Increased salt tolerance with overexpression of cation/proton antiporter 1 genes: a meta‐analysis

Abstract

SummaryCation/proton antiporter 1 (CPA1) genes encode cellular Na+/H+ exchanger proteins, which act to adjust ionic balance. Overexpression of CPA1s can improve plant performance under salt stress. However, the diversified roles of the CPA1 family and the various parameters used in evaluating transgenic plants over‐expressing CPA1s make it challenging to assess the complex functions of CPA1s and their physiological mechanisms in salt tolerance. Using meta‐analysis, we determined how overexpression of CPA1s has influenced several plant characteristics involved in response and resilience to NaCl stress. We also evaluated experimental variables that favour or reduce CPA1 effects in transgenic plants. Viewed across studies, overexpression of CPA1s has increased the magnitude of 10 of the 19 plant characteristics examined, by 25% or more. Among the ten moderating variables, several had substantial impacts on the extent of CPA1 influence: type of culture media, donor and recipient type and genus, and gene family. Genes from monocotyledonous plants stimulated root K+, root K+/Na+, total chlorophyll, total dry weight and root length much more than genes from dicotyledonous species. Genes transformed to or from Arabidopsis have led to smaller CPA1‐induced increases in plant characteristics than genes transferred to or from other genera. Heterogeneous expression of CPA1s led to greater increases in leaf chlorophyll and root length than homologous expression. These findings should help guide future investigations into the function of CPA1s in plant salt tolerance and the use of genetic engineering for breeding of resistance.

Cation Specificity of Vacuolar NHX-Type Cation/H+ Antiporters

“…The experimental evidence strongly supports a role in Na + transport under saline conditions, but more recent functional studies also point to basic roles of vacuolar NHXs under nonsaline conditions that go beyond stress acclimation . In addition to the compartmentation of Na + in the vacuole, NHXs may contribute to salinity tolerance by favorably adjusting cellular K + homeostasis under saline conditions (Ma et al, 2017;Wu et al, 2018).…”

Deletion of the N‐terminal domain of the yeast vacuolar (Na+,K+)/H+ antiporter Vnx1p improves salt tolerance in yeast and transgenic Arabidopsis

“…Vacuolar and endosomal accumulation of K + , and concomitant lowering of cytoplasmic concentrations due to antiporter overexpression, would induce K + uptake mechanisms at the plasma membrane, resulting in maintenance of K + homeostasis in high salt conditions (Huertas et al, 2013;Jiang, Leidi, & Pardo, 2010;Leidi et al, 2009;Rodriguez-Rosales et al, 2008). Several other parameters are also affected, either as a direct consequence of enhanced ion accumulation or through separate pleiotropic mechanisms (Luca, Pardo, & Leidi, 2018;Ma et al, 2017). The studies showing a relationship between the transcript level of vacuolar and endosomal (Na + ,K + )/H + antiporters and salt tolerance were performed in transgenic plants overexpressing a plant gene.…”

Pleiotropic effects of enhancing vacuolar K/H exchange in tomato

“…The protein AtNHX1 of Arabidopsis thaliana was initially described as a main source of salt tolerance in plants by driving Na accumulation into vacuoles (Apse et al , Zhang and Blumwald ). Many subsequent reports confirmed the ability of NHX‐like proteins from various origins to convey salt and drought tolerance to transgenic plants of several species, including crops (Ma et al ), but the underlying mechanism remained uncertain because salt tolerance not always correlated with enhanced Na accumulation (Jiang et al ). A meta‐analysis of a large number of publications reporting tolerance phenotypes of plants overexpressing exchangers of the cation/proton antiporter 1 family (CPA1, which includes NHX proteins) concluded that the transgenic effect on K status was generally more pronounced than on Na content (Ma et al ).…”

“…Many subsequent reports confirmed the ability of NHX‐like proteins from various origins to convey salt and drought tolerance to transgenic plants of several species, including crops (Ma et al ), but the underlying mechanism remained uncertain because salt tolerance not always correlated with enhanced Na accumulation (Jiang et al ). A meta‐analysis of a large number of publications reporting tolerance phenotypes of plants overexpressing exchangers of the cation/proton antiporter 1 family (CPA1, which includes NHX proteins) concluded that the transgenic effect on K status was generally more pronounced than on Na content (Ma et al ). Indeed, AtNHX1 catalyzes K/H and Na/H exchange in biochemical assays with purified vacuoles (Venema et al , Hernandez et al ), and a reverse genetic approach has conclusively shown that the main role for Arabidopsis transporters AtNHX1 and AtNHX2 is the thermodynamically active accumulation of K in cell vacuoles (Bassil et al , Barragan et al , Andres et al ).…”

“…Since the discovery of NHX proteins, many reports have asserted the use of these proteins as determinants of salt tolerance (Ma et al ). However, as indicated above, the NHX1‐overexpression in tomato reduces K cytosolic activity (Leidi et al ) and this also might interfere with key metabolic processes in which K is involved as cofactor or signaling element.…”