A terpene synthase-cytochrome P450 cluster in Dictyostelium discoideum produces a novel trisnorsesquiterpene

  1. Xinlu Chen
  2. Katrin Luck
  3. Patrick Rabe
  4. Christopher QD Dinh
  5. Gadi Shaulsky
  6. David R Nelson
  7. Jonathan Gershenzon
  8. Jeroen S Dickschat
  9. Tobias G Köllner
  10. Feng Chen  Is a corresponding author
  1. University of Tennessee, United States
  2. Max Planck Institute for Chemical Ecology, Germany
  3. University of Bonn, Germany
  4. Baylor College of Medicine, United States
  5. University of Tennessee Health Science Center, United States

Abstract

Terpenoids are enormously diverse, but our knowledge of their biosynthesis and functions is limited. Here we report on a terpene synthase (DdTPS8)-cytochrome P450 (CYP521A1) gene cluster that produces a novel C12 trisnorsesquiterpene and affects the development of Dictyostelium discoideum. DdTPS8 catalyzes the formation of a sesquiterpene discoidol, which is undetectable from the volatile bouquet of wild type D. discoideum. Interestingly, a DdTPS8 knockout mutant lacks not only discoidol, but also a putative trisnorsesquiterpene. This compound was hypothesized to be derived from discoidol via cytochrome P450 (CYP)-catalyzed oxidative cleavage. CYP521A1, which is clustered with DdTPS8, was identified as a top candidate. Biochemical assays demonstrated that CYP521A1 catalyzes the conversion of discoidol to a novel trisnorsesquiterpene named discodiene. The DdTPS8 knockout mutant exhibited slow progression in development. This study points to the untapped diversity of natural products made by D. discoideum, which may have diverse roles in its development and chemical ecology.

Data availability

The sequence for CYP521A1 has been deposited in the GenBank database (accession nos. MH923436).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Xinlu Chen

    Department of Plant Sciences, University of Tennessee, Knoxville, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Katrin Luck

    Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Patrick Rabe

    Kekulé-Institute of Organic Chemistry and Biochemistry, University of Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Christopher QD Dinh

    Department of Biochemistry and Molecular Biology, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Gadi Shaulsky

    Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0532-0551
  6. David R Nelson

    Department of Microbiology, Immunology, and Biochemistry, University of Tennessee Health Science Center, Memphis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0583-5421
  7. Jonathan Gershenzon

    Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Jeroen S Dickschat

    Kekulé-Institute of Organic Chemistry and Biochemistry, University of Bonn, Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Tobias G Köllner

    Department of Biochemistry, Max Planck Institute for Chemical Ecology, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Feng Chen

    Department of Plant Sciences, University of Tennessee, Knoxville, United States
    For correspondence
    fengc@utk.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3267-4646

Funding

University of Tennessee Institute of Agriculture

  • Feng Chen

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

Reviewing Editor

  1. Merijn R Kant, University of Amsterdam, Netherlands

Publication history

  1. Received: December 12, 2018
  2. Accepted: May 3, 2019
  3. Accepted Manuscript published: May 7, 2019 (version 1)
  4. Version of Record published: May 17, 2019 (version 2)

Copyright

© 2019, Chen 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. Xinlu Chen
  2. Katrin Luck
  3. Patrick Rabe
  4. Christopher QD Dinh
  5. Gadi Shaulsky
  6. David R Nelson
  7. Jonathan Gershenzon
  8. Jeroen S Dickschat
  9. Tobias G Köllner
  10. Feng Chen
(2019)
A terpene synthase-cytochrome P450 cluster in Dictyostelium discoideum produces a novel trisnorsesquiterpene
eLife 8:e44352.
https://doi.org/10.7554/eLife.44352
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