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.
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Acton, ACT 2601, Australia;
authors.forename: Kai Xun
authors.identifier: 0000-0003-3554-7228
authors.initials: KX
authors.lastname: Chan
authors.affiliation: Research School of Chemistry, Australian National University, Acton, ACT 2601, Australia;
authors.forename: Peter D
authors.initials: PD
authors.lastname: Mabbitt
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Acton, ACT 2601, Australia;
authors.forename: Su Yin
authors.initials: SY
authors.lastname: Phua
authors.affiliation: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham B15 2TT, United Kingdom; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham B15 2TH, United Kingdom;
authors.forename: Jonathan W
authors.initials: JW
authors.lastname: Mueller
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Acton, ACT 2601, Australia;
authors.forename: Nazia
authors.initials: N
authors.lastname: Nisar
authors.affiliation: Botanical Institute, Cluster of Excellence on Plant Sciences, University of Cologne, 50674 Cologne, Germany;
authors.forename: Tamara
authors.initials: T
authors.lastname: Gigolashvili
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, WA 6009, Australia.
authors.forename: Elke
authors.initials: E
authors.lastname: Stroeher
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, Crawley, WA 6009, Australia.
authors.forename: Julia
authors.initials: J
authors.lastname: Grassl
authors.affiliation: Institute of Metabolism and Systems Research, University of Birmingham, Birmingham B15 2TT, United Kingdom; Centre for Endocrinology, Diabetes and Metabolism, Birmingham Health Partners, Birmingham B15 2TH, United Kingdom;
authors.forename: Wiebke
authors.initials: W
authors.lastname: Arlt
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Acton, ACT 2601, Australia;
authors.forename: Gonzalo M
authors.initials: GM
authors.lastname: Estavillo
authors.affiliation: Research School of Chemistry, Australian National University, Acton, ACT 2601, Australia;
authors.forename: Colin J
authors.initials: CJ
authors.lastname: Jackson
authors.affiliation: Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology, Australian National University, Acton, ACT 2601, Australia; barry.pogson@anu.edu.au.
authors.forename: Barry J
authors.initials: BJ
authors.lastname: Pogson
mesh_terms: D000244:Adenosine Diphosphate / Q000378:metabolism; D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000201:enzymology* / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D002736:Chloroplasts / Q000378:metabolism*; D004220:Disulfides / Q000378:metabolism; D004789:Enzyme Activation; D018506:Gene Expression Regulation, Plant; D005978:Glutathione; D010084:Oxidation-Reduction; D018384:Oxidative Stress; D010744:Phosphoric Monoester Hydrolases / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*; D055503:Protein Multimerization; D017386:Sequence Homology, Amino Acid; D015398:Signal Transduction; D013379:Substrate Specificity
chemical_list: D029681:Arabidopsis Proteins; D004220:Disulfides; D000244:Adenosine Diphosphate; C010840:adenosine 3'-phosphate-5'-phosphate; D010744:Phosphoric Monoester Hydrolases; C053087:inositol-1,4-bisphosphate 1-phosphatase; D005978:Glutathione
keywords: chloroplast; drought stress; redox regulation; retrograde signaling; stress sensing