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Originally published In Press as doi:10.1074/jbc.M205965200 on August 20, 2002

J. Biol. Chem., Vol. 277, Issue 44, 41352-41360, November 1, 2002
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Functional Characterization of Choline Monooxygenase, an Enzyme for Betaine Synthesis in Plants*

Takashi HibinoDagger , Rungaroon Waditee§, Etsuko Araki§, Hiroshi IshikawaDagger , Kenji AokiDagger , Yoshito TanakaDagger , and Teruhiro TakabeDagger §

From the Dagger  Graduate School of Environmental and Human Sciences and the § Research Institute, Meijo University, Nagoya, 468-8502, Japan

In plants, the first step in betaine synthesis was shown to be catalyzed by a novel Rieske-type iron-sulfur enzyme, choline monooxygenase (CMO). Although CMO so far has been found only in Chenopodiaceae and Amaranthaceae, the recent genome sequence suggests the presence of a CMO-like gene in Arabidopsis, a betaine non-accumulating plant. Here, we examined the functional properties of CMO expressed in Escherichia coli, cyanobacterium, and Arabidopsis thaliana. We found that E. coli cells in which choline dehydrogenase (CDH) was replaced with spinach CMO accumulate betaine and complement the salt-sensitive phenotype of the CDH-deleted E. coli mutant. Changes of Cys-181 in spinach CMO to Ser, Thr, and Ala and His-287 to Gly, Val, and Ala abolished the accumulation of betaine. The Arabidopsis CMO-like gene was transcribed in Arabidopsis, but its protein was not detected. When the Arabidopsis CMO-like gene was expressed in E. coli, the protein was detected but was found not to promote betaine sysnthesis. Overexpression of spinach CMO in E. coli, Synechococcus sp. PCC7942, and Arabidopsis conferred resistance to abiotic stress. These facts clearly indicate that CMO, but not the CMO-like protein, could oxidize choline and that Cys-181 and His-287 are involved in the binding of Fe-S cluster and Fe, respectively.

* This work was supported in part by grants-in-aid for scientific research from the Ministry of Education and Science and Culture of Japan and the High-Tech Research Center of Meijo University.The costs of publication of this article were defrayed in part by the payment of page charges. The 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: Research Inst. of Meijo University, Tenpaku-ku, Nagoya, Aichi 468-8502, Japan. Tel.: 81-52-832-1151; Fax: 81-52-832-1545; E-mail: takabe@ccmfs.meijo-u.ac.jp.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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