On the complexity of chloroplast RNA metabolism: psaA trans-splicing can be bypassed in chlamydomonas

Mol Biol Evol. 2014 Oct;31(10):2697-707. doi: 10.1093/molbev/msu215. Epub 2014 Jul 22.

Abstract

In the chloroplast, the posttranscriptional steps of gene expression are remarkably complex. RNA maturation and translation rely on a large cohort of nucleus-encoded proteins that act specifically on a single target transcript or a small set of targets. For example in the chloroplast of Chlamydomonas, trans-splicing of the two split introns of psaA requires at least 14 nucleus-encoded proteins. To investigate the functional significance of this complex trans-splicing pathway, we have introduced an intron-less copy of psaA in the chloroplast genomes of three mutants deficient in trans-splicing and of the wild type. We find that the intron-less psaA gene rescues the mutant phenotypes. The growth of strains with the intron-less psaA is indistinguishable from the wild type under the set of different experimental conditions that were investigated. Thus, the trans-splicing factors do not appear to have any other essential function and trans-splicing of psaA can be bypassed. We discuss how these observations support the hypothesis that complex RNA metabolism in the chloroplast may in part be the result of a nonadaptive evolutionary ratchet. Genetic drift may lead to the accumulation of chloroplast mutations and the recruitment of compensatory nuclear suppressors from large preexisting pools of genes encoding RNA-binding proteins.

Keywords: Chlamydomonas; RNA processing; chloroplast; constructive neutral evolution; splicing; synthetic biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Chlamydomonas reinhardtii / genetics*
  • Chlamydomonas reinhardtii / growth & development
  • Chlamydomonas reinhardtii / metabolism
  • Genetic Drift
  • Introns
  • Iron / metabolism
  • Mutation
  • Phenotype
  • Plant Proteins / genetics
  • Plant Proteins / metabolism*
  • RNA, Chloroplast / genetics
  • RNA, Chloroplast / metabolism*
  • Sequence Analysis, RNA
  • Trans-Splicing*

Substances

  • Plant Proteins
  • RNA, Chloroplast
  • Iron