Playing Hide-and-Seek in Beta-Globin Genes: Gene Conversion Transferring a Beneficial Mutation between Differentially Expressed Gene Duplicates

Increasing evidence suggests that adaptation to diverse environments often involves selection on existing variation rather than new mutations. A previous study identified a nonsynonymous single nucleotide polymorphism (SNP) in exon 2 of two paralogous β-globin genes of the bank vole (Clethr...

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Main Authors: Michaela Strážnická, Silvia Marková, Jeremy B. Searle, Petr Kotlík
Format: Article
Language:English
Published: MDPI AG 2018-10-01
Series:Genes
Subjects:
Online Access:http://www.mdpi.com/2073-4425/9/10/492
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spelling doaj-46d9b89cac8c493891aff37a4beac6e72020-11-24T21:08:45ZengMDPI AGGenes2073-44252018-10-0191049210.3390/genes9100492genes9100492Playing Hide-and-Seek in Beta-Globin Genes: Gene Conversion Transferring a Beneficial Mutation between Differentially Expressed Gene DuplicatesMichaela Strážnická0Silvia Marková1Jeremy B. Searle2Petr Kotlík3Laboratory of Molecular Ecology, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Rumburská 89, 27721 Liběchov, Czech RepublicLaboratory of Molecular Ecology, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Rumburská 89, 27721 Liběchov, Czech RepublicDepartment of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USALaboratory of Molecular Ecology, Institute of Animal Physiology and Genetics, Czech Academy of Sciences, Rumburská 89, 27721 Liběchov, Czech RepublicIncreasing evidence suggests that adaptation to diverse environments often involves selection on existing variation rather than new mutations. A previous study identified a nonsynonymous single nucleotide polymorphism (SNP) in exon 2 of two paralogous β-globin genes of the bank vole (Clethrionomys glareolus) in Britain in which the ancestral serine (Ser) and the derived cysteine (Cys) allele represent geographically partitioned functional variation affecting the erythrocyte antioxidative capacity. Here we studied the geographical pattern of the two-locus Ser/Cys polymorphism throughout Europe and tested for the geographic correlation between environmental variables and allele frequency, expected if the polymorphism was under spatially heterogeneous environment-related selection. Although bank vole population history clearly is important in shaping the dispersal of the oxidative stress protective Cys allele, analyses correcting for population structure suggest the Europe-wide pattern is affected by geographical variation in environmental conditions. The β-globin phenotype is encoded by the major paralog HBB-T1 but we found evidence of bidirectional gene conversion of exon 2 with the low-expression paralog HBB-T2. Our data support the model where gene conversion reshuffling genotypes between high- and low- expressed paralogs enables tuning of erythrocyte thiol levels, which may help maintain intracellular redox balance under fluctuating environmental conditions. Therefore, our study suggests a possible role for gene conversion between differentially expressed gene duplicates as a mechanism of physiological adaptation of populations to new or changing environments.http://www.mdpi.com/2073-4425/9/10/492adaptive phylogeographycysteineantioxidative capacitygene conversionChi motifenvironmental selection
collection DOAJ
language English
format Article
sources DOAJ
author Michaela Strážnická
Silvia Marková
Jeremy B. Searle
Petr Kotlík
spellingShingle Michaela Strážnická
Silvia Marková
Jeremy B. Searle
Petr Kotlík
Playing Hide-and-Seek in Beta-Globin Genes: Gene Conversion Transferring a Beneficial Mutation between Differentially Expressed Gene Duplicates
Genes
adaptive phylogeography
cysteine
antioxidative capacity
gene conversion
Chi motif
environmental selection
author_facet Michaela Strážnická
Silvia Marková
Jeremy B. Searle
Petr Kotlík
author_sort Michaela Strážnická
title Playing Hide-and-Seek in Beta-Globin Genes: Gene Conversion Transferring a Beneficial Mutation between Differentially Expressed Gene Duplicates
title_short Playing Hide-and-Seek in Beta-Globin Genes: Gene Conversion Transferring a Beneficial Mutation between Differentially Expressed Gene Duplicates
title_full Playing Hide-and-Seek in Beta-Globin Genes: Gene Conversion Transferring a Beneficial Mutation between Differentially Expressed Gene Duplicates
title_fullStr Playing Hide-and-Seek in Beta-Globin Genes: Gene Conversion Transferring a Beneficial Mutation between Differentially Expressed Gene Duplicates
title_full_unstemmed Playing Hide-and-Seek in Beta-Globin Genes: Gene Conversion Transferring a Beneficial Mutation between Differentially Expressed Gene Duplicates
title_sort playing hide-and-seek in beta-globin genes: gene conversion transferring a beneficial mutation between differentially expressed gene duplicates
publisher MDPI AG
series Genes
issn 2073-4425
publishDate 2018-10-01
description Increasing evidence suggests that adaptation to diverse environments often involves selection on existing variation rather than new mutations. A previous study identified a nonsynonymous single nucleotide polymorphism (SNP) in exon 2 of two paralogous β-globin genes of the bank vole (Clethrionomys glareolus) in Britain in which the ancestral serine (Ser) and the derived cysteine (Cys) allele represent geographically partitioned functional variation affecting the erythrocyte antioxidative capacity. Here we studied the geographical pattern of the two-locus Ser/Cys polymorphism throughout Europe and tested for the geographic correlation between environmental variables and allele frequency, expected if the polymorphism was under spatially heterogeneous environment-related selection. Although bank vole population history clearly is important in shaping the dispersal of the oxidative stress protective Cys allele, analyses correcting for population structure suggest the Europe-wide pattern is affected by geographical variation in environmental conditions. The β-globin phenotype is encoded by the major paralog HBB-T1 but we found evidence of bidirectional gene conversion of exon 2 with the low-expression paralog HBB-T2. Our data support the model where gene conversion reshuffling genotypes between high- and low- expressed paralogs enables tuning of erythrocyte thiol levels, which may help maintain intracellular redox balance under fluctuating environmental conditions. Therefore, our study suggests a possible role for gene conversion between differentially expressed gene duplicates as a mechanism of physiological adaptation of populations to new or changing environments.
topic adaptive phylogeography
cysteine
antioxidative capacity
gene conversion
Chi motif
environmental selection
url http://www.mdpi.com/2073-4425/9/10/492
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