Tissue-specific root ion profiling reveals essential roles of the CAX and ACA calcium transport systems in response to hypoxia in Arabidopsis

Feifei Wang, Zhong-Hua Chen, Xiaohui Liu, Timothy David Colmer, Meixue Zhou, Sergey Shabala

Research output: Contribution to journalArticle

25 Citations (Scopus)

Abstract

Waterlogging is a major abiotic stress that limits the growth of plants. The crucial role of Ca2+ as a second messenger in response to abiotic and biotic stimuli has been widely recognized in plants. However, the physiological and molecular mechanisms of Ca2+ distribution within specific cell types in different root zones under hypoxia is poorly understood. In this work, whole-plant physiological and tissue-specific Ca2+ changes were studied using several ACA (Ca2+-ATPase) and CAX (Ca2+/proton exchanger) knock-out Arabidopsis mutants subjected to waterlogging treatment. In the wild-type (WT) plants, several days of hypoxia decreased the expression of ACA8, CAX4, and CAX11 by 33% and 50% compared with the control. The hypoxic treatment also resulted in an up to 11-fold tissue-dependent increase in Ca2+ accumulation in root tissues as revealed by confocal microscopy. The increase was much higher in stelar cells in the mature zone of Arabidopsis mutants with loss of function for ACA8, ACA11, CAX4, and CAX11. In addition, a significantly increased Ca2+ concentration was found in the cytosol of stelar cells in the mature zone after hypoxic treatment. Three weeks of waterlogging resulted in dramatic loss of shoot biomass in cax11 plants (67% loss in shoot dry weight), while in the WT and other transport mutants this decline was only 14-22%. These results were also consistent with a decline in leaf chlorophyll fluorescence (Fv/Fm). It is suggested that CAX11 plays a key role in maintaining cytosolic Ca2+ homeostasis and/or signalling in root cells under hypoxic conditions.

Original languageEnglish
Pages (from-to)3747-3762
Number of pages16
JournalJournal of Experimental Botany
Volume67
Issue number12
Early online date17 Feb 2016
DOIs
Publication statusPublished - Jun 2016
Event9th Symposium of the International Society for Root Research - Canberra, Australia
Duration: 5 Oct 20159 Oct 2015

Cite this

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title = "Tissue-specific root ion profiling reveals essential roles of the CAX and ACA calcium transport systems in response to hypoxia in Arabidopsis",
abstract = "Waterlogging is a major abiotic stress that limits the growth of plants. The crucial role of Ca2+ as a second messenger in response to abiotic and biotic stimuli has been widely recognized in plants. However, the physiological and molecular mechanisms of Ca2+ distribution within specific cell types in different root zones under hypoxia is poorly understood. In this work, whole-plant physiological and tissue-specific Ca2+ changes were studied using several ACA (Ca2+-ATPase) and CAX (Ca2+/proton exchanger) knock-out Arabidopsis mutants subjected to waterlogging treatment. In the wild-type (WT) plants, several days of hypoxia decreased the expression of ACA8, CAX4, and CAX11 by 33{\%} and 50{\%} compared with the control. The hypoxic treatment also resulted in an up to 11-fold tissue-dependent increase in Ca2+ accumulation in root tissues as revealed by confocal microscopy. The increase was much higher in stelar cells in the mature zone of Arabidopsis mutants with loss of function for ACA8, ACA11, CAX4, and CAX11. In addition, a significantly increased Ca2+ concentration was found in the cytosol of stelar cells in the mature zone after hypoxic treatment. Three weeks of waterlogging resulted in dramatic loss of shoot biomass in cax11 plants (67{\%} loss in shoot dry weight), while in the WT and other transport mutants this decline was only 14-22{\%}. These results were also consistent with a decline in leaf chlorophyll fluorescence (Fv/Fm). It is suggested that CAX11 plays a key role in maintaining cytosolic Ca2+ homeostasis and/or signalling in root cells under hypoxic conditions.",
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author = "Feifei Wang and Zhong-Hua Chen and Xiaohui Liu and Colmer, {Timothy David} and Meixue Zhou and Sergey Shabala",
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Tissue-specific root ion profiling reveals essential roles of the CAX and ACA calcium transport systems in response to hypoxia in Arabidopsis. / Wang, Feifei; Chen, Zhong-Hua; Liu, Xiaohui; Colmer, Timothy David; Zhou, Meixue; Shabala, Sergey.

In: Journal of Experimental Botany, Vol. 67, No. 12, 06.2016, p. 3747-3762.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Tissue-specific root ion profiling reveals essential roles of the CAX and ACA calcium transport systems in response to hypoxia in Arabidopsis

AU - Wang, Feifei

AU - Chen, Zhong-Hua

AU - Liu, Xiaohui

AU - Colmer, Timothy David

AU - Zhou, Meixue

AU - Shabala, Sergey

PY - 2016/6

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AB - Waterlogging is a major abiotic stress that limits the growth of plants. The crucial role of Ca2+ as a second messenger in response to abiotic and biotic stimuli has been widely recognized in plants. However, the physiological and molecular mechanisms of Ca2+ distribution within specific cell types in different root zones under hypoxia is poorly understood. In this work, whole-plant physiological and tissue-specific Ca2+ changes were studied using several ACA (Ca2+-ATPase) and CAX (Ca2+/proton exchanger) knock-out Arabidopsis mutants subjected to waterlogging treatment. In the wild-type (WT) plants, several days of hypoxia decreased the expression of ACA8, CAX4, and CAX11 by 33% and 50% compared with the control. The hypoxic treatment also resulted in an up to 11-fold tissue-dependent increase in Ca2+ accumulation in root tissues as revealed by confocal microscopy. The increase was much higher in stelar cells in the mature zone of Arabidopsis mutants with loss of function for ACA8, ACA11, CAX4, and CAX11. In addition, a significantly increased Ca2+ concentration was found in the cytosol of stelar cells in the mature zone after hypoxic treatment. Three weeks of waterlogging resulted in dramatic loss of shoot biomass in cax11 plants (67% loss in shoot dry weight), while in the WT and other transport mutants this decline was only 14-22%. These results were also consistent with a decline in leaf chlorophyll fluorescence (Fv/Fm). It is suggested that CAX11 plays a key role in maintaining cytosolic Ca2+ homeostasis and/or signalling in root cells under hypoxic conditions.

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KW - calcium

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KW - confocal microscopy

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KW - hypoxia

KW - potassium

KW - sodium

KW - stele

KW - waterlogging

KW - PROGRAMMED CELL-DEATH

KW - DEPENDENT NA+/CA2+ EXCHANGER

KW - MEMBRANE H+-ATPASE

KW - PLANT CA2+ PUMPS

KW - PLASMA-MEMBRANE

KW - SALINITY TOLERANCE

KW - OXYGEN DEPRIVATION

KW - SALT TOLERANCE

KW - BARLEY ROOTS

KW - WATERLOGGING TOLERANCE

U2 - 10.1093/jxb/erw034

DO - 10.1093/jxb/erw034

M3 - Article

VL - 67

SP - 3747

EP - 3762

JO - Journal of Experimental Botany

JF - Journal of Experimental Botany

SN - 0022-0957

IS - 12

ER -