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PLANTS INTERACTING WITH OTHER ORGANISMS

Functional Diversification of Acyl-Coenzyme A Oxidases in Jasmonic Acid Biosynthesis and Action^1,[W],[OA]

Department of Energy-Plant Research Laboratory (A.L.S., A.J.K.K., G.A.H.), and Department of Biochemistry and Molecular Biology (A.L.S., G.A.H.), Michigan State University, East Lansing, Michigan 48824

The biosynthesis of jasmonic acid (JA) in plant peroxisomes requires the action of acyl-coenzyme A oxidase (ACX). Among the five expressed members (ACX1–5) of the ACX gene family in Arabidopsis (Arabidopsis thaliana), only ACX1 is known to serve a role in JA production. Here, we used transgenic promoter-reporter lines to show that ACX1 is highly expressed in mature and germinating pollen, stem epidermal cells, and other tissues in which jasmonate-signaled processes occur. Wound-induced JA accumulation was reduced in a mutant that is defective in ACX1 and was abolished in a mutant that is impaired in both ACX1 and its closely related paralog, ACX5. The severe JA deficiency in acx1/5 double mutants was accompanied by decreased resistance to the leaf-eating insect Trichoplusia ni. The double mutant also showed reduced pollen viability and fecundity. Treatment of acx1/5 plants with JA restored both protection against T. ni larvae and normal seed set. Unexpectedly, acx1/5 plants accumulated JA in response to infection by the necrotrophic fungal pathogen Alternaria brassicicola. In contrast to mutants that are impaired in jasmonate perception or early steps of the JA biosynthetic pathway, acx1/5 plants maintained resistance to A. brassicicola infection. These results indicate that ACX1/5-mediated JA synthesis is essential for resistance to chewing insects and male reproductive function and further suggest that other ACX isozymes contribute to JA production in response to A. brassicicola challenge. Thus, different types of biotic stress may induce JA synthesis via distinct enzymatic routes.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Gregg A. Howe (howeg{at}msu.edu).

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www.plantphysiol.org/cgi/doi/10.1104/pp.106.092916

^* Corresponding author; e-mail howeg{at}msu.edu; fax 517–353–9168.

Received November 10, 2006; accepted November 28, 2006; published December 15, 2006.

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