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The influence of population structure on gene expression and flowering time variation in the ubiquitous weed Capsella bursa-pastoris (Brassicaceae)
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
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2016 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 25, no 5, p. 1106-1121Article in journal (Refereed) Published
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Text
Abstract [en]

Population structure is a potential problem when testing for adaptive phenotypic differences among populations. The observed phenotypic differences among populations can simply be due to genetic drift, and if the genetic distance between them is not considered, the differentiation may be falsely interpreted as adaptive. Conversely, adaptive and demographic processes might have been tightly associated and correcting for the population structure may lead to false negatives. Here, we evaluated this problem in the cosmopolitan weed Capsella bursa-pastoris. We used RNA-Seq to analyse gene expression differences among 24 accessions, which belonged to a much larger group that had been previously characterized for flowering time and circadian rhythm and were genotyped using genotyping-by-sequencing (GBS) technique. We found that clustering of accessions for gene expression retrieved the same three clusters that were obtained with GBS data previously, namely Europe, the Middle East and Asia. Moreover, the three groups were also differentiated for both flowering time and circadian rhythm variation. Correction for population genetic structure when analysing differential gene expression analysis removed all differences among the three groups. This may suggest that most differences are neutral and simply reflect population history. However, geographical variation in flowering time and circadian rhythm indicated that the distribution of adaptive traits might be confounded by population structure. To bypass this confounding effect, we compared gene expression differentiation between flowering ecotypes within the genetic groups. Among the differentially expressed genes, FLOWERING LOCUS C was the strongest candidate for local adaptation in regulation of flowering time.

Place, publisher, year, edition, pages
2016. Vol. 25, no 5, p. 1106-1121
Keyword [en]
adaptation, circadian rhythm, genetic drift, neutrality, population structure, RNA-Seq, transcriptome
National Category
Biochemistry and Molecular Biology Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-282478DOI: 10.1111/mec.13537ISI: 000371433400007PubMedID: 26797895OAI: oai:DiVA.org:uu-282478DiVA, id: diva2:917145
Funder
Swedish Research Council
Available from: 2016-04-05 Created: 2016-04-05 Last updated: 2018-02-13Bibliographically approved
In thesis
1. Genome evolution and adaptation of a successful allopolyploid, Capsella bursa-pastoris
Open this publication in new window or tab >>Genome evolution and adaptation of a successful allopolyploid, Capsella bursa-pastoris
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The term allopolyploid refers to an organism that originated through hybridization and increased its ploidy level by retaining the unreduced genomes of its parents. Both hybridization and polyploidy usually have negative consequences for the organism. However, there are species that not only survive these modifications but even thrive and can outcompete their diploid relatives. There are many intuitive explanations for the success of polyploids, but the number of empirical studies is limited.

The shepherd's purse (Capsella bursa-pastoris) is an emerging model for studying a successful allopolyploid species. C. bursa-pastoris occurs worldwide, whereas its parental species, Capsella grandiflora and Capsella orientalis, have more limited distribution range. C. grandiflora is confined to Northern Greece and Albania, and C. orientalis is found only in the steppes of Central Asia. We described the genetic variation within C. bursa-pastoris and showed that it is not homogeneous across Eurasia but rather subdivided into three genetically distinct populations: one comprises accessions from Europe and Eastern Siberia, the second one is located in Eastern Asia and the third one groups accessions around the Middle East. Reconstruction of the colonization history suggested that this species originated in the Middle East and subsequently spread to Europe and Eastern Asia. This colonization was probably human-mediated. Interestingly, these three populations survive in different environmental conditions, and yet most gene expression differences between them could be explained by neutral processes. We also found that despite a common history within one species, the two subgenomes retained differences already present between the parental species. In particular, the genetic load was still higher on the subgenome inherited from C. orientalis than on the one inherited from C. grandiflora. The two subgenomes were also differentially influenced by introgression and selection in the three genetic clusters. Gene expression variation was highly correlated between the two subgenomes but the total level of expression showed variation in parental dominance across flower, leaf, and root tissues.

This thesis for the first time shows that the evolutionary pathways of allopolyploids may differ not only on the species level but also between populations within one species. It also supports the theory that alloploidy provides an increased amount of genetic material that enables evolutionary flexibility.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2018. p. 51
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1632
Keyword
allopolyploidy, population structure, selection, genetic drift, gene expression, parental legacy, genetic load
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Functional Genomics
Identifiers
urn:nbn:se:uu:diva-341709 (URN)978-91-513-0236-2 (ISBN)
Public defence
2018-03-27, Lindhalsalen, Norbyväagen 18, Uppsala, 10:00 (English)
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Supervisors
Available from: 2018-03-05 Created: 2018-02-13 Last updated: 2018-04-03

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Kryvokhyzha, DmytroChen, JunGlemin, SylvainLagercrantz, UlfLascoux, Martin

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