A Salt-Signaling Network Involving Ethylene, Extracellular ATP, Hydrogen Peroxide, and Calcium Mediates K+/Na+ Homeostasis in Arabidopsis.

Tao Lang,Shurong Deng,Chen Deng,Huilong Zhang,Yin Wang,Jun Yao

doi:10.3390/ijms21228683

Abstract

This work aimed at investigating the interactive effects of salt-signaling molecules, i.e., ethylene, extracellular ATP (eATP), H2O2, and cytosolic Ca2+ ([Ca2+]cyt), on the regulation of K+/Na+ homeostasis in Arabidopsis thaliana. The presence of eATP shortened Col-0 hypocotyl length under no-salt conditions. Moreover, eATP decreased relative electrolyte leakage and lengthened root length significantly in salt-treated Col-0 plants but had no obvious effects on the ethylene-insensitive mutants etr1-1 and ein3-1eil1-1. Steady-state ionic flux kinetics showed that exogenous 1-aminocyclopropane-1-carboxylic acid (ACC, an ethylene precursor) and eATP-Na2 (an eATP donor) significantly increased Na+ extrusion and suppressed K+ loss during short-term NaCl treatment. Moreover, ACC remarkably raised the fluorescence intensity of salt-elicited H2O2 and cytosolic Ca2+. Our qPCR data revealed that during 12 h of NaCl stress, application of ACC increased the expression of AtSOS1 and AtAHA1, which encode the plasma membrane (PM) Na+/H+ antiporters (SOS1) and H+-ATPase (H+ pumps), respectively. In addition, eATP markedly increased the transcription of AtEIN3, AtEIL1, and AtETR1, and ACC treatment of Col-0 roots under NaCl stress conditions caused upregulation of AtRbohF and AtSOS2/3, which directly contribute to the H2O2 and Ca2+ signaling pathways, respectively. Briefly, ethylene was triggered by eATP, a novel upstream signaling component, which then activated and strengthened the H2O2 and Ca2+ signaling pathways to maintain K+/Na+ homeostasis under salinity.

Highlights

Salinity, a typical abiotic stress, poses a major threat to the growth and development of herbaceous and woody species worldwide [1,2]
To determine whether extracellular ATP (eATP) interacts with ethylene to contribute to salt tolerance, we examined the phenotypes of eATP-treated Arabidopsis Columbia (Col-0) and the ethylene-sensitive mutants of etr1-1 and ein3-1eil1-1, such as root length, hypocotyl length, and relative electrolytic leakage, under short-term salinity treatment
To determine whether ethylene and eATP could respond to NaCl and whether ethylene interacted with eATP in terms of the resulting phenotype and physiological changes, parameters, such as root length, relative electrolyte leakage, and hypocotyl length, were examined in Col-0, etr1-1, and ein3-1eil1-1 with or without salt stress treatment

Summary

Introduction

A typical abiotic stress, poses a major threat to the growth and development of herbaceous and woody species worldwide [1,2]. Salt injury causes direct disturbances in plant ionic balance. To counter the disruption in ionic homeostasis resulting from cytosolic Na+ accumulation, Na+ extrusion and K+ retention in the overall plant and at the intracellular level play a pivotal role in adapting to salt injury [4,5]. Na+/H+ antiporter and H+-ATPase, two functional proteins located in the plasma membrane (PM) of higher plants, are indispensable for maintaining K+/Na+ homeostasis [6,7,8,9,10]. Besides controlling Na+ homeostasis, the upregulation of PM H+ pumps effectively protects the less-depolarized membrane potential and, restricts salt-elicited K+ loss (efflux) through outward rectifying depolarization-activated non-selective cation channels (DA-NSCCs) and K+-permeable channels (DA-KORCs) [9,13]

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