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Originally published In Press as doi:10.1074/jbc.M407151200 on August 20, 2004

J. Biol. Chem., Vol. 279, Issue 44, 45998-46007, October 29, 2004
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Regulation of Plant Arginase by Wounding, Jasmonate, and the Phytotoxin Coronatine*{boxs}

Hui Chen{ddagger}, Bonnie C. McCaig{ddagger}, Maeli Melotto{ddagger}, Sheng Yang He{ddagger}§, and Gregg A. Howe{ddagger}¶||

From the {ddagger}Department of Energy-Plant Research Laboratory, the §Department of Plant Biology, and the Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824

In mammalian cells, induced expression of arginase in response to wound trauma and pathogen infection plays an important role in regulating the metabolism of L-arginine to either polyamines or nitric oxide (NO). In higher plants, which also utilize arginine for the production of polyamines and NO, the potential role of arginase as a control point for arginine homeostasis has not been investigated. Here, we report the characterization of two genes (LeARG1 and LeARG2) from Lycopersicon esculentum (tomato) that encode arginase. Phylogenic analysis showed that LeARG1 and -2, like all other plant arginases, are more similar to agmatinase than to arginases from vertebrates, fungi, and bacteria. Never-theless, recombinant LeARG1 and -2 exhibited specificity for L-arginine over agmatine and related guanidino substrates. The plant enzymes, like mammalian arginases, were inhibited (Ki ~ 14 µM) by the NO precursor NG-hydroxy-L-arginine. These results indicate that plant arginases define a distinct group of ureohydrolases that function as authentic L-arginases. LeARG1 and LeARG2 transcripts accumulated to their highest levels in reproductive tissues. In leaves, LeARG2 expression and arginase activity were induced in response to wounding and treatment with jasmonic acid (JA), a potent signal for plant defense responses. Wound- and JA-induced expression of LeARG2 was not observed in the tomato jasmonic acid-insensitive1 mutant, indicating that this response is strictly dependent on an intact JA signal transduction pathway. Infection of wild-type plants with a virulent strain of Pseudomonas syringae pv. tomato also up-regulated LeARG2 expression and arginase activity. This response was mediated by the bacterial phytotoxin coronatine, which exerts its virulence effects by co-opting the host JA signaling pathway. These results highlight striking similarities in the regulation of arginase in plants and animals and suggest that stress-induced arginase may perform similar roles in diverse biological systems.


Received for publication, June 25, 2004

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EBI Data Bank with accession number(s) AY656837 and AY656838.

* This research was supported in part by grants from the Michigan Life Science Corridor (to G. A. H.) and the United States Department of Energy (to G. A. H. and S. Y. H.). 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.

{boxs} The on-line version of this article (available at http://www.jbc.org) contains Figs. S1 and S2.

|| To whom correspondence should be addressed. Tel.: 517-355-5159; Fax: 517-353-9168; E-mail: howeg{at}msu.edu.


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