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)

Research output: Contribution to journalArticlepeer-review

78 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 languageEnglish
Pages (from-to)E4567-E4576
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number31
Early online date18 Jul 2016
DOIs
Publication statusPublished - 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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