The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique history

  1. Danièle L Filiault
  2. Evangeline S Ballerini
  3. Terezie Mandáková
  4. Gökçe Aköz
  5. Nathan J Derieg
  6. Jeremy Schmutz
  7. Jerry Jenkins
  8. Jane Grimwood
  9. Shengqiang Shu
  10. Richard D Hayes
  11. Uffe Hellsten
  12. Kerrie Barry
  13. Juying Yan
  14. Sirma Mihaltcheva
  15. Miroslava Karafiátová
  16. Viktoria Nizhynska
  17. Elena M Kramer
  18. Martin A Lysak
  19. Scott A Hodges  Is a corresponding author
  20. Magnus Nordborg  Is a corresponding author
  1. Austrian Academy of Sciences, Austria
  2. University of California, Santa Barbara, United States
  3. Masaryk University, Czech Republic
  4. Department of Energy, United States
  5. Centre of the Region Haná for Biotechnological and Agricultural Research, Czech Republic
  6. Harvard University, United States

Abstract

The columbine genus Aquilegia is a classic example of an adaptive radiation, involving a wide variety of pollinators and habitats. Here we present the genome assembly of A. coerulea 'Goldsmith', complemented by high-coverage sequencing data from 10 wild species covering the world-wide distribution. Our analyses reveal extensive allele sharing among species, and demonstrate that introgression and selection played a role in the Aquilegia radiation. We also present the remarkable discovery that the evolutionary history of an entire chromosome differs from that of the rest of the genome - a phenomenon which we do not fully understand, but which highlights the need to consider chromosomes in an evolutionary context.

Data availability

Species resequencingA. barnebyi (SRR7965809), A. aurea (SRR405095), A. vulgaris (SRR404349), A. sibirica (SRR405090), A. formosa (SRR408554), A. japonica (SRR413499), A. oxysepala (SRR413921), A. longissima (SRR7965810), A. chrysantha (SRR408559), A. pubescens (SRR7943924) are available in the Short Read Archive(https://www.ncbi.nlm.nih.gov/sra).Whole genome Aquilegia coerulea 'Goldsmith'Sanger sequences used for genome assembly are available in the NCBI Trace Archive (https://www.ncbi.nlm.nih.gov/Traces).Aquilegia coerulea 'Goldsmith' ESTsAvailable in the NCBI Short Read Archive (SRR505574-SRR505578)Aquilegia formosa 412 ESTsAvailable in the NCBI dbEST (https://www.ncbi.nlm.nih.gov/dbEST/)Aquilegia coerulea 'Goldsmith' X Aquilegia chrysantha mapping populationAvailable in the NCBI Short Read Archive (SRR8000449-SRR8000976)Aquilegia formosa x Aquilegia pubescens mapping populationAvailable in the NCBI Short Read Archive (Bioproject PRJNA489508).grandparentspub.1 (SRR7943925), pub.2 (SRR7943924), form.1 (SRR7790646), form.2 (SRR408554)F1sF1.1 (SRR7943926), F1.2 (SRR7943927)F2sSRR7814612-SRR7814614, SRR7814616-SRR7814619, SRR7814622, SRR7814624-SRR7814686, SRR7826362- SRR7826624RNAseqAvailable in the NCBI Short Read Archive: see Supplementary Table 5 for more details.Other filesA vcf containing biallelic SNPs called in all ten Aquilegia species and Semiaquilegia (AQ.Semi.all.biallelic.SNPs.vcf.gz) and text files of genomic positions passing filtration (AQ.only.kept.positions.txt.gz and AQ.Semi.kept.positions.txt.gz) are available for download at Dryad (doi:10.5061/dryad.j4j12v0).URLsThe A. coerulea 'Goldsmith' v3.1 genome release is available at: https://phytozome.jgi.doe.gov/

The following data sets were generated

Article and author information

Author details

  1. Danièle L Filiault

    Gregor Mendel Institute, Vienna Biocenter, Austrian Academy of Sciences, Vienna, Austria
    Competing interests
    No competing interests declared.
  2. Evangeline S Ballerini

    Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    No competing interests declared.
  3. Terezie Mandáková

    CEITEC - Central-European Institute of Technology, Masaryk University, Brno, Czech Republic
    Competing interests
    No competing interests declared.
  4. Gökçe Aköz

    Gregor Mendel Institute, Vienna Biocenter, Austrian Academy of Sciences, Vienna, Austria
    Competing interests
    No competing interests declared.
  5. Nathan J Derieg

    Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, United States
    Competing interests
    No competing interests declared.
  6. Jeremy Schmutz

    Joint Genome Institute, Department of Energy, Walnut Creek, United States
    Competing interests
    No competing interests declared.
  7. Jerry Jenkins

    Joint Genome Institute, Department of Energy, Walnut Creek, United States
    Competing interests
    No competing interests declared.
  8. Jane Grimwood

    Joint Genome Institute, Department of Energy, Walnut Creek, United States
    Competing interests
    No competing interests declared.
  9. Shengqiang Shu

    Joint Genome Institute, Department of Energy, Walnut Creek, United States
    Competing interests
    No competing interests declared.
  10. Richard D Hayes

    Joint Genome Institute, Department of Energy, Walnut Creek, United States
    Competing interests
    No competing interests declared.
  11. Uffe Hellsten

    Joint Genome Institute, Department of Energy, Walnut Creek, United States
    Competing interests
    No competing interests declared.
  12. Kerrie Barry

    Joint Genome Institute, Department of Energy, Walnut Creek, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8999-6785
  13. Juying Yan

    Joint Genome Institute, Department of Energy, Walnut Creek, United States
    Competing interests
    No competing interests declared.
  14. Sirma Mihaltcheva

    Joint Genome Institute, Department of Energy, Walnut Creek, United States
    Competing interests
    No competing interests declared.
  15. Miroslava Karafiátová

    Institute of Experimental Botany, Centre of the Region Haná for Biotechnological and Agricultural Research, Olomouc, Czech Republic
    Competing interests
    No competing interests declared.
  16. Viktoria Nizhynska

    Gregor Mendel Institute, Vienna Biocenter, Austrian Academy of Sciences, Vienna, Austria
    Competing interests
    No competing interests declared.
  17. Elena M Kramer

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    No competing interests declared.
  18. Martin A Lysak

    CEITEC - Central-European Institute of Technology, Masaryk University, Brno, Czech Republic
    Competing interests
    No competing interests declared.
  19. Scott A Hodges

    Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, United States
    For correspondence
    scott.hodges@lifesci.ucsb.edu
    Competing interests
    No competing interests declared.
  20. Magnus Nordborg

    Gregor Mendel Institute, Vienna Biocenter, Austrian Academy of Sciences, Vienna, Austria
    For correspondence
    magnus.nordborg@gmi.oeaw.ac.at
    Competing interests
    Magnus Nordborg, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7178-9748

Funding

Czech Science Foundation (P501/12/G090)

  • Martin A Lysak

CEITEC 2020 (LQ1601)

  • Martin A Lysak

National Program of Sustainability I (LO1204)

  • Miroslava Karafiátová

Austrian Science Funds (FWF DK W1225-B20)

  • Gökçe Aköz

University of California, Santa Barbara (Harvey L. Karp Discovery Award)

  • Evangeline S Ballerini

National Institutes of Health (Ruth L. Kirschstein National Research Service Award F32GM103154)

  • Evangeline S Ballerini

National Science Foundation (IOS 1456317)

  • Scott A Hodges

National Science Foundation (DEB 1311390)

  • Nathan J Derieg
  • Scott A Hodges

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Gil McVean, Oxford University, United Kingdom

Publication history

  1. Received: March 6, 2018
  2. Accepted: September 17, 2018
  3. Accepted Manuscript published: October 16, 2018 (version 1)
  4. Version of Record published: November 26, 2018 (version 2)

Copyright

© 2018, Filiault et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Danièle L Filiault
  2. Evangeline S Ballerini
  3. Terezie Mandáková
  4. Gökçe Aköz
  5. Nathan J Derieg
  6. Jeremy Schmutz
  7. Jerry Jenkins
  8. Jane Grimwood
  9. Shengqiang Shu
  10. Richard D Hayes
  11. Uffe Hellsten
  12. Kerrie Barry
  13. Juying Yan
  14. Sirma Mihaltcheva
  15. Miroslava Karafiátová
  16. Viktoria Nizhynska
  17. Elena M Kramer
  18. Martin A Lysak
  19. Scott A Hodges
  20. Magnus Nordborg
(2018)
The Aquilegia genome provides insight into adaptive radiation and reveals an extraordinarily polymorphic chromosome with a unique history
eLife 7:e36426.
https://doi.org/10.7554/eLife.36426

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