Ion Homeostasis and Metabolome Analysis of Arabidopsis 14-3-3 Quadruple Mutants to Salt Stress

Salinity is one of the major abiotic stresses that limits agricultural productivity worldwide. Many proteins with defined functions in salt stress adaptation are controlled through interactions with members of the 14-3-3 family. In the present study, we generated three 14-3-3 quadruple knockout muta...

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Main Authors: Jing Gao, Paula J. M. van Kleeff, Mark H. de Boer, Alexander Erban, Joachim Kopka, Dirk K. Hincha, Albertus H. de Boer
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.697324/full
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spelling doaj-1a3b1175fe174e049872af984fc71df72021-09-13T05:42:41ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-09-011210.3389/fpls.2021.697324697324Ion Homeostasis and Metabolome Analysis of Arabidopsis 14-3-3 Quadruple Mutants to Salt StressJing Gao0Jing Gao1Paula J. M. van Kleeff2Paula J. M. van Kleeff3Mark H. de Boer4Alexander Erban5Joachim Kopka6Dirk K. Hincha7Albertus H. de Boer8Albertus H. de Boer9Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, ChinaDepartment of Structural Biology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Structural Biology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, NetherlandsDepartment of Structural Biology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment Willmitzer, Max Planck Institute Molecular Plant Physiology, Potsdam, GermanyDepartment Willmitzer, Max Planck Institute Molecular Plant Physiology, Potsdam, GermanyDepartment Willmitzer, Max Planck Institute Molecular Plant Physiology, Potsdam, GermanyDepartment of Structural Biology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsDepartment of Medicinal Chemistry, Beta Faculty, Vrije Universiteit Amsterdam, Amsterdam, NetherlandsSalinity is one of the major abiotic stresses that limits agricultural productivity worldwide. Many proteins with defined functions in salt stress adaptation are controlled through interactions with members of the 14-3-3 family. In the present study, we generated three 14-3-3 quadruple knockout mutants (qKOs: klpc, klun, and unpc) to study the role of six non-epsilon group 14-3-3 proteins for salt stress adaptation. The relative growth inhibition under 100 mM of NaCl stress was the same for wild-type (Wt) and qKOs, but the accumulation of Na+ in the shoots of klpc was significantly lower than that in Wt. This difference correlated with the higher expression of the HKT1 gene in klpc. Considering the regulatory role of 14-3-3 proteins in metabolism and the effect of salt stress on metabolite accumulation, we analyzed the effect of a 24-h salt treatment on the root metabolome of nutrient solution-grown genotypes. The results indicated that the klpc mutant had metabolome responses that were different from those of Wt. Notably, the reducing sugars, glucose and fructose, were lower in klpc under control and salt stress. On the other hand, their phosphorylated forms, glucose-6P and fructose-6P, were lower under salt stress as compared to Wt. This study provided insight into the functions of the 14-3-3 proteins from non-epsilon group members. In summary, it was found that these proteins control ion homeostasis and metabolite composition under salt stress conditions and non-stressed conditions. The analyses of single, double, and triple mutants that modify subsets from the most effective qKO mutant (klpc) may also reveal the potential redundancy for the observed phenotypes.https://www.frontiersin.org/articles/10.3389/fpls.2021.697324/full14-3-3salinitymetabolismion homeostasisplant abiotic stress
collection DOAJ
language English
format Article
sources DOAJ
author Jing Gao
Jing Gao
Paula J. M. van Kleeff
Paula J. M. van Kleeff
Mark H. de Boer
Alexander Erban
Joachim Kopka
Dirk K. Hincha
Albertus H. de Boer
Albertus H. de Boer
spellingShingle Jing Gao
Jing Gao
Paula J. M. van Kleeff
Paula J. M. van Kleeff
Mark H. de Boer
Alexander Erban
Joachim Kopka
Dirk K. Hincha
Albertus H. de Boer
Albertus H. de Boer
Ion Homeostasis and Metabolome Analysis of Arabidopsis 14-3-3 Quadruple Mutants to Salt Stress
Frontiers in Plant Science
14-3-3
salinity
metabolism
ion homeostasis
plant abiotic stress
author_facet Jing Gao
Jing Gao
Paula J. M. van Kleeff
Paula J. M. van Kleeff
Mark H. de Boer
Alexander Erban
Joachim Kopka
Dirk K. Hincha
Albertus H. de Boer
Albertus H. de Boer
author_sort Jing Gao
title Ion Homeostasis and Metabolome Analysis of Arabidopsis 14-3-3 Quadruple Mutants to Salt Stress
title_short Ion Homeostasis and Metabolome Analysis of Arabidopsis 14-3-3 Quadruple Mutants to Salt Stress
title_full Ion Homeostasis and Metabolome Analysis of Arabidopsis 14-3-3 Quadruple Mutants to Salt Stress
title_fullStr Ion Homeostasis and Metabolome Analysis of Arabidopsis 14-3-3 Quadruple Mutants to Salt Stress
title_full_unstemmed Ion Homeostasis and Metabolome Analysis of Arabidopsis 14-3-3 Quadruple Mutants to Salt Stress
title_sort ion homeostasis and metabolome analysis of arabidopsis 14-3-3 quadruple mutants to salt stress
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-09-01
description Salinity is one of the major abiotic stresses that limits agricultural productivity worldwide. Many proteins with defined functions in salt stress adaptation are controlled through interactions with members of the 14-3-3 family. In the present study, we generated three 14-3-3 quadruple knockout mutants (qKOs: klpc, klun, and unpc) to study the role of six non-epsilon group 14-3-3 proteins for salt stress adaptation. The relative growth inhibition under 100 mM of NaCl stress was the same for wild-type (Wt) and qKOs, but the accumulation of Na+ in the shoots of klpc was significantly lower than that in Wt. This difference correlated with the higher expression of the HKT1 gene in klpc. Considering the regulatory role of 14-3-3 proteins in metabolism and the effect of salt stress on metabolite accumulation, we analyzed the effect of a 24-h salt treatment on the root metabolome of nutrient solution-grown genotypes. The results indicated that the klpc mutant had metabolome responses that were different from those of Wt. Notably, the reducing sugars, glucose and fructose, were lower in klpc under control and salt stress. On the other hand, their phosphorylated forms, glucose-6P and fructose-6P, were lower under salt stress as compared to Wt. This study provided insight into the functions of the 14-3-3 proteins from non-epsilon group members. In summary, it was found that these proteins control ion homeostasis and metabolite composition under salt stress conditions and non-stressed conditions. The analyses of single, double, and triple mutants that modify subsets from the most effective qKO mutant (klpc) may also reveal the potential redundancy for the observed phenotypes.
topic 14-3-3
salinity
metabolism
ion homeostasis
plant abiotic stress
url https://www.frontiersin.org/articles/10.3389/fpls.2021.697324/full
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