title: A fungal endophyte helps plants to tolerate root herbivory through changes in gibberellin and jasmonate signaling.
abstract: Plant-microbe mutualisms can improve plant defense, but the impact of root endophytes on below-ground herbivore interactions remains unknown. We investigated the effects of the root endophyte Piriformospora indica on interactions between rice (Oryza sativa) plants and its root herbivore rice water weevil (RWW; Lissorhoptrus oryzophilus), and how plant jasmonic acid (JA) and GA regulate this tripartite interaction. Glasshouse experiments with wild-type rice and coi1-18 and Eui1-OX mutants combined with nutrient, jasmonate and gene expression analyses were used to test: whether RWW adult herbivory above ground influences subsequent damage caused by larval herbivory below ground; whether P. indica protects plants against RWW; and whether GA and JA signaling mediate these interactions. The endophyte induced plant tolerance to root herbivory. RWW adults and larvae acted synergistically via JA signaling to reduce root growth, while endophyte-elicited GA biosynthesis suppressed the herbivore-induced JA in roots and recovered plant growth. Our study shows for the first time the impact of a root endophyte on plant defense against below-ground herbivores, adds to growing evidence that induced tolerance may be an important root defense, and implicates GA as a signal component of inducible plant tolerance against biotic stress.
authors.affiliation: Functional Biodiversity, Dahlem Center of Plant Sciences, Institute of Biology, Freie Universität Berlin, Königin-Luise-Straße 1-3, 14195, Berlin, Germany.|Department of Plant Propagation, Leibniz-Institute of Vegetable and Ornamental Crops, Kühnhäuser Straße 101, 99090, Erfurt-Kühnhausen, Germany.|Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, PO Box 800.56, 3508 TB, Utrecht, the Netherlands.
authors.forename: Marco
authors.identifier: 0000-0003-1511-8362
authors.initials: M
authors.lastname: Cosme
authors.affiliation: Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745, Jena, Germany.|Institute of Insect Science, Zijingang Campus, Zhejiang University, Yuhangtang Road 866, Hangzhou, 310058, China.
authors.forename: Jing
authors.initials: J
authors.lastname: Lu
authors.affiliation: Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745, Jena, Germany.|Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013, Bern, Switzerland.
authors.forename: Matthias
authors.initials: M
authors.lastname: Erb
authors.affiliation: Department of Entomology, Louisiana State University Agricultural Center, 404 Life Sciences Building, Baton Rouge, LA, 70803, USA.
authors.forename: Michael Joseph
authors.initials: MJ
authors.lastname: Stout
authors.affiliation: Department of Plant Propagation, Leibniz-Institute of Vegetable and Ornamental Crops, Kühnhäuser Straße 101, 99090, Erfurt-Kühnhausen, Germany.|Department of Plant Physiology, Humboldt Universität zu Berlin, Philippstrasse 13, 10115, Berlin, Germany.
authors.forename: Philipp
authors.initials: P
authors.lastname: Franken
authors.affiliation: Functional Biodiversity, Dahlem Center of Plant Sciences, Institute of Biology, Freie Universität Berlin, Königin-Luise-Straße 1-3, 14195, Berlin, Germany.
authors.forename: Susanne
authors.initials: S
authors.lastname: Wurst
mesh_terms: D000222:Adaptation, Physiological; D000818:Animals; D001487:Basidiomycota / Q000502:physiology*; D003517:Cyclopentanes / Q000378:metabolism*; D060467:Disease Resistance; D060026:Endophytes / Q000502:physiology*; D005875:Gibberellins / Q000378:metabolism*; D060434:Herbivory / Q000502:physiology*; D007814:Larva / Q000502:physiology; D012275:Oryza / Q000254:growth & development / Q000378:metabolism / Q000382:microbiology* / Q000469:parasitology*; D054883:Oxylipins / Q000378:metabolism*; D063245:Plant Development; D010935:Plant Diseases / Q000382:microbiology; D018517:Plant Roots / Q000469:parasitology*; D015398:Signal Transduction; D048889:Weevils / Q000502:physiology
chemical_list: D003517:Cyclopentanes; D005875:Gibberellins; D054883:Oxylipins; C011006:jasmonic acid
keywords: GA signaling; Lissorhoptrus oryzophilus (rice water weevil); Oryza sativa (rice); Piriformospora indica (endophyte); induced plant tolerance; jasmonate signaling; phytohormone crosstalk; root herbivory