Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana

  1. Wenwu Zhou
  2. Thomas Brockmöller
  3. Zhihao Ling
  4. Ashton Omdahl
  5. Ian T Baldwin
  6. Shuqing Xu  Is a corresponding author
  1. Max Planck Institute for Chemical Ecology, Germany
  2. Brigham Young University, United States
  3. Max-Planck Institute for Chemical Ecology, Germany

Abstract

Herbivore-induced defenses are widespread, rapidly evolving and relevant for plant fitness. Such induced defenses are often mediated by early defense signaling (EDS) rapidly activated by the perception of herbivore associated elicitors (HAE) that includes transient accumulations of jasmonic acid (JA). Analyzing 60 HAE-induced leaf transcriptomes from closely-related Nicotiana species revealed a key gene co-expression network (M4 module) which is co-activated with the HAE-induced JA accumulations but is elicited independently of JA, as revealed in plants silenced in JA signaling. Functional annotations of the M4 module were consistent with roles in EDS and a newly identified hub gene of the M4 module (NaLRRK1) mediates a negative feedback loop with JA signaling. Phylogenomic analysis revealed preferential gene retention after genome-wide duplications shaped the evolution of HAE-induced EDS in Nicotiana. These results highlight the importance of genome-wide duplications in the evolution of adaptive traits in plants.

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Author details

  1. Wenwu Zhou

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  2. Thomas Brockmöller

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  3. Zhihao Ling

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  4. Ashton Omdahl

    Brigham Young University, Provo, United States
    Competing interests
    No competing interests declared.
  5. Ian T Baldwin

    Department of Molecular Ecology, Max-Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    Ian T Baldwin, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5371-2974
  6. Shuqing Xu

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    For correspondence
    sxu@ice.mpg.de
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7010-4604

Funding

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (PEBZP3-142886)

  • Shuqing Xu

European Research Council (293926)

  • Ian T Baldwin

European Commission (328935)

  • Shuqing Xu

Max-Planck-Gesellschaft

  • Wenwu Zhou
  • Thomas Brockmöller
  • Zhihao Ling
  • Ashton Omdahl
  • Ian T Baldwin
  • Shuqing Xu

Sutter-Stötner-Stiftung

  • Shuqing Xu

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

Reviewing Editor

  1. Joerg Bohlmann, University of British Columbia, Canada

Version history

  1. Received: July 11, 2016
  2. Accepted: November 1, 2016
  3. Accepted Manuscript published: November 4, 2016 (version 1)
  4. Version of Record published: November 18, 2016 (version 2)

Copyright

© 2016, Zhou 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. Wenwu Zhou
  2. Thomas Brockmöller
  3. Zhihao Ling
  4. Ashton Omdahl
  5. Ian T Baldwin
  6. Shuqing Xu
(2016)
Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana
eLife 5:e19531.
https://doi.org/10.7554/eLife.19531

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https://doi.org/10.7554/eLife.19531

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