Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris

Edited by Michael Lynch, Indiana University, Bloomington, IN, and approved January 28, 2015 (received for review June 30, 2014)
February 17, 2015
112 (9) 2806-2811

Significance

Plants have undergone repeated rounds of whole-genome duplication, followed by gene degeneration and loss. Using whole-genome resequencing, we examined the origins of the recent tetraploid Capsella bursa-pastoris and the earliest stages of genome evolution after polyploidization. We conclude the species had a hybrid origin from two distinct Capsella lineages within the past 100,000–300,000 y. Our analyses suggest the absence of rapid gene loss but provide evidence that the species has large numbers of inactivating mutations, many of which were inherited from the parental species. Our results suggest that genome evolution following polyploidy is determined not only by genome redundancy but also by demography, the mating system, and the evolutionary history of the parental species.

Abstract

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 nonfunctionalization can receive a “head start” through a legacy of deleterious variants and differential expression originating in parental diploid populations.

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Data Availability

Data deposition: The sequences reported in this paper have been deposited in the Sequence Read Archive, www.ncbi.nlm.nih.gov/sra [accession nos. PRJNA268827 (Capsella bursa-pastoris genomic data), PRJNA268847 (C. bursa-pastoris RNA-sequencing), and PRJNA268848 (Capsella grandiflora RNA-sequencing)], and the European Bioinformatics Institute, www.ebi.ac.uk [accession no. PRJEB7879 (Capsella orientalis RNA-sequencing data)].

Acknowledgments

We thank Vitor Sousa (University of Bern) for help with fastsimcoal analyses. DNA and RNA sequencing was performed by the Genome Quebec Innovation Centre, and RNA sequencing was performed by the SNP&SEQ Technology Platform, Science for Life Laboratory (Uppsala University), a national infrastructure supported by the Swedish Research Council (VR-RFI) and the Knut and Alice Wallenberg Foundation. This project was funded by a Natural Sciences and Engineering Research Council (NSERC) Discovery grant and a Genome Quebec/Genome Canada grant (to S.I.W.) and by grants from the Swedish Research Council (to T.S. and M.L.). G.M.D. was supported by an NSERC scholarship, and E.B.J. was supported by a National Science Foundation graduate fellowship. The fastsimcoal2.1 computations were performed on resources provided by the Swedish National Infrastructure for Computing through the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) under Project b2012190.

Supporting Information

Supporting Information (PDF)
Supporting Information
pnas.1412277112.sd01.xlsx

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Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 112 | No. 9
March 3, 2015
PubMed: 25691747

Classifications

Data Availability

Data deposition: The sequences reported in this paper have been deposited in the Sequence Read Archive, www.ncbi.nlm.nih.gov/sra [accession nos. PRJNA268827 (Capsella bursa-pastoris genomic data), PRJNA268847 (C. bursa-pastoris RNA-sequencing), and PRJNA268848 (Capsella grandiflora RNA-sequencing)], and the European Bioinformatics Institute, www.ebi.ac.uk [accession no. PRJEB7879 (Capsella orientalis RNA-sequencing data)].

Submission history

Published online: February 17, 2015
Published in issue: March 3, 2015

Keywords

  1. polyploidy
  2. population genomics
  3. speciation
  4. gene loss

Acknowledgments

We thank Vitor Sousa (University of Bern) for help with fastsimcoal analyses. DNA and RNA sequencing was performed by the Genome Quebec Innovation Centre, and RNA sequencing was performed by the SNP&SEQ Technology Platform, Science for Life Laboratory (Uppsala University), a national infrastructure supported by the Swedish Research Council (VR-RFI) and the Knut and Alice Wallenberg Foundation. This project was funded by a Natural Sciences and Engineering Research Council (NSERC) Discovery grant and a Genome Quebec/Genome Canada grant (to S.I.W.) and by grants from the Swedish Research Council (to T.S. and M.L.). G.M.D. was supported by an NSERC scholarship, and E.B.J. was supported by a National Science Foundation graduate fellowship. The fastsimcoal2.1 computations were performed on resources provided by the Swedish National Infrastructure for Computing through the Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) under Project b2012190.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

Gavin M. Douglas1
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
Gesseca Gos1
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
Kim A. Steige1
Department of Ecology and Genetics, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University, 75236 Uppsala, Sweden;
Adriana Salcedo
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
Karl Holm
Department of Ecology and Genetics, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University, 75236 Uppsala, Sweden;
Emily B. Josephs
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
Ramesh Arunkumar
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
J. Arvid Ågren
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
Khaled M. Hazzouri
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates 129188;
Wei Wang
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
Adrian E. Platts
McGill Centre for Bioinformatics, McGill University, Montreal, QC, Canada H3G 0B1;
Robert J. Williamson
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
Barbara Neuffer
Department of Botany, University of Osnabruck, 49076 Osnabruck, Germany; and
Martin Lascoux2 [email protected]
Department of Ecology and Genetics, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University, 75236 Uppsala, Sweden;
Tanja Slotte2 [email protected]
Department of Ecology and Genetics, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University, 75236 Uppsala, Sweden;
Department of Ecology, Environment, and Plant Sciences, Science for Life Laboratory, Stockholm University, 10691 Stockholm, Sweden
Stephen I. Wright2 [email protected]
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;

Notes

2
To whom correspondence may be addressed. Email: [email protected], [email protected], or [email protected].
Author contributions: G.M.D., K.A.S., M.L., T.S., and S.I.W. designed research; G.M.D., G.G., K.A.S., A.S., K.H., R.A., and K.M.H. performed research; B.N. and M.L. contributed new reagents/analytic tools; G.M.D., G.G., K.A.S., A.S., E.B.J., R.A., J.A.A., W.W., A.E.P., R.J.W., T.S., and S.I.W. analyzed data; and G.M.D., G.G., K.A.S., A.S., R.A., T.S., and S.I.W. wrote the paper.
1
G.M.D., G.G., and K.A.S. contributed equally to this work.

Competing Interests

The authors declare no conflict of interest.

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    Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris
    Proceedings of the National Academy of Sciences
    • Vol. 112
    • No. 9
    • pp. 2623-E1051

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