Roles for the chloroplast-localized pentatricopeptide repeat protein 30 and the 'mitochondrial' transcription termination factor 9 in chloroplast quality control

Plant J. 2020 Nov;104(3):735-751. doi: 10.1111/tpj.14963. Epub 2020 Sep 17.

Abstract

Chloroplasts constantly experience photo-oxidative stress while performing photosynthesis. This is particularly true under abiotic stresses that lead to the accumulation of reactive oxygen species (ROS) which oxidize DNA, proteins and lipids. Reactive oxygen species can also act as signals to induce acclimation through chloroplast degradation, cell death and nuclear gene expression. To better understand the mechanisms behind ROS signaling from chloroplasts, we have used the Arabidopsis thaliana mutant plastid ferrochelatase two (fc2) that conditionally accumulates the ROS singlet oxygen (1 O2 ) leading to chloroplast degradation and eventually cell death. Here we have mapped mutations that suppress chloroplast degradation in the fc2 mutant and demonstrate that they affect two independent loci (PPR30 and mTERF9) encoding chloroplast proteins predicted to be involved in post-transcriptional gene expression. These mutants exhibited broadly reduced chloroplast gene expression, impaired chloroplast development and reduced chloroplast stress signaling. Levels of 1 O2 , however, could be uncoupled from chloroplast degradation, suggesting that PPR30 and mTERF9 are involved in ROS signaling pathways. In the wild-type background, ppr30 and mTERF9 mutants were also observed to be less susceptible to cell death induced by excess light stress. While broad inhibition of plastid transcription with rifampicin was also able to suppress cell death in fc2 mutants, specific reductions in plastid gene expression using other mutations was not always sufficient. Together these results suggest that plastid gene expression, or the expression of specific plastid genes by PPR30 and mTERF0, is a necessary prerequisite for chloroplasts to activate the 1 O2 signaling pathways to induce chloroplast quality control pathways and/or cell death.

Keywords: cellular degradation; chloroplast; photosynthesis; reactive oxygen species; singlet oxygen; transcription.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Chloroplast Proteins / genetics
  • Chloroplast Proteins / metabolism
  • Chloroplasts / genetics
  • Chloroplasts / metabolism*
  • Chromosome Mapping
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Gene Expression Regulation, Plant
  • Light
  • Mutation
  • Peptide Termination Factors / genetics
  • Peptide Termination Factors / metabolism*
  • Phenotype
  • Plants, Genetically Modified
  • Plastids / genetics
  • Sigma Factor / genetics
  • Sigma Factor / metabolism
  • Singlet Oxygen / metabolism
  • Tetrapyrroles / biosynthesis

Substances

  • Arabidopsis Proteins
  • Chloroplast Proteins
  • DNA-Binding Proteins
  • GUN1 protein, Arabidopsis
  • MTERF9 protein, Arabidopsis
  • Peptide Termination Factors
  • SIG2 protein, Arabidopsis
  • SIG6 protein, Arabidopsis
  • Sigma Factor
  • Tetrapyrroles
  • Singlet Oxygen