Evolution of cyanobacterial and plant phytochromes

Abstract

Phytochromes are broadly distributed photochromic photoreceptors that are most sensitive in the red and far-red region of the visible spectrum. Three different bilins can be used as chromophores: plant phytochromes incorporate phytochromobilin, while phycocyanobilin serves as a chromophore of some cyanobacterial phytochromes, whereas all other phytochromes, including cyanobacterial orthologs incorporate biliverdin. During the evolution of plant and cyanobacterial phytochromes, the chromophore binding site has changed from a cysteine close to the N-terminus of the protein, the biliverdin attachment site, to a cysteine which lies within the so-called GAF domain and serves as phytochromobilin or phycocyanobilin attachment site. Since phylogenetic analyses imply that plant phytochromes are not direct successors of cyanobacterial phytochromes, chromophore exchange and the switch of the chromophore binding site has probably occurred at least twice in evolution. This may be regarded as an example for convergent evolution at the molecular level.

Evolutionary Studies Illuminate the Structural-Functional Model of Plant Phytochromes

“…It is a region that in PHYA may harbor sites important for protein stability and spectral integrity and in PHYB that are important for efficient signaling (Quail, 1997;Mateos et al, 2006;Trupkin et al, 2006;Kneissl et al, 2008;Oka et al, 2008). The C-terminal regions of plant PHY and of those prokaryotic PHY that have been sequenced are not homologous (Lamparter, 2004;Mathews, 2006); in green plants, this region comprises two PAS and single His kinase and ATPase domains ( Figure 3B), the latter two domains form the core of the His kinase-related domain (HKRD; Rockwell et al, 2006). The PAS repeats and HKRD contain sites necessary for dimerization and nuclear localization (Quail, 1997;Chen et al, 2003) and for modulating phytochrome signaling (Krall and Reed, 2000;Matsushita et al, 2003;Oka et al, 2004;Mü ller et al, 2009).…”

“…Currently, high-resolution structures of the photosensory core of prokaryotic phytochromes are available; this region is homologous with the sensory module of plant phytochromes (Montgomery and Lagarias, 2002;Lamparter, 2004;Karniol et al, 2005) and consists of PAS, GAF, and PHY domains ( Figure 3B). It is necessary for photoreversibility (Rockwell et al, 2006) and is sufficient for signaling when fused with dimerization and nuclear localization signals (Matsushita et al, 2003;Oka et al, 2004).…”

Algae hold clues to eukaryotic origins of plant phytochromes

“…Early phylogenetic analyses to understand diversity in this larger phytochrome superfamily were inconclusive regarding relationships among plant and bacterial phytochromes, but they suggested that cyanobacterial phytochromes were more closely related to bacterial than to plant phytochromes (7,8). In one study, the N-terminal photosensory core and the C-terminal regulatory region were analyzed separately, providing strong evidence that C termini of plant and cyanobacterial phytochromes were not closely related (9). Together, the results of these studies contradicted EGT.…”

A Singular Bacteriophytochrome Acquired by Lateral Gene Transfer

“…Because in phytochromes characterized thus far BV binds to a Cys located at the N-terminal extremity whereas PCB binds to a Cys located in the GAF domain (11,12), we investigated the PCB binding site by mutating the Cys residues (Cys-7 and Cys-16) of the N-terminal region and the Cys residue (Cys-260) located in the GAF domain ( Fig. 2A).…”

“…Whereas BphPs use this simplest linear tetrapyrrole as a chromophore (9), the chromophores of Phys and Cphs are 3E-phytochromobilin (P⌽B) and 3Z-phycocyanobilin (PCB), respectively, modified from BV by bilin reductases (10). These bilins are covalently bound to a Cys residue located in the N-terminal region for BV and in the GAF domain for P⌽B and PCB (11,12). Although little is known about the Fph type, their similarity to BphPs and their biochemical properties are strong indications that BV is also their natural chromophore (13).…”