Complete Plastid Genome of the Recent Holoparasite Lathraea squamaria Reveals Earliest Stages of Plastome Reduction in Orobanchaceae

PLoS One. 2016 Mar 2;11(3):e0150718. doi: 10.1371/journal.pone.0150718. eCollection 2016.

Abstract

Plants from the family Orobanchaceae are widely used as a model to study different aspects of parasitic lifestyle including host-parasite interactions and physiological and genomic adaptations. Among the latter, the most prominent are those that occurred due to the loss of photosynthesis; they include the reduction of the photosynthesis-related gene set in both nuclear and plastid genomes. In Orobanchaceae, the transition to non-photosynthetic lifestyle occurred several times independently, but only one lineage has been in the focus of evolutionary studies. These studies included analysis of plastid genomes and transcriptomes and allowed the inference of patterns and mechanisms of genome reduction that are thought to be general for parasitic plants. Here we report the plastid genome of Lathraea squamaria, a holoparasitic plant from Orobanchaceae, clade Rhinantheae. We found that in this plant the degree of plastome reduction is the least among non-photosynthetic plants. Like other parasites, Lathraea possess a plastome with elevated absolute rate of nucleotide substitution. The only gene lost is petL, all other genes typical for the plastid genome are present, but some of them-those encoding photosystem components (22 genes), cytochrome b6/f complex proteins (4 genes), plastid-encoded RNA polymerase subunits (2 genes), ribosomal proteins (2 genes), ccsA and cemA-are pseudogenized. Genes for cytochrome b6/f complex and photosystems I and II that do not carry nonsense or frameshift mutations have an increased ratio of non-synonymous to synonymous substitution rates, indicating the relaxation of purifying selection. Our divergence time estimates showed that transition to holoparasitism in Lathraea lineage occurred relatively recently, whereas the holoparasitic lineage Orobancheae is about two times older.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Biological Evolution
  • Chloroplast Proteins / genetics*
  • Chromosome Mapping
  • Genome, Plastid*
  • Host-Parasite Interactions
  • Orobanchaceae / classification
  • Orobanchaceae / genetics*
  • Photosynthesis / genetics
  • Photosynthetic Reaction Center Complex Proteins / genetics*
  • Phylogeny*
  • Plastids / genetics*
  • Selection, Genetic
  • Sequence Analysis, DNA

Substances

  • Chloroplast Proteins
  • Photosynthetic Reaction Center Complex Proteins

Grants and funding

This work was supported by a grant 14-50-00029 from Russian Science Foundation (RNF) (genome sequencing, assembly and annotation) and by Russian Foundation for Basic Research (grant 14-04-01486). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.