Abstract
Arrays of repetitive ribosomal DNA (rDNA) sequences are generally expected to evolve as a coherent family, where repeats within such a family are more similar to each other than to orthologs in related species. The continuous homogenization of repeats within individual genomes is a recombination process termed concerted evolution. Here, we investigated the extent and the direction of concerted evolution in 43 yeast strains of the Zygosaccharomyces rouxii species complex (Z. rouxii, Z. sapae, Z. mellis), by analyzing two portions of the 35S rDNA cistron, namely the D1/D2 domains at the 5’ end of the 26S rRNA gene and the segment including the internal transcribed spacers (ITS) 1 and 2 (ITS regions). We demonstrate that intra-genomic rDNA sequence variation is unusually frequent in this clade and that rDNA arrays in single genomes consist of an intermixing of Z. rouxii, Z. sapae and Z. mellis-like sequences, putatively evolved by reticulate evolutionary events that involved repeated hybridization between lineages. The levels and distribution of sequence polymorphisms vary across rDNA repeats in different individuals, reflecting four patterns of rDNA evolution: I) rDNA repeats that are homogeneous within a genome but are chimeras derived from two parental lineages via recombination: Z. rouxii in the ITS region and Z. sapae in the D1/D2 region; II) intra-genomic rDNA repeats that retain polymorphisms only in ITS regions; III) rDNA repeats that vary only in their D1/D2 domains; IV) heterogeneous rDNA arrays that have both polymorphic ITS and D1/D2 regions. We argue that an ongoing process of homogenization following allodiplodization or incomplete lineage sorting gave rise to divergent evolutionary trajectories in different strains, depending upon temporal, structural and functional constraints. We discuss the consequences of these findings for Zygosaccharomyces species delineation and, more in general, for yeast barcoding.
Highlights
IntroductionRDNA Evolution in Zygosaccharomyces rouxii Species Complex on organism and growth conditions [1]
Nuclear genes encoding ribosomal RNA are universally distributed across the tree of life and account for more than 50% of total cellular transcripts produced by the cell, dependingPLOS ONE | DOI:10.1371/journal.pone.0160744 August 8, 2016rDNA Evolution in Zygosaccharomyces rouxii Species Complex on organism and growth conditions [1]
The following strains were used as references for comparative purposes: Z. rouxii CBS 732T, the aneuploid strains CBS 4837 and CBS 4838, Zygosaccharomyces mellis CBS 736T and Zygosaccharomyces bailii CBS 680T were purchased from the Centraalbureau voor Schimmelcultures (CBS; Utrecht, The Netherlands); Zygosaccharomyces pseudorouxii NCYC 3042 from the National Collection of Yeast Culture (NCYC; UK); and allodiploid ATCC 42981 from the American Type Culture Collection (ATCC; Rockville, USA)
Summary
RDNA Evolution in Zygosaccharomyces rouxii Species Complex on organism and growth conditions [1] To support this level of expression, yeasts and higher eukaryotes possess multicopy nuclear rDNA sequences organized as head-to-tail tandem rDNA arrays in nucleolus organizer regions (NORs). Each tandem array comprises a large precursor 35S RNA consisting of coding sequences for its three subunits, namely the 28S/26S large subunit (LSU), the 18S small subunit, and the 5.8S rRNA genes. These coding genes are separated by two intervening and rapidly evolving non-coding regions, the internal transcribed spacers (ITS1 and ITS2), and together constitute a single transcriptional cistron transcribed by RNA polymerase I [2] (Fig 1A). The 5S rRNA gene is present within doi:10.1371/journal.pone.0160744.g001
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