Plant Phytochrome B Assembles an Asymmetric Dimer with Unique Signaling Potential.

Phytochromes (Phy) sense red and far-red light and reversibly interconvert between inactive Pr and active Pfr conformers. Phys typically consist of a photo sensory module (PSM) formed by sequential N-terminal PAS, GAF, and PHY domains, followed by a C-terminal histidine kinase-related domain (HKRD). There are four plant isoforms Phy A through D, and they all contain two additional PAS domains (PAS1 and PAS2) inserted between PSM and HKRD. Despite extensive biochemical and structural studies, there has been a lack of a full-length structure, hindering our understanding of plant Phy signaling. Here we report a 3.3-Å cryo-EM structure of Arabidopsis PhyB dimer. Instead of the widely anticipated parallel association of the two monomers resembling the prokaryotic relatives, Plant PhyB adopts a topologically complex dimeric architecture with the two PSMs in a head-to-tail antiparallel form while the two HKRDs in a head-to-head parallel form. The PAS2 mediates the antiparallel dimerization of PSM that leads to a parallelogram-shaped platform. And a preceding 'modulator' loop assembles tightly with the PSM of its own protomer. We show that these inter- and intra-protomer connections contribute to stabilizing of dimer and accelerate thermal reversion of Pfr back to Pr. Lean of HKRDs towards the platform results in profound asymmetry of PhyB that might enable distinct signaling potentials to the protomers. We propose that this unique structural dynamism creates an extensive photostate-sensitive surface for interaction with their downstream signaling partners.