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12-Hydroxy-Jasmonoyl-l-Isoleucine Is an Active Jasmonate That Signals through CORONATINE INSENSITIVE 1 and Contributes to the Wound Response in Arabidopsis.
Plant Cell Physiol. 2019 Oct 01; 60(10):2152-2166.PC

Abstract

12-hydroxy-jasmonoyl-isoleucine (12OH-JA-Ile) is a metabolite in the catabolic pathway of the plant hormone jasmonate, and is synthesized by the cytochrome P450 subclade 94 enzymes. Contrary to the well-established function of jasmonoyl-isoleucine (JA-Ile) as the endogenous bioactive form of jasmonate, the function of 12OH-JA-Ile is unclear. Here, the potential role of 12OH-JA-Ile in jasmonate signaling and wound response was investigated. Exogenous application of 12OH-JA-Ile mimicked several JA-Ile effects including marker gene expression, anthocyanin accumulation and trichome induction in Arabidopsis thaliana. Genome-wide transcriptomics and untargeted metabolite analyses showed large overlaps between those affected by 12OH-JA-Ile and JA-Ile. 12OH-JA-Ile signaling was blocked by mutation in CORONATINE INSENSITIVE 1. Increased anthocyanin accumulation by 12OH-JA-Ile was additionally observed in tomato and sorghum, and was disrupted by the COI1 defect in tomato jai1 mutant. In silico ligand docking predicted that 12OH-JA-Ile can maintain many of the key interactions with COI1-JAZ1 residues identified earlier by crystal structure studies using JA-Ile as ligand. Genetic alternation of jasmonate metabolic pathways in Arabidopsis to deplete both JA-Ile and 12OH-JA-Ile displayed enhanced jasmonate deficient wound phenotypes and was more susceptible to insect herbivory than that depleted in only JA-Ile. Conversely, mutants overaccumulating 12OH-JA-Ile showed intensified wound responses compared with wild type with similar JA-Ile content. These data are indicative of 12OH-JA-Ile functioning as an active jasmonate signal and contributing to wound and defense response in higher plants.

Authors+Show Affiliations

Department of Biochemistry, University of Missouri, Columbia, MO, USA. Interdisciplinary Plant Group, University of Missouri, Columbia, MO, USA. Christopher S. Bond Life Science Center, University of Missouri, Columbia, MO, USA. Department of Plant Sciences, University of Missouri, Columbia, MO, USA.Department of Biochemistry, University of Missouri, Columbia, MO, USA. Interdisciplinary Plant Group, University of Missouri, Columbia, MO, USA.Department of Biochemistry, University of Missouri, Columbia, MO, USA. Interdisciplinary Plant Group, University of Missouri, Columbia, MO, USA.Informatics Institute, University of Missouri, Columbia, MO, USA.Christopher S. Bond Life Science Center, University of Missouri, Columbia, MO, USA. Department of Electrical Engineering and Computer Science, University of Missouri, Columbia, MO, USA.Christopher S. Bond Life Science Center, University of Missouri, Columbia, MO, USA. Informatics Institute, University of Missouri, Columbia, MO, USA. Health Management and Informatics, University of Missouri, Columbia, MO, USA.Department of Biochemistry, University of Missouri, Columbia, MO, USA. Interdisciplinary Plant Group, University of Missouri, Columbia, MO, USA. Christopher S. Bond Life Science Center, University of Missouri, Columbia, MO, USA. MU Metabolomics Core, University of Missouri, Columbia, MO, MO, USA.Department of Biochemistry, University of Missouri, Columbia, MO, USA. Interdisciplinary Plant Group, University of Missouri, Columbia, MO, USA. Christopher S. Bond Life Science Center, University of Missouri, Columbia, MO, USA. MU Metabolomics Core, University of Missouri, Columbia, MO, MO, USA.Christopher S. Bond Life Science Center, University of Missouri, Columbia, MO, USA. Department of Electrical Engineering and Computer Science, University of Missouri, Columbia, MO, USA.Division of Fundamental Agriscience Research, Research Faculty of Agriculture, Hokkaido University, Sapporo, Japan.Department of Biochemistry, University of Missouri, Columbia, MO, USA. Interdisciplinary Plant Group, University of Missouri, Columbia, MO, USA.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31150089

Citation

Poudel, Arati N., et al. "12-Hydroxy-Jasmonoyl-l-Isoleucine Is an Active Jasmonate That Signals Through CORONATINE INSENSITIVE 1 and Contributes to the Wound Response in Arabidopsis." Plant & Cell Physiology, vol. 60, no. 10, 2019, pp. 2152-2166.
Poudel AN, Holtsclaw RE, Kimberlin A, et al. 12-Hydroxy-Jasmonoyl-l-Isoleucine Is an Active Jasmonate That Signals through CORONATINE INSENSITIVE 1 and Contributes to the Wound Response in Arabidopsis. Plant Cell Physiol. 2019;60(10):2152-2166.
Poudel, A. N., Holtsclaw, R. E., Kimberlin, A., Sen, S., Zeng, S., Joshi, T., Lei, Z., Sumner, L. W., Singh, K., Matsuura, H., & Koo, A. J. (2019). 12-Hydroxy-Jasmonoyl-l-Isoleucine Is an Active Jasmonate That Signals through CORONATINE INSENSITIVE 1 and Contributes to the Wound Response in Arabidopsis. Plant & Cell Physiology, 60(10), 2152-2166. https://doi.org/10.1093/pcp/pcz109
Poudel AN, et al. 12-Hydroxy-Jasmonoyl-l-Isoleucine Is an Active Jasmonate That Signals Through CORONATINE INSENSITIVE 1 and Contributes to the Wound Response in Arabidopsis. Plant Cell Physiol. 2019 Oct 1;60(10):2152-2166. PubMed PMID: 31150089.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - 12-Hydroxy-Jasmonoyl-l-Isoleucine Is an Active Jasmonate That Signals through CORONATINE INSENSITIVE 1 and Contributes to the Wound Response in Arabidopsis. AU - Poudel,Arati N, AU - Holtsclaw,Rebekah E, AU - Kimberlin,Athen, AU - Sen,Sidharth, AU - Zeng,Shuai, AU - Joshi,Trupti, AU - Lei,Zhentian, AU - Sumner,Lloyd W, AU - Singh,Kamlendra, AU - Matsuura,Hideyuki, AU - Koo,Abraham J, PY - 2019/03/04/received PY - 2019/05/21/accepted PY - 2019/6/1/pubmed PY - 2020/2/6/medline PY - 2019/6/1/entrez KW - 12OH-JA-Ile KW - COI1 KW - JA-Ile KW - Jasmonate KW - Plant hormone KW - Wound response SP - 2152 EP - 2166 JF - Plant & cell physiology JO - Plant Cell Physiol VL - 60 IS - 10 N2 - 12-hydroxy-jasmonoyl-isoleucine (12OH-JA-Ile) is a metabolite in the catabolic pathway of the plant hormone jasmonate, and is synthesized by the cytochrome P450 subclade 94 enzymes. Contrary to the well-established function of jasmonoyl-isoleucine (JA-Ile) as the endogenous bioactive form of jasmonate, the function of 12OH-JA-Ile is unclear. Here, the potential role of 12OH-JA-Ile in jasmonate signaling and wound response was investigated. Exogenous application of 12OH-JA-Ile mimicked several JA-Ile effects including marker gene expression, anthocyanin accumulation and trichome induction in Arabidopsis thaliana. Genome-wide transcriptomics and untargeted metabolite analyses showed large overlaps between those affected by 12OH-JA-Ile and JA-Ile. 12OH-JA-Ile signaling was blocked by mutation in CORONATINE INSENSITIVE 1. Increased anthocyanin accumulation by 12OH-JA-Ile was additionally observed in tomato and sorghum, and was disrupted by the COI1 defect in tomato jai1 mutant. In silico ligand docking predicted that 12OH-JA-Ile can maintain many of the key interactions with COI1-JAZ1 residues identified earlier by crystal structure studies using JA-Ile as ligand. Genetic alternation of jasmonate metabolic pathways in Arabidopsis to deplete both JA-Ile and 12OH-JA-Ile displayed enhanced jasmonate deficient wound phenotypes and was more susceptible to insect herbivory than that depleted in only JA-Ile. Conversely, mutants overaccumulating 12OH-JA-Ile showed intensified wound responses compared with wild type with similar JA-Ile content. These data are indicative of 12OH-JA-Ile functioning as an active jasmonate signal and contributing to wound and defense response in higher plants. SN - 1471-9053 UR - https://www.unboundmedicine.com/medline/citation/31150089/12_Hydroxy_Jasmonoyl_l_Isoleucine_Is_an_Active_Jasmonate_That_Signals_through_CORONATINE_INSENSITIVE_1_and_Contributes_to_the_Wound_Response_in_Arabidopsis_ L2 - https://academic.oup.com/pcp/article-lookup/doi/10.1093/pcp/pcz109 DB - PRIME DP - Unbound Medicine ER -