Biphasic activation of survival and death pathways in Arabidopsis thaliana cultured cells by sorbitol-induced hyperosmotic stress

Tingting Zhao; Delphine Arbelet-Bonnin; Daniel Tran; Emanuela Monetti; Arnaud Lehner; Patrice Meimoun; Takashi Kadono; Aurélien Dauphin; Rafik Errakhi; David Reboutier; Sylvie Cangémi; Tomonori Kawano; Stefano Mancuso; Hayat El-Maarouf-Bouteau; Patrick Laurenti; François Bouteau

doi:10.1016/j.plantsci.2021.110844

Biphasic activation of survival and death pathways in Arabidopsis thaliana cultured cells by sorbitol-induced hyperosmotic stress

Plant Sci. 2021 Apr:305:110844. doi: 10.1016/j.plantsci.2021.110844. Epub 2021 Feb 9.

Authors

Tingting Zhao¹, Delphine Arbelet-Bonnin¹, Daniel Tran², Emanuela Monetti³, Arnaud Lehner², Patrice Meimoun⁴, Takashi Kadono⁵, Aurélien Dauphin², Rafik Errakhi², David Reboutier², Sylvie Cangémi¹, Tomonori Kawano⁶, Stefano Mancuso⁷, Hayat El-Maarouf-Bouteau⁸, Patrick Laurenti¹, François Bouteau⁹

Affiliations

¹ Université de Paris, Laboratoire des Energies de Demain, Paris, France.
² former EA3514, Université Paris Diderot, Paris, France.
³ former EA3514, Université Paris Diderot, Paris, France; LINV-DiSPAA, Department of Agri-Food and Environmental Science, University of Florence, Viale delle Idee 30, 50019, Sesto Fiorentino (FI), Italy.
⁴ Université de Paris, Laboratoire des Energies de Demain, Paris, France; former EA3514, Université Paris Diderot, Paris, France; Université de Paris, Paris Interdisciplinary Energy Research Institute (PIERI), Paris, France.
⁵ former EA3514, Université Paris Diderot, Paris, France; Graduate School of Environmental Engineering, University of Kitakyushu, 1-1, Hibikino, Wakamatsu-ku, Kitakyushu 808-0135, Japan.
⁶ LINV-DiSPAA, Department of Agri-Food and Environmental Science, University of Florence, Viale delle Idee 30, 50019, Sesto Fiorentino (FI), Italy; Graduate School of Environmental Engineering, University of Kitakyushu, 1-1, Hibikino, Wakamatsu-ku, Kitakyushu 808-0135, Japan; University of Florence LINV Kitakyushu Research Center (LINV@Kitakyushu), Kitakyushu, Japan; Université de Paris, Paris Interdisciplinary Energy Research Institute (PIERI), Paris, France.
⁷ LINV-DiSPAA, Department of Agri-Food and Environmental Science, University of Florence, Viale delle Idee 30, 50019, Sesto Fiorentino (FI), Italy; University of Florence LINV Kitakyushu Research Center (LINV@Kitakyushu), Kitakyushu, Japan; Université de Paris, Paris Interdisciplinary Energy Research Institute (PIERI), Paris, France.
⁸ Sorbonne Université, UMR7622-IBPS, Paris, France.
⁹ Université de Paris, Laboratoire des Energies de Demain, Paris, France; former EA3514, Université Paris Diderot, Paris, France; LINV-DiSPAA, Department of Agri-Food and Environmental Science, University of Florence, Viale delle Idee 30, 50019, Sesto Fiorentino (FI), Italy; University of Florence LINV Kitakyushu Research Center (LINV@Kitakyushu), Kitakyushu, Japan. Electronic address: francois.bouteau@u-paris.fr.

PMID: 33691971
DOI: 10.1016/j.plantsci.2021.110844

Abstract

Hyperosmotic stresses represent some of the most serious abiotic factors that adversely affect plants growth, development and fitness. Despite their central role, the early cellular events that lead to plant adaptive responses remain largely unknown. In this study, using Arabidopsis thaliana cultured cells we analyzed early cellular responses to sorbitol-induced hyperosmotic stress. We observed biphasic and dual responses of A. thaliana cultured cells to sorbitol-induced hyperosmotic stress. A first set of events, namely singlet oxygen (¹O₂) production and cell hyperpolarization due to a decrease in anion channel activity could participate to signaling and osmotic adjustment allowing cell adaptation and survival. A second set of events, namely superoxide anion (O₂^-) production by RBOHD-NADPH-oxidases and SLAC1 anion channel activation could participate in programmed cell death (PCD) of a part of the cell population. This set of events raises the question of how a survival pathway and a death pathway could be induced by the same hyperosmotic condition and what could be the meaning of the induction of two different behaviors in response to hyperosmotic stress.

Keywords: Anion channels; Arabidopsis thaliana; Hyperosmotic stress; Programmed cell death; Reactive oxygen species.

MeSH terms

Apoptosis / drug effects*
Arabidopsis / metabolism*
Cell Proliferation / drug effects*
Cells, Cultured / drug effects*
Osmoregulation / drug effects*
Osmotic Pressure / drug effects*
Sorbitol / metabolism*

Substances

Sorbitol