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Published on January 20, 2006; 10.1104/pp.105.074211


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Received November 16, 2005
Returned for revision December 5, 2005
Accepted January 5, 2006

MULTIPLE HEME OXYGENASE FAMILY MEMBERS CONTRIBUTE TO THE BIOSYNTHESIS OF THE PHYTOCHROME CHROMOPHORE IN ARABIDOPSIS

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

Department of Genetics, 425-G Henry Mall University of Wisconsin-Madison Madison, Wisconsin 53706 U.S.A

* Corresponding author; email: vierstra{at}wisc.edu.

The oxidative cleavage of heme by heme oxygenases (HO) to form biliverdin IX{alpha} is the committed step in the biosynthesis of the phytochrome (phy) chromophore and thus essential for proper photomorphogenesis in plants. Arabidopsis thaliana contains four possible HO genes (HY1, HO2-4). Genetic analysis of the HY1 locus showed previously that it is the major source of biliverdin IX{alpha} 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 biliverdin IX{alpha} 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 biliverdin IX{alpha}. 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.




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