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

Int J Mol Sci. 2020 Nov 17;21(22):8683. 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 Arabidopsisthaliana. 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.

Keywords: Arabidopsis; H2O2; K+/Na+ homeostasis; NaCl; [Ca2+]cyt; eATP; ethylene.

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / metabolism
  • Calcium / metabolism*
  • Calcium Signaling / drug effects*
  • Ethylenes / metabolism*
  • Homeostasis / drug effects*
  • Hydrogen Peroxide / metabolism*
  • Sodium Chloride / pharmacology*

Substances

  • Arabidopsis Proteins
  • Ethylenes
  • Sodium Chloride
  • Adenosine Triphosphate
  • ethylene
  • Hydrogen Peroxide
  • Calcium