Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in Rice

Rice (Oryza sativa) is a staple food that feeds more than half the world population. As rice is highly sensitive to soil salinity, current trends in soil salinization threaten global food security. To better understand the mechanistic basis of salinity tolerance in rice, three contrasting rice culti...

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Main Authors: Juan Liu, Sergey Shabala, Lana Shabala, Meixue Zhou, Holger Meinke, Gayatri Venkataraman, Zhonghua Chen, Fanrong Zeng, Quanzhi Zhao
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.01361/full
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spelling doaj-6a3b17fd87604b0787b4cb021f00db7d2020-11-25T01:31:27ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-11-011010.3389/fpls.2019.01361486909Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in RiceJuan Liu0Juan Liu1Sergey Shabala2Sergey Shabala3Lana Shabala4Meixue Zhou5Holger Meinke6Gayatri Venkataraman7Zhonghua Chen8Zhonghua Chen9Fanrong Zeng10Quanzhi Zhao11Collaborative Innovation Center of Henan Grain Crops, Henan Key Laboratory of Rice Biology, Henan Agricultural University, Zhengzhou, ChinaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, AustraliaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, AustraliaInternational Research Centre for Environmental Membrane Biology, Foshan University, Foshan, ChinaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, AustraliaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, AustraliaTasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, AustraliaPlant Molecular Biology Laboratory, M.S. Swaminathan Research Foundation, Chennai, IndiaSchool of Science and Health, Western Sydney University, Penrith, NSW, AustraliaHawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW, AustraliaDepartment of Agronomy, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, ChinaCollaborative Innovation Center of Henan Grain Crops, Henan Key Laboratory of Rice Biology, Henan Agricultural University, Zhengzhou, ChinaRice (Oryza sativa) is a staple food that feeds more than half the world population. As rice is highly sensitive to soil salinity, current trends in soil salinization threaten global food security. To better understand the mechanistic basis of salinity tolerance in rice, three contrasting rice cultivars—Reiziq (tolerant), Doongara (moderately tolerant), and Koshihikari (sensitive)—were examined and the differences in operation of key ion transporters mediating ionic homeostasis in these genotypes were evaluated. Tolerant varieties had reduced Na+ translocation from roots to shoots. Electrophysiological and quantitative reverse transcription PCR experiments showed that tolerant genotypes possessed 2-fold higher net Na+ efflux capacity in the root elongation zone. Interestingly, this efflux was only partially mediated by the plasma membrane Na+/H+ antiporter (OsSOS1), suggesting involvement of some other exclusion mechanisms. No significant difference in Na+ exclusion from the mature root zones was found between cultivars, and the transcriptional changes in the salt overly sensitive signaling pathway genes in the elongation zone were not correlated with the genetic variability in salinity tolerance amongst genotypes. The most important hallmark of differential salinity tolerance was in the ability of the plant to retain K+ in both root zones. This trait was conferred by at least three complementary mechanisms: (1) its superior ability to activate H+-ATPase pump operation, both at transcriptional and functional levels; (2) reduced sensitivity of K+ efflux channels to reactive oxygen species; and (3) smaller upregulation in OsGORK and higher upregulation of OsAKT1 in tolerant cultivars in response to salt stress. These traits should be targeted in breeding programs aimed to improve salinity tolerance in commercial rice cultivars.https://www.frontiersin.org/article/10.3389/fpls.2019.01361/fullrootH+-ATPasepotassiumsodiumNa+/H+ exchangerreactive oxygen species
collection DOAJ
language English
format Article
sources DOAJ
author Juan Liu
Juan Liu
Sergey Shabala
Sergey Shabala
Lana Shabala
Meixue Zhou
Holger Meinke
Gayatri Venkataraman
Zhonghua Chen
Zhonghua Chen
Fanrong Zeng
Quanzhi Zhao
spellingShingle Juan Liu
Juan Liu
Sergey Shabala
Sergey Shabala
Lana Shabala
Meixue Zhou
Holger Meinke
Gayatri Venkataraman
Zhonghua Chen
Zhonghua Chen
Fanrong Zeng
Quanzhi Zhao
Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in Rice
Frontiers in Plant Science
root
H+-ATPase
potassium
sodium
Na+/H+ exchanger
reactive oxygen species
author_facet Juan Liu
Juan Liu
Sergey Shabala
Sergey Shabala
Lana Shabala
Meixue Zhou
Holger Meinke
Gayatri Venkataraman
Zhonghua Chen
Zhonghua Chen
Fanrong Zeng
Quanzhi Zhao
author_sort Juan Liu
title Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in Rice
title_short Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in Rice
title_full Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in Rice
title_fullStr Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in Rice
title_full_unstemmed Tissue-Specific Regulation of Na+ and K+ Transporters Explains Genotypic Differences in Salinity Stress Tolerance in Rice
title_sort tissue-specific regulation of na+ and k+ transporters explains genotypic differences in salinity stress tolerance in rice
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2019-11-01
description Rice (Oryza sativa) is a staple food that feeds more than half the world population. As rice is highly sensitive to soil salinity, current trends in soil salinization threaten global food security. To better understand the mechanistic basis of salinity tolerance in rice, three contrasting rice cultivars—Reiziq (tolerant), Doongara (moderately tolerant), and Koshihikari (sensitive)—were examined and the differences in operation of key ion transporters mediating ionic homeostasis in these genotypes were evaluated. Tolerant varieties had reduced Na+ translocation from roots to shoots. Electrophysiological and quantitative reverse transcription PCR experiments showed that tolerant genotypes possessed 2-fold higher net Na+ efflux capacity in the root elongation zone. Interestingly, this efflux was only partially mediated by the plasma membrane Na+/H+ antiporter (OsSOS1), suggesting involvement of some other exclusion mechanisms. No significant difference in Na+ exclusion from the mature root zones was found between cultivars, and the transcriptional changes in the salt overly sensitive signaling pathway genes in the elongation zone were not correlated with the genetic variability in salinity tolerance amongst genotypes. The most important hallmark of differential salinity tolerance was in the ability of the plant to retain K+ in both root zones. This trait was conferred by at least three complementary mechanisms: (1) its superior ability to activate H+-ATPase pump operation, both at transcriptional and functional levels; (2) reduced sensitivity of K+ efflux channels to reactive oxygen species; and (3) smaller upregulation in OsGORK and higher upregulation of OsAKT1 in tolerant cultivars in response to salt stress. These traits should be targeted in breeding programs aimed to improve salinity tolerance in commercial rice cultivars.
topic root
H+-ATPase
potassium
sodium
Na+/H+ exchanger
reactive oxygen species
url https://www.frontiersin.org/article/10.3389/fpls.2019.01361/full
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