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Evolution of Yeast Noncoding RNAs Reveals an Alternative Mechanism for Widespread Intron Loss

Science  05 Nov 2010:
Vol. 330, Issue 6005, pp. 838-841
DOI: 10.1126/science.1194554

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Kicking Out Introns

Many genes in eukaryotes contain introns that must be removed from the messenger RNA for proper gene function. Humans have on average eight introns per gene, whereas more than 90% of the genes in the yeast species Saccharomyces cerevisiae and Candida albicans have none at all. To understand how introns can be lost from genes, Mitrovich et al. (p. 838) compared non–protein-coding genes among the yeasts and found that genes for small nucleolar RNAs (snoRNAs) in C. albicans are intronic. By contrast in S. cerevisiae, snoRNAs are processed from unmodified RNA, suggesting a massive loss of snoRNAs—associated introns in the common ancestor of the Saccharomyces species. The introns seem to have been lost through splice-site degeneration, and associated compaction of linked exons resulted in nested splicing of some snoRNAs.

Abstract

The evolutionary forces responsible for intron loss are unresolved. Whereas research has focused on protein-coding genes, here we analyze noncoding small nucleolar RNA (snoRNA) genes in which introns, rather than exons, are typically the functional elements. Within the yeast lineage exemplified by the human pathogen Candida albicans, we find—through deep RNA sequencing and genome-wide annotation of splice junctions—extreme compaction and loss of associated exons, but retention of snoRNAs within introns. In the Saccharomyces yeast lineage, however, we find it is the introns that have been lost through widespread degeneration of splicing signals. This intron loss, perhaps facilitated by innovations in snoRNA processing, is distinct from that observed in protein-coding genes with respect to both mechanism and evolutionary timing.

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