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

Abstract

The sodium cation (Na + ) is the predominant cation with deleterious effects on crops in saltaffected 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.

Designing salt stress‐resilient crops: Current progress and future challenges

“…Subfamily I HKT members (HKT1), encoded by AtHKT1 from Arabidopsis, OsHKT1;4 and OsHKT1;5 from rice, and GmHKT1;1 from soybean, reduce the transport of Na + from root to shoot by retrieving Na + from the root xylem (Uozumi et al, 2000; Ren et al, 2005; Oda et al, 2018). Similar mechanisms have been reported in wheat for the TmHKT1;4 and TmHKT1;5 genes (Huang et al, 2006; Munns et al, 2012; Byrt et al, 2014) and in maize for ZmHKT1;1 and ZmHKT1;2 (Zhang et al, 2018, 2023b). The Na + permeability of AtHKT1 is inhibited by PP2C49 (a clade G–type PP2C) under salt stress.…”

“…In Chang7-2, an LRT/Gypsy retrotransposon insertion truncates ZmHKT1;1, leading to increased leaf Na + content and a salt-hypersensitive phenotype (Zhang et al, 2018). In addition, a GWAS revealed that another HKT1 family Na + transporter gene known as ZmNC3/ZmHKT1;2 and a HAK family Na + transporter gene ZmNC2/ZmHAK4 are associated with the shoot Na + content of salt-grown maize seedlings (Zhang et al, 2019a(Zhang et al, , 2023b. A naturally occurring non-synonymous SNP (SNP947-G) increases the Na + transport activity of ZmHKT1;2 by approximately two-fold, thereby promoting shoot Na + exclusion and salt tolerance.…”

“…A naturally occurring non‐synonymous SNP (SNP947‐G) increases the Na + transport activity of ZmHKT1;2 by approximately two‐fold, thereby promoting shoot Na + exclusion and salt tolerance. The ZmHKT1;2 SNP947‐G allele originated from the wild grass teosinte but is present in only 6.1% of modern maize inbred lines; notably, introgressing the ZmHKT1;2 SNP947‐G allele into elite maize germplasms reduces the shoot Na + content by up to 80% under salt conditions (Zhang et al, 2023b). For ZmHAK4 , an intron‐located 12,586‐bp insertion reduces transcript levels, leading to higher shoot Na + contents and a salt‐hypersensitive phenotype.…”

The Pivotal Involvement of theRespiratory burst oxidase G(SlRbohG) Gene in H2O2Production Under Stress for Proper Na+Homeostasis Regulation in Tomato

“…One of the main bottlenecks in breeding programs is the strong reduction of phenotypic and genetic diversity in modern germplasms, due to domestication itself firstly and the development of commercial cultivars secondly, which has led to the phenomenon of genetic erosion, as recently remarked by Kromdijk and McCormick (2022) . In fact, the selection of genes related to agronomic traits during the domestication process ( Liang et al ., 2021 ) was accompanied by the loss of alleles involved in abiotic stress tolerance ( Zhang et al ., 2023 ). Therefore, the identification and introduction of genetic determinants that were lost during domestication may facilitate the development of salt-tolerant crops ( Eckardt et al ., 2023 ).…”

Reshifting Na+ from Shoots into Long Roots Is Associated with Salt Tolerance in Two Contrasting Inbred Maize (Zea mays L.) Lines

“…Many studies in a model plant Arabidopsis thaliana and its mutants have uncovered the regulated mechanisms of salt tolerance, including the salinity overly sensitive (SOS) signaling pathway, the calcium signaling pathway, mitogen-activated protein kinase cascades, and reactive oxygen species (ROS) homeostasis [ 11 , 12 ]. In crop plants, many salt-responsive proteins have been reported, such as vacuolar Na + /H + antiporters (NHXs), high-affinity K + transporters (HKTs), and SOSs, which have important roles in the regulation of Na + and K + ion balance [ 13 , 14 , 15 ].…”