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Towards the new normal: Genomic and transcriptomic changes in the two subgenomes of a 100,000 years old tetraploid, Capsella bursa-pastoris
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2018 (English)Manuscript (preprint) (Other academic)
Abstract [en]

Allopolyploidy has played a major role in plant evolution but its impact on genome diversity and expression pattern still remains to be understood and put in a clear temporal perspective. Some studies have described important genomic and transcriptomic changes, whereas others detected a strong legacy from the parental species and much more subtle and concerted changes. These differences across studies could be the result of many factors such as age and demographic history of the alloploid species or extent of the divergence between the parental species. In the present study, we sequenced the transcriptomes of three tissues (root, leaf, and flower) and genomes of the tetraploid selfer C.bursa-pastoris, its two parental species C.grandiflora and C.orientalis, and its close relative C.rubella. In total 84 transcriptomes and 28 genomes were obtained. C.bursa-pastoris was created around 100,000 years ago and one would, therefore, expect the two subgenomes to be more similar in term of genetic polymorphism and their expression to have started to function together. However, at the genome level there was still a significant legacy effect on the number of deleterious genes carried by the two subgenomes of C.bursa-pastoris, with a higher accumulation of derived deleterious mutations in the C.orientalis subgenome. However, the overdispersion of the distribution of deleterious mutations was smaller than for synonymous ones, suggesting that both copies are needed and prevented to accumulate too many deleterious mutations. At the level of gene expression, one could still also detect a legacy effect but there were, however, significant differences among the three tissues with a more pronounced legacy effect of the  C.orientalis expression level in flower, a stronger C.grandiflora one in root and a more balanced situation in leaf. \hl{Flower tissues showed more evidence of trans regulation than leaf and root tissues. Finally, here was no association between expression levels and the number of deleterious mutations.

Place, publisher, year, edition, pages
2018.
Keywords [en]
allopolyploidy, gene expression, deleterious genes, parental legacy
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-341708OAI: oai:DiVA.org:uu-341708DiVA, id: diva2:1182323
Available from: 2018-02-13 Created: 2018-02-13 Last updated: 2018-02-13
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
Keywords
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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Available from: 2018-03-05 Created: 2018-02-13 Last updated: 2018-04-03

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