Conserved Organisation of 45S rDNA Sites and rDNA Gene Copy Number among Major Clades of Early Land Plants

PLoS One. 2016 Sep 13;11(9):e0162544. doi: 10.1371/journal.pone.0162544. eCollection 2016.

Abstract

Genes encoding ribosomal RNA (rDNA) are universal key constituents of eukaryotic genomes, and the nuclear genome harbours hundreds to several thousand copies of each species. Knowledge about the number of rDNA loci and gene copy number provides information for comparative studies of organismal and molecular evolution at various phylogenetic levels. With the exception of seed plants, the range of 45S rDNA locus (encoding 18S, 5.8S and 26S rRNA) and gene copy number variation within key evolutionary plant groups is largely unknown. This is especially true for the three earliest land plant lineages Marchantiophyta (liverworts), Bryophyta (mosses), and Anthocerotophyta (hornworts). In this work, we report the extent of rDNA variation in early land plants, assessing the number of 45S rDNA loci and gene copy number in 106 species and 25 species, respectively, of mosses, liverworts and hornworts. Unexpectedly, the results show a narrow range of ribosomal locus variation (one or two 45S rDNA loci) and gene copies not present in vascular plant lineages, where a wide spectrum is recorded. Mutation analysis of whole genomic reads showed higher (3-fold) intragenomic heterogeneity of Marchantia polymorpha (Marchantiophyta) rDNA compared to Physcomitrella patens (Bryophyta) and two angiosperms (Arabidopsis thaliana and Nicotiana tomentosifomis) suggesting the presence of rDNA pseudogenes in its genome. No association between phylogenetic position, taxonomic adscription and the number of rDNA loci and gene copy number was found. Our results suggest a likely evolutionary rDNA stasis during land colonisation and diversification across 480 myr of bryophyte evolution. We hypothesise that strong selection forces may be acting against ribosomal gene locus amplification. Despite showing a predominant haploid phase and infrequent meiosis, overall rDNA homogeneity is not severely compromised in bryophytes.

MeSH terms

  • Anthocerotophyta / classification
  • Anthocerotophyta / genetics
  • Arabidopsis / classification
  • Arabidopsis / genetics
  • Bryophyta / classification
  • Bryophyta / genetics
  • Chromosomes, Plant / genetics
  • Conserved Sequence
  • Cytogenetic Analysis
  • DNA, Plant / genetics*
  • DNA, Ribosomal / genetics
  • Embryophyta / classification*
  • Embryophyta / genetics*
  • Evolution, Molecular
  • Gene Dosage
  • Genes, Plant
  • Hepatophyta / classification
  • Hepatophyta / genetics
  • In Situ Hybridization, Fluorescence
  • Phylogeny
  • RNA, Plant / genetics
  • RNA, Ribosomal / genetics
  • Real-Time Polymerase Chain Reaction
  • Species Specificity

Substances

  • DNA, Plant
  • DNA, Ribosomal
  • RNA, Plant
  • RNA, Ribosomal
  • RNA, ribosomal, 45S

Grants and funding

This work was supported by funds from the Spanish Ministry of Science and Innovation (Projects CGL2010-22347-C02-01 and CGL2010-15693/BOS), the Catalan Government (Consolidated Research Group 2009SGR608) and the Czech Scientific Foundation (P501/12/G090). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.