A restorer-of-fertility-like pentatricopeptide repeat protein promotes cytoplasmic male sterility in Arabidopsis thaliana

Plant J. 2021 Jan;105(1):124-135. doi: 10.1111/tpj.15045. Epub 2020 Nov 26.

Abstract

Pentatricopeptide repeat (PPR) proteins form a large family of proteins targeted to organelles, where they post-transcriptionally modulate gene expression through binding to specific RNA sequences. Among them, the mitochondria-targeted restorer-of-fertility (Rf) PPRs inhibit peculiar mitochondrial genes that are detrimental to male gametes and cause cytoplasmic male sterility (CMS). Here, we revealed three nuclear loci involved in CMS in a cross between two distant Arabidopsis thaliana strains, Sha and Cvi-0. We identified the causal gene at one of these loci as RFL24, a conserved gene encoding a PPR protein related to known Rf PPRs. By analysing fertile revertants obtained in a male sterile background, we demonstrate that RFL24 promotes pollen abortion, in contrast with the previously described Rf PPRs, which allow pollen to survive in the presence of a sterilizing cytoplasm. We show that the sterility caused by the RFL24 Cvi-0 allele results from higher expression of the gene during early pollen development. Finally, we predict a binding site for RFL24 upstream of two mitochondrial genes, the CMS gene and the important gene cob. These results suggest that the conservation of RFL24 is linked to a primary role of ensuring a proper functioning of mitochondria, and that it was subsequently diverted by the CMS gene to its benefit.

Keywords: Arabidopsis thaliana; Rf-like PPR; cytoplasmic male sterility; natural variation; pollen development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Arabidopsis Proteins / physiology*
  • Gene Expression Regulation, Plant
  • Genes, Plant / physiology
  • Plant Infertility*
  • Pollen / metabolism
  • Quantitative Trait Loci / genetics

Substances

  • Arabidopsis Proteins
  • pentatricopeptide repeat protein, Arabidopsis