PPR

Foxe JP & Wright SI 2009 Signature of diversifying selection on members of the pentatricopeptide repeat protein (PPR) family in Arabidopsis lyrata. Genetics, in press.
doi:10.1534/genetics.109.104778

  • CMS has been documented in over 150 plants and can persist as a reproductive polymorphism in natural populations (gynodioecy)
  • unexpectedly, nuclear restorer genes of CMS cloned from numerous divergent plant species appear to arise almost universally from the pentatricopeptide repeat (PPR) protein family
  • PPR genes exist in high copy numbers in plant genomes and are generally thought to act as gene-specific transcriptional regulators of cytoplasmic genes
  • the molecular action of PPR genes varies and includes RNA editing, stability, cleavage and splicing
  • the expansion of PPR genes in flowering plants may be due to several waves of retrotransposition
  • a subset of PPR locations across the genome may be highly dynamic
  • any outcrossing hermaphrodite plant population is susceptible to invasion by cytoplasmic mutants that increase female fertility by causing male sterility
  • many instances of CMS have emerged from wide intraspecific or interspecific crosses
  • suggesting the exposure of a hidden evolutionary history of CMS and the fixation of nuclear restorers
  • we would not expect to find any evidence for cytonuclear conflicts in highly inbreeding species since pollen sterility mutations will reduce female fertility as well
  • if there is diversifying selection acting on some PPR genes in A. lyrata, this may reflect ongoing evolutionary dynamics associated with cytonuclear conflict
  • results suggest the action of diversifying selection on some PPR genes in this species
  • there may be selection associated with ongoing coevolution between cytoplasmic and nuclear genes
  • the lack of comparable evidence for selection on these loci in the highly selfing A. thaliana is at least consistent with the hypothesis that these unusual diversity patterns are reflective of cytonuclear conflict in the outcrossing A. lyrata
  • high nucleotide diversity in range-wide population samples can be indicative of two types of selective processes, collectively called balancing selection
  • first, frequency-dependent selection and heterozygote advantage
  • second, local adaptation and spatially varying selection across populations
  • one possibility for a mode of selection on some PPR genes is local selection for regulation of population-specific cytoplasmic alleles
  • an alternative possibility is frequency-dependent selection
  • increases in frequency of cytoplasmic mutants reducing male fertility, either quantitatively or qualitatively, could select for rare PPR alleles
  • our primary hypothesis is that PPR genes are under selection mediated by cytonuclear conflict
  • an alternative is that there is selection for compensatory nuclear mutations in response to the fixation of slightly deleterious cytoplasmic mutations
  • crosses between regions may provide an opportunity to unmask cytonuclear effects on male fitness in this species
  • these highly polymorphic PPR loci represent important candidate genes contributing to cytonuclear epistasis in fitness
  • our population genetic data provide preliminary evidence that cytonuclear conflict may be prevalent in outcrossing hermaphrodites and may play an important role in the structuring of genomes and genetic variation
  • this complements other recent genetic and population-level studies of CMS variation in natural populations of Mimulus
  • which suggest the prevalence of cytonuclear conflicts in outcrossing plant populations