Dataset Information

Prevalence of small inversions in yeast gene order evolution.

ABSTRACT: Gene order evolution in two eukaryotes was studied by comparing the Saccharomyces cerevisiae genome sequence to extensive new data from whole-genome shotgun and cosmid sequencing of Candida albicans. Gene order is substantially different between these two yeasts, with only 9% of gene pairs that are adjacent in one species being conserved as adjacent in the other. Inversion of small segments of DNA, less than 10 genes long, has been a major cause of rearrangement, which means that even where a pair of genes has been conserved as adjacent, the transcriptional orientations of the two genes relative to one another are often different. We estimate that about 1,100 single-gene inversions have occurred since the divergence between these species. Other genes that are adjacent in one species are in the same neighborhood in the other, but their precise arrangement has been disrupted, probably by multiple successive multigene inversions. We estimate that gene adjacencies have been broken as frequently by local rearrangements as by chromosomal translocations or long-distance transpositions. A bias toward small inversions has been suggested by other studies on animals and plants and may be general among eukaryotes.

SUBMITTER: Seoighe C

PROVIDER: S-EPMC18936 | biostudies-literature | 2000 Dec

REPOSITORIES: biostudies-literature

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Prevalence of small inversions in yeast gene order evolution.

Seoighe C C Federspiel N N Jones T T Hansen N N Bivolarovic V V Surzycki R R Tamse R R Komp C C Huizar L L Davis R W RW Scherer S S Tait E E Shaw D J DJ Harris D D Murphy L L Oliver K K Taylor K K Rajandream M A MA Barrell B G BG Wolfe K H KH

Proceedings of the National Academy of Sciences of the United States of America 20001201 26

Gene order evolution in two eukaryotes was studied by comparing the Saccharomyces cerevisiae genome sequence to extensive new data from whole-genome shotgun and cosmid sequencing of Candida albicans. Gene order is substantially different between these two yeasts, with only 9% of gene pairs that are adjacent in one species being conserved as adjacent in the other. Inversion of small segments of DNA, less than 10 genes long, has been a major cause of rearrangement, which means that even where a pa ...[more]

PMID: 11087826

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Project description:Chromosomal rearrangements occur readily in nature and are a major reshaping force during genome evolution. Such large scale modifications are usually deleterious causing several fitness defects, but sometimes can confer an advantage and become adaptive. For example the DAL metabolic cluster in yeast was assembled in recent evolutionary times in the Hemiascomycetes lineage, through a set of rearrangements that brought together the genes involved in the allantoin degradation pathway. In eukaryotes, the existence of physical clustering of genes with related functions supports the notion that neighbouring ORFs tend to be co-expressed and that the order of genes along the chromosomes may have biological significance, rather than being random as previously believed. In this study, we investigate the phenotypic effect that inversions have on the DAL gene cluster, expressed during nitrogen starvation. In all Saccharomyces "sensu stricto" species the order of the DAL cluster is conserved, while in the "sensu lato" species Naumovia castellii, which grows significantly worse than S. cerevisiae on allantoin, the cluster includes two nested inversions encompassing three DAL genes. We constructed several inverted and non-inverted S. cerevisiae strains possessing different inversions including those to mimic the configuration of the N. castellii DAL cluster. We showed that the inversion of DAL2 lower its own expression and reduces yeast fitness during nitrogen starvation. This rearrangement also altered the expression of the neighbouring genes DAL1 and DAL4. Moreover, we showed that the expression of the DAL4 anti-sense transcript (SUT614) does not change upon inversions of DAL2 and therefore is unlikely to be involved in its regulation. These results show that the order of the DAL cluster has an impact on the phenotype and gene expression, suggesting that these rearrangements may have been adaptive in the "sensu stricto" group in relation to the low availability of nitrogen in the environment.

Dataset Information

Prevalence of small inversions in yeast gene order evolution.

Publications

Prevalence of small inversions in yeast gene order evolution.

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