Evolutionary routes to biochemical innovation revealed by integrative analysis of a plant-defense related specialized metabolic pathway

  1. Gaurav D Moghe
  2. Bryan J Leong
  3. Steven Hurney
  4. A Daniel Jones
  5. Robert L Last  Is a corresponding author
  1. Michigan State University, United States

Abstract

The diversity of life on Earth is a result of continual innovations in molecular networks influencing morphology and physiology. Plant specialized metabolism produces hundreds of thousands of compounds, offering striking examples of these innovations. To understand how this novelty is generated, we investigated the evolution of the Solanaceae family-specific, trichome-localized acylsugar biosynthetic pathway using a combination of mass spectrometry, RNA-seq, enzyme assays, RNAi and phylogenomics in different non-model species. Our results reveal hundreds of acylsugars produced across the Solanaceae family and even within a single plant, built on simple sugar cores. The relatively short biosynthetic pathway experienced repeated cycles of innovation over the last 100 million years that include gene duplication and divergence, gene loss, evolution of substrate preference and promiscuity. This study provides mechanistic insights into the emergence of plant chemical novelty, and offers a template for investigating the ~300,000 non-model plant species that remain underexplored.

Data availability

The following data sets were generated
    1. Moghe G
    (2015) RNA seq reads from Solanaceae Spp.
    Publicly available at the NCBI BioProject (accession no: PRJNA263038).

Article and author information

Author details

  1. Gaurav D Moghe

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

    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:" 0000-0003-4042-1160
  3. Steven Hurney

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

    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:" 0000-0002-7408-6690
  5. 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 (IOS-1025636)

  • A Daniel Jones
  • Robert L Last

National Institutes of Health (T32-GM110523)

  • Bryan J Leong
  • Robert L Last

U.S. Department of Agriculture (MICL-02143)

  • A Daniel Jones

National Science Foundation (IOS-PGRP-1546617)

  • A Daniel Jones
  • Robert L Last

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

Version history

  1. Received: May 8, 2017
  2. Accepted: July 25, 2017
  3. Accepted Manuscript published: August 30, 2017 (version 1)
  4. Version of Record published: September 12, 2017 (version 2)

Copyright

© 2017, Moghe 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. Gaurav D Moghe
  2. Bryan J Leong
  3. Steven Hurney
  4. A Daniel Jones
  5. Robert L Last
(2017)
Evolutionary routes to biochemical innovation revealed by integrative analysis of a plant-defense related specialized metabolic pathway
eLife 6:e28468.
https://doi.org/10.7554/eLife.28468

Share this article

https://doi.org/10.7554/eLife.28468

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