Integration of light and temperature sensing by liquid-liquid phase separation of phytochrome B

• Published in: Molecular cell 2022-08, Vol.82 (16), p.3015-3029.e6
• Main Authors: Chen, Di, Lyu, Mohan, Kou, Xiaoxia, Li, Jing, Yang, Zhixuan, Gao, Lulu, Li, Yue, Fan, Liu-min, Shi, Hui, Zhong, Shangwei
• Format: Article
• Language: English
• Subjects: biomolecular condensates; oligomerization; photoreceptor; signal clustering; thermosensor
• ISSN: 1097-2765; 1097-4164
• DOI: 10.1016/j.molcel.2022.05.026

Light and temperature in plants are perceived by a common receptor, phytochrome B (phyB). How phyB distinguishes these signals remains elusive. Here, we report that phyB spontaneously undergoes phase separation to assemble liquid-like droplets. This capacity is driven by its C terminus through self-association, whereas the intrinsically disordered N-terminal extension (NTE) functions as a biophysical modulator of phase separation. Light exposure triggers a conformational change to subsequently alter phyB condensate assembly, while temperature sensation is directly mediated by the NTE to modulate the phase behavior of phyB droplets. Multiple signaling components are selectively incorporated into phyB droplets to form concentrated microreactors, allowing switch-like control of phyB signaling activity through phase transitions. Therefore, light and temperature cues are separately read out by phyB via allosteric changes and spontaneous phase separation, respectively. We provide a conceptual framework showing how the distinct but highly correlated physical signals are interpreted and sorted by one receptor. [Display omitted] •Photo-activated phyB proteins undergo LLPS to form liquid droplets•C terminus and NTE are, respectively, the driving force and modifier of phyB LLPS•PhyB selectively recruits its interacting transcription factors into droplets•The NTE directly senses thermal signals to modify phyB phase behaviors Light and temperature are correlated but independent signals. Chen et al. uncover that phyB photobodies are formed through phase separation and function as tunable thermosensors. Light induces conformational changes to subsequently alter phyB photobody formation, while temperature signals are directly sensed by the condensates through the N-terminal extension of phyB.