Plant salt-stress response involves complex physiological processes. Previous studies have shown that some factors promote salt tolerance only under high transpiring condition, thus mediating ...transpiration-dependent salt tolerance (TDST). However, the mechanism underlying crop TDST remains largely unknown. Here, we report that ZmSTL1 (Salt-Tolerant Locus 1) confers natural variation of TDST in maize. ZmSTL1 encodes a dirigent protein (termed ZmESBL) localized to the Casparian strip (CS) domain. Mutants lacking ZmESBL display impaired lignin deposition at endodermal CS domain which leads to a defective CS barrier. Under salt condition, mutation of ZmESBL increases the apoplastic transport of Na
across the endodermis, and then increases the root-to-shoot delivery of Na
via transpiration flow, thereby leading to a transpiration-dependent salt hypersensitivity. Moreover, we show that the ortholog of ZmESBL also mediates CS development and TDST in Arabidopsis. Our study suggests that modification of CS barrier may provide an approach for developing salt-tolerant crops.
Abstract
Sodium (Na
+
) toxicity is one of the major damages imposed on crops by saline-alkaline stress. Here we show that natural maize inbred lines display substantial variations in shoot Na
+
...contents and saline-alkaline (NaHCO
3
) tolerance, and reveal that
ZmNSA1
(
Na
+
Content under Saline-Alkaline Condition
) confers shoot Na
+
variations under NaHCO
3
condition by a genome-wide association study. Lacking of ZmNSA1 promotes shoot Na
+
homeostasis by increasing root Na
+
efflux. A naturally occurred 4-bp deletion decreases the translation efficiency of
ZmNSA1
mRNA, thus promotes Na
+
homeostasis. We further show that, under saline-alkaline condition, Ca
2+
binds to the EF-hand domain of ZmNSA1 then triggers its degradation via 26S proteasome, which in turn increases the transcripts levels of PM-H
+
-ATPases (
MHA2
and
MHA4
), and consequently enhances SOS1 Na
+
/H
+
antiporter-mediated root Na
+
efflux. Our studies reveal the mechanism of Ca
2+
-triggered saline-alkaline tolerance and provide an important gene target for breeding saline-alkaline tolerant maize varieties.
Abstract
Maize (
Zea mays
L.) is a cold-sensitive species that often faces chilling stress, which adversely affects growth and reproduction. However, the genetic basis of low-temperature adaptation ...in maize remains unclear. Here, we demonstrate that natural variation in the type-A
Response Regulator 1
(
ZmRR1
) gene leads to differences in chilling tolerance among maize inbred lines. Association analysis reveals that InDel-35 of
ZmRR1
, encoding a protein harboring a mitogen-activated protein kinase (MPK) phosphorylation residue, is strongly associated with chilling tolerance. ZmMPK8, a negative regulator of chilling tolerance, interacts with and phosphorylates ZmRR1 at Ser15. The deletion of a 45-bp region of ZmRR1 harboring Ser15 inhibits its degradation via the 26 S proteasome pathway by preventing its phosphorylation by ZmMPK8. Transcriptome analysis indicates that ZmRR1 positively regulates the expression of
ZmDREB1
and
Cellulose synthase
(
CesA
) genes to enhance chilling tolerance. Our findings thus provide a potential genetic resource for improving chilling tolerance in maize.
Coordination of shoot photosynthetic carbon fixation with root inorganic nitrogen uptake optimizes plant performance in a fluctuating environment 1. However, the molecular basis of this long-distance ...shoot-root coordination is little understood. Here we show that Arabidopsis ELONGATED HYPOCOTYL5 (HY5), a bZIP transcription factor that regulates growth in response to light 2, 3, is a shoot-to-root mobile signal that mediates light promotion of root growth and nitrate uptake. Shoot-derived HY5 auto-activates root HY5 and also promotes root nitrate uptake by activating NRT2.1, a gene encoding a high-affinity nitrate transporter 4. In the shoot, HY5 promotes carbon assimilation and translocation, whereas in the root, HY5 activation of NRT2.1 expression and nitrate uptake is potentiated by increased carbon photoassimilate (sucrose) levels. We further show that HY5 function is fluence-rate modulated and enables homeostatic maintenance of carbon-nitrogen balance in different light environments. Thus, mobile HY5 coordinates light-responsive carbon and nitrogen metabolism, and hence shoot and root growth, in a whole-organismal response to ambient light fluctuations.
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•HY5 is essential for light-responsive coordination of the growth of shoots and roots•Shoot-to-root translocated HY5 mediate light-activated root growth and N uptake•Carbohydrate photosynthate-induced NRT2.1 expression and N uptake depend upon HY5•HY5 contributes to maintain balance of C and N metabolism at varying light fluence
Chen et al. show that transcription factor HY5 is a shoot-to-root mobile signal that mediates light-responsive coupling of shoot growth and C assimilation with root growth and N uptake in Arabidopsis. HY5 mobility thus contributes to maintain homeostatic balance between whole-plant C and N metabolism in response to a fluctuating environment.
• 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.
Summary
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.
See also the Commentary on this article by Arciniegas Vega & Melino, 236: 313–315.
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.
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.
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.
Excessive sodium ion (Na
) concentrations in cultivated land alter crop yield and quality worldwide. Previous studies have shown that shoot Na
exclusion is essential in most crops for salt tolerance. ...Here, we show by a genome-wide association study that Zea may L. Na
content 2 (ZmNC2), encoding the HAK family ion transporter ZmHAK4, confers the natural variation of shoot Na
exclusion and salt tolerance in maize. The ZmHAK4 locus accounts for ~11% of the shoot Na
variation, and a natural ZmHAK4-deficient allele displays a decreased ZmHAK4 expression level and an increased shoot Na
content. ZmHAK4 is preferentially expressed in the root stele and encodes a novel membrane-localized Na
-selective transporter that mediates shoot Na
exclusion, probably by retrieving Na
from xylem sap. ZmHAK4 orthologues were identified in other plant species, and the orthologues of ZmHAK4 in rice and wheat show identical expression patterns and ion transport properties, suggesting that ZmHAK4 orthologues mediate an evolutionarily conserved salt-tolerance mechanism. Finally, we show that ZmHAK4 and ZmHKT1 (a HKT1 family Na
-selective transporter) confer distinct roles in promoting shoot Na
exclusion and salt tolerance, indicating that the combination of the favourable alleles of ZmHKT1 and ZmHAK4 can facilitate the development of salt-tolerant maize varieties.
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