The Regulation of ROS and Phytohormones in Balancing Crop Yield and Salt Tolerance

Abstract

Salinity affects crop growth and productivity, and this stress can be increased along with drought or high temperature stresses and poor irrigation management. Cultivation of salt-tolerant crops plays a critical role in enhancing crop yield under salt stress. In the past few decades, the mechanisms of plant adaptation to salt stress have been described, especially relying on ionic homeostasis, reactive oxygen species (ROS) scavenging, and phytohormone signaling. The studies of these molecular mechanisms have provided a basis for breeding new salt-tolerant crop germplasm and have facilitated the entry into the era of molecular breeding of salt-tolerant crops. In this review, we outline the recent progress in the molecular regulations underlying crop salt tolerance, focusing on the double-edged sword effect of ROS, the regulatory role of phytohormones, and the trade-off effects of ROS and phytohormones between crop yield and salt tolerance. A future challenge is to identify superior alleles of key salt-tolerant genes that will accelerate the breeding of high-yield and salt-tolerant varieties.

1. Introduction

The area of salt-affected land worldwide is approximately 950 million hectares and is still increasing, which seriously threatens the production of crops [1,2]. As an important reserve of cultivated land resources, the productivity of salt-affected land urgently needs to be enhanced. Therefore, it is of practical significance to improve the salt tolerance of crops and cultivate high-yield salt-tolerant crops. The salt-tolerant varieties generally have no advantage in terms of yield. Generally speaking, the rice variety with the strongest salt-stress tolerance displays the lowest grain yield, and this contradiction restricts the breeding process of high-yield salt-tolerant crops [3].

When plants are exposed to salt stress, the excessive accumulation of Na⁺ disrupts the Na⁺/K⁺ homeostasis within plant cells, resulting in the inhibition of numerous crucial physiological processes [4]. During the adaptation to salt stress, plants have evolved a series of signaling pathways to deal with salt stress. The salt overly sensitive (SOS) signaling pathway is composed of the core components Na⁺/H⁺ antiporter SOS1, serine/threonine protein kinase SOS2, and calcium-binding protein SOS3/SCABP8 [5,6]. Recent studies have indicated that reducing high-affinity K⁺ transporters (HKTs) and increasing vacuolar Na⁺/H⁺ exchanger 1 (NHX1) and the CHX-type ion transporter 1 (CHX1) can jointly enhance Na⁺ efflux, restrict Na⁺ uptake, and sequester Na⁺ in vacuoles to alleviate the damage caused by salt stress [7,8,9].

Salt stress not only induces ionic stress, but also causes the excessive accumulation of ROS, such as hydrogen peroxide (H₂O₂), superoxide radical (O₂^•¯), singlet oxygen (¹O₂), and hydroxyl radical (OH•), resulting in oxidative stress and nutrient deficiency. ROS are products under stresses and signaling molecules for growth and development, and ROS homeostasis is of great significance to plants [10]. Accumulating research has elucidated the signaling, generation, and metabolism of ROS [10,11,12]. Phytohormones are small chemical substances that play a vital role in the growth and development of plants. Moreover, phytohormones also play significant roles when plants cope with stresses. Increased or decreased levels of certain hormones could help plants adapt to salt stress, including abscisic acid (ABA), ethylene (ET), jasmonic acid (JA), salicylic acid (SA), auxin, cytokinin (CK), gibberellic acid (GA), and brassinosteroid (BR) [13]. Whether to regulate the normal growth of plants or mediate the responses to abiotic stress, the integration and coordination of multiple plant hormones are requisites for plants. Moreover, ROS homeostasis and phytohormone signaling pathways are interrelated and form a more complex regulatory network in plants [10,13], revealing the potential functions of ROS and phytohormones in plant growth and salt-stress responses, probably responsible for the key modulation of the collaborative balance between crop yield and salt tolerance. By searching published research in the National Center for Biotechnology Information (NCBI) PubMed https://www.ncbi.nlm.nih.gov/ (accessed on 1 October 2024) database using “ROS or hormones”, “salt stress”, and “crop yield” as key words, a tremendous number of reports were found, followed by a selection focusing on crops (rice, wheat, maize, soybean, potato, etc.). Here, we mainly review the latest research progress in the regulation of ROS homeostasis and phytohormones in crops under salt stress, especially the critical genes in the last ten years.

2. ROS Homeostasis Under Salt Stress

2.1. Signaling Function of ROS Under Salt Stress

ROS have important roles throughout the entire life cycle of plants. Under normal circumstances, ROS are maintained at a relatively low level and can serve as signaling molecules to regulate plant growth and development [14,15]. In the early stage of salt stress, ROS are produced “actively” or “passively” in plant cells [10]. The extracellular ROS burst is mediated by plasma-membrane-localized respiratory burst oxidase homologs (RBOHs), which utilize NADPH in the cytosol to generate O₂^•¯ in the apoplast and convert it into H₂O₂ through the superoxide dismutase [16]. The RBOH family in rice (Oryza sativa) contains nine members (OsRbohA to I) [17]. Research has disclosed that not every RBOH serves as the principal protein for ROS bursts in response to salt stress. OsRBOHA and OsRBOHI are the key factors in rice, whereas AtRBOHD and AtRBOHF are the crucial ones in Arabidopsis (Arabidopsis thaliana) [16,17]. The H₂O₂ generated by RBOHs is capable of mediating calcium ion signaling in peas, further activating RBOHD by binding to the EF-hand domain of RBOHD, thereby augmenting H₂O₂ production [18,19]. It has been discovered that H₂O₂ induced by salt stress in soybeans (Glycine max) promotes oxidative modification of the transcription factor GmNTL1 protein, facilitating its translocation to the nucleus to activate the expression of GmRbohBs, further enhancing the ROS level and thereby rapidly amplifying the ROS signal elicited by salt stress [20]. It has been reported that the trafficking of RBOHs is regulated by the epsin-like clathrin adaptor 4 (ECA4) [21]. Furthermore, RBOHs are also regulated by ubiquitylation, persulfidation, nitrosylation, and endocytosis [10].

Apart from the extracellular space, ROS are also produced in various cellular compartments, such as mitochondria, the cytosol, peroxisomes, and the endoplasmic reticulum [12,22]. Salt stress could also damage the ultrastructure of chloroplasts, resulting in the generation of H₂O₂ and O₂^•¯ in chloroplasts [23]. Due to the fact that aquaporins (AQPs) identified on the plasma membrane and organelle membranes promote the bidirectional transportation of H₂O₂, the H₂O₂ level within the cytoplasm can influence the H₂O₂ level in other cellular compartments, and vice versa [24].

During the process of salt stress, the interplay between the generation and scavenging of ROS in each cellular compartment gives rise to compartment-specific ROS signals [10]. These signals, in combination with other non-ROS signals, traverse the cytoplasm to reach the nucleus, modify nuclear ROS signals, and trigger defense and adaptation responses [25]. It has been discovered that ROS could regulate gene expression through mRNA stability and microRNA abundance during salt-stress responses. For instance, H₂O₂ could enhance the stability of SOS1 mRNA to facilitate the Na⁺ efflux [26]. Stress-induced ROS inhibit the accumulation of miR408 in maize (Zea mays), thereby elevating the transcription levels of its target genes ZmLAC9 and ZmLAC18 and promoting cell wall development and salt tolerance by regulating the polymerization of lignin monomers [27]. In addition to regulating transcription via epigenetic mechanisms during stress, ROS also influence the translocation of different redox-regulated transcriptional regulators. Non-expressor of pathogenesis-related genes 1 (NPR1), heat shock factors (HSFs), and membrane-bound NAC transcription factors have been determined to sense H₂O₂ signals in the cytoplasm and convey them to the nucleus to modulate the expression of salt-stress response genes [12,28,29]. These studies indicate that ROS signals play a crucial role in the salt-stress response.

2.2. Oxidative Stress Induced by ROS Under Salt Stress

Appropriate levels of ROS constitute an essential signaling molecule for activating salt stress tolerance; however, excessive accumulation of ROS could elicit oxidative stress in plants, disrupting the oxidation–reduction balance of cells and resulting in DNA damage, protein degradation, as well as peroxidation of carbohydrates and lipids [30]. At present, there have been detailed reviews discussing the molecular mechanisms of ROS scavenging under oxidative stress [12]. To counteract oxidative stress, there is a large number of antioxidant enzymes that clear ROS [31]. Enzymatic scavengers include superoxide dismutase (SOD), catalase (CAT), ascorbic acid peroxidase (APX), glutathione peroxidase (GPX), glutathione reductase (GR), dehydroascorbate reductase (DHAR), monodehydroascorbate reductase (MDHAR), and glutathione S-transferase (GST) [32,33,34]. In an S-type cytoplasmic male sterile maize line, the moderately expressed sterility gene open reading frame 355 (ZmORF355) in the mitochondria promotes salt tolerance by activating various antioxidant enzymes [35]. Biochemical analyses have revealed that hydroquinone could be transformed into arbutin under the catalysis of UDP-glucose transferases (UGTs). Moreover, the growth regulating factor 7 (OsGRF7) could directly bind to the promoters of OsUGT1 and OsUGT5 to stimulate their expression, thereby increasing arbutin biosynthesis and enlarging grains [36]. Inhibition of ZmmiR169q under salt stress contributes to salt tolerance by mediating ROS elimination, by increasing the expression of its target gene ZmNF-YA8 and enhancing the transcription of the antioxidant enzyme gene peroxidase 1 (ZmPER1) [37]. The salt-tolerant receptor-like cytoplasmic kinase 1 (STRK1) phosphorylates and activates catalase C (CatC), promoting the homeostasis of H₂O₂ in rice. Plants overexpressing OsSTRK1 exhibit a higher catalase activity, a lower H₂O₂ accumulation, and a greater salt tolerance compared to wild-type plants [38]. Further research has found that catalase 1 phosphatase (PC1)-mediated dephosphorylation of CAT can inhibit its activity [39]. These studies indicate that the activity regulation of many antioxidant enzymes under salt stress is a key regulatory node.

In addition to antioxidant enzymes, an increasing number of studies indicate that many non-enzymatic antioxidants are involved in mitigating ROS-induced damage under salt stress, such as ascorbic acid (AsA), anthocyanin, glutathione, and tocopherols [2]. It has been discovered that AsA confers salt tolerance to plants [40]. GDP-mannose pyrophosphorylase VTC1 is a key enzyme in the AsA biosynthesis pathway and positively regulates salt tolerance [41,42,43]. OsVTC1-1 plays a crucial role in rice salt tolerance by promoting the generation of AsA to scavenge excessive ROS [44]. Maize bronze 1 (ZmBZ1) enhances stress tolerance by mediating anthocyanin accumulation [45]. Branched-chain amino transferase 2 (OsBCAT2) governs the catabolism of branched-chain amino acids (BCAAs) and the synthesis of pantothenic acid (vitamin B5, VB5) in rice. Salt stress induces the expression of OsBCAT2, accelerating the intracellular degradation of BCAAs and augmenting the synthesis of the downstream product VB5, thereby enhancing the salt stress tolerance of rice [46]. OsGSA1 encodes a UDP-glucosyltransferase, enabling plants to accumulate flavonoid glycosides, thereby protecting rice from abiotic stress [47], revealing that many antioxidants play a role in crop salt tolerance.

Thus, the studies in recent years have emphasized the significant role of ROS homeostasis in the response to salt stress. ROS show the double-edged sword effects in different crops in terms of their contribution to salt tolerance (Table 1). To prevent damage, it is essential for plants to strictly control ROS concentrations. Enhancing crop salt tolerance by recruiting enzymatic and non-enzymatic antioxidant systems to eliminate excessive ROS is an effective approach (Figure 1).

3. Modulation of Phytohormones in Salt-Stress Responses

The phytohormones facilitate plants’ rapid responses to salt stress. Some hormones exert positive regulatory effects on plant salt tolerance, such as ABA and JA, whereas some have negative regulatory roles, such as GA [13]. Moreover, the regulatory function of some hormones in salt tolerance is opposite in different species. For instance, ethylene has a positive role in salt tolerance in Arabidopsis, while it negatively regulates salt tolerance in rice [51,52,53], demonstrating that phytohormones have complicated regulatory mechanisms.

When plants are exposed to salt stress, the accumulation level of ABA shows a positive correlation with the salt tolerance of plants [54,55]. ABA could activate a variety of downstream signaling factors, such as kinases, phosphatases, and G proteins. It has been discovered that the drought-induced protein GmDi19-5 could negatively regulate the responses of soybeans to drought and salt stress through the ABA-dependent pathway [56,57]. In rice, the transcription factor OsSGL is involved in inhibiting the gene expression of OsNCED3, encoding a key enzyme of ABA biosynthesis. Under salt stress, OsSGL undergoes acetylation modification and nuclear–cytoplasmic distributions, enabling a dynamic regulation of ABA content in plant cells [58,59]. Consequently, ABA, as a stress hormone, plays an important role in regulating salt tolerance in crops.

It has been discovered that ethylene treatments augment the salt sensitivity of rice seedlings, while, for Arabidopsis and soybeans, they enhance salt tolerance [51,60,61]. Salt intolerance 1 (OsSIT1), a lectin receptor-like kinase and an ethylene sensor, actively mediates salt sensitivity by activating the mitogen-activated protein kinase 3/6 (MPK3/6), thereby promoting ethylene biosynthesis, ROS accumulation, and sensitivity to salt stress in rice [62].

GA plays a crucial role in modulating growth under abiotic stress [63]. The genes involved in the GA catabolic pathway, i.e., gibberellin 2-oxidase 5/7 (GA2ox5/7), OsMYB91, and OsCYP71D8L, contribute to decreased GA levels and a retarded growth, thereby enhancing the salt tolerance of plants [64,65,66]. Moreover, OsDSK2a, functioning as a ubiquitin receptor and transporter, promotes the degradation of the GA-inactivating enzyme EUI in rice. The level of OsDSK2a is inhibited by salt stress, giving rise to the accumulation of EUI and the reduced level of biologically active GA, elucidating the mechanism underlying the inhibition of salt stress in the context of plant growth [67]. These studies indicate that growth inhibition under salt stress might be an active adaptive mechanism in crops.

JA plays a key role in plant growth and development, in the defense against insects and pathogens, and in secondary metabolism. It has also been unveiled that JA possesses significant functions in plant responses to salt stress [68]. When plants encounter high-concentration salt stress, degradation of the JA response factor JAZ8 relieves its inhibitory effect on the NF-YA1-YB2-YC9 transcription factor complex, promoting the expression of salt-stress response genes and enhancing salt tolerance in rice [69,70,71]. IbNAC087, a nuclear-localized transcriptional activator in sweet potatoes (Ipomoea batatas), could directly activate the expression of JA synthesis-related genes to increase JA content and, thus, enhance salt and drought resistance [72].

It has been found that the mutation of rice salt tolerance 1 (RST1) in rice, encoding the auxin response factor OsARF18, promotes nitrogen utilization and reduces the accumulation of NH4⁺ under salt stress, thereby enhancing salt tolerance and grain yield [73]. Overexpression of rice big grain 1 (RBG1) leads to an increased grain size due to the elevated cell numbers by increasing auxin accumulation; meanwhile, RBG1 could upregulate stress proteins to enhance the tolerance to the heat and osmotic and salt stresses in rice [74,75]. Therefore, promoting growth to a certain extent is also necessary for improving salt tolerance in crops.

Some reports have indicated that cytokinin regulates salt tolerance in Arabidopsis [76,77,78]. Furthermore, a study on maize has determined that a type A response regulator, ZmRR1, modulates Cl⁻ exclusion and negatively regulates cytokinin signaling. ZmRR1 could interact with a key mediator of cytokinin signaling, ZmHP2, to inhibit Cl⁻ exclusion and salt tolerance [79]. This study demonstrates that cytokinin signaling has a positive role in salt tolerance through ionic homeostasis in crops.

Taken together, the roles of phytohormones in crop growth and development under salt stress are complicated (Table 2), and more in-depth research on some hormones in crops is needed. In particular, the hormones mainly regulating plant growth have a promising route for balancing salt tolerance and crop yield.

4. ROS and Phytohormones Jointly Balance Crop Yield and Salt Tolerance

ROS play a dual role in plant growth and stress responses, and phytohormones are also significant endogenous chemical signals that orchestrate plant growth and development in appropriate environments and under adverse conditions [10,13]. Owing to the high reactivity and oxidizing nature of ROS, ROS signaling is predominantly mediated by protein oxidative post-translational modifications. This characteristic enables ROS to target a broad spectrum of proteins and to dynamically and spatiotemporally regulate signaling transduction pathways under various stress conditions, a phenomenon which is similar to phytohormone signaling pathways [10]. It has been reported that phytohormones could be associated with ROS to jointly regulate plant growth, development, and adaptation to adverse circumstances.

First and foremost, phytohormones are capable of influencing the synthesis, metabolism, and signaling of ROS. Research has discovered that wheat (Triticum aestivum) brassinazole-resistant 1 (TaBZR1) could not only directly bind to the G-box motif in the promoter of the key ABA synthesis gene TaNCED3 to activate its expression and ABA synthesis, but also bind to the promoters of the ROS scavenging-related genes TaGPX2 and TaGPX3 to promote their expression, thereby facilitating ROS scavenging [80]. It is interesting that ethylene inhibits but ABA promotes the accumulation of ROS in Arabidopsis [81]. Furthermore, AsA acts as a key factor in integrating the interaction of ethylene and ABA in the regulation of ROS levels. Ethylene and ABA antagonistically regulate AsA biosynthesis via ethylene-insensitive 3 (EIN3) and ABA insensitive 4 (ABI4), respectively, both of which are key factors in the ethylene and ABA signaling pathways, respectively [81]. In addition, EIN3 and ABI4 collaboratively modulate salt tolerance via AsA biosynthesis [82]. It is noteworthy that the GA signaling factor RGA1 (alpha subunit of heterotrimeric G protein) in rice negatively regulates salt tolerance by participating in ROS scavenging by modulating antioxidant enzymes protein abundance [83]. The most recent study has disclosed that, under salt stress, the downstream transcription factor OsMYB2 of ABA mediates the expression of the amino acid transporter gene ANT1, further enhancing the transportation of amino acids (Pro, Leu, Phe, Tyr) and regulating the balance between rice growth and salt tolerance through the accumulation of amino acids like Pro and Tyr and the reduction of ROS. This research provides novel insights into the function of plant amino acid transporter genes [84].

Secondly, ROS exert an influence on the synthesis, metabolism, and signaling of phytohormones. It has been discovered that GPX3 is not merely a ROS-scavenging enzyme highly sensitive to H₂O₂, and that the redox state of GPX3 could also influence the phosphatase activity of its interacting partner ABA insensitive 2 (ABI2), which is a negative component of the ABA signaling pathway and participates in stomatal closure [85]. H₂O₂ could sulfonate BZR1 to enhance its transcriptional activity, thereby positively regulating BR signaling and plant growth in Arabidopsis [86]. It is notable that H₂O₂ could affect both the contents of IAA and ABA through the tryptophan synthase B subunit 1 (TSB1). Salt-induced sulfoxidation of TSB1 increases ABA accumulation and facilitates salt stress tolerance in Arabidopsis [87]. Thus, ROS-mediated oxidative modification of phytohormone signaling factors confers to plants the ability to adapt to salt stress.

Furthermore, there exist certain transcription factors that could concurrently regulate both ROS and phytohormones. The mutation of the key regulatory factor ITPK4 in Arabidopsis leads to an augmented accumulation of ROS and decreased auxin levels in plants under salt stress [88]. In soybeans, the induced expression of GmSIN1 under salt stress upregulates the cellular levels of ABA and ROS, giving rise to an amplification of the initial salt stress signal [89]. In brief, plants utilize multiple signaling molecules to coordinate developmental processes and responses to environmental stimuli [90] (Table 3).

In recent years, numerous reviews related to balancing crop growth and stress tolerance have been reported [3,91]. Regarding the balance between crop yield and salt tolerance, it seems to be distinct from other stresses, such as drought, heat, and cold, since the salt content in saline–alkali soil changes with the weather [91]. Recent studies have discovered that, in natural populations of wheat, there are many natural variations of the promoter of TaCHP, forming two main haplotypes, Hap1 and Hap2. The salt tolerance of the varieties carrying Hap1 is significantly higher than that of thosse carrying Hap2. TaCHP-Hap1 could stably increase the yield of wheat in saline–alkali soil without affecting the yield in normal soil. Therefore, the salt-tolerant haplotype of TaCHP has a strong application potential in molecular design breeding of wheat [48]. Under saline–alkaline conditions, high pH stress amplifies the harmful effects of salt stress on plants. Recent studies have shown that the Alkaline tolerance 1 (AT1) gene in Sorghum negatively regulates crop tolerance to alkali by modulating ROS homeostasis [49,50]. It has been determined that OsAT1 (known as grain size 3, OsGS3) is a high-yield gene that encodes an atypical G protein γ subunit [92]. Introducing the favorable allele of OsAT1 into the high-quality rice variety Kongyu131 could increase the yield by 27.8% under alkaline stress conditions, indicating that this allele has a great potential value in cultivating alkali-tolerant rice [50]. Recent research has revealed that OsDSK2a, a co-regulatory factor for growth and salt tolerance in rice, could be phosphorylated by the conserved kinase SnRK1A, and natural variations exist at the phosphorylation sites. The varieties contained in the elite haplotype OsDSK2a-G have a higher grain yield than that of the varieties contained in OsDSK2a-S under salt stress [93]. Furthermore, a study has reported, for the first time, a grain length gene GL12 from the common wild rice (Oryza rufipogon) which is capable of concurrently enhancing the grain length and salt tolerance of rice. A G/T variation site in its promoter region influences its spatio-temporal expression pattern in the spikelets and roots, thereby balancing the yield and salt tolerance of rice [94]. Therefore, it is still necessary to explore the key salt-tolerant genes in crop plants, regardless of whether these genes are related to ROS or hormone pathways, and try to identify the associated excellent natural variations as much as possible to provide opportunities for the trade-off between salt tolerance and growth (Figure 2).

5. Conclusions and Future Prospects

Crop yield has been greatly improved after years of breeding, but the improvement in crop salt tolerance is still at a bottleneck. The identification of key salt-tolerant genes in plants and an in-depth exploration of their molecular regulatory mechanisms could provide significant theoretical foundations for the breeding of salt-tolerant crops. However, crop salt tolerance is a quantitative trait controlled by multiple genes. Due to the subtle effect of one or several genes, more genes need to work together to achieve synergistic effects under salt stress. Therefore, highly efficient methods for identifying salt-tolerant genes are a challenge for molecular breeding. Meanwhile, with the development of functional genomics and multiomics technology, a stable phenome identification system under salt stress is very important.

On the other hand, since the modulations of ROS and phytohormones in the context of plant growth and salt stress have been deeply researched in model plants, it is feasible to use these regulations to balance yield and salt tolerance in crops. Phytohormones could play a significant regulatory role in extremely small amounts, providing a potential way for balancing ROS homeostasis, salt tolerance, plant growth, and yield enhancement. GA, which was reduced to increase the harvest index in the Green Revolution, could also improve salt tolerance to a certain level. Identification of key genes referring to the crosstalk between ROS and phytohormones is helpful to control their dose effects.

During the prolonged breeding process, with yield traits as the main target orientation, the genetic diversity of crops has decreased, and superior alleles for salt tolerance have been lost or lacked directed selection. The discovery of superior alleles that can collaboratively improve both yield and salt tolerance remains an exciting challenge. To increase the productivity of salt–alkali land and improve grain yield, it is important to apply modern molecular breeding approaches for precise, rapid, and efficient improvement of crop salt tolerance.

Author Contributions

Conceptualization, J.W., R.H. and L.J.; figure software, L.J.; writing—original draft preparation, L.J.; writing—review and editing, L.J., M.X. and J.W.; supervision, J.W. and R.H. All authors have read and agreed to the published version of the manuscript.

Acknowledgments

All the figures displayed in this review were created with BioRender.com.

Conflicts of Interest

The authors declare no conflicts of interest.

Footnotes

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Figures and Tables

Figure 1. ROS and phytohormones in the context of salt stress. In the early phases of salt stress, RBOHs govern the outburst of ROS in organelles including chloroplasts, mitochondria, peroxisomes, etc. Due to the promotion of bidirectional transportation of H2O2 by AQP/complexes on the cell membrane and organelle membranes, the level of H2O2 in the cytoplasm could influence that in other organelles and vice versa. The ROS signal produced by salt stress regulates some transcription factors (TFs), facilitating the expression of some salt stress responsive genes. The stability of SOS1 mRNA is also enhanced to regulate ionic homeostasis. Persistent salt stress could result in the excessive accumulation of ROS in plant cells when certain TFs are promoted to activate the expression of antioxidant system genes. Antioxidative enzymes, combined with non-enzymatic antioxidants, participate in the control of ROS homeostasis under salt stress. Meanwhile, phytohormone signals are activated or inhibited to regulate salt-stress responses and plant growth. Several regulators involved in phytohormone signals are also controlled by ROS homeostasis, which mediates the crosstalk between ROS and phytohormones under salt stress.

Figure 2. ROS and phytohormones mediate the balance between crop yield and salt tolerance. ROS and phytohormones display an intricate signal crosstalk and jointly govern the growth responses of plants to salt stress. Exploring the key salt-tolerant genes therein and identifying the associated excellent natural variations offer opportunities for striking a balance between salt tolerance and growth.

Table 1

Genes associated with ROS in crop salt–alkali tolerance.

Gene	ROS	Species	Salt–Alkali Tolerance	Ref.
Rbohs	ROS generation	Oryza sativa, Glycine max	Positive	[17][20]
GmNTL1	ROS generation	Glycine max	Positive	[20]
miR408	Regulated by ROS signal	Zea mays	Positive	[27]
HSFB2b	Regulated by ROS signal	Glycine max	Positive	[29]
ZmORF355	ROS scavenging	Zea mays	Positive	[35]
OsGRF7OsUGT1/5	ROS scavenging	Oryza sativa	Positive	[36]
ZmmiR169q	ROS scavenging	Zea mays	Positive	[37]
ZmNF-YA8 ZmPER1	ROS scavenging	Zea mays	Positive	[37]
STRK1	ROS scavenging	Oryza sativa	Positive	[38]
PC1	ROS scavenging	Oryza sativa	Negative	[39]
OsVTC1	ROS scavenging	Oryza sativa	Positive	[44]
ZmBZ1	ROS scavenging	Zea mays	Positive	[45]
OsBCAT2	ROS scavenging	Oryza sativa	Positive	[46]
OsGSA1	ROS scavenging	Oryza sativa	Positive	[47]
TaCHP	ROS scavenging	Triticum aestivum	Positive	[48]
AT1	ROS scavenging	Sorghum bicolorOryza sativaZea mays,Triticumaestivum	Negative	[49,50]

Table 2

Genes associated with phytohormones in crop salt tolerance.

Gene	Phytohormone	Species	Salt Tolerance	Ref.
GmDi19-5	ABA signal	Glycine max	Negative	[56]
OsSGL	ABA synthesis	Oryza sativa	Negative	[58]
OsNCED3	ABA synthesis	Oryza sativa	Positive	[58]
OsSIT1	ET synthesis	Oryza sativa	Negative	[62]
MPK3/6	ET synthesis	Oryza sativa	Negative	[62]
OsGA2ox5	GA metabolism	Oryza sativa	Positive	[65]
OsCYP71D8L	GA metabolismCK metabolism	Oryza sativa	Positive	[66]
OsDSK2a	GA metabolism	Oryza sativa	Positive	[67]
JAZ8	JA signal	Oryza sativa	Positive	[70]
IbNAC087	JA synthesis	Ipomoea batatas	Negative	[72]
OsARF18	Auxin signal	Oryza sativa	Negative	[73]
ZmRR1	CK signal	Zea mays	Negative	[79]
ZmHP2 ZmMATE29	CK signal	Zea mays	Positive	[79]

Table 3

Genes associated with both ROS and phytohormones under salt stress.

Gene	ROS	Phytohormone	Species	Salt Tolerance	Ref.
BZR1	ROS scavenging	BR signalABA synthesis	TriticumAestivum L.Arabidopsis thaliana	Positive	[80,86]
ABI4	ROS scavenging	ABA signalET signal	Arabidopsis thaliana	Negative	[81]
EIN3	ROS scavenging	ET signalABA signal	Arabidopsis thaliana	Positive	[81]
RGA1	ROS scavenging	GA signal	Oryza sativa	Positive	[83]
OsMYB2	ROS scavenging	ABA signal	Oryza sativa	Positive	[84]
GPX3	ROS scavenging	ABA signal	Arabidopsis thaliana	Positive	[85]
TSB1	Regulated by ROS signal	ABA synthesis, auxin metabolism	Arabidopsis thaliana	Positive	[87]
ITPK4	ROS scavenging	Auxin metabolism	Arabidopsis thaliana	Positive	[88]
GmSIN1	ROS generation	ABA synthesis	Glycine max	Positive	[89]

References

1. Ismail, A.M.; Horie, T. Genomics, Physiology, and molecular breeding approaches for improving salt tolerance. Annu. Rev. Plant Biol.; 2017; 68, pp. 405-434. [DOI: https://dx.doi.org/10.1146/annurev-arplant-042916-040936]

2. Yang, Y.; Guo, Y. Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol.; 2018; 217, pp. 523-539. [DOI: https://dx.doi.org/10.1111/nph.14920] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29205383]

3. Zhang, H.; Zhao, Y.; Zhu, J.K. Thriving under Stress: How plants balance growth and the stress response. Dev. Cell; 2020; 55, pp. 529-543. [DOI: https://dx.doi.org/10.1016/j.devcel.2020.10.012] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33290694]

4. Munns, R.; Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol.; 2008; 59, pp. 651-681. [DOI: https://dx.doi.org/10.1146/annurev.arplant.59.032607.092911] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18444910]

5. Zhang, X.Y.; Tang, L.H.; Nie, J.W.; Zhang, C.R.; Han, X.; Li, Q.Y.; Qin, L.; Wang, M.H.; Huang, X.; Yu, F. et al. Structure and activation mechanism of the rice Salt Overly Sensitive 1 (SOS1) Na(+)/H(+) antiporter. Nat. Plants; 2023; 9, pp. 1924-1936. [DOI: https://dx.doi.org/10.1038/s41477-023-01551-5]

6. Zhang, Y.; Zhou, J.; Ni, X.; Wang, Q.; Jia, Y.; Xu, X.; Wu, H.; Fu, P.; Wen, H.; Guo, Y. et al. Structural basis for the activity regulation of Salt Overly Sensitive 1 in Arabidopsis salt tolerance. Nat. Plants; 2023; 9, pp. 1915-1923. [DOI: https://dx.doi.org/10.1038/s41477-023-01550-6] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37884652]

7. Mottaleb, S.A.; Rodriguez-Navarro, A.; Haro, R. Knockouts of Physcomitrella patens CHX1 and CHX2 transporters reveal high complexity of potassium homeostasis. Plant Cell Physiol.; 2013; 54, pp. 1455-1468. [DOI: https://dx.doi.org/10.1093/pcp/pct096]

8. Yang, L.; Wei, Y.; Li, N.; Zeng, J.; Han, Y.; Zuo, Z.; Wang, S.; Zhu, Y.; Zhang, Y.; Sun, J. et al. Declined cadmium accumulation in Na(+)/H(+) antiporter (NHX1) transgenic duckweed under cadmium stress. Ecotoxicol. Environ. Saf.; 2019; 182, 109397. [DOI: https://dx.doi.org/10.1016/j.ecoenv.2019.109397] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31299476]

9. Wang, X.; Shen, X.; Qu, Y.; Zhang, H.; Wang, C.; Yang, F.; Shen, H. Structural insights into ion selectivity and transport mechanisms of Oryza sativa HKT2; 1 and HKT2; 2/1 transporters. Nat. Plants; 2024; 10, pp. 633-644. [DOI: https://dx.doi.org/10.1038/s41477-024-01665-4] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/38570642]

10. Mittler, R.; Zandalinas, S.I.; Fichman, Y.; Van Breusegem, F. Reactive oxygen species signalling in plant stress responses. Nat. Rev. Mol. Cell Biol.; 2022; 23, pp. 663-679. [DOI: https://dx.doi.org/10.1038/s41580-022-00499-2]

11. Waszczak, C.; Carmody, M.; Kangasjarvi, J. Reactive oxygen species in plant signaling. Annu. Rev. Plant Biol.; 2018; 69, pp. 209-236. [DOI: https://dx.doi.org/10.1146/annurev-arplant-042817-040322] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29489394]

12. Wang, P.; Liu, W.C.; Han, C.; Wang, S.; Bai, M.Y.; Song, C.P. Reactive oxygen species: Multidimensional regulators of plant adaptation to abiotic stress and development. J. Integr. Plant Biol.; 2024; 66, pp. 330-367. [DOI: https://dx.doi.org/10.1111/jipb.13601]

13. Yu, Z.; Duan, X.; Luo, L.; Dai, S.; Ding, Z.; Xia, G. How plant hormones mediate salt stress responses. Trends Plant Sci.; 2020; 25, pp. 1117-1130. [DOI: https://dx.doi.org/10.1016/j.tplants.2020.06.008] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32675014]

14. Evans, M.J.; Choi, W.G.; Gilroy, S.; Morris, R.J. A ROS-assisted calcium wave dependent on the AtRBOHD NADPH oxidase and TPC1 cation channel propagates the systemic response to salt stress. Plant Physiol.; 2016; 171, pp. 1771-1784. [DOI: https://dx.doi.org/10.1104/pp.16.00215]

15. Zhang, M.; Smith, J.A.; Harberd, N.P.; Jiang, C. The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol. Biol.; 2016; 91, pp. 651-659. [DOI: https://dx.doi.org/10.1007/s11103-016-0488-1] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/27233644]

16. Miller, G.; Suzuki, N.; Ciftci-Yilmaz, S.; Mittler, R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ.; 2010; 33, pp. 453-467. [DOI: https://dx.doi.org/10.1111/j.1365-3040.2009.02041.x] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/19712065]

17. Wang, G.F.; Li, W.Q.; Li, W.Y.; Wu, G.L.; Zhou, C.Y.; Chen, K.M. Characterization of Rice NADPH oxidase genes and their expression under various environmental conditions. Int. J. Mol. Sci.; 2013; 14, pp. 9440-9458. [DOI: https://dx.doi.org/10.3390/ijms14059440]

18. Ogasawara, Y.; Kaya, H.; Hiraoka, G.; Yumoto, F.; Kimura, S.; Kadota, Y.; Hishinuma, H.; Senzaki, E.; Yamagoe, S.; Nagata, K. et al. Synergistic activation of the Arabidopsis NADPH oxidase AtrbohD by Ca2+ and phosphorylation. J. Biol. Chem.; 2008; 283, pp. 8885-8892. [DOI: https://dx.doi.org/10.1074/jbc.M708106200] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18218618]

19. Zepeda-Jazo, I.; Velarde-Buendia, A.M.; Enriquez-Figueroa, R.; Bose, J.; Shabala, S.; Muniz-Murguia, J.; Pottosin, I.I. Polyamines interact with hydroxyl radicals in activating Ca(2+) and K(+)transport across the root epidermal plasma membranes. Plant Physiol.; 2011; 157, pp. 2167-2180. [DOI: https://dx.doi.org/10.1104/pp.111.179671]

20. Zhang, W.; Zhi, W.; Qiao, H.; Huang, J.; Li, S.; Lu, Q.; Wang, N.; Li, Q.; Zhou, Q.; Sun, J. et al. H2O2-dependent oxidation of the transcription factor GmNTL1 promotes salt tolerance in soybean. Plant Cell; 2023; 36, pp. 112-135. [DOI: https://dx.doi.org/10.1093/plcell/koad250] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37770034]

21. Lee, J.; Hanh, N.H.; Park, Y.; Lin, J.; Hwang, I. Spatial regulation of RBOHD via AtECA4-mediated recycling and clathrin-mediated endocytosis contributes to ROS accumulation during salt stress response but not flg22-induced immune response. Plant J.; 2022; 109, pp. 816-830. [DOI: https://dx.doi.org/10.1111/tpj.15593] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34797009]

22. Janku, M.; Luhova, L.; Petrivalsky, M. On the origin and fate of reactive oxygen species in plant cell compartments. Antioxidants; 2019; 8, 105. [DOI: https://dx.doi.org/10.3390/antiox8040105]

23. Yamane, K.; Taniguchi, M.; Miyake, H. Salinity-induced subcellular accumulation of H(2)O(2) in leaves of rice. Protoplasma; 2012; 249, pp. 301-308. [DOI: https://dx.doi.org/10.1007/s00709-011-0280-7] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/21533665]

24. Rodrigues, O.; Reshetnyak, G.; Grondin, A.; Saijo, Y.; Leonhardt, N.; Maurel, C.; Verdoucq, L. Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. Proc. Natl. Acad. Sci. USA; 2017; 114, pp. 9200-9205. [DOI: https://dx.doi.org/10.1073/pnas.1704754114] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/28784763]

25. Van Breusegem, F.; Bailey-Serres, J.; Mittler, R. Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol.; 2008; 147, pp. 978-984. [DOI: https://dx.doi.org/10.1104/pp.108.122325] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/18612075]

26. Chung, J.S.; Zhu, J.K.; Bressan, R.A.; Hasegawa, P.M.; Shi, H. Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J.; 2008; 53, pp. 554-565. [DOI: https://dx.doi.org/10.1111/j.1365-313X.2007.03364.x] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17996020]

27. Qin, R.; Hu, Y.; Chen, H.; Du, Q.; Yang, J.; Li, W.X. MicroRNA408 negatively regulates salt tolerance by affecting secondary cell wall development in maize. Plant Physiol.; 2023; 192, pp. 1569-1583. [DOI: https://dx.doi.org/10.1093/plphys/kiad135]

28. Jayakannan, M.; Bose, J.; Babourina, O.; Shabala, S.; Massart, A.; Poschenrieder, C.; Rengel, Z. The NPR1-dependent salicylic acid signalling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. J. Exp. Bot.; 2015; 66, pp. 1865-1875. [DOI: https://dx.doi.org/10.1093/jxb/eru528]

29. Bian, X.H.; Li, W.; Niu, C.F.; Wei, W.; Hu, Y.; Han, J.Q.; Lu, X.; Tao, J.J.; Jin, M.; Qin, H. et al. A class B heat shock factor selected for during soybean domestication contributes to salt tolerance by promoting flavonoid biosynthesis. New Phytol.; 2020; 225, pp. 268-283. [DOI: https://dx.doi.org/10.1111/nph.16104]

30. Noctor, G.; Foyer, C.H. Ascorbate and glutathione: Keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol.; 1998; 49, pp. 249-279. [DOI: https://dx.doi.org/10.1146/annurev.arplant.49.1.249] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/15012235]

31. Gill, S.S.; Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem.; 2010; 48, pp. 909-930. [DOI: https://dx.doi.org/10.1016/j.plaphy.2010.08.016] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20870416]

32. Begara-Morales, J.C.; Sanchez-Calvo, B.; Chaki, M.; Mata-Perez, C.; Valderrama, R.; Padilla, M.N.; Lopez-Jaramillo, J.; Luque, F.; Corpas, F.J.; Barroso, J.B. Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J. Exp. Bot.; 2015; 66, pp. 5983-5996. [DOI: https://dx.doi.org/10.1093/jxb/erv306]

33. Madeira, C.; Mendonca, V.; Leal, M.C.; Flores, A.; Cabral, H.N.; Diniz, M.S.; Vinagre, C. Environmental health assessment of warming coastal ecosystems in the tropics—Application of integrative physiological indices. Sci. Total Environ.; 2018; 643, pp. 28-39. [DOI: https://dx.doi.org/10.1016/j.scitotenv.2018.06.152]

34. Palma, J.M.; Mateos, R.M.; Lopez-Jaramillo, J.; Rodriguez-Ruiz, M.; Gonzalez-Gordo, S.; Lechuga-Sancho, A.M.; Corpas, F.J. Plant catalases as NO and H(2)S targets. Redox Biol.; 2020; 34, 101525. [DOI: https://dx.doi.org/10.1016/j.redox.2020.101525]

35. Xiao, S.; Song, W.; Xing, J.; Su, A.; Zhao, Y.; Li, C.; Shi, Z.; Li, Z.; Wang, S.; Zhang, R. et al. ORF355 confers enhanced salinity stress adaptability to S-type cytoplasmic male sterility maize by modulating the mitochondrial metabolic homeostasis. J. Integr. Plant Biol.; 2023; 65, pp. 656-673. [DOI: https://dx.doi.org/10.1111/jipb.13382]

36. Chen, Y.; Dan, Z.; Li, S. GROWTH REGULATING FACTOR 7-mediated arbutin metabolism enhances rice salt tolerance. Plant Cell; 2024; 36, pp. 2834-2850. [DOI: https://dx.doi.org/10.1093/plcell/koae140]

37. Xing, L.; Zhu, M.; Luan, M.; Zhang, M.; Jin, L.; Liu, Y.; Zou, J.; Wang, L.; Xu, M. miR169q and NUCLEAR FACTOR YA8 enhance salt tolerance by activating PEROXIDASE1 expression in response to ROS. Plant Physiol.; 2022; 188, pp. 608-623. [DOI: https://dx.doi.org/10.1093/plphys/kiab498] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34718783]

38. Zhou, Y.B.; Liu, C.; Tang, D.Y.; Yan, L.; Wang, D.; Yang, Y.Z.; Gui, J.S.; Zhao, X.Y.; Li, L.G.; Tang, X.D. et al. The receptor-like cytoplasmic kinase STRK1 phosphorylates and activates CatC, thereby regulating H(2)O(2) homeostasis and improving salt tolerance in rice. Plant Cell; 2018; 30, pp. 1100-1118. [DOI: https://dx.doi.org/10.1105/tpc.17.01000]

39. Liu, C.; Lin, J.Z.; Wang, Y.; Tian, Y.; Zheng, H.P.; Zhou, Z.K.; Zhou, Y.B.; Tang, X.D.; Zhao, X.H.; Wu, T. et al. The protein phosphatase PC1 dephosphorylates and deactivates CatC to negatively regulate H₂O₂ homeostasis and salt tolerance in rice. Plant Cell; 2023; 35, pp. 3604-3625. [DOI: https://dx.doi.org/10.1093/plcell/koad167]

40. Zhang, Z.; Wang, J.; Zhang, R.; Huang, R. The ethylene response factor AtERF98 enhances tolerance to salt through the transcriptional activation of ascorbic acid synthesis in Arabidopsis. Plant J.; 2012; 71, pp. 273-287. [DOI: https://dx.doi.org/10.1111/j.1365-313X.2012.04996.x]

41. Wang, J.; Yu, Y.; Zhang, Z.; Quan, R.; Zhang, H.; Ma, L.; Deng, X.W.; Huang, R. Arabidopsis CSN5B interacts with VTC1 and modulates ascorbic acid synthesis. Plant Cell; 2013; 25, pp. 625-636. [DOI: https://dx.doi.org/10.1105/tpc.112.106880] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/23424245]

42. Li, S.; Wang, J.; Yu, Y.; Wang, F.; Dong, J.; Huang, R. D27E mutation of VTC1 impairs the interaction with CSN5B and enhances ascorbic acid biosynthesis and seedling growth in Arabidopsis. Plant Mol. Biol.; 2016; 92, pp. 473-482. [DOI: https://dx.doi.org/10.1007/s11103-016-0525-0]

43. Li, Y.; Chu, Z.; Luo, J.; Zhou, Y.; Cai, Y.; Lu, Y.; Xia, J.; Kuang, H.; Ye, Z.; Ouyang, B. The C2H2 zinc-finger protein SlZF3 regulates AsA synthesis and salt tolerance by interacting with CSN5B. Plant Biotechnol. J.; 2018; 16, pp. 1201-1213. [DOI: https://dx.doi.org/10.1111/pbi.12863] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29193661]

44. Qin, H.; Wang, Y.; Wang, J.; Liu, H.; Zhao, H.; Deng, Z.; Zhang, Z.; Huang, R.; Zhang, Z. Knocking down the expression of GMPase gene OsVTC1-1 decreases salt tolerance of rice at seedling and reproductive stages. PLoS ONE; 2016; 11, e0168650. [DOI: https://dx.doi.org/10.1371/journal.pone.0168650]

45. Wang, J.; Li, D.; Peng, Y.; Cai, M.; Liang, Z.; Yuan, Z.; Du, X.; Wang, J.; Schnable, P.S.; Gu, R. et al. The anthocyanin accumulation related ZmBZ1, facilitates seedling salinity stress tolerance via ROS scavenging. Int. J. Mol. Sci.; 2022; 23, 16123. [DOI: https://dx.doi.org/10.3390/ijms232416123] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/36555763]

46. Sun, Y.; Zhou, Y.; Long, Q.; Xing, J.; Guo, P.; Liu, Y.; Zhang, C.; Zhang, Y.; Fernie, A.R.; Shi, Y. et al. OsBCAT2, a gene responsible for the degradation of branched-chain amino acids, positively regulates salt tolerance by promoting the synthesis of vitamin B5. New Phytol.; 2024; 241, pp. 2558-2574. [DOI: https://dx.doi.org/10.1111/nph.19551] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/38258425]

47. Dong, N.Q.; Sun, Y.; Guo, T.; Shi, C.L.; Zhang, Y.M.; Kan, Y.; Xiang, Y.H.; Zhang, H.; Yang, Y.B.; Li, Y.C. et al. UDP-glucosyltransferase regulates grain size and abiotic stress tolerance associated with metabolic flux redirection in rice. Nat. Commun.; 2020; 11, 2629. [DOI: https://dx.doi.org/10.1038/s41467-020-16403-5] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32457405]

48. Xiao, G.; Wang, M.; Li, X.; Jiang, Z.; Zhang, H.; Gao, D.; Zhang, B.; Xia, G.; Wang, M. TaCHP encoding C1-domain protein stably enhances wheat yield in saline-alkaline fields. J. Integr. Plant Biol.; 2024; 66, pp. 169-171. [DOI: https://dx.doi.org/10.1111/jipb.13605]

49. Sun, W.; Zhang, H.; Yang, S.; Liu, L.; Xie, P.; Li, J.; Zhu, Y.; Ouyang, Y.; Xie, Q.; Zhang, H. et al. Genetic modification of Ggamma subunit AT1 enhances salt-alkali tolerance in main graminaceous crops. Natl. Sci. Rev.; 2023; 10, nwad075. [DOI: https://dx.doi.org/10.1093/nsr/nwad075]

50. Zhang, H.; Yu, F.; Xie, P.; Sun, S.; Qiao, X.; Tang, S.; Chen, C.; Yang, S.; Mei, C.; Yang, D. et al. A Gγ protein regulates alkaline sensitivity in crops. Science; 2023; 379, eade8416. [DOI: https://dx.doi.org/10.1126/science.ade8416]

51. Ellouzi, H.; Ben, H.K.; Hernandez, I.; Cela, J.; Muller, M.; Magne, C.; Abdelly, C.; Munne-Bosch, S. A comparative study of the early osmotic, ionic, redox and hormonal signaling response in leaves and roots of two halophytes and a glycophyte to salinity. Planta; 2014; 240, pp. 1299-1317. [DOI: https://dx.doi.org/10.1007/s00425-014-2154-7] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/25156490]

52. Tao, J.J.; Chen, H.W.; Ma, B.; Zhang, W.K.; Chen, S.Y.; Zhang, J.S. The role of ethylene in plants under salinity stress. Front. Plant Sci.; 2015; 6, 1059. [DOI: https://dx.doi.org/10.3389/fpls.2015.01059]

53. Qin, H.; Wang, J.; Chen, X.; Wang, F.; Peng, P.; Zhou, Y.; Miao, Y.; Zhang, Y.; Gao, Y.; Qi, Y. et al. Rice OsDOF15 contributes to ethylene-inhibited primary root elongation under salt stress. New Phytol.; 2019; 223, pp. 798-813. [DOI: https://dx.doi.org/10.1111/nph.15824]

54. Huang, Y.; Guo, Y.; Liu, Y.; Zhang, F.; Wang, Z.; Wang, H.; Wang, F.; Li, D.; Mao, D.; Luan, S. et al. 9-cis-epoxycarotenoid dioxygenase 3 regulates plant growth and enhances multi-abiotic stress tolerance in rice. Front. Plant Sci.; 2018; 9, 162. [DOI: https://dx.doi.org/10.3389/fpls.2018.00162] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29559982]

55. Huang, Y.; Jiao, Y.; Xie, N.; Guo, Y.; Zhang, F.; Xiang, Z.; Wang, R.; Wang, F.; Gao, Q.; Tian, L. et al. OsNCED5, a 9-cis-epoxycarotenoid dioxygenase gene, regulates salt and water stress tolerance and leaf senescence in rice. Plant Sci.; 2019; 287, 110188. [DOI: https://dx.doi.org/10.1016/j.plantsci.2019.110188] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31481229]

56. Feng, Z.J.; Cui, X.Y.; Cui, X.Y.; Chen, M.; Yang, G.X.; Ma, Y.Z.; He, G.Y.; Xu, Z.S. The soybean GmDi19-5 interacts with GmLEA3.1 and increases sensitivity of transgenic plants to abiotic stresses. Front. Plant Sci.; 2015; 6, 179. [DOI: https://dx.doi.org/10.3389/fpls.2015.00179]

57. Yang, Y.; Ren, R.; Karthikeyan, A.; Yin, J.; Jin, T.; Fang, F.; Cai, H.; Liu, M.; Wang, D.; Zhi, H. et al. The soybean GmPUB21-interacting protein GmDi19-5 responds to drought and salinity stresses via an ABA-dependent pathway. Crop J.; 2023; 11, pp. 1152-1162. [DOI: https://dx.doi.org/10.1016/j.cj.2023.05.005]

58. Liu, Z.; Jiang, S.; Jiang, L.; Li, W.; Tang, Y.; He, W.; Wang, M.; Xing, J.; Cui, Y.; Lin, Q. et al. Transcription factor OsSGL is a regulator of starch synthesis and grain quality in rice. J. Exp. Bot.; 2022; 73, pp. 3417-3430. [DOI: https://dx.doi.org/10.1093/jxb/erac068] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/35182423]

59. Jiang, L.; Xiao, W.; Chen, H.; Qi, Y.; Kuang, X.; Shi, J.; Liu, Z.; Cao, J.; Lin, Q.; Yu, F. et al. The OsGAPC1-OsSGL module negatively regulates salt tolerance by mediating abscisic acid biosynthesis in rice. New Phytol.; 2024; 244, pp. 825-839. [DOI: https://dx.doi.org/10.1111/nph.20061]

60. Ma, H.; Song, L.; Shu, Y.; Wang, S.; Niu, J.; Wang, Z.; Yu, T.; Gu, W.; Ma, H. Comparative proteomic analysis of seedling leaves of different salt tolerant soybean genotypes. J. Proteom.; 2012; 75, pp. 1529-1546. [DOI: https://dx.doi.org/10.1016/j.jprot.2011.11.026] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/22155470]

61. Yang, C.; Ma, B.; He, S.J.; Xiong, Q.; Duan, K.X.; Yin, C.C.; Chen, H.; Lu, X.; Chen, S.Y.; Zhang, J.S. MAOHUZI6/ETHYLENE INSENSITIVE3-LIKE1 and ETHYLENE INSENSITIVE3-LIKE2 regulate ethylene response of roots and coleoptiles and negatively affect salt tolerance in rice. Plant Physiol.; 2015; 169, pp. 148-165. [DOI: https://dx.doi.org/10.1104/pp.15.00353]

62. Li, C.H.; Wang, G.; Zhao, J.L.; Zhang, L.Q.; Ai, L.F.; Han, Y.F.; Sun, D.Y.; Zhang, S.W.; Sun, Y. The receptor-like kinase SIT1 mediates salt sensitivity by activating MAPK3/6 and regulating ethylene homeostasis in rice. Plant Cell; 2014; 26, pp. 2538-2553. [DOI: https://dx.doi.org/10.1105/tpc.114.125187] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24907341]

63. Colebrook, E.H.; Thomas, S.G.; Phillips, A.L.; Hedden, P. The role of gibberellin signalling in plant responses to abiotic stress. J. Exp. Biol.; 2014; 217, pp. 67-75. [DOI: https://dx.doi.org/10.1242/jeb.089938] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24353205]

64. Magome, H.; Yamaguchi, S.; Hanada, A.; Kamiya, Y.; Oda, K. The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J.; 2008; 56, pp. 613-626. [DOI: https://dx.doi.org/10.1111/j.1365-313X.2008.03627.x]

65. Shan, C.; Mei, Z.; Duan, J.; Chen, H.; Feng, H.; Cai, W. OsGA2ox5, a gibberellin metabolism enzyme, is involved in plant growth, the root gravity response and salt stress. PLoS ONE; 2014; 9, e87110. [DOI: https://dx.doi.org/10.1371/journal.pone.0087110] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/24475234]

66. Zhou, J.; Li, Z.; Xiao, G.; Zhai, M.; Pan, X.; Huang, R.; Zhang, H. CYP71D8L is a key regulator involved in growth and stress responses by mediating gibberellin homeostasis in rice. J. Exp. Bot.; 2020; 71, pp. 1160-1170.

67. Wang, J.; Qin, H.; Zhou, S.; Wei, P.; Zhang, H.; Zhou, Y.; Miao, Y.; Huang, R. The ubiquitin-binding protein OsDSK2a mediates seedling growth and salt responses by regulating gibberellin metabolism in rice. Plant Cell; 2020; 32, pp. 414-428. [DOI: https://dx.doi.org/10.1105/tpc.19.00593]

68. Toda, Y.; Tanaka, M.; Ogawa, D.; Kurata, K.; Kurotani, K.; Habu, Y.; Ando, T.; Sugimoto, K.; Mitsuda, N.; Katoh, E. et al. RICE SALT SENSITIVE3 forms a ternary complex with JAZ and class-C bHLH factors and regulates jasmonate-induced gene expression and root cell elongation. Plant Cell; 2013; 25, pp. 1709-1725. [DOI: https://dx.doi.org/10.1105/tpc.113.112052]

69. Yamada, S.; Kano, A.; Tamaoki, D.; Miyamoto, A.; Shishido, H.; Miyoshi, S.; Taniguchi, S.; Akimitsu, K.; Gomi, K. Involvement of OsJAZ8 in jasmonate-induced resistance to bacterial blight in rice. Plant Cell Physiol.; 2012; 53, pp. 2060-2072. [DOI: https://dx.doi.org/10.1093/pcp/pcs145]

70. Peethambaran, P.K.; Glenz, R.; Honinger, S.; Shahinul, I.S.; Hummel, S.; Harter, K.; Kolukisaoglu, U.; Meynard, D.; Guiderdoni, E.; Nick, P. et al. Salt-inducible expression of OsJAZ8 improves resilience against salt-stress. BMC Plant Biol.; 2018; 18, 311. [DOI: https://dx.doi.org/10.1186/s12870-018-1521-0]

71. Li, X.; Li, C.; Shi, L.; Lv, G.; Li, X.; Liu, Y.; Jia, X.; Liu, J.; Chen, Y.; Zhu, L. et al. Jasmonate signaling pathway confers salt tolerance through a NUCLEAR FACTOR-Y trimeric transcription factor complex in Arabidopsis. Cell Rep.; 2024; 43, 113825. [DOI: https://dx.doi.org/10.1016/j.celrep.2024.113825]

72. Li, X.; Wang, Z.; Sun, S.; Dai, Z.; Zhang, J.; Wang, W.; Peng, K.; Geng, W.; Xia, S.; Liu, Q. et al. IbNIEL-mediated degradation of IbNAC087 regulates jasmonic acid-dependent salt and drought tolerance in sweet potato. J. Integr. Plant Biol.; 2024; 66, pp. 176-195. [DOI: https://dx.doi.org/10.1111/jipb.13612] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/38294064]

73. Deng, P.; Jing, W.; Cao, C.; Sun, M.; Chi, W.; Zhao, S.; Dai, J.; Shi, X.; Wu, Q.; Zhang, B. et al. Transcriptional repressor RST1 controls salt tolerance and grain yield in rice by regulating gene expression of asparagine synthetase. Proc. Natl. Acad. Sci. USA; 2022; 119, e2210338119. [DOI: https://dx.doi.org/10.1073/pnas.2210338119]

74. Lo, S.F.; Cheng, M.L.; Hsing, Y.C.; Chen, Y.S.; Lee, K.W.; Hong, Y.F.; Hsiao, Y.; Hsiao, A.S.; Chen, P.J.; Wong, L.I. et al. Rice Big Grain 1 promotes cell division to enhance organ development, stress tolerance and grain yield. Plant Biotechnol. J.; 2020; 18, pp. 1969-1983. [DOI: https://dx.doi.org/10.1111/pbi.13357] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/32034845]

75. Mao, C.; He, J.; Liu, L.; Deng, Q.; Yao, X.; Liu, C.; Qiao, Y.; Li, P.; Ming, F. OsNAC2 integrates auxin and cytokinin pathways to modulate rice root development. Plant Biotechnol. J.; 2020; 18, pp. 429-442. [DOI: https://dx.doi.org/10.1111/pbi.13209] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31389120]

76. Nishiyama, R.; Watanabe, Y.; Fujita, Y.; Le, D.T.; Kojima, M.; Werner, T.; Vankova, R.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Kakimoto, T. et al. Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell; 2011; 23, pp. 2169-2183. [DOI: https://dx.doi.org/10.1105/tpc.111.087395]

77. Wu, X.; He, J.; Chen, J.; Yang, S.; Zha, D. Alleviation of exogenous 6-benzyladenine on two genotypes of eggplant (Solanum melongena Mill.) growth under salt stress. Protoplasma; 2014; 251, pp. 169-176. [DOI: https://dx.doi.org/10.1007/s00709-013-0535-6]

78. Yan, Z.; Wang, J.; Wang, F.; Xie, C.; Lv, B.; Yu, Z.; Dai, S.; Liu, X.; Xia, G.; Tian, H. et al. MPK3/6-induced degradation of ARR1/10/12 promotes salt tolerance in Arabidopsis. EMBO Rep.; 2021; 22, e52457. [DOI: https://dx.doi.org/10.15252/embr.202152457] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34402578]

79. Yin, P.; Liang, X.; Zhao, H.; Xu, Z.; Chen, L.; Yang, X.; Qin, F.; Zhang, J.; Jiang, C. Cytokinin signaling promotes salt tolerance by modulating shoot chloride exclusion in maize. Mol. Plant; 2023; 16, pp. 1031-1047. [DOI: https://dx.doi.org/10.1016/j.molp.2023.04.011] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37101396]

80. Yang, R.; Yang, Z.; Xing, M.; Jing, Y.; Zhang, Y.; Zhang, K.; Zhou, Y.; Zhao, H.; Qiao, W.; Sun, J. TaBZR1 enhances wheat salt tolerance via promoting ABA biosynthesis and ROS scavenging. J. Genet. Genom.; 2023; 50, pp. 861-871. [DOI: https://dx.doi.org/10.1016/j.jgg.2023.09.006] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/37734712]

81. Yu, Y.; Wang, J.; Li, S.; Kakan, X.; Zhou, Y.; Miao, Y.; Wang, F.; Qin, H.; Huang, R. Ascorbic acid integrates the antagonistic modulation of ethylene and abscisic acid in the accumulation of reactive oxygen species. Plant Physiol.; 2019; 179, pp. 1861-1875. [DOI: https://dx.doi.org/10.1104/pp.18.01250] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30723177]

82. Kakan, X.; Yu, Y.; Li, S.; Li, X.; Huang, R.; Wang, J. Ascorbic acid modulation by ABI4 transcriptional repression of VTC2 in the salt tolerance of Arabidopsis. BMC Plant Biol.; 2021; 21, 112. [DOI: https://dx.doi.org/10.1186/s12870-021-02882-1] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33627094]

83. Peng, P.; Gao, Y.; Li, Z.; Yu, Y.; Qin, H.; Guo, Y.; Huang, R.; Wang, J. Proteomic analysis of a rice mutant sd58 possessing a novel d1 allele of heterotrimeric G protein alpha subunit (RGA1) in salt stress with a focus on ROS scavenging. Int. J. Mol. Sci.; 2019; 20, 167. [DOI: https://dx.doi.org/10.3390/ijms20010167] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30621186]

84. Nie, S.; Huang, W.; He, C.; Wu, B.; Duan, H.; Ruan, J.; Zhao, Q.; Fang, Z. Transcription factor OsMYB2 triggers amino acid transporter OsANT1 expression to regulate rice growth and salt tolerance. Plant Physiol.; 2024; [DOI: https://dx.doi.org/10.1093/plphys/kiae559]

85. Miao, Y.; Lv, D.; Wang, P.; Wang, X.C.; Chen, J.; Miao, C.; Song, C.P. An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell; 2006; 18, pp. 2749-2766. [DOI: https://dx.doi.org/10.1105/tpc.106.044230]

86. Tian, Y.; Fan, M.; Qin, Z.; Lv, H.; Wang, M.; Zhang, Z.; Zhou, W.; Zhao, N.; Li, X.; Han, C. et al. Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor. Nat. Commun.; 2018; 9, 1063. [DOI: https://dx.doi.org/10.1038/s41467-018-03463-x] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/29540799]

87. Liu, W.C.; Song, R.F.; Qiu, Y.M.; Zheng, S.Q.; Li, T.T.; Wu, Y.; Song, C.P.; Lu, Y.T.; Yuan, H.M. Sulfenylation of ENOLASE2 facilitates H(2)O(2)-conferred freezing tolerance in Arabidopsis. Dev. Cell; 2022; 57, pp. 1883-1898. [DOI: https://dx.doi.org/10.1016/j.devcel.2022.06.012]

88. Ren, Y.; Jiang, M.; Zhu, J.K.; Zhou, W.; Zhao, C. Simultaneous mutations in ITPK4 and MRP5 genes result in a low phytic acid level without compromising salt tolerance in Arabidopsis. J. Integr. Plant Biol.; 2024; 66, pp. 2109-2125. [DOI: https://dx.doi.org/10.1111/jipb.13745] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/39031490]

89. Li, S.; Wang, N.; Ji, D.; Zhang, W.; Wang, Y.; Yu, Y.; Zhao, S.; Lyu, M.; You, J.; Zhang, Y. et al. A GmSIN1/GmNCED3s/GmRbohBs feed-forward loop acts as a signal amplifier that regulates root growth in soybean exposed to salt stress. Plant Cell; 2019; 31, pp. 2107-2130. [DOI: https://dx.doi.org/10.1105/tpc.18.00662] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31227558]

90. Fichman, Y.; Mittler, R. Integration of electric, calcium, reactive oxygen species and hydraulic signals during rapid systemic signaling in plants. Plant J.; 2021; 107, pp. 7-20. [DOI: https://dx.doi.org/10.1111/tpj.15360]

91. Liang, X.; Li, J.; Yang, Y.; Jiang, C.; Guo, Y. Designing salt stress-resilient crops: Current progress and future challenges. J. Integr. Plant Biol.; 2024; 66, pp. 303-329. [DOI: https://dx.doi.org/10.1111/jipb.13599] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/38108117]

92. Mao, H.; Sun, S.; Yao, J.; Wang, C.; Yu, S.; Xu, C.; Li, X.; Zhang, Q. Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc. Natl. Acad. Sci. USA; 2010; 107, pp. 19579-19584. [DOI: https://dx.doi.org/10.1073/pnas.1014419107] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/20974950]

93. Wang, J.; Zhu, R.; Meng, Q.; Qin, H.; Quan, R.; Wei, P.; Li, X.; Jiang, L.; Huang, R. A natural variation in OsDSK2a modulates plant growth and salt tolerance through phosphorylation by SnRK1A in rice. Plant Biotechnol. J.; 2024; 22, pp. 1881-1896. [DOI: https://dx.doi.org/10.1111/pbi.14308]

94. Wang, Y.; Chen, W.; Xing, M.; Sun, J.; Wang, S.; Yang, Z.; Huang, J.; Nie, Y.; Zhao, M.; Li, Y. et al. Wild rice GL12 synergistically improves grain length and salt tolerance in cultivated rice. Nat. Commun.; 2024; 15, 9453. [DOI: https://dx.doi.org/10.1038/s41467-024-53611-9] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/39487109]