Dataset Information

Origin and Spread of Spliceosomal Introns: Insights from the Fungal Clade Zymoseptoria.

ABSTRACT: Spliceosomal introns are a key feature of eukaryote genome architecture and have been proposed to originate from selfish group II introns from an endosymbiotic bacterium, that is, the ancestor of mitochondria. However, the mechanisms underlying the wide spread of spliceosomal introns across eukaryotic genomes have been obscure. In this study, we characterize the dynamic evolution of spliceosomal introns in the fungal genus Zymoseptoria at different evolutionary scales, that is, within a genome, among conspecific strains within species, and between different species. Within the genome, spliceosomal introns can proliferate in unrelated genes and intergenic regions. Among conspecific strains, spliceosomal introns undergo rapid turnover (gains and losses) and frequent sequence exchange between geographically distinct strains. Furthermore, spliceosomal introns could undergo introgression between distinct species, which can further promote intron invasion and proliferation. The dynamic invasion and proliferation processes of spliceosomal introns resemble the life cycles of mobile selfish (group I/II) introns, and these intron movements, at least in part, account for the dramatic processes of intron gain and intron loss during eukaryotic evolution.

SUBMITTER: Wu B

PROVIDER: S-EPMC5647799 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Publications

Origin and Spread of Spliceosomal Introns: Insights from the Fungal Clade Zymoseptoria.

Wu Baojun B Macielog Allison I AI Hao Weilong W

Genome biology and evolution 20171001 10

Spliceosomal introns are a key feature of eukaryote genome architecture and have been proposed to originate from selfish group II introns from an endosymbiotic bacterium, that is, the ancestor of mitochondria. However, the mechanisms underlying the wide spread of spliceosomal introns across eukaryotic genomes have been obscure. In this study, we characterize the dynamic evolution of spliceosomal introns in the fungal genus Zymoseptoria at different evolutionary scales, that is, within a genome, ...[more]

PMID: 29048531

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Project description:BACKGROUND:In the primary transcript of nuclear genes, coding sequences-exons-usually alternate with non-coding sequences-introns. In the evolution of spliceosomal intron-exon structure, extant intron positions can be abandoned and new intron positions can be occupied. Spliceosomal twin introns ("stwintrons") are unconventional intervening sequences where a standard "internal" intron interrupts a canonical splicing motif of a second, "external" intron. The availability of genome sequences of more than a thousand species of fungi provides a unique opportunity to study spliceosomal intron evolution throughout a whole kingdom by means of molecular phylogenetics. RESULTS:A new stwintron was encountered in Aspergillus nidulans and Aspergillus niger. It is present across three classes of Leotiomyceta in the transcript of a well-conserved gene encoding a putative lipase (lipS). It occupies the same position as a standard intron in the orthologue gene in species of the early divergent classes of the Pezizomycetes and the Orbiliomycetes, suggesting that an internal intron has appeared within a pre-extant intron. On the other hand, the stwintron has been lost from certain taxa in Leotiomycetes and Eurotiomycetes at several occasions, most likely by a mechanism involving reverse transcription and homologous recombination. Another ancient stwintron present across whole Pezizomycotina orders-in the transcript of the bifunctional biotin biosynthesis gene bioDA-occurs at the same position as a standard intron in many species of non-Dikarya. Nevertheless, also the bioDA stwintron has disappeared from certain lineages within the taxa where it occurs, i.e., Sordariomycetes and Botryosphaeriales. Intriguingly, only the internal intron was lost from the Sordariomycetes bioDA stwintron at all but one occasion, leaving a standard intron in the same position, while where the putative lipase stwintron was lost, no intronic sequences remain. CONCLUSIONS:Molecular phylogeny of the peptide product was used to monitor the existence and fate of a stwintron in the transcripts of two neatly defined fungal genes, encoding well conserved proteins. Both defining events-stwintron emergence and loss-can be explained with extant models for intron insertion and loss. We thus demonstrate that stwintrons can serve as model systems to study spliceosomal intron evolution.

Dataset Information

Origin and Spread of Spliceosomal Introns: Insights from the Fungal Clade Zymoseptoria.

Publications

Origin and Spread of Spliceosomal Introns: Insights from the Fungal Clade Zymoseptoria.

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