Massive mitochondrial gene transfer in a parasitic flowering plant clade

PLoS Genet. 2013;9(2):e1003265. doi: 10.1371/journal.pgen.1003265. Epub 2013 Feb 14.

Abstract

Recent studies have suggested that plant genomes have undergone potentially rampant horizontal gene transfer (HGT), especially in the mitochondrial genome. Parasitic plants have provided the strongest evidence of HGT, which appears to be facilitated by the intimate physical association between the parasites and their hosts. A recent phylogenomic study demonstrated that in the holoparasite Rafflesia cantleyi (Rafflesiaceae), whose close relatives possess the world's largest flowers, about 2.1% of nuclear gene transcripts were likely acquired from its obligate host. Here, we used next-generation sequencing to obtain the 38 protein-coding and ribosomal RNA genes common to the mitochondrial genomes of angiosperms from R. cantleyi and five additional species, including two of its closest relatives and two host species. Strikingly, our phylogenetic analyses conservatively indicate that 24%-41% of these gene sequences show evidence of HGT in Rafflesiaceae, depending on the species. Most of these transgenic sequences possess intact reading frames and are actively transcribed, indicating that they are potentially functional. Additionally, some of these transgenes maintain synteny with their donor and recipient lineages, suggesting that native genes have likely been displaced via homologous recombination. Our study is the first to comprehensively assess the magnitude of HGT in plants involving a genome (i.e., mitochondria) and a species interaction (i.e., parasitism) where it has been hypothesized to be potentially rampant. Our results establish for the first time that, although the magnitude of HGT involving nuclear genes is appreciable in these parasitic plants, HGT involving mitochondrial genes is substantially higher. This may represent a more general pattern for other parasitic plant clades and perhaps more broadly for angiosperms.

Publication types

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

MeSH terms

  • DNA, Mitochondrial / genetics
  • Evolution, Molecular*
  • Flowers / genetics
  • Gene Transfer, Horizontal / genetics*
  • Genome, Mitochondrial
  • Genome, Plant
  • Host-Parasite Interactions / genetics*
  • Phylogeny
  • Plants / genetics*
  • Plants / parasitology
  • RNA, Ribosomal / genetics
  • Symbiosis

Substances

  • DNA, Mitochondrial
  • RNA, Ribosomal

Grants and funding

This work was supported by the National Science Foundation (NSF) Assembling the Tree of Life grant DEB-0622764 and NSF DEB-1120243 (to CCD) and by the China Scholarship Council Program for Visiting Scholars (to YW). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.