Introduction of regioselective bacterial heme oxygenases into Arabidopsis hy1-1 supports the retrograde heme signaling hypothesis

Heme is synthesized in the plastid and catabolized by heme oxygenase (HO). In Arabidopsis, HO1/HY1/GUN2 predominantly functions for heme catabolism. Previously, we demonstrated that introduction of either plastid-or cytosol-localized HO1 into gun2 or hy1-1 complemented the phenotypes including genomes uncoupling (gun), indicating the assembly of functional phytochromes, as well as supporting the heme signaling hypothesis. To dissect the heme signaling and phytochrome assembly, in this study, we introduced either of the two types of regiospecific bacterial HOs that produce biliverdin IX (BVIX) or BVIX{beta}/{delta} into hy1-1. Introduction of BVIX-producing HO complemented the long hypocotyl, low pigmentation, and gun phenotypes of hy1-1. Interestingly, the introduction of BVIX{beta}/{delta}-producing HO failed to complement the long hypocotyl and low pigmentation phenotypes, suggesting failure of functional phytochrome assembly. However, these lines restored the gun phenotype, thus supporting the heme signaling hypothesis. Based on the levels of complementation of the gun phenotype, we found that the expression of photosynthesis-associated nuclear genes (PhANGs) can be separated into phytochrome-dependent and -independent groups. Our results demonstrate that heme functions as a retrograde mobile biogenic signal from plastids, passing through the cytosol, to regulate the expression of PhANGs, and this regulation is distinct in its dependency of phytochromes.