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Cis-regulatory variation and divergence in Capsella
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Cis-regulatory changes in e.g. promoters or enhancers that affect the expression of a linked focal gene have long been thought to be important for adaptation. In this thesis, I investigate the selective importance and genomic correlates of cis-regulatory variation and divergence in the genus Capsella, using massively parallel sequencing data. This genus provides an opportunity to investigate cis-regulatory changes in response to polyploidization and mating system shifts, as it harbors three diploid species, the outcrosser Capsella grandiflora and the selfers Capsella orientalis and Capsella rubella, as well as the tetraploid Capsella bursa-pastoris. We first identify cis-regulatory changes associated with adaptive floral evolution in connection with the recent switch to self-fertilization in C. rubella and show that cis-regulatory changes between C. rubella and its outcrossing close relative C. grandiflora are associated with differences in transposable element content. Second, we show that variation in positive and purifying selection is important for the distribution of cis-regulatory variation across the genome of C. grandiflora. Interestingly, the presence of polymorphic transposable elements is strongly associated with cis-regulatory variation in C. grandiflora. Third, we show that the tetraploid C. bursa-pastoris is of hybrid origin and investigate the contribution of both parental species to gene expression. We show that gene expression in the tetraploid is partly explained by cis-regulatory divergence between the parental species. Nonetheless, within C. bursa-pastoris there is a great deal of variation in homeolog expression. In summary, this thesis explores the role of cis-regulatory changes for adaptive morphological changes in connection to a shift in mating system, the role of cis-regulatory divergence between progenitor species for an allopolyploid as well as the impact of positive and purifying selection on cis-regulatory variation within a species.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2016. , 45 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1332
Keyword [en]
Capsella, Shepherd's Purse, cis-regulatory changes, allele-specific expression, mating system shift, floral evolution, polyploidy, positive selection, purifying selection, transposable elements, small RNA, methylation, transposable element silencing, distribution of fitness effects
National Category
Natural Sciences
Identifiers
URN: urn:nbn:se:uu:diva-268953ISBN: 978-91-554-9442-1 (print)OAI: oai:DiVA.org:uu-268953DiVA: diva2:881899
Public defence
2016-02-15, Lindahlsalen, Norbyvägen 18 A, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2016-01-22 Created: 2015-12-11 Last updated: 2016-02-12
List of papers
1. Cis-Regulatory Changes Associated with a Recent Mating System Shift and Floral Adaptation in Capsella
Open this publication in new window or tab >>Cis-Regulatory Changes Associated with a Recent Mating System Shift and Floral Adaptation in Capsella
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2015 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 32, no 10, 2501-2514 p.Article in journal (Refereed) Published
Abstract [en]

The selfing syndrome constitutes a suite of floral and reproductive trait changes that have evolved repeatedly across many evolutionary lineages in response to the shift to selfing. Convergent evolution of the selfing syndrome suggests that these changes are adaptive, yet our understanding of the detailed molecular genetic basis of the selfing syndrome remains limited. Here, we investigate the role of cis-regulatory changes during the recent evolution of the selfing syndrome in Capsella rubella, which split from the outcrosser Capsella grandiflora less than 200 ka. We assess allele-specific expression (ASE) in leaves and flower buds at a total of 18,452 genes in three interspecific F1 C. grandiflora x C. rubella hybrids. Using a hierarchical Bayesian approach that accounts for technical variation using genomic reads, we find evidence for extensive cis-regulatory changes. On average, 44% of the assayed genes show evidence of ASE; however, only 6% show strong allelic expression biases. Flower buds, but not leaves, show an enrichment of cis-regulatory changes in genomic regions responsible for floral and reproductive trait divergence between C. rubella and C. grandiflora. We further detected an excess of heterozygous transposable element (TE) insertions near genes with ASE, and TE insertions targeted by uniquely mapping 24-nt small RNAs were associated with reduced expression of nearby genes. Our results suggest that cis-regulatory changes have been important during the recent adaptive floral evolution in Capsella and that differences in TE dynamics between selfing and outcrossing species could be important for rapid regulatory divergence in association with mating system shifts.

Keyword
gene expression, adaptation, self-fertilization, allele-specific expression, mating system evolution, cis-regulatory evolution
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-265690 (URN)10.1093/molbev/msv169 (DOI)000361987100001 ()26318184 (PubMedID)
Funder
Swedish Research CouncilKnut and Alice Wallenberg FoundationThe Royal Swedish Academy of Sciences
Available from: 2015-11-03 Created: 2015-11-02 Last updated: 2017-12-01Bibliographically approved
2. The impact of natural selection on the distribution of cis-regulatory variation across the genome of an outcrossing plant
Open this publication in new window or tab >>The impact of natural selection on the distribution of cis-regulatory variation across the genome of an outcrossing plant
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(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-268923 (URN)
Available from: 2015-12-11 Created: 2015-12-11 Last updated: 2016-02-12
3. Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris
Open this publication in new window or tab >>Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris
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2015 (English)In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 112, no 9, 2806-2811 p.Article in journal (Refereed) Published
Abstract [en]

Whole-genome duplication (WGD) events have occurred repeatedly during flowering plant evolution, and there is growing evidence for predictable patterns of gene retention and loss following polyploidization. Despite these important insights, the rate and processes governing the earliest stages of diploidization remain poorly understood, and the relative importance of genetic drift, positive selection, and relaxed purifying selection in the process of gene degeneration and loss is unclear. Here, we conduct whole-genome resequencing in Capsella bursa-pastoris, a recently formed tetraploid with one of the most widespread species distributions of any angiosperm. Whole-genome data provide strong support for recent hybrid origins of the tetraploid species within the past 100,000-300,000 y from two diploid progenitors in the Capsella genus. Major-effect inactivating mutations are frequent, but many were inherited from the parental species and show no evidence of being fixed by positive selection. Despite a lack of large-scale gene loss, we observe a decrease in the efficacy of natural selection genome-wide due to the combined effects of demography, selfing, and genome redundancy from WGD. Our results suggest that the earliest stages of diploidization are associated with quantitative genome-wide decreases in the strength and efficacy of selection rather than rapid gene loss, and that non-functionalization can receive a "head start" through a legacy of deleterious variants and differential expression originating in parental diploid populations.

Keyword
polyploidy, population genomics, speciation, gene loss
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-248808 (URN)10.1073/pnas.1412277112 (DOI)000350224900057 ()25691747 (PubMedID)
Available from: 2015-04-09 Created: 2015-04-08 Last updated: 2017-12-04Bibliographically approved
4. The role of transposable elements for gene expression in Capsella hybrids and allopolyploids
Open this publication in new window or tab >>The role of transposable elements for gene expression in Capsella hybrids and allopolyploids
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(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-268925 (URN)
Available from: 2015-12-11 Created: 2015-12-11 Last updated: 2016-02-12

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