Impact of chromosomal inversions on the yeast DAL cluster.

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 yeas...

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Main Authors: Samina Naseeb, Daniela Delneri
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22916115/pdf/?tool=EBI
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spelling doaj-d2e0df89975c4043a015afc238b395f72021-03-04T00:25:50ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0178e4202210.1371/journal.pone.0042022Impact of chromosomal inversions on the yeast DAL cluster.Samina NaseebDaniela DelneriChromosomal 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.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22916115/pdf/?tool=EBI
collection DOAJ
language English
format Article
sources DOAJ
author Samina Naseeb
Daniela Delneri
spellingShingle Samina Naseeb
Daniela Delneri
Impact of chromosomal inversions on the yeast DAL cluster.
PLoS ONE
author_facet Samina Naseeb
Daniela Delneri
author_sort Samina Naseeb
title Impact of chromosomal inversions on the yeast DAL cluster.
title_short Impact of chromosomal inversions on the yeast DAL cluster.
title_full Impact of chromosomal inversions on the yeast DAL cluster.
title_fullStr Impact of chromosomal inversions on the yeast DAL cluster.
title_full_unstemmed Impact of chromosomal inversions on the yeast DAL cluster.
title_sort impact of chromosomal inversions on the yeast dal cluster.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2012-01-01
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.
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22916115/pdf/?tool=EBI
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