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

Kai Xun Chan; Peter D. Mabbitt; Su Yin Phua; Jonathan W. Mueller; Nazia Nisar; Tamara Gigolashvili; Elke Stroeher; Julia Grassl; Wiebke Arlt; Gonzalo M. Estavillo; Colin J. Jackson; Barry J. 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 D. Mabbitt, Su Yin Phua, Jonathan W. Mueller, Nazia Nisar, Tamara Gigolashvili, Elke Stroeher, Julia Grassl, Wiebke Arlt, Gonzalo M. Estavillo, Colin J. Jackson, Barry J. Pogson (Lead / Corresponding author)

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132 Citations (Scopus)

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 previously unidentified 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 with 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	Proceedings of the National Academy of Sciences of the United States of America
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

Adenosine Diphosphate/metabolism
Amino Acid Sequence
Arabidopsis/enzymology
Arabidopsis Proteins/chemistry
Chloroplasts/metabolism
Disulfides/metabolism
Enzyme Activation
Gene Expression Regulation, Plant
Glutathione
Oxidation-Reduction
Oxidative Stress
Phosphoric Monoester Hydrolases/chemistry
Protein Multimerization
Sequence Homology, Amino Acid
Signal Transduction
Substrate Specificity

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

@article{c223036f629f42deaae20572276685f6,

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'-phosphoadenosine 5'-phosphate (PAP) phosphatase SAL1 as a previously unidentified 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 with 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 = "Adenosine Diphosphate/metabolism, Amino Acid Sequence, Arabidopsis/enzymology, Arabidopsis Proteins/chemistry, Chloroplasts/metabolism, Disulfides/metabolism, Enzyme Activation, Gene Expression Regulation, Plant, Glutathione, Oxidation-Reduction, Oxidative Stress, Phosphoric Monoester Hydrolases/chemistry, Protein Multimerization, Sequence Homology, Amino Acid, Signal Transduction, Substrate Specificity",

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

year = "2016",

month = aug,

day = "2",

doi = "10.1073/pnas.1604936113",

language = "English",

volume = "113",

pages = "E4567--E4576",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

number = "31",

}

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

Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase. / Chan, Kai Xun; Mabbitt, Peter D.; Phua, Su Yin et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 31, 02.08.2016, p. E4567-E4576.

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

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 D.

AU - Phua, Su Yin

AU - Mueller, Jonathan W.

AU - Nisar, Nazia

AU - Gigolashvili, Tamara

AU - Stroeher, Elke

AU - Grassl, Julia

AU - Arlt, Wiebke

AU - Estavillo, Gonzalo M.

AU - Jackson, Colin J.

AU - Pogson, Barry J.

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 previously unidentified 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 with 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 previously unidentified 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 with 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 - Adenosine Diphosphate/metabolism

KW - Amino Acid Sequence

KW - Arabidopsis/enzymology

KW - Arabidopsis Proteins/chemistry

KW - Chloroplasts/metabolism

KW - Disulfides/metabolism

KW - Enzyme Activation

KW - Gene Expression Regulation, Plant

KW - Glutathione

KW - Oxidation-Reduction

KW - Oxidative Stress

KW - Phosphoric Monoester Hydrolases/chemistry

KW - Protein Multimerization

KW - Sequence Homology, Amino Acid

KW - Signal Transduction

KW - Substrate Specificity

U2 - 10.1073/pnas.1604936113

DO - 10.1073/pnas.1604936113

M3 - Article

C2 - 27432987

SN - 0027-8424

VL - 113

SP - E4567-E4576

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 31

ER -

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

Abstract

Keywords

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