title: Hormone crosstalk in wound stress response: wound-inducible amidohydrolases can simultaneously regulate jasmonate and auxin homeostasis in Arabidopsis thaliana.
abstract: Jasmonate (JA) and auxin are essential hormones in plant development and stress responses. While the two govern distinct physiological processes, their signaling pathways interact at various levels. Recently, members of the Arabidopsis indole-3-acetic acid (IAA) amidohydrolase (IAH) family were reported to metabolize jasmonoyl-isoleucine (JA-Ile), a bioactive form of JA. Here, we characterized three IAH members, ILR1, ILL6, and IAR3, for their function in JA and IAA metabolism and signaling. Expression of all three genes in leaves was up-regulated by wounding or JA, but not by IAA. Purified recombinant proteins showed overlapping but distinct substrate specificities for diverse amino acid conjugates of JA and IAA. Perturbed patterns of the endogenous JA profile in plants overexpressing or knocked-out for the three genes were consistent with ILL6 and IAR3, but not ILR1, being the JA amidohydrolases. Increased turnover of JA-Ile in the ILL6- and IAR3-overexpressing plants created symptoms of JA deficiency whereas increased free IAA by overexpression of ILR1 and IAR3 made plants hypersensitive to exogenous IAA conjugates. Surprisingly, ILL6 overexpression rendered plants highly resistant to exogenous IAA conjugates, indicating its interference with IAA conjugate hydrolysis. Fluorescent protein-tagged IAR3 and ILL6 co-localized with the endoplasmic reticulum-localized JA-Ile 12-hydroxylase, CYP94B3. Together, these results demonstrate that in wounded leaves JA-inducible amidohydrolases contribute to regulate active IAA and JA-Ile levels, promoting auxin signaling while attenuating JA signaling. This mechanism represents an example of a metabolic-level crosstalk between the auxin and JA signaling pathways.
authors.affiliation: Division of Biochemistry, University of Missouri, Columbia, MO 65211, USA Interdisciplinary Plant Group, University of Missouri, Columbia, MO 65211, USA.
authors.forename: Tong
authors.initials: T
authors.lastname: Zhang
authors.affiliation: Interdisciplinary Plant Group, University of Missouri, Columbia, MO 65211, USA Division of Plant Sciences, University of Missouri, Columbia, MO 65211, USA.
authors.forename: Arati N
authors.initials: AN
authors.lastname: Poudel
authors.affiliation: Institute of Biological Chemistry, Washington State University, Pullman, WA 99163, USA.
authors.forename: Jeremy B
authors.initials: JB
authors.lastname: Jewell
authors.affiliation: Laboratory of Bioorganic Chemistry, Division of Applied Bioscience, Research Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan.
authors.forename: Naoki
authors.initials: N
authors.lastname: Kitaoka
authors.affiliation: Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE 68521, USA.
authors.forename: Paul
authors.initials: P
authors.lastname: Staswick
authors.affiliation: Laboratory of Bioorganic Chemistry, Division of Applied Bioscience, Research Faculty of Agriculture, Hokkaido University, Sapporo 060-8589, Japan.
authors.forename: Hideyuki
authors.initials: H
authors.lastname: Matsuura
authors.affiliation: Division of Biochemistry, University of Missouri, Columbia, MO 65211, USA Interdisciplinary Plant Group, University of Missouri, Columbia, MO 65211, USA kooaj@missouri.edu.
authors.forename: Abraham J
authors.initials: AJ
authors.lastname: Koo
mesh_terms: D000581:Amidohydrolases / Q000378:metabolism*; D017360:Arabidopsis / Q000201:enzymology / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000378:metabolism*; D003517:Cyclopentanes / Q000378:metabolism*; D004721:Endoplasmic Reticulum / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D007210:Indoleacetic Acids / Q000378:metabolism*; D054883:Oxylipins / Q000378:metabolism*; D010935:Plant Diseases; D010937:Plant Growth Regulators / Q000378:metabolism*; D030821:Plants, Genetically Modified; D015398:Signal Transduction; D013379:Substrate Specificity
chemical_list: D029681:Arabidopsis Proteins; D003517:Cyclopentanes; D007210:Indoleacetic Acids; D054883:Oxylipins; D010937:Plant Growth Regulators; C011006:jasmonic acid; D000581:Amidohydrolases; C000612601:ILL6 protein, Arabidopsis; C118815:IAR3 protein, Arabidopsis; C094266:ILR1 protein, Arabidopsis
keywords: Auxin; crosstalk; hormone metabolism; jasmonate; signaling; wound stress.