Blumenols as shoot markers for root symbiosis with arbuscular mycorrhizal fungi

  1. Ming Wang
  2. Martin Schäfer
  3. Dapeng Li
  4. Rayko Halitschke
  5. Chuanfu Dong
  6. Erica McGale
  7. Christian Paetz
  8. Yuanyuan Song
  9. Suhua Li
  10. Junfu Dong
  11. Sven Heiling
  12. Karin Groten
  13. Philipp Franken
  14. Michael Bitterlich
  15. Maria J Harrison
  16. Uta Paszkowski
  17. Ian T Baldwin  Is a corresponding author
  1. Max Planck Institute for Chemical Ecology, Germany
  2. Leibniz-Institute of Vegetable and Ornamental Crops, Germany
  3. Boyce Thompson Institute for Plant Research, United States
  4. University of Cambridge, United Kingdom

Abstract

High-through-put (HTP) screening for functional arbuscular mycorrhizal fungi (AMF)-associations is challenging because roots must be excavated and colonization evaluated by transcript analysis or microscopy. Here we show that specific leaf-metabolites provide broadly applicable accurate proxies of these associations, suitable for HTP-screens. With a combination of untargeted and targeted metabolomics, we show that shoot accumulations of hydroxy- and carboxyblumenol C-glucosides mirror root AMF-colonization in Nicotiana attenuata plants. Genetic/pharmacologic manipulations indicate that these AMF-indicative foliar blumenols are synthesized and transported from roots to shoots. These blumenol-derived foliar markers, found in many di- and monocotyledonous crop and model plants (Solanum lycopersicum, Solanum tuberosum, Hordeum vulgare, Triticum aestivum, Medicago truncatula and Brachypodium distachyon), are not restricted to particular plant-AMF interactions, and are shown to be applicable for field-based QTL mapping of AMF-related genes.

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 all figures.

Article and author information

Author details

  1. Ming Wang

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    Ming Wang, European patent application EP 18 15 8922.7.
  2. Martin Schäfer

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    Martin Schäfer, European patent application EP 18 15 8922.7.
  3. Dapeng Li

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    Dapeng Li, European patent application EP 18 15 8922.7.
  4. Rayko Halitschke

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    Rayko Halitschke, European patent application EP 18 15 8922.7.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1109-8782
  5. Chuanfu Dong

    Department of Bioorganic Chemistry, 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:" 0000-0003-3043-7257
  6. Erica McGale

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    Erica McGale, European patent application EP 18 15 8922.7.
  7. Christian Paetz

    Research Group Biosynthesis / NMR, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  8. Yuanyuan Song

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  9. Suhua Li

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  10. Junfu Dong

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  11. Sven Heiling

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    Sven Heiling, European patent application EP 18 15 8922.7.
  12. Karin Groten

    Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    No competing interests declared.
  13. Philipp Franken

    Leibniz-Institute of Vegetable and Ornamental Crops, Erfurt, Germany
    Competing interests
    No competing interests declared.
  14. Michael Bitterlich

    Leibniz-Institute of Vegetable and Ornamental Crops, Erfurt, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3562-7327
  15. Maria J Harrison

    Boyce Thompson Institute for Plant Research, Ithaca, United States
    Competing interests
    Maria J Harrison, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8716-1875
  16. Uta Paszkowski

    Department of Plant Sciences, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7279-7632
  17. 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, eLifeEuropean patent application EP 18 15 8922.7.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5371-2974

Funding

Max-Planck-Gesellschaft (Open-access funding)

  • Ming Wang
  • Martin Schäfer
  • Dapeng Li
  • Rayko Halitschke
  • Chuanfu Dong
  • Erica McGale
  • Christian Paetz
  • Yuanyuan Song
  • Suhua Li
  • Junfu Dong
  • Sven Heiling
  • Karin Groten
  • Ian T Baldwin

ERC Advanced Grant (ClockworkGreen (293926))

  • Ian T Baldwin

Elsa Neumann Grant

  • Philipp Franken

European Innovation Partnership Agri (276033540220041)

  • Philipp Franken

Ministry of Consumer Protection, Food and Agriculture of Germany

  • Philipp Franken
  • Michael Bitterlich

Ministry for Science, Research and Culture of the State of Brandenburg, Germany

  • Philipp Franken
  • Michael Bitterlich

Thuringian Ministry of Infrastructure and Agriculture

  • Philipp Franken
  • Michael Bitterlich

U.S. Department of Energy (# DESC0012460)

  • Maria J Harrison

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

Reviewing Editor

  1. Detlef Weigel, Max Planck Institute for Developmental Biology, Germany

Version history

  1. Received: March 29, 2018
  2. Accepted: August 22, 2018
  3. Accepted Manuscript published: August 28, 2018 (version 1)
  4. Version of Record published: September 25, 2018 (version 2)

Copyright

© 2018, Wang 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. Ming Wang
  2. Martin Schäfer
  3. Dapeng Li
  4. Rayko Halitschke
  5. Chuanfu Dong
  6. Erica McGale
  7. Christian Paetz
  8. Yuanyuan Song
  9. Suhua Li
  10. Junfu Dong
  11. Sven Heiling
  12. Karin Groten
  13. Philipp Franken
  14. Michael Bitterlich
  15. Maria J Harrison
  16. Uta Paszkowski
  17. Ian T Baldwin
(2018)
Blumenols as shoot markers for root symbiosis with arbuscular mycorrhizal fungi
eLife 7:e37093.
https://doi.org/10.7554/eLife.37093

Share this article

https://doi.org/10.7554/eLife.37093

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