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First published online January 20, 2006; 10.1104/pp.105.074211

Plant Physiology 140:856-868 (2006)
© 2006 American Society of Plant Biologists

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CELL BIOLOGY AND SIGNAL TRANSDUCTION

Multiple Heme Oxygenase Family Members Contribute to the Biosynthesis of the Phytochrome Chromophore in Arabidopsis1

Thomas J. Emborg, Joseph M. Walker, Bosl Noh2 and Richard D. Vierstra*

Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706

The oxidative cleavage of heme by heme oxygenases (HOs) to form biliverdin IX{alpha} (BV) is the committed step in the biosynthesis of the phytochrome (phy) chromophore and thus essential for proper photomorphogenesis in plants. Arabidopsis (Arabidopsis thaliana) contains four possible HO genes (HY1, HO24). Genetic analysis of the HY1 locus showed previously that it is the major source of BV with hy1 mutant plants displaying long hypocotyls and decreased chlorophyll accumulation consistent with a substantial deficiency in photochemically active phys. More recent analysis of HO2 suggested that it also plays a role in phy assembly and photomorphogenesis but the ho2 mutant phenotype is more subtle than that of hy1 mutants. Here, we define the functions of HO3 and HO4 in Arabidopsis. Like HY1, the HO3 and HO4 proteins have the capacity to synthesize BV from heme. Through a phenotypic analysis of T-DNA insertion mutants affecting HO3 and HO4 in combination with mutants affecting HY1 or HO2, we demonstrate that both of the encoded proteins also have roles in photomorphogenesis, especially in the absence of HY1. Disruption of HO3 and HO4 in the hy1 background further desensitizes seedlings to red and far-red light and accelerates flowering time, with the triple mutant strongly resembling seedlings deficient in the synthesis of multiple phy apoproteins. The hy1/ho3/ho4 mutant can be rescued phenotypically and for the accumulation of holo-phy by feeding seedlings BV. Taken together, we conclude that multiple members of the Arabidopsis HO family are important for synthesizing the bilin chromophore used to assemble photochemically active phys.


1 This work was supported by the U.S. Department of Energy (grant no. DE–FG02–88ER13968), the National Science Foundation (grant no. MCB–0424062), and the Research Division of the University of Wisconsin College of Agriculture and Life Sciences (Hatch grant no. 142–E443).

2 Present address: Plant Metabolism Research Center, Kyung Hee University, Suwon 449–701, Korea.

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: Richard D. Vierstra (vierstra{at}wisc.edu).

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.074211.

* Corresponding author; e-mail vierstra{at}wisc.edu; fax 608–262–2976.

Received November 16, 2005; returned for revision December 9, 2005; accepted January 5, 2006.




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