Light-induced remodeling of phytochrome B enables signal transduction by phytochrome-interacting factor

Phytochrome B (phyB) and phytochrome-interacting factors (PIFs) constitute a well-established signaling module critical for plants adapting to ambient light. However, mechanisms underlying phyB photoactivation and PIF binding for signal transduction remain elusive. Here, we report the cryo-electron microscopy (cryo-EM) structures of the photoactivated phyB or the constitutively active phyBY276H mutant in complex with PIF6, revealing a similar trimer. The light-induced configuration switch of the chromophore drives a conformational transition of the nearby tongue signature within the phytochrome-specific (PHY) domain of phyB. The resulting α-helical PHY tongue further disrupts the head-to-tail dimer of phyB in the dark-adapted state. These structural remodelings of phyB facilitate the induced-fit recognition of PIF6, consequently stabilizing the N-terminal extension domain and a head-to-head dimer of activated phyB. Interestingly, the phyB dimer exhibits slight asymmetry, resulting in the binding of only one PIF6 molecule. Overall, our findings solve a key question with respect to how light-induced remodeling of phyB enables PIF signaling in phytochrome research. [Display omitted] •Red light activates phyB by remodeling the head-to-tail dimer in the dark-adapted state•PIF6-APB binding stabilizes the NTE domain and a head-to-head dimer of activated phyB•The asymmetric phyB dimer can accommodate only one PIF6-APB molecule•The constitutively active phyBY276H assembles a similar trimeric complex with PIF6-APB Cryo-EM structures of Arabidopsis photoactivated phyB and its constitutively active phyBY276H mutant in complex with the N terminus of PIF6 provide insights into light-induced photoreceptor remodeling and signal transduction.