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.
Highlights
Genes encoding ribosomal RNA are universal key constituents of eukaryotic genomes because their products form the backbones of the functional cytoplasmic, plastid, and mitochondrial ribosomes [1]
Nuclear rDNA has long been regarded as being merely involved in the biogenesis of ribosomes and the nucleolus [3,4,5], but recent evidence has dramatically changed this perception, suggesting that it is involved in other cell processes
Results rDNA loci analysed by molecular cytogenetics
Summary
Genes encoding ribosomal RNA (rDNA) are universal key constituents of eukaryotic genomes because their products form the backbones of the functional cytoplasmic, plastid, and mitochondrial ribosomes [1]. In contrast with the single or low-copy number of rRNA genes present in the plastidial and mitochondrial genomes, the nuclear genome harbours hundreds to several thousand copies of each ribosomal species (18S, 5.8S, 25S/26S, 5S) that are usually arranged in distinct arrays of tandemly-repeated cistrons (45S, formed by the 18S, 5.8S, 25S/ 26S units) or genes (5S) [2]. RDNA is one of the most abundant gene families occupying a large fraction of the nuclear genome, it is structurally one of the most unstable genomic regions [6]. The reasons for this instability are not fully understood; it has been reported that rDNA loci are the predominant sites of repeated recombination [11]. Transposition may promote the evolutionary dynamics of rDNA loci across species radiation and during intraspecies differentiation and domestication, producing karyological rearrangements that may be at the ongoing of speciation processes, towards genetic differentiation [15]
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