title: A Latex Metabolite Benefits Plant Fitness under Root Herbivore Attack.
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.
authors.affiliation: Root Herbivore Interactions Group, Max-Planck Institute for Chemical Ecology, Jena, Germany.|Department of Biochemistry, Max-Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Meret
authors.initials: M
authors.lastname: Huber
authors.affiliation: Fraunhofer Institute for Molecular Biology and Applied Ecology, Münster, Germany.
authors.forename: Janina
authors.initials: J
authors.lastname: Epping
authors.affiliation: Fraunhofer Institute for Molecular Biology and Applied Ecology, Münster, Germany.
authors.forename: Christian
authors.initials: C
authors.lastname: Schulze Gronover
authors.affiliation: Institute of Plant Sciences, University of Bern, Bern, Switzerland.
authors.forename: Julia
authors.initials: J
authors.lastname: Fricke
authors.affiliation: Root Herbivore Interactions Group, Max-Planck Institute for Chemical Ecology, Jena, Germany.|Department of Biochemistry, Max-Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Zohra
authors.initials: Z
authors.lastname: Aziz
authors.affiliation: Root Herbivore Interactions Group, Max-Planck Institute for Chemical Ecology, Jena, Germany.|Department of Biochemistry, Max-Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Théo
authors.initials: T
authors.lastname: Brillatz
authors.affiliation: Root Herbivore Interactions Group, Max-Planck Institute for Chemical Ecology, Jena, Germany.|Department of Biochemistry, Max-Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Swyers
authors.affiliation: Department of Biochemistry, Max-Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Tobias G
authors.initials: TG
authors.lastname: Köllner
authors.affiliation: Department of Entomology, Max-Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Heiko
authors.initials: H
authors.lastname: Vogel
authors.affiliation: Department of Biochemistry, Max-Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Almuth
authors.initials: A
authors.lastname: Hammerbacher
authors.affiliation: Root Herbivore Interactions Group, Max-Planck Institute for Chemical Ecology, Jena, Germany.|Department of Biochemistry, Max-Planck Institute for Chemical Ecology, Jena, Germany.|Institute of Plant Sciences, University of Bern, Bern, Switzerland.
authors.forename: Daniella
authors.initials: D
authors.lastname: Triebwasser-Freese
authors.affiliation: Root Herbivore Interactions Group, Max-Planck Institute for Chemical Ecology, Jena, Germany.|Institute of Plant Sciences, University of Bern, Bern, Switzerland.
authors.forename: Christelle A M
authors.initials: CA
authors.lastname: Robert
authors.affiliation: Netherlands Institute of Ecology, Wageningen, Netherlands.
authors.forename: Koen
authors.initials: K
authors.lastname: Verhoeven
authors.affiliation: Netherlands Institute of Ecology, Wageningen, Netherlands.
authors.forename: Veronica
authors.initials: V
authors.lastname: Preite
authors.affiliation: Department of Biochemistry, Max-Planck Institute for Chemical Ecology, Jena, Germany.
authors.forename: Jonathan
authors.initials: J
authors.lastname: Gershenzon
authors.affiliation: Root Herbivore Interactions Group, Max-Planck Institute for Chemical Ecology, Jena, Germany.|Institute of Plant Sciences, University of Bern, Bern, Switzerland.
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
mesh_terms: D000818:Animals; D018533:Biomass; D001517:Coleoptera; D005960:Glucosides / Q000302:isolation & purification / Q000378:metabolism*; D060434:Herbivory; D007783:Lactones / Q000302:isolation & purification / Q000378:metabolism*; D007814:Larva; D007840:Latex / Q000737:chemistry / Q000378:metabolism*; D018517:Plant Roots / Q000378:metabolism; D034622:RNA Interference; D012098:Reproduction; D012717:Sesquiterpenes / Q000302:isolation & purification / Q000378:metabolism*; D031205:Taraxacum / Q000737:chemistry / Q000235:genetics / Q000378:metabolism*
chemical_list: D005960:Glucosides; D007783:Lactones; D007840:Latex; D012717:Sesquiterpenes; C000608106:taraxinic acid glucopyranosyl ester