miRNAs involved in transcriptome remodeling during pollen development and heat stress response in Solanum lycopersicum. Sci. Rep. 10, 10694.

Khraiwesh, B., Zhu, J.K. and Zhu, J. (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochimica et Biophysica Acta – Gene Regulatory Mechanisms 1819, 137–148.

Kim, W., Iizumi, T. and Nishimori, M. (2019) Global patterns of crop production losses associated with droughts from 1983 to 2009. J. Appl. Meteorol. Climatol. 58, 1233–1244.

Kitazumi, A., Kawahara, Y., Onda, T.S., De Koeyer, D. and de los Reyes, B.G. (2015) Implications of miR166 and miR159 induction to the basal response mechanisms of an andigena potato (Solanum tuberosum subsp. Andigena) to salinity stress, predicted from network models in Arabidopsis. Genome 58, 13–24.

Kohli, D., Joshi, G., Deokar, A.A., Bhardwaj, A.R., Agarwal, M., Katiyar‐Agarwal, S., Srinivasan, R. et al. (2014) Identification and characterization of wilt and salt stress‐responsive MicroRNAs in chickpea through high‐throughput sequencing. PLoS One 9, e108851.

Kong, X., Peng, K., Shan, Y., Yun, Z., Dalmay, T., Duan, X., Jiang, Y. et al. (2025) Transcriptional regulation of miR528‐PPO module by miR156 targeted SPLs orchestrates chilling response in banana. Molecular Horticulture 5, 2.

Korek, M. and Marzec, M. (2023) Strigolactones and abscisic acid interactions affect plant development and response to abiotic stresses. BMC Plant Biol. 23, 314.

Kouhi, F., Sorkheh, K. and Ercisli, S. (2020) MicroRNA expression patterns unveil differential expression of conserved miRNAs and target genes against abiotic stress in safflower. PLoS One 15, e0228850.

Kristensen, L.S., Jakobsen, T., Hager, H. and Kjems, J. (2022) The emerging roles of circRNAs in cancer and oncology. Nat. Rev. Clin. Oncol. 19, 188–206.

Kulcheski, F.R., de Oliveira, L.F., Molina, L.G., Almerão, M.P., Rodrigues, F.A., Marcolino, J., Barbosa, J.F. et al. (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12, 307.

Kumar, R.S., Sinha, H., Datta, T., Asif, M.H. and Trivedi, P.K. (2023) microRNA408 and its encoded peptide regulate sulfur assimilation and arsenic stress response in Arabidopsis. Plant Physiol. 192, 837–856.

Kundu, A., Paul, S., Dey, A. and Pal, A. (2017) High throughput sequencing reveals modulation of microRNAs in Vigna mungo upon Mungbean Yellow Mosaic India Virus inoculation highlighting stress regulation. Plant Sci. 257, 96–105.

Lei, M.‐Q., He, R.‐R., Zhou, Y.‐F., Yang, L., Zhang, Z.‐F., Yuan, C., Zhao, W.‐L. et al. (2025) The long noncoding RNA ALEX1 confers a functional phase state of ARF3 to enhance rice resistance to bacterial pathogens. Mol. Plant 18, 114–129.

Lei, N., Yu, X., Li, S., Zeng, C., Zou, L., Liao, W. and Peng, M. (2017) Phylogeny and expression pattern analysis of TCP transcription factors in cassava seedlings exposed to cold and/or drought stress. Sci. Rep. 7, 10016.

Leng, X., Wang, P., Zhu, X., Li, X., Zheng, T., Shangguan, L. and Fang, J. (2017) Ectopic expression of CSD1 and CSD2 targeting genes of miR398 in grapevine is associated with oxidative stress tolerance. Funct. Integr. Genomics 17, 697–710.

Li, A.‐L., Wen, Z., Yang, K. and Wen, X.‐P. (2019a) Conserved miR396b‐GRF Regulation Is Involved in Abiotic Stress Responses in Pitaya (Hylocereus polyrhizus). Int. J. Mol. Sci. 20, 2501.

Li, B., Qin, Y., Duan, H., Yin, W. and Xia, X. (2011a) Genome‐wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J. Exp. Bot. 62, 3765–3779.

Li, B., Tao, P., Xu, F., He, P. and Wang, J. (2023) Function of soybean miR159 family members in plant responses to low phosphorus, high salinity, and abscisic acid treatment. Agronomy 13, 1798.

Li, H., Dong, Y., Yin, H., Wang, N., Yang, J., Liu, X., Wang, Y. et al. (2011b) Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol. 11, 170.

Li, J., Shen, Y., Zhu, J., Liu, S., Zeng, N. and Zhan, X. (2020) miR398 is involved in the relief of phenanthrene‐induced oxidative toxicity in wheat roots. Environ. Pollut. 258, 113701.

Li, J., Song, Q., Zuo, Z.‐F. and Liu, L. (2022) MicroRNA398: a master regulator of plant development and stress responses. Int. J. Mol. Sci. 23, 10803.

Li, J., Zhang, H., Zhu, J., Shen, Y., Zeng, N., Liu, S., Wang, H. et al. (2021a) Role of miR164 in the growth of wheat new adventitious roots exposed to phenanthrene. Environ. Pollut. 284, 117204.

Li, L., Yi, H., Xue, M. and Yi, M. (2017a) miR398 and miR395 are involved in response to SO2 stress in Arabidopsis thaliana. Ecotoxicology 26, 1181–1187.

Li, S., Cao, L., Zhou, Z., Cheng, Y., Zhang, X. and Li, Y. (2024) The miR164a targets CsNAC1 to negatively regulate cold tolerance of tea plants (Camellia sinensis). J. Integr. Agric. https://doi.org/10.1016/j.jia.2024.12.033

Li, S., Liu, J., Liu, Z., Li, X., Wu, F. and He, Y. (2014) HEAT‐INDUCED TAS1 TARGET1 mediates thermotolerance via HEAT STRESS TRANSCRIPTION FACTOR A1a–directed pathways in Arabidopsis. Plant Cell 26, 1764–1780.

Li, S., Yu, X., Lei, N., Cheng, Z., Zhao, P., He, Y., Wang, W. et al. (2017b) Genome‐wide identification and functional prediction of cold and/or drought‐responsive lncRNAs in cassava. Sci. Rep. 7, 45981.

Li, W., Cui, X., Meng, Z., Huang, X., Xie, Q., Wu, H., Jin, H. et al. (2012) Transcriptional regulation of Arabidopsis MIR168a and ARGONAUTE1 homeostasis in abscisic acid and abiotic stress responses1[W]. Plant Physiol. 158, 1279–1292.

Li, W.‐X., Oono, Y., Zhu, J., He, X.‐J., Wu, J.‐M., Iida, K., Lu, X.‐Y. et al. (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20, 2238–2251.

Li, Y., Cao, X.‐L., Zhu, Y., Yang, X.‐M., Zhang, K.‐N., Xiao, Z.‐Y., Wang, H. et al. (2019b) Osa‐miR398b boosts H2O2 production and rice blast disease‐resistance via multiple superoxide dismutases. New Phytol. 222, 1507–1522.

Li, Y., Wang, L.‐F., Bhutto, S.H., He, X.‐R., Yang, X.‐M., Zhou, X.‐H., Lin, X.‐Y. et al. (2021b) Blocking miR530 improves rice resistance, yield, and maturity. Front. Plant Sci. 12, 729560.

Li, Y., Zhang, Q.Q., Zhang, J., Wu, L., Qi, Y. and Zhou, J.M. (2010) Identification of microRNAs involved in pathogen‐associated molecular pattern‐triggered plant innate immunity. Plant Physiol. 152, 2222–2231.

Li, Y., Zheng, Y.‐P., Zhou, X.‐H., Yang, X.‐M., He, X.‐R., Feng, Q., Zhu, Y. et al. (2021c) Rice miR1432 fine‐tunes the balance of yield and blast disease resistance via different modules. Rice 14, 87.

Liang, G., He, H. and Yu, D. (2012) Identification of nitrogen starvation‐responsive MicroRNAs in Arabidopsis thaliana. PLoS One 7, e48951.

Lin, J.‐S., Kuo, C.‐C., Yang, I.‐C., Tsai, W.‐A., Shen, Y.‐H., Lin, C.‐C., Liang, Y.‐C. et al. (2018) MicroRNA160 modulates plant development and heat shock protein gene expression to mediate heat tolerance in Arabidopsis. Front. Plant Sci. 9, 68.

Lin, K.‐Y., Wu, S.‐Y., Hsu, Y.‐H. and Lin, N.‐S. (2022) MiR398‐regulated antioxidants contribute to Bamboo mosaic virus accumulation and symptom manifestation. Plant Physiol. 188, 593–607.

Lin, S.‐I., Santi, C., Jobet, E., Lacut, E., El Kholti, N., Karlowski, W.M., Verdeil, J.‐L. et al. (2010) Complex regulation of two target genes encoding SPX‐MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol. 51, 2119–2131.

Liu, H.‐H., Tian, X., Li, Y.‐J., Wu, C.‐A. and Zheng, C.‐C. (2008) Microarray‐based analysis of stress‐regulated microRNAs in Arabidopsis thaliana. RNA 14, 836–843.

Liu, J., Ren, Y., Sun, Y., Yin, Y., Han, B., Zhang, L., Song, Y. et al. (2024) Identification and Analysis of the MIR399 Gene Family in Grapevine Reveal Their Potential Functions in Abiotic Stress. Int. J. Mol. Sci. 25, 2979.

Liu, P., Zhang, X., Zhang, F., Xu, M., Ye, Z., Wang, K., Liu, S. et al. (2021) A virus‐derived siRNA activates plant immunity by interfering with ROS scavenging. Mol. Plant 14, 1088–1103.

Liu, Q., Hu, H., Zhu, L., Li, R., Feng, Y., Zhang, L., Yang, Y. et al. (2015) Involvement of miR528 in the regulation of arsenite tolerance in rice (Oryza sativa L.). J. Agric. Food Chem. 63, 8849–8861.

Liu, S., Guo, X.Y., Shang, Q.J. and Gao, P. (2023a) The biogenesis, biological functions and modification of Circular RNAs. Exp. Mol. Pathol. 131, 104861.

Liu, W. and Stewart, C.N. (2016) Plant synthetic promoters and transcription factors. Curr. Opin. Biotechnol. 37, 36–44.

Liu, W., Zhou, Y., Li, X., Wang, X., Dong, Y., Wang, N., Liu, X. et al. (2017a) Tissue‐specific regulation of Gma‐miR396 family on coordinating development and low water availability responses. Front. Plant Sci. 8, 1112.

Liu, X., Tan, C., Cheng, X., Zhao, X., Li, T. and Jiang, J. (2020a) miR168 targets Argonaute1A mediated miRNAs regulation pathways in response to potassium deficiency stress in tomato. BMC Plant Biol. 20, 477.

Liu, Y., Li, D., Yan, J., Wang, K., Luo, H. and Zhang, W. (2019) MiR319 mediated salt tolerance by ethylene. Plant Biotechnol. J. 17, 2370–2383.

Liu, Y., Teng, C., Xia, R. and Meyers, B.C. (2020) PhasiRNAs in plants: their biogenesis, genic sources, and roles in stress responses, development, and reproduction. Plant Cell 32, 3059–3080.

Liu, Y., Wang, K., Li, D., Yan, J. and Zhang, W. (2017b) Enhanced cold tolerance and tillering in switchgrass (Panicum virgatum L.) by heterologous expression of Osa‐miR393a. Plant Cell Physiol. 58, 2226–2240.

Liu, Y., Yu, Y., Fei, S., Chen, Y., Xu, Y., Zhu, Z. and He, Y. (2023b) Overexpression of Sly‐miR398b compromises disease resistance against Botrytis cinerea through regulating ROS homeostasis and JA‐related defense genes in tomato. Plants 12, 2572.

López‐Galiano, M.J., García‐Robles, I., González‐Hernández, A.I., Camañes, G., Vicedo, B., Real, M.D. and Rausell, C. (2019) Expression of miR159 is altered in tomato plants undergoing drought stress. Plan. Theory 8, 201.

Lu, F., Wang, K., Yan, L., Peng, Y., Qu, J., Wu, J., Cao, Y. et al. (2020a) Isolation and characterization of maize ZmPP2C26 gene promoter in drought‐response. Physiol. Mol. Biol. Plants 26, 2189–2197.

Lu, G., Tian, Z., Hao, Y., Xu, M., Lin, Y., Wei, J. and Zhao, Y. (2023) Overexpression of soybean microRNA156b enhanced tolerance to phosphorus deficiency and seed yield in Arabidopsis. Sci. Rep. 13, 652.

Lu, Q., Guo, F., Xu, Q. and Cang, J. (2020b) LncRNA improves cold resistance of winter wheat by interacting with miR398. Funct. Plant Biol. 47, 544–557.

Lu, S., Sun, Y., Amerson, H. and Chiang, V.L. (2007) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. Plant J. 51, 1077–1098.

Lu, X., Chen, X., Mu, M., Wang, J., Wang, X., Wang, D., Yin, Z. et al. (2016) Genome‐wide analysis of long noncoding RNAs and their responses to drought stress in cotton (Gossypium hirsutum L.). PLoS One 11, e0156723.

Lu, X., Dun, H., Lian, C., Zhang, X., Yin, W. and Xia, X. (2017) The role of peu‐miR164 and its target PeNAC genes in response to abiotic stress in Populus euphratica. Plant Physiol. Biochem. 115, 418–438.

Lu, Y., Feng, Z., Bian, L., Xie, H. and Liang, J. (2010) miR398 regulation in rice of the responses to abiotic and biotic stresses depends on CSD1 and CSD2 expression. Funct. Plant Biol. 38, 44–53.

Luan, M., Xu, M., Lu, Y., Zhang, L., Fan, Y. and Wang, L. (2015) Expression of zma‐miR169 miRNAs and their target ZmNF‐YA genes in response to abiotic stress in maize leaves. Gene 555, 178–185.

Luan, Y., Wang, W. and Liu, P. (2014) Identification and functional analysis of novel and conserved microRNAs in tomato. Mol. Biol. Rep. 41, 5385–5394.

Luo, Y., Wang, L., Zhu, J., Tian, J., You, L., Luo, Q., Li, J. et al. (2024) The grapevine miR827a regulates the synthesis of stilbenes by targeting VqMYB14 and gives rise to susceptibility in plant immunity. Theor. Appl. Genet. 137, 95.

Lv, L., Yu, K., Lü, H., Zhang, X., Liu, X., Sun, C., Xu, H. et al. (2020) Transcriptome‐wide identification of novel circular RNAs in soybean in response to low‐phosphorus stress. PLoS One 15, e0227243.

Lv, Y., Hu, F., Zhou, Y., Wu, F. and Gaut, B.S. (2019) Maize transposable elements contribute to long non‐coding RNAs that are regulatory hubs for abiotic stress response. BMC Genomics 20, 864.

Lyu, Q.R., Zhang, S., Zhang, Z. and Tang, Z. (2023) Functional knockout of long non‐coding RNAs with genome editing. Front. Genet. 14, 1242129.

Ma, C., Burd, S. and Lers, A. (2015) Mi408 is involved in abiotic stress responses in Arabidopsis. Plant J. 84, 169–187.

Macovei, A. and Tuteja, N. (2012) microRNAs targeting DEAD‐box helicases are involved in salinity stress response in rice (Oryza sativa L.). BMC Plant Biol. 12, 183.

Magee, R. and Rigoutsos, I. (2020) On the expanding roles of tRNA fragments in modulating cell behavior. Nucleic Acids Res. 48, 9433–9448.

Magwanga, R.O., Kirungu, J.N., Lu, P., Cai, X., Zhou, Z., Xu, Y., Hou, Y. et al. (2019) Map‐based functional analysis of the GhNLP genes reveals their roles in enhancing tolerance to N‐deficiency in cotton. Int. J. Mol. Sci. 20, 4953.

Mahale, B.M., Fakrudin, B., Ghosh, S. and Krishnaraj, P.U. (2014) LNA mediated in situ hybridization of miR171 and miR397a in leaf and ambient root tissues revealed expressional homogeneity in response to shoot heat shock in Arabidopsis thaliana. J. Plant Biochem. Biotechnol. 23, 93–103.

Mallory, A.C. and Vaucheret, H. (2006) Functions of microRNAs and related small RNAs in plants. Nat. Genet. 38(Suppl), S31–S36.

Matthews, C., Arshad, M. and Hannoufa, A. (2019) Alfalfa response to heat stress is modulated by microRNA156. Physiol. Plant. 165, 830–842.

Mattick, J.S., Amaral, P.P., Carninci, P., Carpenter, S., Chang, H.Y., Chen, L.‐L., Chen, R. et al. (2023) Long non‐coding RNAs: definitions, functions, challenges and recommendations. Nat. Rev. Mol. Cell Biol. 24, 430–447.

Mattick, J.S. and Rinn, J.L. (2015) Discovery and annotation of long noncoding RNAs. Nat. Struct. Mol. Biol. 22, 5–7.

Medina, C., Da Rocha, M., Magliano, M., Ratpopoulo, A., Revel, B., Marteu, N., Magnone, V. et al. (2017) Characterization of microRNAs from Arabidopsis galls highlights a role for miR159 in the plant response to the root‐knot nematode Meloidogyne incognita. New Phytol. 216, 882–896.

Meng, X., Li, A., Yu, B. and Li, S. (2021) Interplay between miRNAs and lncRNAs: Mode of action and biological roles in plant development and stress adaptation. Comput. Struct. Biotechnol. J. 19, 2567–2574.

Moldovan, D., Spriggs, A., Yang, J., Pogson, B.J., Dennis, E.S. and Wilson, I.W. (2010) Hypoxia‐responsive microRNAs and trans‐acting small interfering RNAs in Arabidopsis. J. Exp. Bot. 61, 165–177.

Natarajan, B., Kalsi, H.S., Godbole, P., Malankar, N., Thiagarayaselvam, A., Siddappa, S., Thulasiram, H.V. et al. (2018) MiRNA160 is associated with local defense and systemic acquired resistance against Phytophthora infestans infection in potato. J. Exp. Bot. 69, 2023–2036.

Naya, L., Paul, S., Valdés‐López, O., Mendoza‐Soto, A.B., Nova‐Franco, B., Sosa‐Valencia, G., Reyes, J.L. et al. (2014) Regulation of copper homeostasis and biotic interactions by MicroRNA 398b in common bean. PLoS One 9, e84416.

Nguyen, D.Q., Nguyen, N.L., Nguyen, V.T., Tran, T.H.G., Nguyen, T.H., Nguyen, T.K.L. and Nguyen, H.H. (2023) Comparative analysis of microRNA expression profiles in shoot and root tissues of contrasting rice cultivars (Oryza sativa L.) with different salt stress tolerance. PLoS One 18, e0286140.

Ni, Z., Hu, Z., Jiang, Q. and Zhang, H. (2013) GmNFYA3, a target gene of miR169, is a positive regulator of plant tolerance to drought stress. Plant Mol. Biol. 82, 113–129.

Niemeier, S., Alves, L. and Merkle, T. (2010) Improvement of the design and generation of highly specific plant knockdown lines using primary synthetic microRNAs (pri‐smiRNAs). BMC. Res. Notes 3, 59.

Odell, J.T., Nagy, F. and Chua, N.‐H. (1985) Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313, 810–812.

Pagano, L., Rossi, R., Paesano, L., Marmiroli, N. and Marmiroli, M. (2021) miRNA regulation and stress adaptation in plants. Environ. Exp. Bot. 184, 104369.

Pan, X., Nichols, R.L., Li, C. and Zhang, B. (2019) MicroRNA‐target gene responses to root knot nematode (Meloidogyne incognita) infection in cotton (Gossypium hirsutum L.). Genomics 111, 383–390.

Panstruga, R. (2024) Transfer RNA and ribosomal RNA fragments – emerging players in plant–microbe interactions. New Phytol. 241, 567–577.

Park, S.‐Y. and Grabau, E. (2017) Bypassing miRNA‐mediated gene regulation under drought stress: alternative splicing affects CSD1 gene expression. Plant Mol. Biol. 95, 243–252.

Patra, G.K., Gupta, D., Rout, G.R. and Panda, S.K. (2023) Role of long non coding RNA in plants under abiotic and biotic stresses. Plant Physiol. Biochem. 194, 96–110.

Pegler, J.L., Nguyen, D.Q., Oultram, J.M.J., Grof, C.P.L. and Eamens, A.L. (2021) Molecular manipulation of the miR396 and miR399 expression modules alters the response of Arabidopsis thaliana to phosphate stress. Plan. Theory 10, 2570.

Pegler, J.L., Oultram, J.M.J., Grof, C.P.L. and Eamens, A.L. (2020) Molecular manipulation of the miR399/PHO2 expression module alters the salt stress response of Arabidopsis thaliana. Plants 10, 73.

Pei, L., Gao, X., Tian, X., Liu, N., Chen, M., Fernie, A.R. and Li, H. (2024) A microRNA528‐ module regulates low phosphate tolerance in maize. Plant J. 118, 2233–2248.

Peng, K., Tian, Y., Sun, X., Song, C., Ren, Z., Bao, Y., Xing, J. et al. (2021) Tae‐miR399‐UBC24 module enhances freezing tolerance in winter wheat via a CBF signaling pathway. J. Agric. Food Chem. 69, 13398–13415.

Peng, X., Feng, C., Wang, Y.‐T., Zhang, X., Wang, Y.‐Y., Sun, Y.‐T., Xiao, Y.‐Q. et al. (2022) miR164g‐MsNAC022 acts as a novel module mediating drought response by transcriptional regulation of reactive oxygen species scavenging systems in apple. Horticulture Res. 9, uhac192.

Pieczynski, M., Marczewski, W., Hennig, J., Dolata, J., Bielewicz, D., Piontek, P., Wyrzykowska, A. et al. (2013) Down‐regulation of CBP 80 gene expression as a strategy to engineer a drought‐tolerant potato. Plant Biotechnol. J. 11, 459–469.

Pinweha, N., Asvarak, T., Viboonjun, U. and Narangajavana, J. (2015) Involvement of miR160/miR393 and their targets in cassava responses to anthracnose disease. J. Plant Physiol. 174, 26–35.

Pradhan, M., Rocha, C., Halitschke, R., Baldwin, I.T. and Pandey, S.P. (2021) microRNA390 modulates's tolerance response to herbivory. Plant Direct 5, e350.

Puri, A., Pajak, A., Hannoufa, A. and Marsolais, F. (2023) Quantitative proteomic analysis of the role of miRNA156 in alfalfa under drought stress. Environ. Exp. Bot. 214, 105449.

Qin, L., Zhao, L., Wu, C., Qu, S. and Wang, S. (2021) Identification of microRNA transcriptome in apple response to Alternaria alternata infection and evidence that miR390 is negative regulator of defense response. Sci. Hortic. 289, 110435.

Qin, R., Hu, Y., Chen, H., Du, Q., Yang, J. and Li, W.‐X. (2023) MicroRNA408 negatively regulates salt tolerance by affecting secondary cell wall development in maize. Plant Physiol. 192, 1569–1583.

Rajput, R., Naik, J., Misra, P., Trivedi, P.K. and Pandey, A. (2023) Gene pyramiding in transgenic plant development: approaches and challenges. J. Plant Growth Regulation 42, 6038–6056.

Rao, S., Gupta, A., Bansal, C., Sorin, C., Crespi, M. and Mathur, S. (2022) A conserved HSF:miR169:NF‐YA loop involved in tomato and Arabidopsis heat stress tolerance. Plant J. 112, 7–26.

Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B. and Bartel, D.P. (2002) MicroRNAs in plants. Genes Dev. 16, 1616–1626.

Ren, B., Wang, X., Duan, J. and Ma, J. (2019) Rhizobial tRNA‐derived small RNAs are signal molecules regulating plant nodulation. Science 365, 919–922.

Ren, L., Zhang, T., Wu, H., Ge, X., Wan, H., Chen, S., Li, Z. et al. (2022) Blocking IbmiR319a impacts plant architecture and reduces drought tolerance in sweet potato. Gen 13, 404.

Ren, Y., Li, J., Liu, J., Zhang, Z., Song, Y., Fan, D., Liu, M. et al. (2023) Functional differences of grapevine circular RNA Vv‐circPTCD1 in Arabidopsis and grapevine callus under abiotic stress. Plan. Theory 12, 2332.

Reyes, C.A., Ocolotobiche, E.E., Marmisollé, F.E., Robles Luna, G., Borniego, M.B., Bazzini, A.A., Asurmendi, S. et al. (2016) Citrus psorosis virus 24K protein interacts with citrus miRNA precursors, affects their processing and subsequent miRNA accumulation and target expression. Mol. Plant Pathol. 17, 317–329.

Reyes, J.L. and Chua, N. (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J. 49, 592–606.

Robert‐Seilaniantz, A., MacLean, D., Jikumaru, Y., Hill, L., Yamaguchi, S., Kamiya, Y. and Jones, J.D.G. (2011) The microRNA miR393 re‐directs secondary metabolite biosynthesis away from camalexin and towards glucosinolates. Plant J. 67, 218–231.

Salamon, S., Żok, J., Gromadzka, K. and Błaszczyk, L. (2021) Expression patterns of miR398, miR167, and miR159 in the interaction between bread wheat (Triticum aestivum L.) and Pathogenic Fusarium culmorum and beneficial trichoderma fungi. Pathogens 10, 1461.

Samad, A.F.A., Sajad, M., Nazaruddin, N., Fauzi, I.A., Murad, A.M.A., Zainal, Z. and Ismail, I. (2017) MicroRNA and transcription factor: key players in plant regulatory network. Front. Plant Sci. 8, 565.

Şanlı, B.A. and Öztürk Gökçe, Z.N. (2021) Investigating effect of miR160 through overexpression in potato cultivars under single or combination of heat and drought stresses. Plant Biotechnol. Rep. 15, 335–348.

Schommer, C., Bresso, E.G., Spinelli, S.V. and Palatnik, J.F. (2012) Role of MicroRNA miR319 in plant development. In MicroRNAs in Plant Development and Stress Responses(Sunkar, R., ed), pp. 29–47. Berlin, Heidelberg: Springer.

Sengupta, S., Pehlivan, N., Mangu, V., Rajasekaran, K. and Baisakh, N. (2022) Characterization of a stress‐enhanced promoter from the grass halophyte, Spartina alterniflora L. Biology 11, 1828.

Septiani, P., Pramesti, Y., Ghildan, M., Aprilia, K.Z., Awaludin, R., Medina, S., Subandiyah, S. et al. (2025) RNAi‐based biocontrol for crops: a revised expectation for a non‐recent technology. Planta 261, 44.

Shahid, S., Kim, G., Johnson, N.R., Wafula, E., Wang, F., Coruh, C., Bernal‐Galeano, V. et al. (2018) MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 553, 82–85.

Shan, T., Fu, R., Xie, Y., Chen, Q., Wang, Y., Li, Z., Song, X. et al. (2020) Regulatory mechanism of maize (Zea mays L.) miR164 in salt stress response. Russian J. Genetics 56, 835–842.

Sharma, A., Ruiz‐Manriquez, L.M., Serrano‐Cano, F.I., Reyes‐Pérez, P.R., Tovar Alfaro, C.K., Barrón Andrade, Y.E., Hernández Aros, A.K. et al. (2020) Identification of microRNAs and their expression in leaf tissues of guava (Psidium guajava L.) under salinity stress. Agronomy 10, 1920.

Shen, X., He, J., Ping, Y., Guo, J., Hou, N., Cao, F., Li, X. et al. (2022) The positive feedback regulatory loop of miR160‐Auxin Response Factor 17‐HYPONASTIC LEAVES 1 mediates drought tolerance in apple trees. Plant Physiol. 188, 1686–1708.

Shen, X., Song, Y., Ping, Y., He, J., Xie, Y., Ma, F., Li, X. et al. (2023) The RNA‐binding protein MdHYL1 modulates cold tolerance and disease resistance in apple. Plant Physiol. 192, 2143–2160.

Shi, J., Jiang, Q., Zhang, S., Dai, X., Wang, F. and Ma, Y. (2022) MIR390 is involved in regulating anthracnose resistance in apple. Plan. Theory 11, 3299.

Shi, X., Jiang, F., Wen, J. and Wu, Z. (2019) Overexpression of Solanum habrochaites microRNA319d (sha‐miR319d) confers chilling and heat stress tolerance in tomato (S. lycopersicum). BMC Plant Biol. 19, 214.

Shinde, H., Dudhate, A., Anand, L., Tsugama, D., Gupta, S.K., Liu, S. and Takano, T. (2020) Small RNA sequencing reveals the role of pearl millet miRNAs and their targets in salinity stress responses. South African Journal of Botany 132, 395–402.

Singroha, G., Sharma, P. and Sunkur, R. (2021) Current status of microRNA‐mediated regulation of drought stress responses in cereals. Physiol. Plant. 172, 1808–1821.

St. Laurent, G., Wahlestedt, C. and Kapranov, P. (2015) The Landscape of long noncoding RNA classification. Trends Genet. 31, 239–251.

Steg, L. (2018) Limiting climate change requires research on climate action. Nature Climate Change 8, 759–761.

Sun, G., Stewart, C.N., Xiao, P. and Zhang, B. (2012) MicroRNA expression analysis in the cellulosic biofuel crop switchgrass (Panicum virgatum) under abiotic stress. PLoS One 7, e32017.

Sun, M., Shen, Y., Yang, J., Cai, X., Li, H., Zhu, Y., Jia, B. et al. (2020a) miR535 negatively regulates cold tolerance in rice. Molecular Breeding 40, 14.

Sun, M., Yang, J., Cai, X., Shen, Y., Cui, N., Zhu, Y., Jia, B. et al. (2018) The opposite roles of OsmiR408 in cold and drought stress responses in Oryza sativa. Molecular Breeding 38, 120.

Sun, X., Tian, R., Zhao, M., Yan, J., Chu, J. and Zhang, W.‐H. (2025) MtCIR2 negatively regulates seed germination to salt stress by disrupting metabolisms and signaling of abscisic acid and gibberellins. Plant Physiol. Biochem. 220, 109493.

Sun, X., Xu, L., Wang, Y., Yu, R., Zhu, X., Luo, X., Gong, Y. et al. (2015) Identification of novel and salt‐responsive miRNAs to explore miRNA‐mediated regulatory network of salt stress response in radish (Raphanus sativus L.). BMC Genomics 16, 197.

Sun, X., Zheng, H., Li, J., Liu, L., Zhang, X. and Sui, N. (2020b) Comparative transcriptome analysis reveals new lncRNAs responding to salt stress in sweet sorghum. Front. Bioeng. Biotechnol. 8, 331. https://doi.org/10.3389/fbioe.2020.00331

Sun, Z., Kumar, R.M.S., Li, J., Yang, G. and Xie, Y. (2022) In Silico search and biological validation of MicroR171 family related to abiotic stress response in mulberry (Morus alba). Horticultural Plant J. 8, 184–194.

Sun, Z., Shu, L., Zhang, W. and Wang, Z. (2020c) Cca‐miR398 increases copper sulfate stress sensitivity via the regulation of CSD mRNA transcription levels in transgenic Arabidopsis thaliana. PeerJ 8, e9105.

Surdonja, K., Eggert, K., Hajirezaei, M.R., Harshavardhan, V.T., Seiler, C., von Wirén, N., Sreenivasulu, N. et al. (2017) Increase of DNA methylation at the hvckx2.1 promoter by terminal drought stress in barley. Epigenomes. 1, 9.

Suzuki, T., Ikeda, S., Kasai, A., Taneda, A., Fujibayashi, M., Sugawara, K., Okuta, M. et al. (2019) RNAi‐mediated down‐regulation of Dicer‐Like 2 and 4 changes the response of ‘Moneymaker’ tomato to potato spindle tuber viroid infection from tolerance to lethal systemic necrosis, accompanied by up‐regulation of miR398, 398a‐3p and production of excessive amount of reactive oxygen species. Viruses 11, 344.

Tagami, Y., Inaba, N., Kutsuna, N., Kurihara, Y. and Watanabe, Y. (2007) Specific enrichment of miRNAs in Arabidopsis thaliana infected with tobacco mosaic virus. DNA Res. 14, 227–233.

Tang, G., Yan, J., Gu, Y., Qiao, M., Fan, R., Mao, Y. and Tang, X. (2012a) Construction of short tandem target mimic (STTM) to block the functions of plant and animal microRNAs. Methods 58, 118–125.

Tang, Q., Lv, H., Li, Q., Zhang, X., Li, L., Xu, J., Wu, F. et al. (2022a) Characteristics of microRNAs and target genes in maize root under drought stress. Int. J. Mol. Sci. 23, 4968.

Tang, R., Yang, Y., Ji, C., Su, Y., Jiao, B., Yuan, B., Yang, X. et al. (2024) MiR827 positively regulates the resistance to chilli veinal mottle virus by affecting the expression of in Nicotiana benthamiana. Physiol. Plant. 176, e14375.

Tang, W. and Thompson, W.A. (2019) OsmiR528 enhances cold stress tolerance by repressing expression of stress response‐related transcription factor genes in plant cells. Curr. Genomics 20, 100–114.

Tang, Y., Du, G., Xiang, J., Hu, C., Li, X., Wang, W., Zhu, H. et al. (2022b) Genome‐wide identification of auxin response factor (ARF) gene family and the miR160‐ARF18‐mediated response to salt stress in peanut (Arachis hypogaea L.). Genomics 114, 171–184.

Tang, Y., Rong, H., Jia, X., Chen, Y., Wang, Z., Wei, J., Yang, C. et al. (2025) Unveiling the molecular symphony: MicroRNA160a‐Auxin Response Factor 18 module orchestrates low potassium tolerance in banana (Musa acuminata L.). Plant Sci. 350, 112288.

Tang, Z., Zhang, L., Xu, C., Yuan, S., Zhang, F., Zheng, Y. and Zhao, C. (2012b) Uncovering small RNA‐mediated responses to cold stress in a wheat thermosensitive genic male‐sterile line by deep sequencing. Plant Physiol. 159, 721–738.

Thiebaut, F., Rojas, C.A., Almeida, K.L., Grativol, C., Domiciano, G.C., Lamb, C.R.C., De Almeida Engler, J. et al. (2012) Regulation of miR319 during cold stress in sugarcane. Plant Cell Environ. 35, 502–512.

Tong, A., Yuan, Q., Wang, S., Peng, J., Lu, Y., Zheng, H., Lin, L. et al. (2017) Altered accumulation of osa‐miR171b contributes to rice stripe virus infection by regulating disease symptoms. J. Exp. Bot. 68, 4357–4367.

Trebicki, P. (2020) Climate change and plant virus epidemiology. Virus Res. 286, 198059.

Tsai, W.‐A., Sung, P.‐H., Kuo, Y.‐W., Chen, M.‐C., Jeng, S.‐T. and Lin, J.‐S. (2023) Involvement of microRNA164 in responses to heat stress in Arabidopsis. Plant Sci. 329, 111598.

Um, T., Choi, J., Park, T., Chung, P.J., Jung, S.E., Shim, J.S., Kim, Y.S. et al. (2022) Rice microRNA171f/SCL6 module enhances drought tolerance by regulation of flavonoid biosynthesis genes. Plant Direct 6, e374.

Valdés‐López, O., Yang, S.S., Aparicio‐Fabre, R., Graham, P.H., Reyes, J.L., Vance, C.P. and Hernández, G. (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol. 187, 805–818.

Valiollahi, E., Farsi, M. and Kakhki, A.M. (2014) Sly‐miR166 and Sly‐miR319 are components of the cold stress response in Solanum lycopersicum. Plant Biotechnology Reports 8, 349–356.

Vidal, E.A., Araus, V., Lu, C., Parry, G., Green, P.J., Coruzzi, G.M. and Gutiérrez, R.A. (2010) Nitrate‐responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc. Natl. Acad. Sci. 107, 4477–4482.

Visentin, I., Pagliarani, C., Deva, E., Caracci, A., Turečková, V., Novák, O., Lovisolo, C. et al. (2020) A novel strigolactone‐miR156 module controls stomatal behaviour during drought recovery. Plant Cell Environ. 43, 1613–1624.

Waititu, J.K., Zhang, C., Liu, J. and Wang, H. (2020) Plant non‐coding RNAs: origin, biogenesis, mode of action and their roles in abiotic stress. Int. J. Mol. Sci. 21, 8401.

Wang, B., Sun, Y., Song, N., Wei, J., Wang, X., Feng, H., Yin, Z. et al. (2014a) MicroRNAs involving in cold, wounding and salt stresses in Triticum aestivum L. Plant Physiol. Biochem. 80, 90–96.

Wang, B., Sun, Y.F., Song, N., Wang, X.J., Feng, H., Huang, L.L. and Kang, Z.S. (2013a) Identification of UV‐B‐induced microRNAs in wheat. Genet. Mol. Res. 12, 4213–4221.

Wang, C., Li, X., Zhuang, Y., Sun, W., Cao, H., Xu, R., Kong, F. et al. (2024) A novel miR160a–GmARF16–GmMYC2 module determines soybean salt tolerance and adaptation. New Phytol. 241, 2176–2192.

Wang, G., Wang, X., Zhang, Y., Yang, J., Li, Z., Wu, L., Wu, J. et al. (2021a) Dynamic characteristics and functional analysis provide new insights into long non‐coding RNA responsive to Verticillium dahliae infection in Gossypium hirsutum. BMC Plant Biol. 21, 68.

Wang, H., Jiao, X., Kong, X., Hamera, S., Wu, Y., Chen, X., Fang, R. et al. (2016) A signaling cascade from miR444 to RDR1 in rice antiviral RNA silencing pathway. Plant Physiol. 170, 2365–2377.

Wang, J., Yu, W., Yang, Y., Li, X., Chen, T., Liu, T., Ma, N. et al. (2015) Genome‐wide analysis of tomato long non‐coding RNAs and identification as endogenous target mimic for microRNA in response to TYLCV infection. Sci. Rep. 5, 16946.

Wang, L., Li, J., Guo, B., Xu, L., Li, L., Song, X., Wang, X. et al. (2022) Exonic circular RNAs are involved in arabidopsis immune response against bacterial and fungal pathogens and function synergistically with corresponding linear RNAs. Phytopathology 112, 608–619.

Wang, L., Yu, X., Wang, H., Lu, Y.‐Z., de Ruiter, M., Prins, M. and He, Y.‐K. (2011a) A novel class of heat‐responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa). BMC Genomics 12, 289.

Wang, M. and Dean, R.A. (2020) Movement of small RNAs in and between plants and fungi. Mol. Plant Pathol. 21, 589–601.

Wang, M., Guo, W., Li, J., Pan, X., Pan, L., Zhao, J., Zhang, Y. et al. (2021b) The miR528‐AO module confers enhanced salt tolerance in rice by modulating the ascorbic acid and abscisic acid metabolism and ROS scavenging. J. Agric. Food Chem. 69, 8634–8648.

Wang, M., Wang, Q. and Zhang, B. (2013b) Response of miRNAs and their targets to salt and drought stresses in cotton (Gossypium hirsutum L.). Gene 530, 26–32.

Wang, S., Sun, X., Hoshino, Y., Yu, Y., Jia, B., Sun, Z., Sun, M. et al. (2014b) MicroRNA319 positively regulates cold tolerance by targeting OsPCF6 and OsTCP21 in rice (Oryza sativa L.). PLoS One 9, e91357.

Wang, T., Chen, L., Zhao, M., Tian, Q. and Zhang, W.‐H. (2011b) Identification of drought‐responsive microRNAs in Medicago truncatula by genome‐wide high‐throughput sequencing. BMC Genomics 12, 367.

Wang, Y., Sun, F., Cao, H., Peng, H., Ni, Z., Sun, Q. and Yao, Y. (2012) TamiR159 directed wheat TaGAMYB cleavage and its involvement in anther development and heat response. PLoS One 7, e48445.

Wang, Y.‐G., An, M., Zhou, S.‐F., She, Y.‐H., Li, W.‐C. and Fu, F.‐L. (2014c) Expression profile of maize MicroRNAs corresponding to their target genes under drought stress. Biochem. Genet. 52, 474–493.

Wen, F.L., Yue, Y., He, T.F., Gao, X.M., Zhou, Z.S. and Long, X.H. (2020) Identification of miR390‐TAS3‐ARF pathway in response to salt stress in Helianthus tuberosus L. Gene 738, 144460.

Wierzbicki, A.T., Blevins, T. and Swiezewski, S. (2021) Long noncoding RNAs in plants. Annu. Rev. Plant Biol. 72, 245–271.

Wilusz, J.E. and Sharp, P.A. (2013) A Circuitous Route to Noncoding RNA. Science 340, 440–441.

Wu, F., Shu, J. and Jin, W. (2014) Identification and validation of miRNAs associated with the resistance of maize (Zea mays L.) to Exserohilum turcicum. PLoS One 9, e87251.

Wu, J., Yang, R., Yang, Z., Yao, S., Zhao, S., Wang, Y., Li, P. et al. (2017) ROS accumulation and antiviral defence control by microRNA528 in rice. Nature Plants 3, 1–7.

Xia, K., Wang, R., Ou, X., Fang, Z., Tian, C., Duan, J., Wang, Y. et al. (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One 7, e30039.

Xiang, L., Cai, C., Cheng, J., Wang, L., Wu, C., Shi, Y., Luo, J. et al. (2018) Identification of circularRNAs and their targets in Gossypium under Verticillium wilt stress based on RNA‐seq. PeerJ 6, e4500.

Xie, F., Stewart, C.N., Taki, F.A., He, Q., Liu, H. and Zhang, B. (2014) High‐throughput deep sequencing shows that microRNAs play important roles in switchgrass responses to drought and salinity stress. Plant Biotechnol. J. 12, 354–366.

Xie, F., Wang, Q., Sun, R. and Zhang, B. (2015) Deep sequencing reveals important roles of microRNAs in response to drought and salinity stress in cotton. J. Exp. Bot. 66, 789–804.

Xie, S., Li, H., Lu, J., Li, J., Song, Z. and Jiang, H. (2024) A novel member of miR169 family negatively regulates maize resistance against Bipolaris maydis. Plant Disease 108, 3518–3526.

Xin, C., Teng, C., Xin, C.H.Y., Teng, C.C., Samad, A.F.A. and Samad, A. (2023) Identification and evaluation of regulatory role of miR164b in Malaysian rice variety (MR303) under drought stress. J. Trop. Life Sci. 13, 399–406.

Xin, M., Wang, Y., Yao, Y., Song, N., Hu, Z., Qin, D., Xie, C. et al. (2011) Identification and characterization of wheat long non‐protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol. 11, 61.

Xin, M., Wang, Y., Yao, Y., Xie, C., Peng, H., Ni, Z. and Sun, Q. (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol. 10, 123.

Xing, L., Zhang, L., Zheng, H., Zhang, Z., Luo, Y., Liu, Y. and Wang, L. (2023) ZmmiR169q/ZmNF‐YA8 is a module that homeostatically regulates primary root growth and salt tolerance in maize. Front. Plant Sci. 14, 1163228. https://doi.org/10.3389/fpls.2023.1163228

Xu, C., Huang, X., Ma, N., Liu, Y., Xu, A., Zhang, X., Li, D. et al. (2024) MicroRNA164 affects plant responses to UV radiation in perennial ryegrass. Plan. Theory 13, 1242.

Xu, W., Meng, Y. and Wise, R.P. (2014) Mla‐ and Rom1‐mediated control of microRNA398 and chloroplast copper/zinc superoxide dismutase regulates cell death in response to the barley powdery mildew fungus. New Phytol. 201, 1396–1412.

Xue, M. and Yi, H. (2018) Enhanced Arabidopsis disease resistance against Botrytis cinerea induced by sulfur dioxide. Ecotoxicol. Environ. Saf. 147, 523–529.

Yadav, A., Mathan, J., Dubey, A.K. and Singh, A. (2024) The emerging role of non‐coding RNAs (ncRNAs) in plant growth, development, and stress response signaling. Non‐Coding RNA 10, 13.

Yan, G., Hua, Y., Jin, H., Huang, Q., Zhou, G., Xu, Y., He, Y. et al. (2023a) Sly‐miR398 participates in cadmium stress acclimation by regulating antioxidant system and cadmium transport in tomato (Solanum lycopersicum). Int. J. Mol. Sci. 24, 1953.

Yan, J., Qiu, R., Wang, K., Liu, Y. and Zhang, W. (2023b) Enhancing alfalfa resistance to Spodoptera herbivory by sequestering microRNA396 expression. Plant Cell Rep. 42, 805–819.

Yang, C., Li, D., Mao, D., Liu, X., Ji, C., Li, X., Zhao, X. et al. (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Ryza sativa L.). Plant Cell Environ. 36, 2207–2218.

Yang, F., Zhao, D., Fan, H., Zhu, X., Wang, Y., Liu, X., Duan, Y. et al. (2020) Functional analysis of long non‐coding RNAs reveal their novel roles in biocontrol of bacteria‐induced tomato resistance to Meloidogyne incognita. Int. J. Mol. Sci. 21, 911.

Yang, J., Zhang, N., Bai, J., Duan, X., Zhang, L., Liu, S., Tang, X. et al. (2022) Stu‐miR827‐targeted StWRKY48 transcription factor negatively regulates drought tolerance of potato by increasing leaf stomatal density. Int. J. Mol. Sci. 23, 14805.

Yang, Y., Xu, L., Hao, C., Wan, M., Tao, Y., Zhuang, Y., Su, Y. et al. (2024) The microRNA408‐plantacyanin module balances plant growth and drought resistance by regulating reactive oxygen species homeostasis in guard cells. Plant Cell 36, 4338–4355.

Yao, S., Yang, Z., Yang, R., Huang, Y., Guo, G., Kong, X., Lan, Y. et al. (2019) Transcriptional regulation of miR528 by OsSPL9 orchestrates antiviral response in rice. Mol. Plant 12, 1114–1122.

Yao, Y., Ni, Z., Peng, H., Sun, F., Xin, M., Sunkar, R., Zhu, J.K. et al. (2010) Non‐coding small RNAs responsive to abiotic stress in wheat (Triticum aestivum L.). Funct. Integr. Genomics 10, 187–190.

Ye, C.‐Y., Zhang, X., Chu, Q., Liu, C., Yu, Y., Jiang, W., Zhu, Q.‐H. et al. (2017) Full‐length sequence assembly reveals circular RNAs with diverse non‐GT/AG splicing signals in rice. RNA Biol. 14, 1055–1063.

Ye, Y., Wang, J., Wang, W. and Xu, L.‐A. (2020) ARF family identification in Tamarix chinensis reveals the salt responsive expression of TcARF6 targeted by miR167. PeerJ 8, e8829.

Yin, X., Wang, J., Cheng, H., Wang, X. and Yu, D. (2013) Detection and evolutionary analysis of soybean miRNAs responsive to soybean mosaic virus. Planta 237, 1213–1225.

Yin, Z., Li, Y., Yu, J., Liu, Y., Li, C., Han, X. and Shen, F. (2012) Difference in miRNA expression profiles between two cotton cultivars with distinct salt sensitivity. Mol. Biol. Rep. 39, 4961–4970.

Yu, X., Hou, Y., Chen, W., Wang, S., Wang, P. and Qu, S. (2017) Malus hupehensis miR168 Targets to ARGONAUTE1 and contributes to the resistance against Botryosphaeria dothidea infection by altering defense responses. Plant Cell Physiol. 58, 1541–1557.

Yuan, N., Yuan, S., Li, Z., Li, D., Hu, Q. and Luo, H. (2016) Heterologous expression of a rice miR395 gene in Nicotiana tabacum impairs sulfate homeostasis. Sci. Rep. 6, 28791.

Yuan, S., Li, Z., Li, D., Yuan, N., Hu, Q. and Luo, H. (2015) Constitutive expression of rice MicroRNA528 alters plant development and enhances tolerance to salinity stress and nitrogen starvation in creeping bentgrass. Plant Physiol. 169, 576–593.

Yuan, S., Zhao, J., Li, Z., Hu, Q., Yuan, N., Zhou, M., Xia, X. et al. (2019a) MicroRNA396‐mediated alteration in plant development and salinity stress response in creeping bentgrass. Horticulture Res. 6, 48.

Yuan, W., Suo, J., Shi, B., Zhou, C., Bai, B., Bian, H., Zhu, M. et al. (2019b) The barley miR393 has multiple roles in regulation of seedling growth, stomatal density, and drought stress tolerance. Plant Physiol. Biochem. 142, 303–311.

Yue, E., Cao, H. and Liu, B. (2020) OsmiR535, a potential genetic editing target for drought and salinity stress tolerance in Oryza sativa. Plan. Theory 9, 1337.

Yue, E., Rong, F., Liu, Z., Ruan, S., Lu, T. and Qian, H. (2023) Cadmium induced a non‐coding RNA microRNA535 mediates Cd accumulation in rice. J. Environ. Sci. 130, 149–162.

Zandalinas, S.I., Fritschi, F.B. and Mittler, R. (2021) Global warming, climate change, and environmental pollution: recipe for a multifactorial stress combination disaster. Trends Plant Sci. 26, 588–599.

Zeeshan, M., Qiu, C.‐W., Naz, S., Cao, F. and Wu, F. (2021) Genome‐wide discovery of miRNAs with differential expression patterns in responses to salinity in the two contrasting wheat cultivars. Int. J. Mol. Sci. 22, 12556.

Zeng, J., Ye, Z., He, X. and Zhang, G. (2019) Identification of microRNAs and their targets responding to low‐potassium stress in two barley genotypes differing in low‐K tolerance. J. Plant Physiol. 234, 234–235.

Zhan, J. and Meyers, B.C. (2023) Plant small RNAs: their biogenesis, regulatory roles, and functions. Annu. Rev. Plant Biol. 74, 21–51.

Zhang, B. (2015) MicroRNA: A new target for improving plant tolerance to abiotic stress. J. Exp. Bot. 66, 1749–1761.

Zhang, H., Zhu, J., Gong, Z. and Zhu, J.‐K. (2022a) Abiotic stress responses in plants. Nat. Rev. Genet. 23, 104–119.

Zhang, J., Zhou, Z., Bai, J., Tao, X., Wang, L., Zhang, H. and Zhu, J.‐K. (2020a) Disruption of MIR396e and MIR396f improves rice yield under nitrogen‐deficient conditions. Natl. Sci. Rev. 7, 102–112.

Zhang, L., Ding, H., Jiang, H., Wang, H., Chen, K., Duan, J., Feng, S. et al. (2020b) Regulation of cadmium tolerance and accumulation by miR156 in Arabidopsis. Chemosphere 242, 125168.

Zhang, L., Wang, M., Li, N., Wang, H., Qiu, P., Pei, L., Xu, Z. et al. (2018) Long noncoding RNAs involve in resistance to Verticillium dahliae, a fungal disease in cotton. Plant Biotechnol. J. 16, 1172–1185.

Zhang, L.‐L., Huang, Y.‐Y., Zheng, Y.‐P., Liu, X.‐X., Zhou, S.‐X., Yang, X.‐M., Liu, S.‐L. et al. (2022b) Osa‐miR535 targets SQUAMOSA promoter binding protein‐like 4 to regulate blast disease resistance in rice. Plant J. 110, 166–178.

Zhang, L.‐L., Li, Y., Zheng, Y.‐P., Wang, H., Yang, X., Chen, J.‐F., Zhou, S.‐X. et al. (2020c) Expressing a target mimic of miR156fhl‐3p enhances rice blast disease resistance without yield penalty by improving SPL14 expression. Front. Genet. 11, 327.

Zhang, L.W., Song, J.B., Shu, X.X., Zhang, Y. and Yang, Z.M. (2013) miR395 is involved in detoxification of cadmium in Brassica napus. J. Hazard. Mater. 250, 204–211.

Zhang, P., Li, S. and Chen, M. (2020d) Characterization and function of circular RNAs in Plants. Front. Mol. Biosci. 7, 91. https://doi.org/10.3389/fmolb.2020.00091

Zhang, Q., Li, Y., Zhang, Y., Wu, C., Wang, S., Hao, L., Wang, S. et al. (2017) Md‐miR156ab and Md‐miR395 target WRKY transcription factors to influence apple resistance to leaf spot disease. Front. Plant Sci. 8, 526. https://doi.org/10.3389/fpls.2017.00526

Zhang, T., Zhao, Y.‐L., Zhao, J.‐H., Wang, S., Jin, Y., Chen, Z.‐Q., Fang, Y.‐Y. et al. (2016) Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nature Plants 2, 16153.

Zhang, W., Gao, S., Zhou, X., Chellappan, P., Chen, Z., Zhou, X., Zhang, X. et al. (2011a) Bacteria‐responsive microRNAs regulate plant innate immunity by modulating plant hormone networks. Plant Mol. Biol. 75, 93–105.

Zhang, X., Dong, J., Deng, F., Wang, W., Cheng, Y., Song, L., Hu, M. et al. (2019) The long non‐coding RNA lncRNA973 is involved in cotton response to salt stress. BMC Plant Biol. 19, 459.

Zhang, X., Xia, J., Lii, Y.E., Barrera‐Figueroa, B.E., Zhou, X., Gao, S., Lu, L. et al. (2012) Genome‐wide analysis of plant nat‐siRNAs reveals insights into their distribution, biogenesis and function. Genome Biol. 13, R20.

Zhang, X., Zhao, H., Gao, S., Wang, W.‐C., Katiyar‐Agarwal, S., Huang, H.‐D., Raikhel, N. et al. (2011b) Arabidopsis argonaute 2 regulates innate immunity via miRNA393*−mediated silencing of a golgi‐localized SNARE gene, MEMB12. Mol. Cell 42, 356–366.

Zhang, X., Zou, Z., Gong, P., Zhang, J., Ziaf, K., Li, H., Xiao, F. et al. (2011c) Over‐expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol. Lett. 33, 403–409.

Zhang, Z., Fu, Z., Chen, W., Wang, L., Zhao, S., Yuanyuan, E., Zhang, H. et al. (2024) Salt stress induces complicated miRNA responses of sugar beet (Beta vulgaris L.). Sugar Tech 26, 1297–1305.

Zhao, B., Ge, L., Liang, R., Li, W., Ruan, K., Lin, H. and Jin, Y. (2009) Members of miR‐169 family are induced by high salinity and transiently inhibit the NF‐YA transcription factor. BMC Mol. Biol. 10, 29.

Zhao, J., Shi, M., Yu, J. and Guo, C. (2022) SPL9 mediates freezing tolerance by directly regulating the expression of CBF2 in Arabidopsis thaliana. BMC Plant Biol. 22, 59.

Zhao, J., Yuan, S., Zhou, M., Yuan, N., Li, Z., Hu, Q., Bethea, F.G. et al. (2019) Transgenic creeping bentgrass overexpressing Osa‐miR393a exhibits altered plant development and improved multiple stress tolerance. Plant Biotechnol. J. 17, 233–251.

Zhao, J.‐P., Jiang, X.‐L., Zhang, B.‐Y. and Su, X.‐H. (2012) Involvement of microRNA‐mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS One 7, e44968.

Zhao, M., Ding, H., Zhu, J.‐K., Zhang, F. and Li, W.‐X. (2011) Involvement of miR169 in the nitrogen‐starvation responses in Arabidopsis. New Phytol. 190, 906–915.

Zhao, M., Wang, T., Sun, T., Yu, X., Tian, R. and Zhang, W.‐H. (2020) Identification of tissue‐specific and cold‐responsive lncRNAs in Medicago truncatula by high‐throughput RNA sequencing. BMC Plant Biol. 20, 99.

Zhao, W., Li, Z., Fan, J., Hu, C., Yang, R., Qi, X., Chen, H. et al. (2015) Identification of jasmonic acid‐associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root‐knot nematode stress in tomato. J. Exp. Bot. 66, 4653–4667.

Zhao, Z., Yang, Y., Iqbal, A., Wu, Q. and Zhou, L. (2024) Biological insights and recent advances in plant long non‐coding RNA. Int. J. Mol. Sci. 25, 11964.

Zheng, Z., Wang, N., Jalajakumari, M., Blackman, L., Shen, E., Verma, S., Wang, M.‐B. et al. (2020) miR159 represses a constitutive pathogen defense response in tobacco. Plant Physiol. 182, 2182–2198.

Zhou, C., Zhu, J., Qian, N., Guo, J. and Yan, C. (2021) Bacillus subtilis SL18r induces tomato resistance against botrytis cinerea, involving activation of long non‐coding RNA, MSTRG18363, to Decoy miR1918. Front. Plant Sci. 8, 634819. https://doi.org/10.3389/fpls.2020.634819

Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M. and Luo, L. (2010) Genome‐wide identification and analysis of drought‐responsive microRNAs in Oryza sativa. J. Exp. Bot. 61, 4157–4168.

Zhou, M., Li, D., Li, Z., Hu, Q., Yang, C., Zhu, L. and Luo, H. (2013) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiol. 161, 1375–1391.

Zhou, M. and Tang, W. (2019) MicroRNA156 amplifies transcription factor‐associated cold stress tolerance in plant cells. Mol. Genet. Genomics 294, 379–393.

Zhou, X., Wang, G. and Zhang, W. (2007) UV‐B responsive microRNA genes in Arabidopsis thaliana. Mol. Syst. Biol. 3, 103.

Zhu, C., Yuan, T., Yang, K., Liu, Y., Li, Y. and Gao, Z. (2023) Identification and characterization of CircRNA‐associated CeRNA networks in moso bamboo under nitrogen stress. BMC Plant Biol. 23, 142.

Zhu, H., Chen, C., Zeng, J., Yun, Z., Liu, Y., Qu, H., Jiang, Y. et al. (2020) MicroRNA528, a hub regulator modulating ROS homeostasis via targeting of a diverse set of genes encoding copper‐containing proteins in monocots. New Phytol. 225, 385–399.

Zhu, H., Zhang, Y., Tang, R., Qu, H., Duan, X. and Jiang, Y. (2019a) Banana sRNAome and degradome identify microRNAs functioning in differential responses to temperature stress. BMC Genomics 20, 33.

Zhu, L., Ow, D.W. and Dong, Z. (2018) Transfer RNA‐derived small RNAs in plants. Sci. China Life Sci. 61, 155–161.

Zhu, Q.‐H., Stephen, S., Taylor, J., Helliwell, C.A. and Wang, M.‐B. (2014) Long noncoding RNAs responsive to usarium oxysporum infection in Arabidopsis thaliana. New Phytol. 201, 574–584.

Zhu, Y.‐X., Jia, J.‐H., Yang, L., Xia, Y.‐C., Zhang, H.‐L., Jia, J.‐B., Zhou, R. et al. (2019b) Identification of cucumber circular RNAs responsive to salt stress. BMC Plant Biol. 19, 164.

Zhuang, Y., Zhou, X.‐H. and Liu, J. (2014) Conserved miRNAs and their response to salt stress in wild eggplant Solanum linnaeanum roots. Int. J. Mol. Sci. 15, 839–849.

Zuo, J., Wang, Q., Zhu, B., Luo, Y. and Gao, L. (2016) Deciphering the roles of circRNAs on chilling injury in tomato. Biochem. Biophys. Res. Commun. 479, 132–138.

Word count: 34990

Show less

© 2025. This work is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.

Non‐coding RNAs in plant stress responses: molecular insights and agricultural applications

Content area

Abstract

Full text