First published online December 15, 2006; 10.1104/pp.106.092916
Plant Physiology 143:812-824 (2007)
© 2007 American Society of Plant Biologists
OPEN ACCESS ARTICLE
PLANTS INTERACTING WITH OTHER ORGANISMS
Functional Diversification of Acyl-Coenzyme A Oxidases in Jasmonic Acid Biosynthesis and Action1,[W],[OA]
Anthony L. Schilmiller,
Abraham J.K. Koo and
Gregg A. Howe*
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.
1 This work was supported by Michigan State University (Graduate School Dissertation Completion Fellowship to A.L.S.), by the National Institutes of Health (grant no. GM57795), and by the U.S. Department of Energy (grant no. DE–FG02–91ER20021 to G.A.H.).
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).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription.
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.
This article has been cited by other articles:
|
|
|
|
 
C. Ren, C. Han, W. Peng, Y. Huang, Z. Peng, X. Xiong, Q. Zhu, B. Gao, and D. Xie
A Leaky Mutation in DWARF4 Reveals an Antagonistic Role of Brassinosteroid in the Inhibition of Root Growth by Jasmonate in Arabidopsis
Plant Physiology,
November 1, 2009;
151(3):
1412 - 1420.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. S. Chung and G. A. Howe
A Critical Role for the TIFY Motif in Repression of Jasmonate Signaling by a Stabilized Splice Variant of the JASMONATE ZIM-Domain Protein JAZ10 in Arabidopsis
PLANT CELL,
January 1, 2009;
21(1):
131 - 145.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Eubel, E. H. Meyer, N. L. Taylor, J. D. Bussell, N. O'Toole, J. L. Heazlewood, I. Castleden, I. D. Small, S. M. Smith, and A. H. Millar
Novel Proteins, Putative Membrane Transporters, and an Integrated Metabolic Network Are Revealed by Quantitative Proteomic Analysis of Arabidopsis Cell Culture Peroxisomes
Plant Physiology,
December 1, 2008;
148(4):
1809 - 1829.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. K. Zolman, N. Martinez, A. Millius, A. R. Adham, and B. Bartel
Identification and Characterization of Arabidopsis Indole-3-Butyric Acid Response Mutants Defective in Novel Peroxisomal Enzymes
Genetics,
September 1, 2008;
180(1):
237 - 251.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Herde, K. Gartner, T. G. Kollner, B. Fode, W. Boland, J. Gershenzon, C. Gatz, and D. Tholl
Identification and Regulation of TPS04/GES, an Arabidopsis Geranyllinalool Synthase Catalyzing the First Step in the Formation of the Insect-Induced Volatile C16-Homoterpene TMTT
PLANT CELL,
April 1, 2008;
20(4):
1152 - 1168.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Wang, S. Allmann, J. Wu, and I. T. Baldwin
Comparisons of LIPOXYGENASE3- and JASMONATE-RESISTANT4/6-Silenced Plants Reveal That Jasmonic Acid and Jasmonic Acid-Amino Acid Conjugates Play Different Roles in Herbivore Resistance of Nicotiana attenuata
Plant Physiology,
March 1, 2008;
146(3):
904 - 915.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. S. Chung, A. J.K. Koo, X. Gao, S. Jayanty, B. Thines, A. D. Jones, and G. A. Howe
Regulation and Function of Arabidopsis JASMONATE ZIM-Domain Genes in Response to Wounding and Herbivory
Plant Physiology,
March 1, 2008;
146(3):
952 - 964.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Kienow, K. Schneider, M. Bartsch, H.-P. Stuible, H. Weng, O. Miersch, C. Wasternack, and E. Kombrink
Jasmonates meet fatty acids: functional analysis of a new acyl-coenzyme A synthetase family from Arabidopsis thaliana
J. Exp. Bot.,
February 10, 2008;
(2008)
erm325v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Wasternack
Jasmonates: An Update on Biosynthesis, Signal Transduction and Action in Plant Stress Response, Growth and Development
Ann. Bot.,
October 1, 2007;
100(4):
681 - 697.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Footitt, J. E. Cornah, I. Pracharoenwattana, J. H. Bryce, and S. M. Smith
The Arabidopsis 3-ketoacyl-CoA thiolase-2 (kat2-1) mutant exhibits increased flowering but reduced reproductive success
J. Exp. Bot.,
August 28, 2007;
(2007)
erm146v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Footitt, D. Dietrich, A. Fait, A. R. Fernie, M. J. Holdsworth, A. Baker, and F. L. Theodoulou
The COMATOSE ATP-Binding Cassette Transporter Is Required for Full Fertility in Arabidopsis
Plant Physiology,
July 1, 2007;
144(3):
1467 - 1480.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Chen, E. Gonzales-Vigil, C. G. Wilkerson, and G. A. Howe
Stability of Plant Defense Proteins in the Gut of Insect Herbivores
Plant Physiology,
April 1, 2007;
143(4):
1954 - 1967.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
