Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)

  1. Tobias Züst  Is a corresponding author
  2. Susan R Strickler
  3. Adrian F Powell
  4. Makenzie E Mabry
  5. Hong An
  6. Mahdieh Mirzaei
  7. Thomas York
  8. Cynthia K Holland
  9. Pavan Kumar
  10. Matthias Erb
  11. Georg Petschenka
  12. José-María Gomez
  13. Francisco Perfectti
  14. Caroline Müller
  15. J Chris Pires
  16. Lukas A Mueller
  17. Georg Jander
  1. University of Bern, Switzerland
  2. Boyce Thompson Institute, United States
  3. University of Missouri, United States
  4. Justus-Liebig-Universität, Germany
  5. Estación Experimental de Zonas Áridas, Spain
  6. Universidad de Granada, Spain
  7. Bielefeld University, Germany

Abstract

Phytochemical diversity is thought to result from coevolutionary cycles as specialization in herbivores imposes diversifying selection on plant chemical defenses. Plants in the speciose genus Erysimum (Brassicaceae) produce both ancestral glucosinolates and evolutionarily novel cardenolides as defenses. Here we test macroevolutionary hypotheses on co-expression, co-regulation, and diversification of these potentially redundant defenses across this genus. We sequenced and assembled the genome of E. cheiranthoides and foliar transcriptomes of 47 additional Erysimum species to construct a phylogeny from 9,869 orthologous genes, revealing several geographic clades but also high levels gene discordance. Concentrations, inducibility, and diversity of the two defenses varied independently among species, with no evidence for trade-offs. Closely related, geographically co-occurring species shared similar cardenolide traits, but not glucosinolate traits, likely as a result of specific selective pressures acting on each defense. Ancestral and novel chemical defenses in Erysimum thus appear to provide complementary rather than redundant functions.

Data availability

Sequence data are available under GenBank project ID PRJNA563696 and www.erysimum.org, while all trait data and R code for trait and phylogenetic analyses are available from the Dryad Digital Repository

The following data sets were generated

Article and author information

Author details

  1. Tobias Züst

    Institute of Plant Sciences, University of Bern, Bern, Switzerland
    For correspondence
    tobias.zuest@ips.unibe.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7142-8731
  2. Susan R Strickler

    Boyce Thompson Institute, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Adrian F Powell

    Boyce Thompson Institute, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Makenzie E Mabry

    Division of Biological Sciences, University of Missouri, Columbia, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Hong An

    Division of Biological Sciences, University of Missouri, Columbia, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Mahdieh Mirzaei

    Boyce Thompson Institute, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Thomas York

    Boyce Thompson Institute, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Cynthia K Holland

    Boyce Thompson Institute, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Pavan Kumar

    Boyce Thompson Institute, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4718-3601
  10. Matthias Erb

    Institute of Plant Sciences, University of Bern, Bern, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4446-9834
  11. Georg Petschenka

    Institut für Insektenbiotechnologie, Justus-Liebig-Universität, Gießen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9639-3042
  12. José-María Gomez

    Department of Functional and Evolutionary Ecology, Estación Experimental de Zonas Áridas, Almería, Spain
    Competing interests
    The authors declare that no competing interests exist.
  13. Francisco Perfectti

    Genetics, Universidad de Granada, Granada, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5551-213X
  14. Caroline Müller

    Department of Chemical Ecology, Bielefeld University, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. J Chris Pires

    Division of Biological Sciences, University of Missouri, Columbia, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Lukas A Mueller

    Boyce Thompson Institute, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  17. Georg Jander

    Boyce Thompson Institute, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9675-934X

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (PZ00P3-161472)

  • Tobias Züst

National Science Foundation (1811965)

  • Cynthia K Holland

Triad Foundation

  • Susan R Strickler
  • Georg Jander

National Science Foundation (1645256)

  • Georg Jander

Deutsche Forschungsgemeinschaft (DFG-PE 2059/3-1)

  • Georg Petschenka

Agencia Estata de Investigacion, Spain (CGL2017-86626-C2-2-P)

  • Francisco Perfectti

LOEWE Program Insect Biotechnology and Bioresources

  • Georg Petschenka

Junta de Andalucia Programa Operativo (FEDER 2014-2020 A-RNM-505-UGR18)

  • Francisco Perfectti

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

Reviewing Editor

  1. Daniel J Kliebenstein, University of California, Davis, United States

Publication history

  1. Received: September 8, 2019
  2. Accepted: March 24, 2020
  3. Accepted Manuscript published: April 7, 2020 (version 1)
  4. Version of Record published: April 23, 2020 (version 2)

Copyright

© 2020, Züst 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. Tobias Züst
  2. Susan R Strickler
  3. Adrian F Powell
  4. Makenzie E Mabry
  5. Hong An
  6. Mahdieh Mirzaei
  7. Thomas York
  8. Cynthia K Holland
  9. Pavan Kumar
  10. Matthias Erb
  11. Georg Petschenka
  12. José-María Gomez
  13. Francisco Perfectti
  14. Caroline Müller
  15. J Chris Pires
  16. Lukas A Mueller
  17. Georg Jander
(2020)
Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)
eLife 9:e51712.
https://doi.org/10.7554/eLife.51712

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