Manipulating ZmEXPA4 expression ameliorates the drought-induced prolonged anthesis and silking interval in maize.

Drought poses a major environmental threat to maize (Zea mays) production worldwide. Since maize is a monoecious plant, maize grain yield is dependent on the synchronous development of male and female inflorescences. When a drought episode occurs during flowering, however, an asynchronism occurs in the anthesis and silking interval (ASI) that results in significant yield losses. The underlying mechanism responsible for this asynchronism is still unclear. Here, we obtained a comprehensive development-drought transcriptome atlas of maize ears. Genes that function in cell expansion and growth were highly repressed by drought in 50 mm ears. Notably, an association study using a natural-variation population of maize revealed a significant relationship between the level of α-expansin4 (ZmEXPA4) expression and drought-induced increases in ASI. Furthermore, genetic manipulation of ZmEXPA4 expression using a drought-inducible promoter in developing maize ears reduced the ASI under drought conditions. These findings provide important insights into the molecular mechanism underlying the increase in ASI in maize ears subjected to drought and provide a promising strategy that can be used for trait improvement.

Designing salt stress-resilient crops: Current progress and future challenges.

Excess soil salinity affects large regions of land and is a major hindrance to crop production worldwide. Therefore, understanding the molecular mechanisms of plant salt tolerance has scientific importance and practical significance. In recent decades, studies have characterized hundreds of genes associated with plant responses to salt stress in different plant species. These studies have substantially advanced our molecular and genetic understanding of salt tolerance in plants and have introduced an era of molecular design breeding of salt-tolerant crops. This review summarizes our current knowledge of plant salt tolerance, emphasizing advances in elucidating the molecular mechanisms of osmotic stress tolerance, salt-ion transport and compartmentalization, oxidative stress tolerance, alkaline stress tolerance, and the trade-off between growth and salt tolerance. We also examine recent advances in understanding natural variation in the salt tolerance of crops and discuss possible strategies and challenges for designing salt stress-resilient crops. We focus on the model plant Arabidopsis (Arabidopsis thaliana) and the four most-studied crops: rice (Oryza sativa), wheat (Triticum aestivum), maize (Zea mays), and soybean (Glycine max).

A teosinte-derived allele of an HKT1 family sodium transporter improves salt tolerance in maize.

The sodium cation (Na+ ) is the predominant cation with deleterious effects on crops in salt-affected agricultural areas. Salt tolerance of crop can be improved by increasing shoot Na+ exclusion. Therefore, it is crucial to identify and use genetic variants of various crops that promote shoot Na+ exclusion. Here, we show that a HKT1 family gene ZmNC3 (Zea mays L. Na+ Content 3; designated ZmHKT1;2) confers natural variability in shoot-Na+ accumulation and salt tolerance in maize. ZmHKT1;2 encodes a Na+ -preferential transporter localized in the plasma membrane, which mediates shoot Na+ exclusion, likely by withdrawing Na+ from the root xylem flow. A naturally occurring nonsynonymous SNP (SNP947-G) increases the Na+ transport activity of ZmHKT1;2, promoting shoot Na+ exclusion and salt tolerance in maize. SNP947-G first occurred in the wild grass teosinte (at a allele frequency of 43%) and has become a minor allele in the maize population (allele frequency 6.1%), suggesting that SNP947-G is derived from teosinte and that the genomic region flanking SNP947 likely has undergone selection during domestication or post-domestication dispersal of maize. Moreover, we demonstrate that introgression of the SNP947-G ZmHKT1;2 allele into elite maize germplasms reduces shoot Na+ content by up to 80% and promotes salt tolerance. Taken together, ZmNC3/ZmHKT1;2 was identified as an important QTL promoting shoot Na+ exclusion, and its favourable allele provides an effective tool for developing salt-tolerant maize varieties.

The classical SOS pathway confers natural variation of salt tolerance in maize.

Sodium (Na+ ) is the major cation damaging crops in the salinised farmland. Previous studies have shown that the Salt Overly Sensitive (SOS) pathway is important for salt tolerance in Arabidopsis. Nevertheless, the SOS pathway remains poorly investigated in most crops. This study addresses the function of the SOS pathway and its association with the natural variation of salt tolerance in maize. First, we showed that a naturally occurring 4-bp frame-shifting deletion in ZmSOS1 caused the salt hypersensitive phenotype of the maize inbred line LH65. Accordingly, mutants lacking ZmSOS1 also displayed a salt hypersensitive phenotype, due to an impaired root-to-rhizosphere Na+ efflux and an increased shoot Na+ concentration. We next showed that the maize SOS3/SOS2 complex (ZmCBL4/ZmCIPK24a and ZmCBL8/ZmCIPK24a) phosphorylates ZmSOS1 therefore activating its Na+ -transporting activity, with their loss-of-function mutants displaying salt hypersensitive phenotypes. Moreover, we observed that a LTR/Gypsy insertion decreased the expression of ZmCBL8, thereby increasing shoot Na+ concentration in natural maize population. Taken together, our study demonstrated that the maize SOS pathway confers a conservative salt-tolerant role, and the components of SOS pathway (ZmSOS1 and ZmCBL8) confer the natural variations of Na+ regulation and salt tolerance in maize, therefore providing important gene targets for breeding salt-tolerant maize.

Metabolomics-driven gene mining and genetic improvement of tolerance to salt-induced osmotic stress in maize.

The farmland of the world's main corn-producing area is increasingly affected by salt stress. Therefore, the breeding of salt-tolerant cultivars is necessary for the long-term sustainability of global corn production. Previous studies have shown that natural maize varieties display a large diversity of salt tolerance, yet the genetic variants underlying such diversity remain poorly discovered and applied, especially those mediating the tolerance to salt-induced osmotic stress (SIOS). Here we report a metabolomics-driven understanding and genetic improvement of maize SIOS tolerance. Using a LC-MS-based untargeted metabolomics approach, we profiled the metabolomes of 266 maize inbred lines under control and salt conditions, and then identified 37 metabolite biomarkers of SIOS tolerance (METO1-37). Follow-up metabolic GWAS (mGWAS) and genotype-to-phenotype modeling identified 10 candidate genes significantly associating with the SIOS tolerance and METO abundances. Furthermore, we validated that a citrate synthase, a glucosyltransferase and a cytochrome P450 underlie the genotype-METO-SIOS tolerance associations, and showed that their favorable alleles additively improve the SIOS tolerance of elite maize inbred lines. Our study provides a novel insight into the natural variation of maize SIOS tolerance, which boosts the genetic improvement of maize salt tolerance, and demonstrates a metabolomics-based approach for mining crop genes associated with this complex agronomic trait.

A domestication-associated reduction in K+ -preferring HKT transporter activity underlies maize shoot K+ accumulation and salt tolerance.

Maize was domesticated from Balsas teosinte c. 10 000 yr ago. Previous studies have suggested that increased tolerance to environmental stress occurred during maize domestication. However, the underlying genetic basis remains largely unknown. We used a maize (W22)-teosinte recombinant inbred line (RIL) to investigate the salt wild-type tolerance aspects of maize domestication. We revealed that ZmHKT2 is a major QTL that regulates K+ homeostasis in saline soils. ZmHKT2 encodes a K+ -preferring HKT family transporter and probably reduces shoot K+ content by removing K+ ions from root-to-shoot flowing xylem sap, ZmHKT2 deficiency increases xylem sap and shoot K+ concentrations, and increases salt tolerance. A coding sequence polymorphism in the ZmHKT2W22 allele (SNP389-G) confers an amino acid variant ZmHKT2 that increases xylem sap K+ concentration, thereby increasing shoot K+ content and salt tolerance. Additional analyses showed that SNP389-G first existed in teosinte (allele frequency 56% in assayed accessions), then swept through the maize population (allele frequency 98%), and that SNP389-G probably underwent positive selection during maize domestication. We conclude that a domestication-associated reduction in K+ transport activity in ZmHKT2 underlies maize shoot K+ content and salt tolerance, and propose that CRISPR-based editing of ZmHKT2 might provide a feasible strategy for improving maize salt tolerance.

Phosphoproteomic Analysis of Two Contrasting Maize Inbred Lines Provides Insights into the Mechanism of Salt-Stress Tolerance.

Salinity is a major abiotic stress that limits maize yield and quality throughout the world. We investigated phosphoproteomics differences between a salt-tolerant inbred line (Zheng58) and a salt-sensitive inbred line (Chang7-2) in response to short-term salt stress using label-free quantitation. A total of 9448 unique phosphorylation sites from 4116 phosphoproteins in roots and shoots of Zheng58 and Chang7-2 were identified. A total of 209 and 243 differentially regulated phosphoproteins (DRPPs) in response to NaCl treatment were detected in roots and shoots, respectively. Functional analysis of these DRPPs showed that they were involved in carbon metabolism, glutathione metabolism, transport, and signal transduction. Among these phosphoproteins, the expression of 6-phosphogluconate dehydrogenase 2, pyruvate dehydrogenase, phosphoenolpyruvate carboxykinase, glutamate decarboxylase, glutamate synthase, l-gulonolactone oxidase-like, potassium channel AKT1, high-affinity potassium transporter, sodium/hydrogen exchanger, and calcium/proton exchanger CAX1-like protein were significantly regulated in roots, while phosphoenolpyruvate carboxylase 1, phosphoenolpyruvate carboxykinase, sodium/hydrogen exchanger, plasma membrane intrinsic protein 2, glutathione transferases, and abscisic acid-insensitive 5-like protein were significantly regulated in shoots. Zheng58 may activate carbon metabolism, glutathione and ascorbic acid metabolism, potassium and sodium transportation, and the accumulation of glutamate to enhance its salt tolerance. Our results help to elucidate the mechanisms of salt response in maize seedlings. They also provide a basis for further study of the mechanism underlying salt response and tolerance in maize and other crops.

A retrotransposon in an HKT1 family sodium transporter causes variation of leaf Na+ exclusion and salt tolerance in maize.

Soil salinity is one of several major abiotic stresses that constrain maize productivity worldwide. An improved understanding of salt-tolerance mechanisms will thus enhance the breeding of salt-tolerant maize and boost productivity. Previous studies have indicated that the maintenance of leaf Na+ concentration is essential for maize salt tolerance, and the difference in leaf Na+ exclusion has previously been associated with variation in salt tolerance between maize varieties. Here, we report the identification and functional characterization of a maize salt-tolerance quantitative trait locus (QTL), Zea mays Na+ Content1 (ZmNC1), which encodes an HKT-type transporter (designated as ZmHKT1). We show that a natural ZmHKT1 loss-of-function allele containing a retrotransposon insertion confers increased accumulation of Na+ in leaves, and salt hypersensitivity. We next show that ZmHKT1 encodes a plasma membrane-localized Na+ -selective transporter, and is preferentially expressed in root stele (including the parenchyma cells surrounding the xylem vessels). We also show that loss of ZmHKT1 function increases xylem sap Na+ concentration and causes increased root-to-shoot Na+ delivery, indicating that ZmHKT1 promotes leaf Na+ exclusion and salt tolerance by withdrawing Na+ from the xylem sap. We conclude that ZmHKT1 is a major salt-tolerance QTL and identifies an important new gene target in breeding for improved maize salt tolerance.

Environmentally responsive genome-wide accumulation of de novo Arabidopsis thaliana mutations and epimutations.

Evolution is fueled by phenotypic diversity, which is in turn due to underlying heritable genetic (and potentially epigenetic) variation. While environmental factors are well known to influence the accumulation of novel variation in microorganisms and human cancer cells, the extent to which the natural environment influences the accumulation of novel variation in plants is relatively unknown. Here we use whole-genome and whole-methylome sequencing to test if a specific environmental stress (high-salinity soil) changes the frequency and molecular profile of accumulated mutations and epimutations (changes in cytosine methylation status) in mutation accumulation (MA) lineages of Arabidopsis thaliana. We first show that stressed lineages accumulate ∼100% more mutations, and that these mutations exhibit a distinctive molecular mutational spectrum (specific increases in relative frequency of transversion and insertion/deletion [indel] mutations). We next show that stressed lineages accumulate ∼45% more differentially methylated cytosine positions (DMPs) at CG sites (CG-DMPs) than controls, and also show that while many (∼75%) of these CG-DMPs are inherited, some can be lost in subsequent generations. Finally, we show that stress-associated CG-DMPs arise more frequently in genic than in nongenic regions of the genome. We suggest that commonly encountered natural environmental stresses can accelerate the accumulation and change the profiles of novel inherited variants in plants. Our findings are significant because stress exposure is common among plants in the wild, and they suggest that environmental factors may significantly alter the rates and patterns of incidence of the inherited novel variants that fuel plant evolution.

The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses.

Soil salinity is one of the most commonly encountered environmental stresses affecting plant growth and crop productivity. Accordingly, plants have evolved a variety of morphological, physiological and biochemical strategies that enable them to adapt to saline growth conditions. For example, it has long been known that salinity-stress increases both the production of the gaseous stress hormone ethylene and the in planta accumulation of reactive oxygen species (ROS). Recently, there has been significant progress in understanding how the fine-tuning of ethylene biosynthesis and signaling transduction can promote salinity tolerance, and how salinity-induced ROS accumulation also acts as a signal in the mediation of salinity tolerance. Furthermore, recent advances have indicated that ethylene signaling modulates salinity responses largely via regulation of ROS-generating and ROS-scavenging mechanisms. This review focuses on these recent advances in understanding the linked roles of ethylene and ROS in salt tolerance.

ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis.

Sodium (Na) is ubiquitous in soils, and is transported to plant shoots via transpiration through xylem elements in the vascular tissue. However, excess Na is damaging. Accordingly, control of xylem-sap Na concentration is important for maintenance of shoot Na homeostasis, especially under Na stress conditions. Here we report that shoot Na homeostasis of Arabidopsis thaliana plants grown in saline soils is conferred by reactive oxygen species (ROS) regulation of xylem-sap Na concentrations. We show that lack of A. thaliana respiratory burst oxidase protein F (AtrbohF; an NADPH oxidase catalysing ROS production) causes hypersensitivity of shoots to soil salinity. Lack of AtrbohF-dependent salinity-induced vascular ROS accumulation leads to increased Na concentrations in root vasculature cells and in xylem sap, thus causing delivery of damaging amounts of Na to the shoot. We also show that the excess shoot Na delivery caused by lack of AtrbohF is dependent upon transpiration. We conclude that AtrbohF increases ROS levels in wild-type root vasculature in response to raised soil salinity, thereby limiting Na concentrations in xylem sap, and in turn protecting shoot cells from transpiration-dependent delivery of excess Na.

An Arabidopsis soil-salinity-tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis.

High soil Na concentrations damage plants by increasing cellular Na accumulation and K loss. Excess soil Na stimulates ethylene-induced soil-salinity tolerance, the mechanism of which we here define via characterization of an Arabidopsis thaliana mutant displaying transpiration-dependent soil-salinity tolerance. This phenotype is conferred by a loss-of-function allele of ethylene overproducer1 (ETO1; mutant alleles of which cause increased production of ethylene). We show that lack of ETO1 function confers soil-salinity tolerance through improved shoot Na/K homeostasis, effected via the ethylene resistant1-constitutive triple response1 ethylene signaling pathway. Under transpiring conditions, lack of ETO1 function reduces root Na influx and both stelar and xylem sap Na concentrations, thereby restricting root-to-shoot delivery of Na. These effects are associated with increased accumulation of respiratory burst oxidase homolog F (RBOHF)-dependent reactive oxygen species in the root stele. Additionally, lack of ETO1 function leads to significant enhancement of tissue K status by an RBOHF-independent mechanism associated with elevated high-affinity K(+) TRANSPORTER5 transcript levels. We conclude that ethylene promotes soil-salinity tolerance via improved Na/K homeostasis mediated by RBOHF-dependent regulation of Na accumulation and RBOHF-independent regulation of K accumulation.

Genome-wide analysis of mutations in mutant lineages selected following fast-neutron irradiation mutagenesis of Arabidopsis thaliana.

Ionizing radiation has long been known to induce heritable mutagenic change in DNA sequence. However, the genome-wide effect of radiation is not well understood. Here we report the molecular properties and frequency of mutations in phenotypically selected mutant lines isolated following exposure of the genetic model flowering plant Arabidopsis thaliana to fast neutrons (FNs). Previous studies suggested that FNs predominantly induce deletions longer than a kilobase in A. thaliana. However, we found a higher frequency of single base substitution than deletion mutations. While the overall frequency and molecular spectrum of fast-neutron (FN)-induced single base substitutions differed substantially from those of "background" mutations arising spontaneously in laboratory-grown plants, G:C>A:T transitions were favored in both. We found that FN-induced G:C>A:T transitions were concentrated at pyrimidine dinucleotide sites, suggesting that FNs promote the formation of mutational covalent linkages between adjacent pyrimidine residues. In addition, we found that FNs induced more single base than large deletions, and that these single base deletions were possibly caused by replication slippage. Our observations provide an initial picture of the genome-wide molecular profile of mutations induced in A. thaliana by FN irradiation and are particularly informative of the nature and extent of genome-wide mutation in lines selected on the basis of mutant phenotypes from FN-mutagenized A. thaliana populations.

Patterns of homoeologous gene expression shown by RNA sequencing in hexaploid bread wheat.

BACKGROUND: Bread wheat (Triticum aestivum) has a large, complex and hexaploid genome consisting of A, B and D homoeologous chromosome sets. Therefore each wheat gene potentially exists as a trio of A, B and D homoeoloci, each of which may contribute differentially to wheat phenotypes. We describe a novel approach combining wheat cytogenetic resources (chromosome substitution 'nullisomic-tetrasomic' lines) with next generation deep sequencing of gene transcripts (RNA-Seq), to directly and accurately identify homoeologue-specific single nucleotide variants and quantify the relative contribution of individual homoeoloci to gene expression. RESULTS: We discover, based on a sample comprising ~5-10% of the total wheat gene content, that at least 45% of wheat genes are expressed from all three distinct homoeoloci. Most of these genes show strikingly biased expression patterns in which expression is dominated by a single homoeolocus. The remaining ~55% of wheat genes are expressed from either one or two homoeoloci only, through a combination of extensive transcriptional silencing and homoeolocus loss. CONCLUSIONS: We conclude that wheat is tending towards functional diploidy, through a variety of mechanisms causing single homoeoloci to become the predominant source of gene transcripts. This discovery has profound consequences for wheat breeding and our understanding of wheat evolution.

Microarray-based ultra-high resolution discovery of genomic deletion mutations.

BACKGROUND: Oligonucleotide microarray-based comparative genomic hybridization (CGH) offers an attractive possible route for the rapid and cost-effective genome-wide discovery of deletion mutations. CGH typically involves comparison of the hybridization intensities of genomic DNA samples with microarray chip representations of entire genomes, and has widespread potential application in experimental research and medical diagnostics. However, the power to detect small deletions is low. RESULTS: Here we use a graduated series of Arabidopsis thaliana genomic deletion mutations (of sizes ranging from 4 bp to ~5 kb) to optimize CGH-based genomic deletion detection. We show that the power to detect smaller deletions (4, 28 and 104 bp) depends upon oligonucleotide density (essentially the number of genome-representative oligonucleotides on the microarray chip), and determine the oligonucleotide spacings necessary to guarantee detection of deletions of specified size. CONCLUSIONS: Our findings will enhance a wide range of research and clinical applications, and in particular will aid in the discovery of genomic deletions in the absence of a priori knowledge of their existence.

HANDS: a tool for genome-wide discovery of subgenome-specific base-identity in polyploids.

BACKGROUND: The analysis of polyploid genomes is problematic because homeologous subgenome sequences are closely related. This relatedness makes it difficult to assign individual sequences to the specific subgenome from which they are derived, and hinders the development of polyploid whole genome assemblies. RESULTS: We here present a next-generation sequencing (NGS)-based approach for assignment of subgenome-specific base-identity at sites containing homeolog-specific polymorphisms (HSPs): 'HSP base Assignment using NGS data through Diploid Similarity' (HANDS). We show that HANDS correctly predicts subgenome-specific base-identity at >90% of assayed HSPs in the hexaploid bread wheat (Triticum aestivum) transcriptome, thus providing a substantial increase in accuracy versus previous methods for homeolog-specific base assignment. CONCLUSION: We conclude that HANDS enables rapid and accurate genome-wide discovery of homeolog-specific base-identity, a capability having multiple applications in polyploid genomics.

Genetic and molecular exploration of maize environmental stress resilience: Toward sustainable agriculture.

Global climate change exacerbates the effects of environmental stressors, such as drought, flooding, extreme temperatures, salinity, and alkalinity, on crop growth and grain yield, threatening the sustainability of the food supply. Maize (Zea mays) is one of the most widely cultivated crops and the most abundant grain crop in production worldwide. However, the stability of maize yield is highly dependent on environmental conditions. Recently, great progress has been made in understanding the molecular mechanisms underlying maize responses to environmental stresses and in developing stress-resilient varieties due to advances in high-throughput sequencing technologies, multi-omics analysis platforms, and automated phenotyping facilities. In this review, we summarize recent advances in dissecting the genetic factors and networks that contribute to maize abiotic stress tolerance through diverse strategies. We also discuss future challenges and opportunities for the development of climate-resilient maize varieties.

Genome assembly and genetic dissection of a prominent drought-resistant maize germplasm.

In the context of climate change, drought is one of the most limiting factors that influence crop production. Maize, as a major crop, is highly vulnerable to water deficit, which causes significant yield loss. Thus, identification and utilization of drought-resistant germplasm are crucial for the genetic improvement of the trait. Here we report on a high-quality genome assembly of a prominent drought-resistant genotype, CIMBL55. Genomic and genetic variation analyses revealed that 65 favorable alleles of 108 previously identified drought-resistant candidate genes were found in CIMBL55, which may constitute the genetic basis for its excellent drought resistance. Notably, ZmRtn16, encoding a reticulon-like protein, was found to contribute to drought resistance by facilitating the vacuole H+-ATPase activity, which highlights the role of vacuole proton pumps in maize drought resistance. The assembled CIMBL55 genome provided a basis for genetic dissection and improvement of plant drought resistance, in support of global food security.

Cytokinin signaling promotes salt tolerance by modulating shoot chloride exclusion in maize.

Excessive accumulation of chloride (Cl-) in the aboveground tissues under saline conditions is harmful to crops. Increasing the exclusion of Cl- from shoots promotes salt tolerance in various crops. However, the underlying molecular mechanisms remain largely unknown. In this study, we demonstrated that a type A response regulator (ZmRR1) modulates Cl- exclusion from shoots and underlies natural variation of salt tolerance in maize. ZmRR1 negatively regulates cytokinin signaling and salt tolerance, likely by interacting with and inhibiting His phosphotransfer (HP) proteins that are key mediators of cytokinin signaling. A naturally occurring non-synonymous SNP variant enhances the interaction between ZmRR1 and ZmHP2, conferring maize plants with a salt-hypersensitive phenotype. We found that ZmRR1 undergoes degradation under saline conditions, leading to the release of ZmHP2 from ZmRR1 inhibition, and subsequently ZmHP2-mediated signaling improves salt tolerance primarily by promoting Cl- exclusion from shoots. Furthermore, we showed that ZmMATE29 is transcriptionally upregulated by ZmHP2-mediated signaling under highly saline conditions and encodes a tonoplast-located Cl- transporter that promotes Cl- exclusion from shoots by compartmentalizing Cl- into the vacuoles of root cortex cells. Collectively, our study provides an important mechanistic understanding of the cytokinin signaling-mediated promotion of Cl- exclusion from shoots and salt tolerance and suggests that genetic modification to promote Cl- exclusion from shoots is a promising route for developing salt-tolerant maize.

Inhibition of the maize salt overly sensitive pathway by ZmSK3 and ZmSK4.

Soil salinity is a worldwide problem that adversely affects plant growth and crop productivity. The salt overly sensitive (SOS) pathway is evolutionarily conserved and essential for plant salt tolerance. In this study, we reveal how the maize shaggy/glycogen synthase kinase 3-like kinases ZmSK3 and ZmSK4, orthologs of brassinosteroid insensitive 2 in Arabidopsis thaliana, regulate the maize SOS pathway. ZmSK3 and ZmSK4 interact with and phosphorylate ZmSOS2, a core member of the maize SOS pathway. The mutants defective in ZmSK3 or ZmSK4 are hyposensitive to salt stress, with higher salt-induced activity of ZmSOS2 than that in the wild type. Furthermore, the Ca2+ sensors ZmSOS3 and ZmSOS3-like calcium binding protein 8 (ZmSCaBP8) activate ZmSOS2 to maintain Na+/K+ homeostasis under salt stress and may participate in the regulation of ZmSOS2 by ZmSK3 and ZmSK4. These findings discover the regulation of the maize SOS pathway and provide important gene targets for breeding salt-tolerant maize.