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Research ArticleLARGE-SCALE BIOLOGY ARTICLE
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A Global Coexpression Network Approach for Connecting Genes to Specialized Metabolic Pathways in Plants

Jennifer H. Wisecaver, Alexander T. Borowsky, Vered Tzin, Georg Jander, Daniel J. Kliebenstein, Antonis Rokas
Jennifer H. Wisecaver
Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee 37235
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Alexander T. Borowsky
Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee 37235
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Vered Tzin
French Associates Institute for Agriculture and Biotechnology of Drylands, Jacob Blaustein Institute for Desert Research, Ben Gurion University, Sede-Boqer Campus 84990, Israel
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Georg Jander
Boyce Thompson Institute for Plant Research, Tower Road, Ithaca, New York 14853
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Daniel J. Kliebenstein
Department of Plant Sciences, University of California-Davis, Davis, California 95616
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Antonis Rokas
Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee 37235
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  • For correspondence: antonis.rokas@vanderbilt.edu

Published May 2017. DOI: https://doi.org/10.1105/tpc.17.00009

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  • © 2017 American Society of Plant Biologists. All rights reserved.

Abstract

Plants produce diverse specialized metabolites (SMs), but the genes responsible for their production and regulation remain largely unknown, hindering efforts to tap plant pharmacopeia. Given that genes comprising SM pathways exhibit environmentally dependent coregulation, we hypothesized that genes within a SM pathway would form tight associations (modules) with each other in coexpression networks, facilitating their identification. To evaluate this hypothesis, we used 10 global coexpression data sets, each a meta-analysis of hundreds to thousands of experiments, across eight plant species to identify hundreds of coexpressed gene modules per data set. In support of our hypothesis, 15.3 to 52.6% of modules contained two or more known SM biosynthetic genes, and module genes were enriched in SM functions. Moreover, modules recovered many experimentally validated SM pathways, including all six known to form biosynthetic gene clusters (BGCs). In contrast, bioinformatically predicted BGCs (i.e., those lacking an associated metabolite) were no more coexpressed than the null distribution for neighboring genes. These results suggest that most predicted plant BGCs are not genuine SM pathways and argue that BGCs are not a hallmark of plant specialized metabolism. We submit that global gene coexpression is a rich, largely untapped resource for discovering the genetic basis and architecture of plant natural products.

  • Glossary

    SM
    specialized metabolite
    BGC
    biosynthetic gene cluster
    MR
    mutual rank
    PCC
    Pearson’s correlation coefficient
    metGSL
    methionine-derived aliphatic glucosinolate
    DIMBOA
    benzoxazinoid 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one
    DIBOA
    2,4-dihydroxy-1, 4-benzoxazin-3-one
    EC
    Enzyme Commission
    • Received January 6, 2017.
    • Revised March 12, 2017.
    • Accepted April 9, 2017.
    • Published April 13, 2017.
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    A Global Coexpression Network Approach for Connecting Genes to Specialized Metabolic Pathways in Plants
    Jennifer H. Wisecaver, Alexander T. Borowsky, Vered Tzin, Georg Jander, Daniel J. Kliebenstein, Antonis Rokas
    The Plant Cell May 2017, 29 (5) 944-959; DOI: 10.1105/tpc.17.00009

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    A Global Coexpression Network Approach for Connecting Genes to Specialized Metabolic Pathways in Plants
    Jennifer H. Wisecaver, Alexander T. Borowsky, Vered Tzin, Georg Jander, Daniel J. Kliebenstein, Antonis Rokas
    The Plant Cell May 2017, 29 (5) 944-959; DOI: 10.1105/tpc.17.00009
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    The Plant Cell: 29 (5)
    The Plant Cell
    Vol. 29, Issue 5
    May 2017
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