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J. Biol. Chem., Vol. 280, Issue 14, 13962-13972, April 8, 2005

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A New Type of Peroxisomal Acyl-Coenzyme A Synthetase from Arabidopsis thaliana Has the Catalytic Capacity to Activate Biosynthetic Precursors of Jasmonic Acid^*

Katja Schneider, Lucie Kienow, Elmon Schmelzer, Thomas Colby, Michael Bartsch, Otto Miersch, Claus Wasternack, Erich Kombrink¶, and Hans-Peter Stuible

From the Max Planck Institute for Plant Breeding Research, Department of Plant-Microbe Interactions, Carl-von-Linné-Weg 10, 50829 Köln and the Leibniz Institute of Plant Biochemistry, Department of Natural Product Biotechnology, Weinberg 3, 06120 Halle, Germany

Arabidopsis thaliana contains a large number of genes that encode carboxylic acid-activating enzymes, including nine long-chain fatty acyl-CoA synthetases, four 4-coumarate:CoA ligases (4CL), and 25 4CL-like proteins of unknown biochemical function. Because of their high structural and sequence similarity with bona fide 4CLs and their highly hydrophobic putative substrate-binding pockets, the 4CL-like proteins At4g05160 and At5g63380 were selected for detailed analysis. Following heterologous expression, the purified proteins were subjected to a large scale screen to identify their preferred in vitro substrates. This study uncovered a significant activity of At4g05160 with medium-chain fatty acids, medium-chain fatty acids carrying a phenyl substitution, long-chain fatty acids, as well as the jasmonic acid precursors 12-oxo-phytodienoic acid and 3-oxo-2-(2'-pentenyl)-cyclopentane-1-hexanoic acid. The closest homolog of At4g05160, namely At5g63380, showed high activity with long-chain fatty acids and 12-oxo-phytodienoic acid, the latter representing the most efficiently converted substrate. By using fluorescent-tagged variants, we demonstrated that both 4CL-like proteins are targeted to leaf peroxisomes. Collectively, these data demonstrate that At4g05160 and At5g63380 have the capacity to contribute to jasmonic acid biosynthesis by initiating the -oxidative chain shortening of its precursors.

Received for publication, December 2, 2004 , and in revised form, January 19, 2005.

^* This work was supported by Deutsche Forschungsgemeinschaft Grant KO1192/6-1/2. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶ To whom correspondence should be addressed. Tel.: 49-221-5062-320; Fax: 49-221-5062-353; E-mail: kombrink{at}mpiz-koeln.mpg.de.

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