Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase

Kai Xun Chan; Peter Mabbitt; Su Yin  Phua; Jonathan Wolf Mueller; Nazia  Nisar; Tamara Gigolashvilli; Elke Stroeher; Julia Grassl; Wiebke Arlt; Gonzalo Estavillo; Colin Jackson; Barry  Pogson

doi:10.1073/pnas.1604936113

Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase

Kai Xun Chan, Peter Mabbitt, Su Yin Phua, Jonathan Wolf Mueller, Nazia Nisar, Tamara Gigolashvilli, Elke Stroeher, Julia Grassl, Wiebke Arlt, Gonzalo Estavillo, Colin Jackson, Barry Pogson

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Abstract

Intracellular signaling during oxidative stress is complex, with organelle-to-nucleus retrograde communication pathways ill-defined or incomplete. Here we identify the 3’-phosphoadenosine 5’-phosphate (PAP) phosphatase SAL1 as a novel and conserved oxidative stress sensor in plant chloroplasts. Arabidopsis thaliana SAL1 (AtSAL1) senses changes in photosynthetic redox poise, hydrogen peroxide, and superoxide concentrations in chloroplasts via redox regulatory mechanisms. AtSAL1 phosphatase activity is suppressed by dimerization, intramolecular disulfide formation and glutathionylation, allowing accumulation of its substrate, PAP; a chloroplast stress retrograde signal that regulates expression of Plastid Redox Associated Nuclear Genes (PRANGs). This redox regulation of SAL1 for activation of chloroplast signaling is conserved in the plant kingdom, and the plant protein has evolved enhanced redox sensitivity compared to its yeast ortholog. Our results indicate that, in addition to sulfur metabolism, SAL1 orthologs have evolved secondary functions in oxidative stress sensing in the plant kingdom.

Original language	English
Pages (from-to)	E4567-E4576
Number of pages	10
Journal	National Academy of Sciences. Proceedings
Volume	113
Issue number	31
Early online date	18 Jul 2016
DOIs	https://doi.org/10.1073/pnas.1604936113
Publication status	Published - 2 Aug 2016

Keywords

retrograde signaling
redox regulation
stress sensing
chloroplast
drought stress

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10.1073/pnas.1604936113Licence: None: All rights reserved

ChanK2016SensingAccepted author manuscript, 2.02 MBLicence: None: All rights reserved
ChanK2016SensingSupplAppendix Accepted author manuscript, 187 KBLicence: None: All rights reserved

Pre-Receptor Regulation of Dehydroepiandrosterone Synthesis, Metabolism and Action
Arlt, W.
Medical Research Council
1/08/04 → 31/10/09
Project: Research Councils

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Chan, K. X., Mabbitt, P., Phua, S. Y., Mueller, J. W., Nisar, N., Gigolashvilli, T., Stroeher, E., Grassl, J., Arlt, W., Estavillo, G., Jackson, C., & Pogson, B. (2016). Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase. National Academy of Sciences. Proceedings, 113(31), E4567-E4576. https://doi.org/10.1073/pnas.1604936113

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title = "Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase",

abstract = "Intracellular signaling during oxidative stress is complex, with organelle-to-nucleus retrograde communication pathways ill-defined or incomplete. Here we identify the 3{\textquoteright}-phosphoadenosine 5{\textquoteright}-phosphate (PAP) phosphatase SAL1 as a novel and conserved oxidative stress sensor in plant chloroplasts. Arabidopsis thaliana SAL1 (AtSAL1) senses changes in photosynthetic redox poise, hydrogen peroxide, and superoxide concentrations in chloroplasts via redox regulatory mechanisms. AtSAL1 phosphatase activity is suppressed by dimerization, intramolecular disulfide formation and glutathionylation, allowing accumulation of its substrate, PAP; a chloroplast stress retrograde signal that regulates expression of Plastid Redox Associated Nuclear Genes (PRANGs). This redox regulation of SAL1 for activation of chloroplast signaling is conserved in the plant kingdom, and the plant protein has evolved enhanced redox sensitivity compared to its yeast ortholog. Our results indicate that, in addition to sulfur metabolism, SAL1 orthologs have evolved secondary functions in oxidative stress sensing in the plant kingdom.",

keywords = "retrograde signaling, redox regulation, stress sensing, chloroplast, drought stress",

author = "Chan, {Kai Xun} and Peter Mabbitt and Phua, {Su Yin} and Mueller, {Jonathan Wolf} and Nazia Nisar and Tamara Gigolashvilli and Elke Stroeher and Julia Grassl and Wiebke Arlt and Gonzalo Estavillo and Colin Jackson and Barry Pogson",

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doi = "10.1073/pnas.1604936113",

language = "English",

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journal = "National Academy of Sciences. Proceedings",

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Chan, KX, Mabbitt, P, Phua, SY, Mueller, JW, Nisar, N, Gigolashvilli, T, Stroeher, E, Grassl, J, Arlt, W, Estavillo, G, Jackson, C & Pogson, B 2016, 'Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase', National Academy of Sciences. Proceedings, vol. 113, no. 31, pp. E4567-E4576. https://doi.org/10.1073/pnas.1604936113

TY - JOUR

T1 - Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase

AU - Chan, Kai Xun

AU - Mabbitt, Peter

AU - Phua, Su Yin

AU - Mueller, Jonathan Wolf

AU - Nisar, Nazia

AU - Gigolashvilli, Tamara

AU - Stroeher, Elke

AU - Grassl, Julia

AU - Arlt, Wiebke

AU - Estavillo, Gonzalo

AU - Jackson, Colin

AU - Pogson, Barry

PY - 2016/8/2

Y1 - 2016/8/2

N2 - Intracellular signaling during oxidative stress is complex, with organelle-to-nucleus retrograde communication pathways ill-defined or incomplete. Here we identify the 3’-phosphoadenosine 5’-phosphate (PAP) phosphatase SAL1 as a novel and conserved oxidative stress sensor in plant chloroplasts. Arabidopsis thaliana SAL1 (AtSAL1) senses changes in photosynthetic redox poise, hydrogen peroxide, and superoxide concentrations in chloroplasts via redox regulatory mechanisms. AtSAL1 phosphatase activity is suppressed by dimerization, intramolecular disulfide formation and glutathionylation, allowing accumulation of its substrate, PAP; a chloroplast stress retrograde signal that regulates expression of Plastid Redox Associated Nuclear Genes (PRANGs). This redox regulation of SAL1 for activation of chloroplast signaling is conserved in the plant kingdom, and the plant protein has evolved enhanced redox sensitivity compared to its yeast ortholog. Our results indicate that, in addition to sulfur metabolism, SAL1 orthologs have evolved secondary functions in oxidative stress sensing in the plant kingdom.

AB - Intracellular signaling during oxidative stress is complex, with organelle-to-nucleus retrograde communication pathways ill-defined or incomplete. Here we identify the 3’-phosphoadenosine 5’-phosphate (PAP) phosphatase SAL1 as a novel and conserved oxidative stress sensor in plant chloroplasts. Arabidopsis thaliana SAL1 (AtSAL1) senses changes in photosynthetic redox poise, hydrogen peroxide, and superoxide concentrations in chloroplasts via redox regulatory mechanisms. AtSAL1 phosphatase activity is suppressed by dimerization, intramolecular disulfide formation and glutathionylation, allowing accumulation of its substrate, PAP; a chloroplast stress retrograde signal that regulates expression of Plastid Redox Associated Nuclear Genes (PRANGs). This redox regulation of SAL1 for activation of chloroplast signaling is conserved in the plant kingdom, and the plant protein has evolved enhanced redox sensitivity compared to its yeast ortholog. Our results indicate that, in addition to sulfur metabolism, SAL1 orthologs have evolved secondary functions in oxidative stress sensing in the plant kingdom.

KW - retrograde signaling

KW - redox regulation

KW - stress sensing

KW - chloroplast

KW - drought stress

U2 - 10.1073/pnas.1604936113

DO - 10.1073/pnas.1604936113

M3 - Article

SN - 1091-6490

VL - 113

SP - E4567-E4576

JO - National Academy of Sciences. Proceedings

JF - National Academy of Sciences. Proceedings

IS - 31

ER -

Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase

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Pre-Receptor Regulation of Dehydroepiandrosterone Synthesis, Metabolism and Action

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