Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation.

Although single genes underlying several evolutionary adaptations have been identified, the genetic basis of complex, polygenic adaptations has been far more challenging to pinpoint. Here we report that the budding yeast Saccharomyces paradoxus has recently evolved resistance to citrinin, a naturall...

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Main Authors: Santiago Naranjo, Justin D Smith, Carlo G Artieri, Mian Zhang, Yiqi Zhou, Michael E Palmer, Hunter B Fraser
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-12-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1005751
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spelling doaj-d97c1a111ad74b71a7f8c580d52749e32021-04-21T14:24:10ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042015-12-011112e100575110.1371/journal.pgen.1005751Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation.Santiago NaranjoJustin D SmithCarlo G ArtieriMian ZhangYiqi ZhouMichael E PalmerHunter B FraserAlthough single genes underlying several evolutionary adaptations have been identified, the genetic basis of complex, polygenic adaptations has been far more challenging to pinpoint. Here we report that the budding yeast Saccharomyces paradoxus has recently evolved resistance to citrinin, a naturally occurring mycotoxin. Applying a genome-wide test for selection on cis-regulation, we identified five genes involved in the citrinin response that are constitutively up-regulated in S. paradoxus. Four of these genes are necessary for resistance, and are also sufficient to increase the resistance of a sensitive strain when over-expressed. Moreover, cis-regulatory divergence in the promoters of these genes contributes to resistance, while exacting a cost in the absence of citrinin. Our results demonstrate how the subtle effects of individual regulatory elements can be combined, via natural selection, into a complex adaptation. Our approach can be applied to dissect the genetic basis of polygenic adaptations in a wide range of species.https://doi.org/10.1371/journal.pgen.1005751
collection DOAJ
language English
format Article
sources DOAJ
author Santiago Naranjo
Justin D Smith
Carlo G Artieri
Mian Zhang
Yiqi Zhou
Michael E Palmer
Hunter B Fraser
spellingShingle Santiago Naranjo
Justin D Smith
Carlo G Artieri
Mian Zhang
Yiqi Zhou
Michael E Palmer
Hunter B Fraser
Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation.
PLoS Genetics
author_facet Santiago Naranjo
Justin D Smith
Carlo G Artieri
Mian Zhang
Yiqi Zhou
Michael E Palmer
Hunter B Fraser
author_sort Santiago Naranjo
title Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation.
title_short Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation.
title_full Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation.
title_fullStr Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation.
title_full_unstemmed Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation.
title_sort dissecting the genetic basis of a complex cis-regulatory adaptation.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2015-12-01
description Although single genes underlying several evolutionary adaptations have been identified, the genetic basis of complex, polygenic adaptations has been far more challenging to pinpoint. Here we report that the budding yeast Saccharomyces paradoxus has recently evolved resistance to citrinin, a naturally occurring mycotoxin. Applying a genome-wide test for selection on cis-regulation, we identified five genes involved in the citrinin response that are constitutively up-regulated in S. paradoxus. Four of these genes are necessary for resistance, and are also sufficient to increase the resistance of a sensitive strain when over-expressed. Moreover, cis-regulatory divergence in the promoters of these genes contributes to resistance, while exacting a cost in the absence of citrinin. Our results demonstrate how the subtle effects of individual regulatory elements can be combined, via natural selection, into a complex adaptation. Our approach can be applied to dissect the genetic basis of polygenic adaptations in a wide range of species.
url https://doi.org/10.1371/journal.pgen.1005751
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