title: COI1-Regulated Hydroxylation of Jasmonoyl-L-isoleucine Impairs Nicotiana attenuata's Resistance to the Generalist Herbivore Spodoptera litura.
abstract: The phytohormone jasmonoyl-L-isoleucine (JA-Ile) is well-known as the key signaling molecule that elicits plant defense responses after insect herbivory. Oxidation, which is catalyzed by the cytochrome P450s of the CYP94 family, is thought to be one of the main catabolic pathways of JA-Ile. In this study, we identified four CYP94B3 homologues in the wild tobacco plant Nicotiana attenuata. Individually silencing the four homologues revealed that NaCYP94B3 like-1 and NaCYP94B3 like-2, but not NaCYP94B3 like-3 and NaCYP94B3 like-4, are involved in the C-12-hydroxylation of JA-Ile. Simultaneously silencing three of the NaCYP94B3 like genes, NaCYP94B3 like-1, -2, and -4, in the VIGS-NaCYP94B3s plants doubled herbivory-induced JA-Ile levels and greatly enhanced plant resistance to the generalist insect herbivore, Spodoptera litura. The poor larval performance was strongly correlated with the high concentrations of several JA-Ile-dependent direct defense metabolites in VIGS-NaCYP94B3s plants. Furthermore, we show that the abundance of 12-hydroxy-JA-Ile was dependent on JA-Ile levels as well as COI1, the receptor of JA-Ile. COI1 appeared to transcriptionally control NaCYP94B3 like-1 and -2 and thus regulates the catabolism of its own ligand molecule, JA-Ile. These results highlight the important role of JA-Ile degradation in jasmonate homeostasis and provide new insight into the feedback regulation of JA-Ile catabolism. Given that silencing these CYP94 genes did not detectably alter plant growth and highly increased plant defense levels, we propose that CYP94B3 genes can be potential targets for genetic improvement of herbivore-resistant crops.
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.|University of Chinese Academy of Sciences , Beijing 100049, China.
authors.forename: Ji
authors.initials: J
authors.lastname: Luo
authors.affiliation: State Key Laboratory of Phytochemistry and Plant Resources in West China, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.
authors.forename: Kun
authors.initials: K
authors.lastname: Wei
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.|University of Chinese Academy of Sciences , Beijing 100049, China.
authors.forename: Shuanghua
authors.initials: S
authors.lastname: Wang
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.
authors.forename: Weiye
authors.initials: W
authors.lastname: Zhao
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.|University of Chinese Academy of Sciences , Beijing 100049, China.
authors.forename: Canrong
authors.initials: C
authors.lastname: Ma
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.
authors.forename: Christian
authors.initials: C
authors.lastname: Hettenhausen
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.
authors.forename: Jinsong
authors.initials: J
authors.lastname: Wu
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.
authors.forename: Guoyan
authors.initials: G
authors.lastname: Cao
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.
authors.forename: Guiling
authors.initials: G
authors.lastname: Sun
authors.affiliation: Department of Molecular Ecology, Max Planck Institute for Chemical Ecology , Jena 07745, Germany.
authors.forename: Ian T
authors.initials: IT
authors.lastname: Baldwin
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.
authors.forename: Jianqiang
authors.initials: J
authors.lastname: Wu
authors.affiliation: Department of Economic Plants and Biotechnology, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming 650201, China.
authors.forename: Lei
authors.initials: L
authors.lastname: Wang
mesh_terms: D000818:Animals; D003517:Cyclopentanes / Q000378:metabolism*; D003577:Cytochrome P-450 Enzyme System / Q000235:genetics / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D060434:Herbivory; D006900:Hydroxylation; D007532:Isoleucine / Q000031:analogs & derivatives* / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000276:immunology*; D030821:Plants, Genetically Modified / Q000235:genetics / Q000378:metabolism / Q000469:parasitology; D018411:Spodoptera / Q000502:physiology*; D014026:Nicotiana / Q000235:genetics / Q000378:metabolism* / Q000469:parasitology*
chemical_list: D003517:Cyclopentanes; D010940:Plant Proteins; C532883:jasmonoyl-isoleucine; D007532:Isoleucine; D003577:Cytochrome P-450 Enzyme System
keywords: JA-Ile; Nicotiana attenuata; Spodoptera litura; catabolism; cytochrome P450; defense; plant-insect interaction