1. Biochemistry and Chemical Biology
  2. Plant Biology
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Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity

  1. Pengxiang Fan
  2. Peipei Wang
  3. Yann-Ru Lou
  4. Bryan J Leong
  5. Bethany M Moore
  6. Craig A Schenck
  7. Rachel Combs
  8. Pengfei Cao
  9. Federica Brandizzi
  10. Shin-Han Shiu
  11. Robert L Last  Is a corresponding author
  1. Michigan State University, United States
  2. Ohio State University, United States
Research Article
  • Cited 2
  • Views 1,862
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Cite this article as: eLife 2020;9:e56717 doi: 10.7554/eLife.56717

Abstract

Plants produce phylogenetically and spatially restricted, as well as structurally diverse specialized metabolites via multistep metabolic pathways. Hallmarks of specialized metabolic evolution include enzymatic promiscuity and recruitment of primary metabolic enzymes and examples of genomic clustering of pathway genes. Solanaceae glandular trichomes produce defensive acylsugars, with sidechains that vary in length across the family. We describe a tomato gene cluster on chromosome 7 involved in medium chain acylsugar accumulation due to trichome specific acyl-CoA synthetase and enoyl-CoA hydratase genes. This cluster co-localizes with a tomato steroidal alkaloid gene cluster and is syntenic to a chromosome 12 region containing another acylsugar pathway gene. We reconstructed the evolutionary events leading to this gene cluster and found that its phylogenetic distribution correlates with medium chain acylsugar accumulation across the Solanaceae. This work reveals insights into the dynamics behind gene cluster evolution and cell-type specific metabolite diversity.

Article and author information

Author details

  1. Pengxiang Fan

    Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Peipei Wang

    Plant BIology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Yann-Ru Lou

    Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Bryan J Leong

    Department of Plant Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4042-1160
  5. Bethany M Moore

    Plant Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Craig A Schenck

    Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5711-7213
  7. Rachel Combs

    Translational Plant Sciences, Ohio State University, Columbus, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6626-0903
  8. Pengfei Cao

    MSU-DOE Plant Research Lab, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6998-9302
  9. Federica Brandizzi

    MSU-DOE Plant Research Lab, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0580-8888
  10. Shin-Han Shiu

    Plant BIology, Computational Mathematics Science and Engineering, Michigan State University, East Lansing, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Robert L Last

    Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, United States
    For correspondence
    lastr@msu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6974-9587

Funding

National Science Foundation (1546617)

  • Shin-Han Shiu
  • Robert L Last

National Science Foundation (1655386)

  • Shin-Han Shiu

U.S. Department of Energy (BER DE-SC0018409)

  • Shin-Han Shiu

National Science Foundation (1727362)

  • Federica Brandizzi

National Institutes of Health (GM110523)

  • Bryan J Leong
  • Robert L Last

National Science Foundation (1757043)

  • Rachel Combs
  • Robert L Last

National Science Foundation (1811055)

  • Craig A Schenck

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

Reviewing Editor

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

Publication history

  1. Received: March 7, 2020
  2. Accepted: July 1, 2020
  3. Accepted Manuscript published: July 2, 2020 (version 1)
  4. Version of Record published: July 28, 2020 (version 2)

Copyright

© 2020, Fan 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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