Rapidly evolving protointrons in Saccharomyces genomes revealed by a hungry spliceosome.


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
08 2019
Historique:
received: 26 01 2019
accepted: 15 06 2019
revised: 04 09 2019
pubmed: 23 8 2019
medline: 8 1 2020
entrez: 23 8 2019
Statut: epublish

Résumé

Introns are a prevalent feature of eukaryotic genomes, yet their origins and contributions to genome function and evolution remain mysterious. In budding yeast, repression of the highly transcribed intron-containing ribosomal protein genes (RPGs) globally increases splicing of non-RPG transcripts through reduced competition for the spliceosome. We show that under these "hungry spliceosome" conditions, splicing occurs at more than 150 previously unannotated locations we call protointrons that do not overlap known introns. Protointrons use a less constrained set of splice sites and branchpoints than standard introns, including in one case AT-AC in place of GT-AG. Protointrons are not conserved in all closely related species, suggesting that most are not under positive selection and are fated to disappear. Some are found in non-coding RNAs (e. g. CUTs and SUTs), where they may contribute to the creation of new genes. Others are found across boundaries between noncoding and coding sequences, or within coding sequences, where they offer pathways to the creation of new protein variants, or new regulatory controls for existing genes. We define protointrons as (1) nonconserved intron-like sequences that are (2) infrequently spliced, and importantly (3) are not currently understood to contribute to gene expression or regulation in the way that standard introns function. A very few protointrons in S. cerevisiae challenge this classification by their increased splicing frequency and potential function, consistent with the proposed evolutionary process of "intronization", whereby new standard introns are created. This snapshot of intron evolution highlights the important role of the spliceosome in the expansion of transcribed genomic sequence space, providing a pathway for the rare events that may lead to the birth of new eukaryotic genes and the refinement of existing gene function.

Identifiants

pubmed: 31437148
doi: 10.1371/journal.pgen.1008249
pii: PGENETICS-D-19-00154
pmc: PMC6726248
doi:

Substances chimiques

RNA, Untranslated 0
Ribosomal Proteins 0
Saccharomyces cerevisiae Proteins 0

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1008249

Subventions

Organisme : NIGMS NIH HHS
ID : R01 GM040478
Pays : United States

Commentaires et corrections

Type : ErratumIn

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Jason Talkish (J)

Center for Molecular Biology of RNA, Department of Molecular, Cell & Developmental Biology, University of California, Santa Cruz, Santa Cruz, California, United States of America.

Haller Igel (H)

Center for Molecular Biology of RNA, Department of Molecular, Cell & Developmental Biology, University of California, Santa Cruz, Santa Cruz, California, United States of America.

Rhonda J Perriman (RJ)

Center for Molecular Biology of RNA, Department of Molecular, Cell & Developmental Biology, University of California, Santa Cruz, Santa Cruz, California, United States of America.

Lily Shiue (L)

Center for Molecular Biology of RNA, Department of Molecular, Cell & Developmental Biology, University of California, Santa Cruz, Santa Cruz, California, United States of America.

Sol Katzman (S)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, California, United States of America.

Elizabeth M Munding (EM)

Center for Molecular Biology of RNA, Department of Molecular, Cell & Developmental Biology, University of California, Santa Cruz, Santa Cruz, California, United States of America.

Robert Shelansky (R)

Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, California, United States of America.

John Paul Donohue (JP)

Center for Molecular Biology of RNA, Department of Molecular, Cell & Developmental Biology, University of California, Santa Cruz, Santa Cruz, California, United States of America.

Manuel Ares (M)

Center for Molecular Biology of RNA, Department of Molecular, Cell & Developmental Biology, University of California, Santa Cruz, Santa Cruz, California, United States of America.

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Classifications MeSH