Microsatellites as Agents of Adaptive Change: An RNA-Seq-Based Comparative Study of Transcriptomes from Five <i>Helianthus</i> Species

Mutations that provide environment-dependent selective advantages drive adaptive divergence among species. Many phenotypic differences among related species are more likely to result from gene expression divergence rather than from non-synonymous mutations. In this regard, cis-regulatory mutations p...

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Main Authors: Chathurani Ranathunge, Sreepriya Pramod, Sébastien Renaut, Gregory L. Wheeler, Andy D. Perkins, Loren H. Rieseberg, Mark E. Welch
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:Symmetry
Subjects:
Online Access:https://www.mdpi.com/2073-8994/13/6/933
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spelling doaj-c762be9f1e7c4b3fb36ac5e32ab70d912021-06-01T00:57:51ZengMDPI AGSymmetry2073-89942021-05-011393393310.3390/sym13060933Microsatellites as Agents of Adaptive Change: An RNA-Seq-Based Comparative Study of Transcriptomes from Five <i>Helianthus</i> SpeciesChathurani Ranathunge0Sreepriya Pramod1Sébastien Renaut2Gregory L. Wheeler3Andy D. Perkins4Loren H. Rieseberg5Mark E. Welch6Department of Biological Sciences, Mississippi State University, Starkville, MS 39762, USADepartment of Biological Sciences, Mississippi State University, Starkville, MS 39762, USADepartment of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC V6T 1Z4, CanadaDepartment of Biological Sciences, Mississippi State University, Starkville, MS 39762, USADepartment of Computer Science and Engineering, Mississippi State University, Starkville, MS 39762, USADepartment of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, BC V6T 1Z4, CanadaDepartment of Biological Sciences, Mississippi State University, Starkville, MS 39762, USAMutations that provide environment-dependent selective advantages drive adaptive divergence among species. Many phenotypic differences among related species are more likely to result from gene expression divergence rather than from non-synonymous mutations. In this regard, cis-regulatory mutations play an important part in generating functionally significant variation. Some proposed mechanisms that explore the role of cis-regulatory mutations in gene expression divergence involve microsatellites. Microsatellites exhibit high mutation rates achieved through symmetric or asymmetric mutation processes and are abundant in both coding and non-coding regions in positions that could influence gene function and products. Here we tested the hypothesis that microsatellites contribute to gene expression divergence among species with 50 individuals from five closely related <i>Helianthus</i> species using an RNA-seq approach. Differential expression analyses of the transcriptomes revealed that genes containing microsatellites in non-coding regions (UTRs and introns) are more likely to be differentially expressed among species when compared to genes with microsatellites in the coding regions and transcripts lacking microsatellites. We detected a greater proportion of shared microsatellites in 5′UTRs and coding regions compared to 3′UTRs and non-coding transcripts among <i>Helianthus</i> spp. Furthermore, allele frequency differences measured by pairwise F<sub>ST</sub> at single nucleotide polymorphisms (SNPs), indicate greater genetic divergence in transcripts containing microsatellites compared to those lacking microsatellites. A gene ontology (GO) analysis revealed that microsatellite-containing differentially expressed genes are significantly enriched for GO terms associated with regulation of transcription and transcription factor activity. Collectively, our study provides compelling evidence to support the role of microsatellites in gene expression divergence.https://www.mdpi.com/2073-8994/13/6/933gene expression<i>Helianthus</i>microsatellitestranscriptomics
collection DOAJ
language English
format Article
sources DOAJ
author Chathurani Ranathunge
Sreepriya Pramod
Sébastien Renaut
Gregory L. Wheeler
Andy D. Perkins
Loren H. Rieseberg
Mark E. Welch
spellingShingle Chathurani Ranathunge
Sreepriya Pramod
Sébastien Renaut
Gregory L. Wheeler
Andy D. Perkins
Loren H. Rieseberg
Mark E. Welch
Microsatellites as Agents of Adaptive Change: An RNA-Seq-Based Comparative Study of Transcriptomes from Five <i>Helianthus</i> Species
Symmetry
gene expression
<i>Helianthus</i>
microsatellites
transcriptomics
author_facet Chathurani Ranathunge
Sreepriya Pramod
Sébastien Renaut
Gregory L. Wheeler
Andy D. Perkins
Loren H. Rieseberg
Mark E. Welch
author_sort Chathurani Ranathunge
title Microsatellites as Agents of Adaptive Change: An RNA-Seq-Based Comparative Study of Transcriptomes from Five <i>Helianthus</i> Species
title_short Microsatellites as Agents of Adaptive Change: An RNA-Seq-Based Comparative Study of Transcriptomes from Five <i>Helianthus</i> Species
title_full Microsatellites as Agents of Adaptive Change: An RNA-Seq-Based Comparative Study of Transcriptomes from Five <i>Helianthus</i> Species
title_fullStr Microsatellites as Agents of Adaptive Change: An RNA-Seq-Based Comparative Study of Transcriptomes from Five <i>Helianthus</i> Species
title_full_unstemmed Microsatellites as Agents of Adaptive Change: An RNA-Seq-Based Comparative Study of Transcriptomes from Five <i>Helianthus</i> Species
title_sort microsatellites as agents of adaptive change: an rna-seq-based comparative study of transcriptomes from five <i>helianthus</i> species
publisher MDPI AG
series Symmetry
issn 2073-8994
publishDate 2021-05-01
description Mutations that provide environment-dependent selective advantages drive adaptive divergence among species. Many phenotypic differences among related species are more likely to result from gene expression divergence rather than from non-synonymous mutations. In this regard, cis-regulatory mutations play an important part in generating functionally significant variation. Some proposed mechanisms that explore the role of cis-regulatory mutations in gene expression divergence involve microsatellites. Microsatellites exhibit high mutation rates achieved through symmetric or asymmetric mutation processes and are abundant in both coding and non-coding regions in positions that could influence gene function and products. Here we tested the hypothesis that microsatellites contribute to gene expression divergence among species with 50 individuals from five closely related <i>Helianthus</i> species using an RNA-seq approach. Differential expression analyses of the transcriptomes revealed that genes containing microsatellites in non-coding regions (UTRs and introns) are more likely to be differentially expressed among species when compared to genes with microsatellites in the coding regions and transcripts lacking microsatellites. We detected a greater proportion of shared microsatellites in 5′UTRs and coding regions compared to 3′UTRs and non-coding transcripts among <i>Helianthus</i> spp. Furthermore, allele frequency differences measured by pairwise F<sub>ST</sub> at single nucleotide polymorphisms (SNPs), indicate greater genetic divergence in transcripts containing microsatellites compared to those lacking microsatellites. A gene ontology (GO) analysis revealed that microsatellite-containing differentially expressed genes are significantly enriched for GO terms associated with regulation of transcription and transcription factor activity. Collectively, our study provides compelling evidence to support the role of microsatellites in gene expression divergence.
topic gene expression
<i>Helianthus</i>
microsatellites
transcriptomics
url https://www.mdpi.com/2073-8994/13/6/933
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