ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis

Caifu Jiang; Eric J. Belfield; Aziz Mithani; Anne Visscher; Jiannis Ragoussis; Richard Mott; J. Andrew C. Smith; Nicholas P. Harberd

doi:10.1038/emboj.2012.273

ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis

Caifu Jiang, Eric J. Belfield, Aziz Mithani, Anne Visscher, Jiannis Ragoussis, Richard Mott, J. Andrew C. Smith, Nicholas P. Harberd

Research output: Contribution to journal › Article › peer-review

154 Scopus citations

Abstract

Sodium (Na) is ubiquitous in soils, and is transported to plant shoots via transpiration through xylem elements in the vascular tissue. However, excess Na is damaging. Accordingly, control of xylem-sap Na concentration is important for maintenance of shoot Na homeostasis, especially under Na stress conditions. Here we report that shoot Na homeostasis of Arabidopsis thaliana plants grown in saline soils is conferred by reactive oxygen species (ROS) regulation of xylem-sap Na concentrations. We show that lack of A. thaliana respiratory burst oxidase protein F (AtrbohF; an NADPH oxidase catalysing ROS production) causes hypersensitivity of shoots to soil salinity. Lack of AtrbohF-dependent salinity-induced vascular ROS accumulation leads to increased Na concentrations in root vasculature cells and in xylem sap, thus causing delivery of damaging amounts of Na to the shoot. We also show that the excess shoot Na delivery caused by lack of AtrbohF is dependent upon transpiration. We conclude that AtrbohF increases ROS levels in wild-type root vasculature in response to raised soil salinity, thereby limiting Na concentrations in xylem sap, and in turn protecting shoot cells from transpiration-dependent delivery of excess Na. © 2012 European Molecular Biology Organization.

Original language	English (US)
Pages (from-to)	4359-4370
Number of pages	12
Journal	EMBO JOURNAL
Volume	31
Issue number	22
DOIs	https://doi.org/10.1038/emboj.2012.273
State	Published - 2012
Externally published	Yes

Bibliographical note

KAUST Repository Item: Exported on 2021-09-21
Acknowledgements: We thank Liam Dolan for atrbohI, atrbohJ, atrbohH, atrbohE and atrbohC seeds, Jian-Kang Zhu and Yan Guo for stimulating discussion, and Xiangchao Gan for assistance with genome sequence analysis. This publication is based on the work supported by Award No. KUK-I1-002-03, made by King Abdullah University of Science and Technology, and by Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/F020759/1 and BB/F022697/1. RM and JR are supported by the Wellcome Trust grant 075491/Z/04.
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

ASJC Scopus subject areas

General Neuroscience
General Biochemistry, Genetics and Molecular Biology
Molecular Biology
General Immunology and Microbiology

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10.1038/emboj.2012.273

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title = "ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis",

abstract = "Sodium (Na) is ubiquitous in soils, and is transported to plant shoots via transpiration through xylem elements in the vascular tissue. However, excess Na is damaging. Accordingly, control of xylem-sap Na concentration is important for maintenance of shoot Na homeostasis, especially under Na stress conditions. Here we report that shoot Na homeostasis of Arabidopsis thaliana plants grown in saline soils is conferred by reactive oxygen species (ROS) regulation of xylem-sap Na concentrations. We show that lack of A. thaliana respiratory burst oxidase protein F (AtrbohF; an NADPH oxidase catalysing ROS production) causes hypersensitivity of shoots to soil salinity. Lack of AtrbohF-dependent salinity-induced vascular ROS accumulation leads to increased Na concentrations in root vasculature cells and in xylem sap, thus causing delivery of damaging amounts of Na to the shoot. We also show that the excess shoot Na delivery caused by lack of AtrbohF is dependent upon transpiration. We conclude that AtrbohF increases ROS levels in wild-type root vasculature in response to raised soil salinity, thereby limiting Na concentrations in xylem sap, and in turn protecting shoot cells from transpiration-dependent delivery of excess Na. {\textcopyright} 2012 European Molecular Biology Organization.",

author = "Caifu Jiang and Belfield, {Eric J.} and Aziz Mithani and Anne Visscher and Jiannis Ragoussis and Richard Mott and Smith, {J. Andrew C.} and Harberd, {Nicholas P.}",

note = "KAUST Repository Item: Exported on 2021-09-21 Acknowledgements: We thank Liam Dolan for atrbohI, atrbohJ, atrbohH, atrbohE and atrbohC seeds, Jian-Kang Zhu and Yan Guo for stimulating discussion, and Xiangchao Gan for assistance with genome sequence analysis. This publication is based on the work supported by Award No. KUK-I1-002-03, made by King Abdullah University of Science and Technology, and by Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/F020759/1 and BB/F022697/1. RM and JR are supported by the Wellcome Trust grant 075491/Z/04. This publication acknowledges KAUST support, but has no KAUST affiliated authors.",

year = "2012",

doi = "10.1038/emboj.2012.273",

language = "English (US)",

volume = "31",

pages = "4359--4370",

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AU - Jiang, Caifu

AU - Belfield, Eric J.

AU - Mithani, Aziz

AU - Visscher, Anne

AU - Ragoussis, Jiannis

AU - Mott, Richard

AU - Smith, J. Andrew C.

AU - Harberd, Nicholas P.

N1 - KAUST Repository Item: Exported on 2021-09-21 Acknowledgements: We thank Liam Dolan for atrbohI, atrbohJ, atrbohH, atrbohE and atrbohC seeds, Jian-Kang Zhu and Yan Guo for stimulating discussion, and Xiangchao Gan for assistance with genome sequence analysis. This publication is based on the work supported by Award No. KUK-I1-002-03, made by King Abdullah University of Science and Technology, and by Biotechnology and Biological Sciences Research Council (BBSRC) grants BB/F020759/1 and BB/F022697/1. RM and JR are supported by the Wellcome Trust grant 075491/Z/04. This publication acknowledges KAUST support, but has no KAUST affiliated authors.

PY - 2012

Y1 - 2012

N2 - Sodium (Na) is ubiquitous in soils, and is transported to plant shoots via transpiration through xylem elements in the vascular tissue. However, excess Na is damaging. Accordingly, control of xylem-sap Na concentration is important for maintenance of shoot Na homeostasis, especially under Na stress conditions. Here we report that shoot Na homeostasis of Arabidopsis thaliana plants grown in saline soils is conferred by reactive oxygen species (ROS) regulation of xylem-sap Na concentrations. We show that lack of A. thaliana respiratory burst oxidase protein F (AtrbohF; an NADPH oxidase catalysing ROS production) causes hypersensitivity of shoots to soil salinity. Lack of AtrbohF-dependent salinity-induced vascular ROS accumulation leads to increased Na concentrations in root vasculature cells and in xylem sap, thus causing delivery of damaging amounts of Na to the shoot. We also show that the excess shoot Na delivery caused by lack of AtrbohF is dependent upon transpiration. We conclude that AtrbohF increases ROS levels in wild-type root vasculature in response to raised soil salinity, thereby limiting Na concentrations in xylem sap, and in turn protecting shoot cells from transpiration-dependent delivery of excess Na. © 2012 European Molecular Biology Organization.

AB - Sodium (Na) is ubiquitous in soils, and is transported to plant shoots via transpiration through xylem elements in the vascular tissue. However, excess Na is damaging. Accordingly, control of xylem-sap Na concentration is important for maintenance of shoot Na homeostasis, especially under Na stress conditions. Here we report that shoot Na homeostasis of Arabidopsis thaliana plants grown in saline soils is conferred by reactive oxygen species (ROS) regulation of xylem-sap Na concentrations. We show that lack of A. thaliana respiratory burst oxidase protein F (AtrbohF; an NADPH oxidase catalysing ROS production) causes hypersensitivity of shoots to soil salinity. Lack of AtrbohF-dependent salinity-induced vascular ROS accumulation leads to increased Na concentrations in root vasculature cells and in xylem sap, thus causing delivery of damaging amounts of Na to the shoot. We also show that the excess shoot Na delivery caused by lack of AtrbohF is dependent upon transpiration. We conclude that AtrbohF increases ROS levels in wild-type root vasculature in response to raised soil salinity, thereby limiting Na concentrations in xylem sap, and in turn protecting shoot cells from transpiration-dependent delivery of excess Na. © 2012 European Molecular Biology Organization.

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UR - http://emboj.embopress.org/cgi/doi/10.1038/emboj.2012.273

UR - http://www.scopus.com/inward/record.url?scp=84869233862&partnerID=8YFLogxK

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DO - 10.1038/emboj.2012.273

M3 - Article

SN - 1460-2075

VL - 31

SP - 4359

EP - 4370

JO - EMBO JOURNAL

JF - EMBO JOURNAL

IS - 22

ER -

ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis

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