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

Proc Natl Acad Sci U S A. 2016 Aug 2;113(31):E4567-76. doi: 10.1073/pnas.1604936113. Epub 2016 Jul 18.


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: chloroplast; drought stress; redox regulation; retrograde signaling; stress sensing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

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


  • Arabidopsis Proteins
  • Disulfides
  • Adenosine Diphosphate
  • adenosine 3'-phosphate-5'-phosphate
  • Phosphoric Monoester Hydrolases
  • inositol-1,4-bisphosphate 1-phosphatase
  • Glutathione

Associated data

  • PDB/5ESY