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

Publication 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.

Metrics

  • 3,039
    Page views
  • 425
    Downloads
  • 24
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Ecology
    2. Epidemiology and Global Health
    Carolina Oliveira de Santana, Pieter Spealman, Gabriel G Perron
    Insight

    The global spread of antibiotic resistance could be due to a number of factors, and not just the overuse of antibiotics in agriculture and medicine as previously thought.

    1. Ecology
    2. Evolutionary Biology
    Naïma Madi, Daisy Chen ... Nandita R Garud
    Research Advance Updated

    How the ecological process of community assembly interacts with intra-species diversity and evolutionary change is a longstanding question. Two contrasting hypotheses have been proposed: Diversity Begets Diversity (DBD), in which taxa tend to become more diverse in already diverse communities, and Ecological Controls (EC), in which higher community diversity impedes diversification. Previously, using 16S rRNA gene amplicon data across a range of microbiomes, we showed a generally positive relationship between taxa diversity and community diversity at higher taxonomic levels, consistent with the predictions of DBD (Madi et al., 2020). However, this positive 'diversity slope' plateaus at high levels of community diversity. Here we show that this general pattern holds at much finer genetic resolution, by analyzing intra-species strain and nucleotide variation in static and temporally sampled metagenomes from the human gut microbiome. Consistent with DBD, both intra-species polymorphism and strain number were positively correlated with community Shannon diversity. Shannon diversity is also predictive of increases in polymorphism over time scales up to ~4-6 months, after which the diversity slope flattens and becomes negative – consistent with DBD eventually giving way to EC. Finally, we show that higher community diversity predicts gene loss at a future time point. This observation is broadly consistent with the Black Queen Hypothesis, which posits that genes with functions provided by the community are less likely to be retained in a focal species' genome. Together, our results show that a mixture of DBD, EC, and Black Queen may operate simultaneously in the human gut microbiome, adding to a growing body of evidence that these eco-evolutionary processes are key drivers of biodiversity and ecosystem function.