Parental legacy, demography, and admixture influenced the evolution of the two subgenomes of the tetraploid Capsella bursa-pastoris (Brassicaceae)

Autor: Kryvokhyzha, Dmytro, Salcedo, Adriana, Eriksson, Mimmi C., Duan, Tianlin, Tawari, Nilesh, Chen, Jun, Guerrina, Maria, Kreiner, Julia M., Kent, Tyler V., Lagercrantz, Ulf, Stinchcombe, John R., Glémin, Sylvain, Wright, Stephen I., Lascoux, Martin
Přispěvatelé: Department of Ecology and Genetics [Uppsala] (EBC), Uppsala University, Department of Ecology and Evolutionary Biology [University of Toronto] (EEB), University of Toronto, Department of Biological and Environmental Sciences [Gothenburg], University of Gothenburg (GU), Ecosystèmes, biodiversité, évolution [Rennes] (ECOBIO), Centre National de la Recherche Scientifique (CNRS)-Observatoire des Sciences de l'Univers de Rennes (OSUR)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES), Vetenskapsrådet, Université de Rennes (UR)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Observatoire des Sciences de l'Univers de Rennes (OSUR), Université de Rennes (UR)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Rennes 2 (UR2)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Rennes 2 (UR2)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Centre National de la Recherche Scientifique (CNRS)
Jazyk: angličtina
Rok vydání: 2019
Předmět:
Gene Flow
Viral Diseases
Computer and Information Sciences
Heredity
Asia
DNA
Plant
lcsh:QH426-470
Gene Expression
Geographical Locations
Polyploidy
Evolution
Molecular
[SDV.GEN.GPL]Life Sciences [q-bio]/Genetics/Plants genetics
Evolutionsbiologi
Middle East
Species Specificity
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]
Medicine and Health Sciences
Genetics
Evolutionary Systematics
Capsella
Rubella
Phylogeny
Taxonomy
Data Management
Evolutionary Biology
[SDV.GEN.GPO]Life Sciences [q-bio]/Genetics/Populations and Evolution [q-bio.PE]
Population Biology
Models
Genetic
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
Biology and Life Sciences
Phylogenetic Analysis
Diploidy
Phylogenetics
Europe
Tetraploidy
Phylogeography
lcsh:Genetics
Infectious Diseases
Deletion Mutation
Genetics
Population
People and Places
Mutation
Hybridization
Genetic
Departures from Diploidy
Population Genetics
Genome
Plant
Research Article
Zdroj: PLoS Genetics
PLoS Genetics, Public Library of Science, 2019, 15 (2), pp.e1007949. ⟨10.1371/journal.pgen.1007949⟩
PLoS Genetics, Vol 15, Iss 2, p e1007949 (2019)
PLoS Genetics, 2019, 15 (2), pp.e1007949. ⟨10.1371/journal.pgen.1007949⟩
ISSN: 1553-7390
1553-7404
DOI: 10.1371/journal.pgen.1007949⟩
Popis: Allopolyploidy is generally perceived as a major source of evolutionary novelties and as an instantaneous way to create isolation barriers. However, we do not have a clear understanding of how two subgenomes evolve and interact once they have fused in an allopolyploid species nor how isolated they are from their relatives. Here, we address these questions by analyzing genomic and transcriptomic data of allotetraploid Capsella bursa-pastoris in three differentiated populations, Asia, Europe, and the Middle East. We phased the two subgenomes, one descended from the outcrossing and highly diverse Capsella grandiflora (CbpCg) and the other one from the selfing and genetically depauperate Capsella orientalis (CbpCo). For each subgenome, we assessed its relationship with the diploid relatives, temporal changes of effective population size (Ne), signatures of positive and negative selection, and gene expression patterns. In all three regions, Ne of the two subgenomes decreased gradually over time and the CbpCo subgenome accumulated more deleterious changes than CbpCg. There were signs of widespread admixture between C. bursa-pastoris and its diploid relatives. The two subgenomes were impacted differentially depending on geographic region suggesting either strong interploidy gene flow or multiple origins of C. bursa-pastoris. Selective sweeps were more common on the CbpCg subgenome in Europe and the Middle East, and on the CbpCo subgenome in Asia. In contrast, differences in expression were limited with the CbpCg subgenome slightly more expressed than CbpCo in Europe and the Middle-East. In summary, after more than 100,000 generations of co-existence, the two subgenomes of C. bursa-pastoris still retained a strong signature of parental legacy but their evolutionary trajectory strongly varied across geographic regions.
Author summary Allopolyploid species have two or more sets of chromosomes that originate from hybridization of different species. It remains largely unknown how the two genomes evolve in the same organism and how strongly their evolutionary trajectory depends on the initial differences between the two parental species and the specific demographic history of the newly formed allopolyploid species. To address these questions, we analyzed the genomic and gene expression variation of the shepherd’s purse, a recent allopolyploid species, in three regions of its natural range. After ∼100,000 generations of co-existence within the same species, the two subgenomes had still retained part of the initial difference between the two parental species in the number of deleterious mutations reflecting a history of mating system differences. This difference, as well as differences in patterns of positive selection and levels of gene expression, also strongly depended on the specific histories of the three regions considered. Most strikingly, and unexpectedly, the allopolyploid species showed signs of hybridization with different diploid relatives or multiple origins in different parts of its range. Regardless if it was hybridization or multiple origins, this profoundly altered the relationship between the two subgenomes in different regions. Hence, our study illustrates how both the genomic structure and ecological arena interact to determine the evolutionary trajectories of allopolyploid species.
Databáze: OpenAIRE
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