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

Abstract

The oxidative cleavage of heme by heme oxygenases (HOs) to form biliverdin IXa (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, HO2-4). 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.

Arabidopsis thaliana life without phytochromes

“…One is to combine mutations to block phytochrome chromophore biosynthesis. This approach has not been successful because of the close linkage of some gene family members (19) and the leakiness of mutants at some loci (20). The second strategy is to combine alleles of the five PHY apoprotein genes.…”

Analysis of PHOTOPERIOD SENSITIVITY5 Sheds Light on the Role of Phytochromes in Photoperiodic Flowering in Rice

“…Phytochromes are involved in a number of processes that affect plant development. Mutations in heme oxygenase genes have been previously described in rice (se5), Arabidopsis (hy1), pea (Pisum sativum; pcd1), tomato (Solanum lycopersicum; yg-2), and tobacco (Nicotiana tabacum; pew1; Emborg et al, 2006;Linley et al, 2006). Most of these mutants share phenotypic characteristics, such as abnormal stem or hypocotyl elongation, a decrease in red and far-red light responses during deetiolation, and a yellowish color.…”

“…SE5 encodes a heme oxygenase that functions in phytochrome chromophore biosynthesis. Mutations in this gene lead to a decrease or an absence of photochemical activity of functional phytochromes (Izawa et al, 2000;Emborg et al, 2006). Phytochromes are involved in a number of processes that affect plant development.…”

The RPN5 Subunit of the 26s Proteasome Is Essential for Gametogenesis, Sporophyte Development, and Complex Assembly inArabidopsis

“…The fusions were introduced into wild-type Col-0 plants by the floral dip method using the Agrobacterium tumefaciens strain GV3101 (Smalle et al, 2002). Hygromycin-resistant seedlings were screened for GUS expression by histochemical assay with the substrate 5-bromo-4-chloro-3-indolyl b-D-glucuronic acid (X-Gluc) (Emborg et al, 2006). Three independent insertion lines were examined for each construction to avoid artifacts generated by the site of transgene insertion.…”