Cytokinin transfer by a free-living mirid to Nicotiana attenuata recapitulates a strategy of endophytic insects

Abstract

Endophytic insects provide the textbook examples of herbivores that manipulate their host plant's physiology, putatively altering source/sink relationships by transferring cytokinins (CK) to create 'green islands' that increase the nutritional value of infested tissues. However, unambiguous demonstrations of CK transfer are lacking. Here we show that feeding by the free-living herbivore Tupiocoris notatus on Nicotiana attenuata is characterized by stable nutrient levels, increased CK levels and alterations in CK-related transcript levels in attacked leaves, in striking similarity to endophytic insects. Using 15N-isotope labeling, we demonstrate that the CK N6-isopentenyladenine (IP) is transferred from insects to plants via their oral secretions. In the field, T. notatus preferentially attacks leaves with transgenically increased CK levels; plants with abrogated CK-perception are less tolerant of T. notatus feeding damage. We infer that this free-living insect uses CKs to manipulate source/sink relationships to increase food quality and minimize the fitness consequences of its feeding.

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All data generated or analysed during this study are available on Dryad Digital Repository

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Article and author information

Author details

  1. Christoph Brütting

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  2. Cristina Maria Crava

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3774-4567
  3. Martin Schäfer

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  4. Meredith C Schuman

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3159-3534
  5. Stefan Meldau

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  6. Nora Adam

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  7. Ian T Baldwin

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    For correspondence
    baldwin@ice.mpg.de
    Competing interests
    Ian T Baldwin, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5371-2974

Funding

Max-Planck-Gesellschaft (Open-access funding)

  • Christoph Brütting
  • Cristina Maria Crava
  • Martin Schäfer
  • Meredith C Schuman
  • Stefan Meldau
  • Nora Adam
  • Ian T Baldwin

European Commission (ERC Advanced Grant no. 293926)

  • Christoph Brütting
  • Meredith C Schuman
  • Stefan Meldau

Deutsche Forschungsgemeinschaft (Collaborative Research Centre)

  • Cristina Maria Crava
  • Martin Schäfer

German Center for Integrative Biodiversity Research

  • Nora Adam

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

Publication history

  1. Received: March 1, 2018
  2. Accepted: July 5, 2018
  3. Accepted Manuscript published: July 17, 2018 (version 1)
  4. Version of Record published: July 25, 2018 (version 2)
  5. Version of Record updated: July 26, 2018 (version 3)

Copyright

© 2018, Brütting 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. Christoph Brütting
  2. Cristina Maria Crava
  3. Martin Schäfer
  4. Meredith C Schuman
  5. Stefan Meldau
  6. Nora Adam
  7. Ian T Baldwin
(2018)
Cytokinin transfer by a free-living mirid to Nicotiana attenuata recapitulates a strategy of endophytic insects
eLife 7:e36268.
https://doi.org/10.7554/eLife.36268

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