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Cited by 97Insect-Plant Interactions and ControlPlant biochemistry and biosynthesisInsect Pest Control Strategies

A Latex Metabolite Benefits Plant Fitness under Root Herbivore Attack

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Huber, Meret, Epping, Janina, Schulze Gronover, Christian, Fricke, Julia, Aziz, Zohra, Brillatz, Théo, Swyers, Michael, Köllner, Tobias G. +8 more·2016·PLOS Biology
DOI 10.1371/journal.pbio.1002332PMC PMC4701418
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Abstract

Plants produce large amounts of secondary metabolites in their shoots and roots and store them in specialized secretory structures. Although secondary metabolites and their secretory structures are commonly assumed to have a defensive function, evidence that they benefit plant fitness under herbivore attack is scarce, especially below ground. Here, we tested whether latex secondary metabolites produced by the common dandelion (Taraxacum officinale agg.) decrease the performance of its major native insect root herbivore, the larvae of the common cockchafer (Melolontha melolontha), and benefit plant vegetative and reproductive fitness under M. melolontha attack. Across 17 T. officinale genotypes screened by gas and liquid chromatography, latex concentrations of the sesquiterpene lactone taraxinic acid β-D-glucopyranosyl ester (TA-G) were negatively associated with M. melolontha larval growth. Adding purified TA-G to artificial diet at ecologically relevant concentrations reduced larval feeding. Silencing the germacrene A synthase ToGAS1, an enzyme that was identified to catalyze the first committed step of TA-G biosynthesis, resulted in a 90% reduction of TA-G levels and a pronounced increase in M. melolontha feeding. Transgenic, TA-G-deficient lines were preferred by M. melolontha and suffered three times more root biomass reduction than control lines. In a common garden experiment involving over 2,000 T. officinale individuals belonging to 17 different genotypes, high TA-G concentrations were associated with the maintenance of high vegetative and reproductive fitness under M. melolontha attack. Taken together, our study demonstrates that a latex secondary metabolite benefits plants under herbivore attack, a result that provides a mechanistic framework for root herbivore driven natural selection and evolution of plant defenses below ground.

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  • Alterations in primary metabolites are observed in various plants with altered secondary metabolism.

    “Furthermore, alterations in primary metabolites are observed in various plants with altered secondary metabolism (Mayer et al., 2001;Narayanan et al., 2011;Huber et al., 2016;Machado et al., 2017;Zhang et al., 2020), and the accumulation of specific secondary metabolites has been associated with storage and growth in microevolutionary studies (Heath et al., 2014).”

    From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Huber et al., 2016

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Authors
Huber, M., Epping, J., Schulze Gronover, C., Fricke, J., Aziz, Z., Brillatz, T., Swyers, M., Köllner, T. G., Vogel, H., Hammerbacher, A., Triebwasser-Freese, D., Robert, C. A. M., Verhoeven, K., Preite, V., Gershenzon, J., & Erb, M.
Affiliations
  • Max Planck Institute for Chemical Ecology (DE)
  • Fraunhofer Institute for Molecular Biology and Applied Ecology (DE)
  • University of Bern (CH)
  • Netherlands Institute of Ecology (NL)
Corresponding author
  • Huber, Meret
  • Epping, Janina
  • Fricke, Julia
  • Aziz, Zohra
  • Brillatz, Théo
  • Swyers, Michael
  • Köllner, Tobias G.
  • Vogel, Heiko
  • Hammerbacher, Almuth
  • Triebwasser-Freese, Daniella
  • Robert, Christelle A. M.
  • Verhoeven, Koen
  • Preite, Veronica
  • Gershenzon, Jonathan
  • Erb, Matthias
ORCID
Venue
PLOS Biology
Publisher
Public Library of Science (PLoS)
Published
2016-01-05
Volume
14
Issue
1
Pages
e1002332
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
DOI
10.1371/journal.pbio.1002332
PMC
PMC4701418
OpenAlex
W2225656222
Cited by
97
References
2
Citations by year
2026: 5 · 2025: 4 · 2024: 8 · 2023: 8 · 2022: 8 · 2021: 12 · 2020: 15 · 2019: 13 · 2018: 11 · 2017: 6 · 2016: 5
FWCI
12.66
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, cc-by)
  • Socio-Environmental Systems Modeling (acceptedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion, cc-by)
  • MPG.PuRe (Max Planck Society) (submittedVersion, cc-by)
  • Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by)
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  • Figshare (submittedVersion, cc-by)
  • Publikationsdatenbank der Fraunhofer-Gesellschaft (Fraunhofer-Gesellschaft) (submittedVersion, other-oa)
  • Fraunhofer-Publica (Fraunhofer-Gesellschaft) (submittedVersion)
  • Open Access CRIS of the University of Bern
Funders
  • National Science Foundation
  • European Commission (FP7-PEOPLE-2013-CIG, 629134, FP7-PEOPLE-2013)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (153517, 140196)
  • Max-Planck-Gesellschaft
  • FP7 People: Marie-Curie Actions (2013-CIG, 629134, FP7-PEOPLE-2013, FP7-PEOPLE-2013-CIG)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Insect Pest Control Strategies
Keywords
sesquiterpene lactones, root herbivory, Melolontha melolontha, Taraxacum officinale, germacrene A synthase, plant defense evolution, plant fitness, root biomass
MeSH terms
Animals, Coleoptera, Glucosides, Lactones, Larva, Latex, Reproduction, Sesquiterpenes, Plant Roots, Biomass, Taraxacum, RNA Interference, Herbivory

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