Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance

  1. Ruo Sun
  2. Xingcong Jiang
  3. Michael Reichelt
  4. Jonathan Gershenzon
  5. Sagar Subhash Pandit  Is a corresponding author
  6. Daniel Giddings Vassão  Is a corresponding author
  1. Max Planck Institute for Chemical Ecology, Germany
  2. Indian Institute of Science Education and Research, India

Abstract

Insect herbivores are frequently reported to metabolize plant defense compounds, but the physiological and ecological consequences are not fully understood. It has rarely been studied whether such metabolism is genuinely beneficial to the insect, and whether there are any effects on higher trophic levels. Here, we manipulated the detoxification of plant defenses in the herbivorous pest diamondback moth (Plutella xylostella) to evaluate changes in fitness, and additionally examined the effects on a predatory lacewing (Chrysoperla carnea). Silencing glucosinolate sulfatase genes resulted in the systemic accumulation of toxic isothiocyanates in P. xylostella larvae, impairing larval development and adult reproduction. The predatory lacewing C. carnea, however, efficiently degraded ingested isothiocyanates via a general conjugation pathway, with no negative effects on survival, reproduction, or even prey preference. These results illustrate how plant defenses and their detoxification strongly influence herbivore fitness but might only subtly affect a third trophic level.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for figures and figure supplements.

Article and author information

Author details

  1. Ruo Sun

    Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9861-6097
  2. Xingcong Jiang

    Department of Evolutionary Neuroethology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Michael Reichelt

    Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6691-6500
  4. Jonathan Gershenzon

    Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Sagar Subhash Pandit

    Molecular and Chemical Ecology Lab, Indian Institute of Science Education and Research, Pune, India
    For correspondence
    sagar@iiserpune.ac.in
    Competing interests
    The authors declare that no competing interests exist.
  6. Daniel Giddings Vassão

    Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
    For correspondence
    vassao@ice.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8455-9298

Funding

China Scholarship Council

  • Ruo Sun

Max-Planck-Gesellschaft

  • Ruo Sun
  • Xingcong Jiang
  • Michael Reichelt
  • Jonathan Gershenzon
  • Sagar Subhash Pandit
  • Daniel Giddings Vassão

The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Reviewing Editor

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

Version history

  1. Received: August 12, 2019
  2. Accepted: December 13, 2019
  3. Accepted Manuscript published: December 16, 2019 (version 1)
  4. Version of Record published: December 27, 2019 (version 2)

Copyright

© 2019, Sun 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. Ruo Sun
  2. Xingcong Jiang
  3. Michael Reichelt
  4. Jonathan Gershenzon
  5. Sagar Subhash Pandit
  6. Daniel Giddings Vassão
(2019)
Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance
eLife 8:e51029.
https://doi.org/10.7554/eLife.51029

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https://doi.org/10.7554/eLife.51029

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