Recent omics progress in nanobiotechnology for plant abiotic stress tolerance improvement

Abstract

Use of nanomaterials (NMs) to improve plant abiotic stress tolerance (AST) is a hot topic in NM-enabled agriculture. Previous studies mainly focused on the physiological and biochemical responses of plants treated with NMs under abiotic stress. To use NMs for improving plant AST, it is necessary to understand how they act on this tolerance at the omics and epigenetics levels. In this review, we summarized the knowledge of NM-improved abiotic stress tolerance in relation to omics (such as metabolic, transcriptomic, proteomic, and microRNA), DNA methylation, and histone modifications. Overall, NMs can improve plant abiotic stress tolerance through the modulation at omics and epigenetics levels.

Headnote

ABSTRACT

Use of nanomaterials (NMs) to improve plant abiotic stress tolerance (AST) is a hot topic in NM-enabled agriculture. Previous studies mainly focused on the physiological and biochemical responses of plants treated with NMs under abiotic stress. To use NMs for improving plant AST, it is necessary to understand how they act on this tolerance at the omics and epigenetics levels. In this review, we summarized the knowledge of NM-improved abiotic stress tolerance in relation to omics (such as metabolic, transcriptomic, proteomic, and microRNA), DNA methylation, and histone modifications. Overall, NMs can improve plant abiotic stress tolerance through the modulation at omics and epigenetics levels.

Keywords:

Nanomaterials

Omics

Molecular mechanisms

Epigenetics

DNA methylation

Histone modification

(ProQuest: ... denotes formulae omitted.)

1. Introduction

Abiotic stresses such as high temperature, drought, waterlogged conditions, or salinity threaten agricultural production. Many approaches including breeding and practical management have been adopted to address these threats. Nanobiotechnology has been used to improve plant AST and is widely used in agriculture [1,2]. Nanomaterials (NMs) are materials at least with one dimension in the range of 1–100 nm [3]. NMs can be used as nanofertilizers, nanoregulators and nanopesticides to increase crop yield and growth under abiotic stresses [4,5]. They maintain plant nutrient use efficiency, regulate osmolytes, activate antioxidant defense mechanisms, and improve photosynthesis and phytohormone biosynthesis [6–8]. Our knowledge of NM effects on plant AST at the omics and epigenetics level is limited (Fig. 1).

Epigenetics is the study of heritable changes in gene expression that occur without changes in the nucleotide sequence. Known epigenetic mechanisms include DNA methylation, histone modifications, non-coding RNA expression, and RNA degradation [9]. NMs have been shown to change the epigenetic mechanisms of plants [10]. However, our understanding of the potential impacts of NMs on plant epigenetics remains limited. Future studies need to elucidate the mechanisms by which nanotechnology affects plant epigenetics. The results of NMs inducing epigenetic changes suggest that NMs may act as exogenous chemicals that stimulate plant-related epigenetics processes, influencing gene expression. The epigenetic effects of NMs may be passed on to the next generation. Therefore, nanotechnology has great potential for improving plant tolerance to abiotic stress through epigenetic modification and regulation.

In this review, we focus on the effects of nanoparticles (NPs) in improving plant AST, examining the secondary metabolome, transcriptome, proteome, miRNA, and genetics. We summarize the omics responses and epigenetic effects of the interactions between NPs and plants under abiotic stress. To better explain how NMs improve plant AST, we emphasize combining multiple omics approaches.

2. Effects of nanoparticles on plant abiotic stress tolerance

2.1. A view at the metabolic and phytohormones levels

NMs can induce metabolic changes in terms of plant stress responses. By characterizing the metabolic profiles of plants under stress conditions, researchers can identify metabolites that respond to stress conditions and the pathways associated with stress tolerance mechanisms [11]. Distinct metabolic profiles are described in plants under stress due to the resetting of primary and secondary metabolism [12]. The application of NMs in plants can affect their physiological behavior by modulating intermediate metabolic pathways. NMs in plants adjusted carbohydrate metabolism by affecting the photosynthesis or respiratory rate [13]. NMs may also affect nitrogen metabolism via amino acid metabolism or protein degradation. These changes can affect plant growth and development under abiotic stress conditions [14].

The application of NMs affects both primary and secondary metabolites in plants, thereby improving stress tolerance. Primary metabolites include amino acids, soluble sugars, and proteins, while secondary metabolites include terpenoids, phenols, flavonoids, nitrogen-containing compounds, and phytohormones. Seeds treated with ZnNP (40 mg L-1 ) exhibited improved salt resistance by inducing the accumulation of proline, sugar solubility, total protein solubility, and free amino acid formation [15]. Fe3O4 (20 nm, 50 mg L-1 ) or ZnO-NPs (30 nm, 50 mg L-1 ) increased tobacco growth under Cd stress, modulating the biosynthesis of amino acids, nicotinate, nicotinamide metabolism, arginine, and proline metabolism, and flavone [16]. Foliar applied nanozyme Mn3O4NPs (8.9 nm, -7.70 mV, 1 mg plant1 ) stimulated endogenous antioxidant system and increased cucumber salt stress resistance through the shikimic acid and phenylpropanoid pathways [17]. TiO2-NPs (5 nm, 10 mg L-1 ) affected the metabolism of flavonoids in Arabidopsis thaliana under UV-B stress [18]. The multifunctionality of NMs has great potential in agricultural applications. MoS2-NPs (106.8 nm, 10 mg kg-1 ) increased the long-term biological fixation of nitrogen in soybean by sustaining the release of Mo andprotecting nodules from active ROS stress [19]. However, whether or not the plant is under stress, induction of flavonoid metabolism is commonly observed in plants treated with Zn NPs, TiO2 NPs, Se20 NPs, Mn3O4 NPs, CeO2 NPs, AgAu NPs and AuCu NPs [20–23]. Flavonoids are antioxidant metabolites in plants. Induction of flavonoid metabolism by NMs could thus improve a plant's ability to combat oxidative stress.

NMs can affect the levels of phytohormones and even interact with them in response to stress. Selenium NPs (0.2 mg L-1 ) increased Capsicum annuum tolerance to Cd by inducing biosynthesis of hormones: brassinosteroids (BRs), abscisic acid (ABA), and jasmonic acid (JA) [24]. Iron oxide NP (Fe2O3) treatment increase Cd stress tolerance in rice, in association with upregulation of ABA, IAA (indole-3-acetic acid), GA4 (gibberellin A4), and BR [25]. Variations in plant hormone responses to NMs across plant parts were demonstrated in Arabidopsis thaliana exposed to ZnO-NPs (30 nm, 100 mg L-1 ). This exposure resulted in increased salicylic acid (SA) content in leaves and roots, while simultaneously suppressing JA synthesis in both tissues [26]. High concentrations of NPs can impair plant growth by altering plant hormone levels. Mesoporous carbon nanoparticles (MCNs, 150 nm, 150 mg L-1 ) resulted in over 29% decrease in shoot length, while the concentrations of BR, IPA (indole propionic acid), and DHZR (dihydrozeatinriboside) in rice shoot were increased [27]. The influence of NMs on plant secondary metabolites and phytohormones cannot be simply explained by a single mode. Induction depends on size, morphology, concentration of NMs, plant species, and other factors.

2.2. A view at the transcriptional level

The transcriptome is an effective tool to identify genes and pathways involved in increasing plant stress tolerance. RNA sequencing is a technique that can be utilized to assess the expression levels of plant genes. It can comprehensively characterize the transcriptional response of plants to external stress. Not surprisingly, transcriptome technology has also been widely used to analyze the mechanisms involved in NMs enabled plant stress tolerance. AgNPs (50–100 nm, 20 mg L-1 ) increased pearl millet salt tolerance by modulating the expression level of genes involved in MAPK signaling, biosynthesis of secondary metabolites, and hormonal signal transduction [28]. The polyhydroxy fullerene-fuller (50 mg L-1 ) increased rapeseed drought tolerance by affecting the pathways of carbohydrate metabolism, amino acid metabolism, and secondary metabolite metabolism [29]. In addition to modulating osmotic level and endogenous hormone levels, CeO2-NPs (50 mg L-1 ) increased Medicago sativa seed salt seed stress tolerance by regulating genes involved in plant hormone synthesis [30].

At the transcriptional level, NMs consistently modulate the expression levels of genes involved in photosynthesis and the response to oxidative stress [31–35]. Up-regulation of FerredoxinNADP reductase (PetH) and down-regulation of photosystem II lipoprotein (Psb27) were found in pak choi treated with CeO2-NPs (0.7 mg kg-1 , 24.4 nm) [33]. AgNPs stimulated ROS-activated stress signaling pathways by modulating stress-responsive kinases, hormones, and transcription factors [34]. Zn-NPs (30 nm, 15 mg L-1 ) also upregulated genes associated with photosynthesis and oxidative stress in Brassica napus, in agreement with proteomic results [35]. In future, more efforts need to be made to investigate differences in NM's effects on plant tissues at the transcriptional level. Understanding the transcriptomic results together with other omics data can help us to better understand the mechanisms by which NMs improve plant stress tolerance.

2.3. A view at the proteomic level

Proteins are the executors of plant physiological functions [36]. However, our knowledge about how NMs improve plant stress tolerance at the protein level is insufficient. NMs affect plant protein content [37–39]. BSAg-NPs (16 nm, 10 mg L-1 , biosynthesized) increased the biomass of soybean seedlings compared to CSAg-NPs (15 nm, 10 mg L-1 , chemically synthesized) treatment. Accumulation of proteins related to protein degradation and ATP content increased under BSAg-NPs treatment [36]. Rice plants treated with Ag-NPs (18.34 nm, 30 lg L-1 ) showed an abundance of proteins associated with the oxidative stress tolerance, Ca2+ regulation and signaling [38]. Fiber-ZnO NPs (fiber cross-linked with ZnO-NPs, 200 nm, 10 mg L-1 ) increased plant resistance by increasing the content of proteins, such as NADPH oxidoreductase [39].

NMs can also modulate protein levels to improve plant stress tolerance. We take flooding stress as an example. Ag-NPs (15 nm, 5 mg L-1 ) reduce the negative effects of flooding on soybeans by regulating the proteins associated with amino acid synthesis and wax formation [40]. Al2O3-NPs (30–60 nm, 50 mg L-1 ) treated soybean plants under flooding conditions showed changes in protein abundance, which are related to protein synthesis and cell walls [41]. Soybean plants treated with Al2O3-NPs contained more S-adenosyl-L-methionine dependent methyltransferases than a control group under flooding. This indicates that Al2O3-NPs may affect the levels of DNA methylation, ethylene metabolism, or glutathione synthesis by activating S-adenosyl-L-methionine. Al2O3 promoted soybean growth under flooding by affecting protein levels of energy metabolism and cell death [42]. Ag-NPs (15 nm, 5 mg L-1 ) have positive effects on soybean seedlings during flooding by regulating the protein quality control for misfolded proteins in the endoplasmic reticulum, [43]. Overall, it is clear that the modulation of NMs on proteins functions in plant stress response. However, to date, progress on elucidating how NMs increase plant stress tolerance at the proteomic level does not meet expectations [44,45]. In a proteomic study, Cu-NPs (15–30 nm, mg L-1 ) enhance increased the stress resistance of wheat by regulating the process of starch degradation, glycolysis and tricarboxylic acid cycle in high-yielding wheat, compared with drought- and salttolerant wheat [44]. Future studies should further investigate the influence of NMs' properties such as size, zeta potential, and morphology on protein levels in plants under stress conditions.

2.4. A view at the microRNA level

Emerging evidences suggest that miRNAs are involved in NM-improved plant AST. MicroRNAs (miRNAs) are essential participants in the post-transcriptional regulation of gene expression in plants [46]. miRNAs regulate plant development, including leaf and root development, as well as abiotic stress responses, by altering gene expression [47]. However, to date, our knowledge about how miRNAs are involved in NM-enabled plant stress tolerance is insufficient. Only a few studies have been conducted at the miRNA level to investigate how NMs can improve plant stress tolerance. Se-NPs (10–40 nm, 4 mg L-1 ) treated tomato seedlings modulated transcriptional changes of miR172, leading to an increase in drought tolerance [48]. ZnO-NPs (10–30 nm; 10 mg L-1 ) upregulated the expression of miR171 and miR156, leading to an increased number of wheat spikelets and seed weight [49]. miRNAs may alleviate the negative impacts of the inappropriate application of NMs [50,51]. High levels of TiO2-NPs (0.1, 0.5, 1.0, 2.5 mg L-1 ) negatively impaired the growth and development of switchgrass (Panicum virgatum) seedlings, leading to an increase in the expression of miR390 and miR399. These miRNAs may be involved in regulating the resistance of tobacco to TiO2-NP stress [50]. Thus, miRNAs can alleviate the negative effects of NPs on plants, further suggesting that these miRNAs could be effective targets for NM-enabled agriculture.

2.5. Nanoparticles and epigenetic regulation: a view from DNA methylation and histone modification

DNA methylation and histone modification are conserved epigenetic modifications that mediate plant stress responses by inhibiting or activating gene expression. NMs can change DNA methylation levels in animals and humans [52,53]. However, to date, studies about the impact of NMs on DNA methylation levels under plant AST is relatively rare. DNA methylation increased in Lepidium sativum exposed to CuO-NPs (5 and 10 mg L-1 ) [54]. Application of NiO-NP (50–500 mg L1 ) increased the rate of DNA polymorphism and DNA methylation in Allium cepa roots and BY-2 callus of tobacco, indicating that these NMs can induce epigenetic changes in plants [55]. CNTs (carbon nanotubes) promoted rice root growth by affecting the histone acetylation and methylation statuses in the local promoter region of the CullinRING ligases 1 (CRL1) gene, boosting the expression of CRL1 [56]. Most studies have focused on the relationship between DNA methylation and NM induced plant toxicity, due primarily to high doses or larger particle sizes [57–59]. nSe-NPs (10–45 nm) at concentration of 10 and 30 mg L-1 caused DNA hypermethylation, reducing the growth of C. annuum [56].

Histone modification is part of the epigenetic regulatory system [60]. In maize, SWCNTs (single wall CNTs, OD 1–2 nm, length 30 nm, 20 mg L-1 ) blocked total histone acetylation during seed germination. This led to global deacetylation of histone H3, and thus inhibited root hair growth [61]. Expression of histone deacetylase 3 genes was upregulated in Datura stramonium seedlings exposed to ZnO-NPs (10–30 nm, -26 mV, 100, 500 mg L-1 ) [62]. Application of Quercetin-Loaded Silicon-Stabilized Hybrid Lipid NP (sshLNP) (>100 nm, -31 to 34.6 mV) up-regulated the histone-lysine N-methyltransferase activity gene and improved salt tolerance of tomatoes [63], indicating epigenetic modification caused by ZnO-NPs. These studies suggest that NMs may remodel the transcription program to confer stress tolerance in plants. Future studies of NM-improved plant stress tolerance should be conducted at the epigenetics level. A systematic assessment of the interaction between epigenetic modifications and NM-improved plant stress tolerance is needed.

Studying the key genes involved in NMs improved plant stress tolerance is important for NM-enabled agriculture. PNC (9.9 nm, 31.0 mV) improved cucumber salt tolerance. Gene expression data from knockout CsAKT1 cucumber (CRISPR-Cas9 lines) showed that the K+ transporter 1(AKT1) improves K+ maintenance and CsAKT1 is a key responsive gene for PNC improved cucumber salt tolerance [64]. NPs with over-size or high doses, always show negative effects on plants, especially when applied to roots and seeds. The negative effects of improperly applied NMs on plants are associated mainly with DNA damage, reduction of the abundance of photosynthesis proteins, modulation of miRNA and hypermethylation, and reduction of secondary metabolism (Fig. 2). Explaining these mechanisms is crucial for minimizing the potential negative effects of NMs on plants and for better understanding and designing NMs for agricultural use.

However, NMs may pose risks, especially at high concentrations [65]. High doses of NPs may cause toxic reactions in plants and humans [66]. Widespread application of NMs will lead to their continued release into the environment. NMs may enter the food chain through plants [67,68]. Minimizing the possible negative effect or biosafety concern of NMs is important for the sustainable development of NM-enabled agriculture. Among the main factors for NMs enabled agriculture, the design and use of environmentally friendly NMs should be the primary criterion. Then, the low cost and optimal dose of NMs for agricultural application should be considered. Optimizing the combination between the use of NMs (dose, application times, plant stage for application) and crop cultivation (sowing date, plant density, water and nutrient supply) also can reduce the amount of NMs used in agriculture. Use of NMs with controlled properties (free of toxic elements) and proper application mode (with optimized dose and application times) could largely remove the concerns for its biosafety in agriculture and ecological environments.

3. Conclusions and perspectives

Insufficient knowledge about the multi-omics mechanisms underlying NMs improved plant AST impedes the progress of designing and thus use of NMs in agricultural practices. We hope that with a better understanding of NMs and improved plant stress tolerance at the multi-omics level, the use or adoption of NMs in agriculture for improving crop AST can be accelerated. Plants are constantly exposed to multiple/combined stresses in field conditions. Comparing the mechanisms of NM-improved plant tolerance between single and combined stress levels could benefit the development of NM-enabled agriculture (Fig. 3).

CRediT authorship contribution statement

Lingling Chen: Conceptualization, Writing – original draft. Lan Zhu: Data curation, Writing – original draft, Writing – review & editing. Xiaohui Liu: Data curation, Funding acquisition, Writing – original draft. Lu Chen: Writing – review & editing. Han Zhou: Data curation. Huixin Ma: Data curation. Guilan Sun: Data curation. Ashadu Nyande: Writing – review & editing. Zhaohu Li: Conceptualization. Honghong Wu: Conceptualization, Funding acquisition, Writing – original draft.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was supported by National Key Research and Development Program of China (2022YFD2300205), the National Natural Science Foundation of China (32071971, 32001463), the China Postdoctoral Science Foundation (2022M711278), the Key Research and Development Projects of Henan Province (231111113000), Fundamental Research Funds for the Central Universities (2662023ZKPY002), the HZAU-AGIS Cooperation Fund (SZYJY2021008), and the Hubei Agricultural Science and Technology Innovation Center Program (2021-620-000-001-032).

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ARTICLE INFO

Article history:

Received 11 January 2024

Revised 27 March 2024

Accepted 25 May 2024

Available online 5 July 2024

Footnote

* Corresponding author.

E-mail address: [email protected] (H. Wu).

1 These authors contributed equally to this work.

References

References

[1] C.Y. Wang, J. Yang, J.C. Qin, Y.W. Yang, Eco-friendly nanoplatforms for crop quality control, protection, and nutrition, Adv. Sci. 8 (2021) 2004525.

[2] L. Zhao, T. Bai, H. Wei, J.L. Gardea-Torresdey, A. Keller, J.C. White, Nanobiotechnology-based strategies for enhanced crop stress resilience, Nat. Food 3 (2022) 829–836.

[3] L.P.W. Clausen, S.F. Hansen, The ten decrees of nanomaterials regulations, Nat. Nanotechnol. 13 (2018) 766–768.

[4] J. Du, B. Liu, T. Zhao, X. Xu, H. Lin, Y. Ji, X. Ding, Silica nanoparticles protect rice against biotic and abiotic stresses, J. Nanobiotechnol. 20 (2022) 197.

[5] M. Kah, N. Tufenkji, J.C. White, Nano-enabled strategies to enhance crop nutrition and protection, Nat. Nanotechnol. 14 (2019) 532–540.

[6] M.N. Khan, C. Fu, J. Li, Y. Tao, Y. Li, J. Hu, L. Chen, Z. Khan, H. Wu, Z. Li, Seed nanopriming: how do nanomaterials improve seed tolerance to salinity and drought?, Chemosphere 310 (2023) 136911

[7] J. Liu, J Gu, J. Hu, H. Ma, Y. Tao, G. Li, L. Yue, Y. Li, L. Chen, F. Cao, H. Wu, Z. Li, Use of Mn3O4 nanozyme to improve cotton salt tolerance, Plant Biotechnol. J. 21 (2023) 1935–1937. [8] L. Zhao, L. Lu, A. Wang, H. Zhang, M. Huang, H. Wu, B. Xing, Z. Wang, R. Ji, Nanobiotechnology in agriculture: use of nanomaterials to promote plant growth and stress tolerance, J. Agric. Food. Chem. 68 (2020) 1935–1947.

[9] G. Titir, B. Sandip, M. Amitava, K. Rita, Nano-scale zero-valent iron modulates Fe/Cd transporters and immobilizes soil Cd for production of Cd free rice, Chemosphere 260 (2020) 127533.

[10] M. Pogribna, G. Hammons, Epigenetic effects of nanomaterials and nanoparticles, J. Nanobiotechnol. 19 (2021) 1–18.

[11] J. Krasensky, C. Jonak, Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks, J. Exp. Bot. 63 (2012) 1593–1608.

[12] T. Obata, Metabolons in plant primary and secondary metabolism, Phytochem. Rev. 18 (2019) 1483–1507.

[13] F. Hayat, F. Khanum, J. Li, S. Iqbal, U. Khan, H.U. Javed, J. Chen, Nanoparticles and their potential role in plant adaptation to abiotic stress in horticultural crops: a review, Sci. Hortic. 321 (2023) 112285.

[14] M. Inam, I. Attique, M. Zahra, A.K. Khan, M. Hahim, C. Hano, S. Anjum, Metal oxide nanoparticles and plant secondary metabolism: unraveling the gamechanger nano-elicitors, Plant Cell Tissue Organ Cult. 155 (2023) 327–344.

[15] M.U. Chattha, T. Amjad, I. Khan, M. Nawaz, M. Ali, M.B. Chattha, H.M. Ali, Mulberry-based zinc nano-particles mitigate salinity induced toxic effects and improve the grain yield and zinc bio-fortification of wheat by improving antioxidant activities, photosynthetic performance, and accumulation of osmolytes and hormones, Front. Plant Sci. 13 (2022) 920570.

[16] C. Zou, T. Lu, R. Wang, P. Xu, Y. Jing, R. Wang, J. Xu, J. Wan, Comparative physiological and metabolomic analyses reveal that Fe3O4 and ZnO nanoparticles alleviate Cd toxicity in tobacco, J. Nanobiotechnol. 20 (2022) 302.

[17] L. Lu, M. Huang, Y. Huang, P.F.X. Corvini, R. Ji, L. Zhao, Mn3O4 nano zymes boost endogenous antioxidant metabolites in cucumber (Cucumis sativus) plant and enhance resistance to salinity stress, Environ. Sci. Nano 7 (2020) 1692–1703.

[18] J. Wang, M. Li, J. Feng, X. Yan, H. Chen, R. Han, Effects of TiO2-NPs pretreatment on UV-B stress tolerance in Arabidopsis thaliana, Chemosphere 281 (2021) 130809.

[19] M.S. Li, P. Zhang, Z.L. Guo, W.D. Cao, L. Gao, Y.B. Li, C.F. Tian, Q. Chen, Y.Z. Shen, F.Z. Ren, Y.K. Rui, J.C. White, I. Lynch, Molybdenum nanofertilizer boosts biological nitrogen fixation and yield of soybean through delaying nodule senescence and nutrition enhancement, ACS Nano 17 (2023) 14761–14774.

[20] C. Deng, Y. Wang, G. Navarro, Y. Sun, K. Cota-Ruiz, J.A. Hernandez-Viezcas, G. Niu, C. Li, J.C. White, J. Gardea-Torresdey, Copper oxide (CuO) nanoparticles affect yield, nutritional quality, and auxin associated gene expression in weedy and cultivated rice (Oryza sativa L.) grains, Sci. Total Environ. 810 (2022) 152260.

[21] M. Mukarram, P. Petrik, Z. Mushtaq, M.M.A. Khan, M. Gulfishan, A. Lux, Silicon nanoparticles in higher plants: uptake, action, stress tolerance, and crosstalk with phytohormones, antioxidants, and other signaling molecules, Environ. Pollut. 310 (2022) 119855.

[22] Z. Mylona, E. Panteris, M. Moustakas, T. Kevrekidis, P. Malea, Physiological, structural and ultrastructural impacts of silver nanoparticles on the seagrass Cymodocea nodosa, Chemosphere 248 (2020) 126066.

[23] S. Anjum, I. Anjum, C. Hano, S. Kousar, Advances in nanomaterials as novel elicitors of pharmacologically active plant specialized metabolites: current status and future outlooks, RSC Adv. 9 (2019) 40404–40423.

[24] D. Li, C. Zhou, J. M a, Y. Wu, L. Kang, Q. An, J. Zhang, K. Deng, J.Q. Li, C. Pan, Nanoselenium transformation and inhibition of cadmium accumulation by regulating the lignin biosynthetic pathway and plant hormone signal transduction in pepper plants, J. Nanobiotechnol. 19 (2021) 316.

[25] P.F. Zhou, P. Zhang, M.K. He, Y. Cao, M.H. Adeel, N. Shakoor, Y.Q. Jiang, W.C. Zhao, Y.B. Li, M.S. Li, I. Azeem, L. Jia, Y.K. Rui, X.M. Ma, I. Lynch, Iron-based nanomaterials reduce cadmium toxicity in rice (Oryza sativa L.) by modulating phytohormones, phytochelatin, cadmium transport genes and iron plaque formation, Environ. Pollut. 320 (2023) 121063.

[26] R. Vankova, P. Landa, R. Podlipna, P.I. Dobrev, S. Prerostova, L. Langhansova, A. Gaudinova, K. Motkova, V. Knirsch, T. Vanek, ZnO nanoparticle effects on hormonal pools in Arabidopsis thaliana, Sci. Total Environ. 593 (2017) 535–542.

[27] Y. Hao, B. Xu, C. Ma, J.Y. Shang, W.Q. Gu, W. Li, T.Q. Hou, Y.X. Xiang, W.D. Cao, B. S. Xing, Y.K. Rui, Synthesis of novel mesoporous carbon nanoparticles and their phytotoxicity to rice (Oryza sativa L.), J. Saudi Chem. Soc. 23 (2019) 75–82.

[28] I. Khan, S.A. Awan, M. Rizwan, M.A. Akram, M. Zia-Ur-Rehman, X. Wang, X. Zhang, L. Huang, Physiological and transcriptome analyses demonstrate the silver nanoparticles mediated alleviation of salt stress in pearl millet (Pennisetum glaucum L.), Environ. Pollut. 318 (2023) 120863.

[29] J.L. Xiong, N. Ma, Transcriptomic and metabolomic analyses reveal that fullerol improves drought tolerance in Brassica napus L., Int. J. Mol. Sci. 23 (2022) 15304.

[30] J. Gao, Y. Liu, D. Zhao, Y. Ding, L. Gao, X. Su, K. Song, X. He, CeO2NP priming enhances the seed vigor of alfalfa (Medicago sativa) under salt stress, Front. Plant Sci. 14 (2024) 1264698.

[31] X. Yan, S. Chen, Z. Pan, W. Zhao, Y. Rui, L. Zhao, AgNPs-triggered seed metabolic and transcriptional reprogramming enhanced Rice salt tolerance and blast resistance, ACS Nano 17 (2023) 492–504.

[32] M. Zeeshan, Y.X. Hu, X.H. Guo, C.Y. Sun, A. Salam, S. Ahmad, I. Muhammad, J. Nasar, M.S. Jahan, S. Fahad, X.B. Zhou, Physiological and transcriptomic study reveal SeNPs-mediated AsIII stress detoxification mechanisms involved modulation of antioxidants, metal transporters, and transcription factors in Glycine max L. (Merr.) roots, Environ. Pollut. 317 (2023) 120637.

[33] J. Hong, S. Jia, C. Wang, Y. Li, F. He, J.L. Gardea-Torresdey, Transcriptome reveals the exposure effects of CeO2 nanoparticles on pakchoi (Brassica chinensis L.) photosynthesis, J. Hazard. Mater. 444 (2023) 130427.

[34] S. Chen, Z. Pan, W. Zhao, Y. Zhou, Y. Rui, C. Jiang, Y. Wang, J.C. White, L. Zhao, Engineering climate-resilient rice using a nanobiostimulant-based "Stress Training" strategy, ACS Nano 17 (2023) 10760–10773.

[35] L. Sohail, E. Sawati, Y.D. Ferrari, B. Stierhof, Z.U.M. Kemmerling, Molecular effects of biogenic zinc nanoparticles on the growth and development of Brassica napus L. revealed by proteomics and transcriptomics, Fro nt. Plant Sci. 13 (2022) 798751.

[36] L. Niu, C. Li, W. Wang, J. Zhang, M. Scali, W. Li, H. Liu, F. Tai, X. Hu, X. Wu, Cadmium tolerance and hyperaccumulation in plants-A proteomic perspective of phytoremediation, Ecotoxicol. Environ. Saf. 256 (2023) 114882.

[37] G. Mustafa, M. Hasan, H. Yamaguchi, K. Hitachi, K. Tsuchida, S.A. Komatsu, Comparative proteomic analysis of engineered and biosynthesized silver nanoparticles on soybean seedlings, J. Proteomics 224 (2020) 103833.

[38] F. Mirzajani, H. Askari, S. Hamzelou, Y. Schober, A. Römpp, A. Ghassempour, B. Spengler, Proteomics study of silver nanoparticles toxicity on Oryza sativa L., Ecotoxicol. Environ. Saf. 108 (2014) 335–339.

[39] S. Komatsu, K. Murata, S. Yakeishi, K. Shimada, H. Yamaguchi, K. Hitachi, K. Tsuchida, R. Obi, S. Akita, R. Fukuda, Morphological and proteomic analyses of soybean seedling interaction mechanism affected by fiber crosslinked with zinc-oxide nanoparticles, Int. J. Mol. Sci. 23 (2022) 7415.

[40] G. Mustafa, K. Sakata, S. Komatsu, Proteomic analysis of soybean root exposed to varying sizes of silver nanoparticles under flooding stress, J. Proteomics 148 (2016) 113–125.

[41] F. Yasmeen, N.I. Raja, G. Mustafa, K. Sakata, S. Komatsu, Quantitative proteomic analysis of post-flooding recovery in soybean root exposed to aluminum oxide nanoparticles, J. Proteomics 143 (2016) 136–150.

[42] G. Mustafa, K. Sakata, S. Komatsu, Proteomic analysis of flooded soybean root exposed to aluminum oxide nanoparticles, J. Proteomics 128 (2015) 280–297.

[43] T. Hashimoto, G. Mustafa, T. Nishiuchi, S. Komatsu, Comparative analysis of the effect of inorganic and organic chemicals with silver nanoparticles on soybean under flooding stress, Int. J. Mol. Sci. 21 (2020) 1300.

[44] F. Yasmeen, N.I. Raja, A. Razzaq, S. Komatsu, Proteomic and physiological analyses of wheat seeds exposed to copper and iron nanoparticles, Biochim. Biophys. Acta Prot. Proteom. 2017 (1865) 28–42.

[45] F. Yasmeen, N.I. Raja, A. Razzaq, S. Komatsu, Gel-free/label-free proteomic analysis of wheat shoot in stress-tolerant varieties under iron nanoparticles exposure, Biochim. Biophys. Acta 2016 (1864) 1586–1598.

[46] F. Betti, M.J. Ladera-Carmona, D.A. Weits, G. Ferri, S. Iacopino, G. Novi, B. Svezia, A.B. Kunkowska, A. Santaniello, A. Piaggesi, E. Loreti, P. Perata, Exogenous miRNAs induce post-transcriptional gene silencing in plants?, Nat. Plants 7 (2021) 1379–1388.

[47] C.E. Wong, Y.T. Zhao, X.J. Wang, L. Croft, Z.H. Wang, F. Haerizadeh, J.S. Mattick, M.B. Singh, B.J. Carroll, P.L. Bhalla, MicroRNAs in the shoot apical meristem of soybean, J. Exp. Bot. 62 (2011) 2495–2506.

[48] M. Neysanian, A. Iranbakhsh, R. Ahmadvand, Z.O. Ardebili, M. Ebadi, Selenium nanoparticles conferred drought tolerance in tomato plants by altering the transcription pattern of microRNA-172 (miR-172), bZIP, and CRTISO genes, upregulating the antioxidant system, and stimulating secondary metabolism, Protoplasma 31 (2024) 1–13.

[49] A. Niazi, A. Iranbakhsh, M. Esmaeel Zadeh, M. Ebadi, Z. Oraghi Ardebili, Zinc oxide nanoparticles (ZnONPs) influenced seed development, grain quality, and remobilization by affecting the transcription of microRNA 171 (miR171), miR156, NAM, and SUT genes in wheat (Triticum aestivum): a biological advantage and risk assessment study, Protoplasma 260 (2023) 839–851.

[50] I.N. Boykov, E. Shuford, B. Zhang, Nanoparticle titanium dioxide affects the growth and microRNA expression of switchgrass (Panicum virgatum), Genomics 111 (2019) 450–456.

[51] S. Adhikari, A. Adhikari, S. Ghosh, D. Roy, I. Azahar, D. Basuli, Z. Hossain, Assessment of ZnO-NPs toxicity in maize: an integrative microRNAomic approach, Chemosphere 249 (2020) 126197.

[52] M. Iwasaki, J. Paszkowski, Epigenetic memory in plants, EMBO J. 33 (2014) 1987–1998.

[53] L. Moreira, C. Costa, J. Pires, J.P. Teixeira, S. Fraga, How can exposure to engineered nanomaterials influence our epigenetic code? A review of the mechanisms and molecular targets, Mutat. Res. Rev. Mutat. Res. 788 (2021) 108385.

[54] A. Alcazar Magana, K. Wrobel, A.R. Corrales Escobosa, K. Wrobel, Application of liquid chromatography/electrospray ionization ion trap tandem mass spectrometry for the evaluation of global nucleic acids: methylation in garden cress under exposure to CuO nanoparticles, Rapid Commun. Mass Spectrom. 30 (2016) 209–220.

[55] I. Manna, S. Sahoo, M. Bandyopadhyay, Dynamic changes in global methylation and plant cell death mechanism in response to NiO nanoparticles, Planta 257 (2023) 93.

[56] S. Yan, H. Zhang, Y. Huang, J. Tan, P. Wang, Y. Wang, H. Hou, J. Huang, L. Li, Single-wall and multi-wall carbon nanotubes promote rice root growth by eliciting the similar molecular pathways and epigenetic regulation, IET Nanobiotechnol. 10 (2016) 222–229.

[57] S. Sotoodehnia-Korani, A. Iranbakhsh, M. Ebadi, A. Majd, Z. Oraghi Ardebil, Selenium nanoparticles induced variations in growth, morphology, anatomy, biochemistry, gene expression, and epigenetic DNA methylation in Capsicum annuum: an in vitro study, Environ. Pollut. 265 (2020) 114727.

[58] I. Ghosh, A. Sadhu, Y. Moriyasu, M. Bandyopadhyay, A. Mukherjee, Manganese oxide nanoparticles induce genotoxicity and DNA hypomethylation in the moss Physcomitrella patens, Mutat. Res. Genet. Toxicol. Environ. Mutagen. 842 (2019) 146–157.

[59] M. Ghosh, S. Bhadra, A. Adegoke, M. Bandyopadhyay, A. Mukherjee, MWCNT uptake in Allium cepa root cells induces cytotoxic and genotoxic responses and results in DNA hyper-methylation, Mutat. Res. 774 (2015) 49–58.

[60] M. Ueda, M. Seki, Histone modifications form epigenetic regulatory networks to regulate abiotic stress response, Plant Physiol. 182 (2020) 15–26.

[61] S. Yan, L. Zhao, H. Li, Q. Zhang, J. Tan, M. Huang, S. He, L. Li, Single-walled carbon nanotubes selectively influence maize root tissue development accompanied by the change in the related gene expression, J. Hazard. Mater. 246 (2013) 110–118.

[62] A. Vafaie Moghadam, A. Iranbakhsh, S. Saadatmand, M. Ebadi, Z. Oraghi Ardebili, New insights into the transcriptional, epigenetic, and physiological responses to zinc oxide nanoparticles in Datura stramonium; potential species for phytoremediation, J. Plant Growth Regul. 41 (2022) 271–281.

[63] G. Guerriero, F.M. Sutera, J. Hoffmann, C. Leclercq, S. Planchon, R. Berni, S. Saffie-Siebert, Nanoporous quercetin-loaded silicon-stabilized hybrid lipid nanoparticles alleviate salt stress in tomato plants, ACS Appl. Nano Mater. 6 (2023) 3647–3660.

[64] Y.Q. Peng, L.L. Chen, L. Zhu, L.J. Cui, L. Yang, H.H. Wu, Z.L. Bie, CsAKT1 is a key gene for the CeO2 nanoparticle's improved cucumber salt tolerance: a validation from CRISPR-Cas9 lines, Environ. Sci. Nano 9 (2022) 4367–4381.

[65] I.O. Adisa, V.L.R. Pullagurala, J.R. Peralta-Videa, C.O. Dimkpa, W.H. Elmer, J.L. Gardea-Torresdey, J.C. White, Recent advances in nano-enabled fertilizers and pesticides: a critical review of mechanisms of action, Envion. Sci. Nano 6 (2019) 2002–2030.

[66] A. Cox, P. Venkatachalam, S. Sahi, N. Sharma, Reprint of: silver and titanium dioxide nanoparticle toxicity in plants: a review of current research, Plant Physiol. Biochem. 110 (2017) 33–49.

[67] M. Abbas, K. Yan, J. Li, S. Zafar, Z. Hasnain, N. Aslam, N. Iqbal, S.S. Hussain, M. Usman, M. Abbas, M. Tahir, S. Abbas, S.K. Abbas, Q.L. Huang, X. Zhao, A.H. El-Sappah, Agri-nanotechnology and tree augmentation in crop yield, biosafety, and biomass accumulation, Front. Bioeng. Biotechnol. 10 (2022) 853045.

[68] M. Gao, J. Chang, Z. Wang, H. Zhang, T. Wang, Advances in transport and toxicity of nanoparticles in plants, J. Nanobiotechbol. 21 (2023) 75.