Photobody formation spatially segregates two opposing phytochrome B signaling actions to titrate plant environmental responses

Abstract

ABSTRACTPhotoactivation of the plant photoreceptor and thermosensor phytochrome B (PHYB) triggers its condensation into subnuclear photobodies (PBs). However, the function of PBs remains frustratingly elusive. Here, we found that PHYB recruits PHYTOCHROME-INTERACTING FACTOR5 (PIF5) to PBs. Surprisingly, PHYB exerts opposing roles in degrading and stabilizing PIF5. Perturbing PB size by overproducing PHYB provoked a biphasic PIF5 response: while a moderate increase in PHYB enhanced PIF5 degradation, further elevating the PHYB level stabilized PIF5 by retaining more of it in enlarged PBs. These results reveal a PB-mediated light and temperature sensing mechanism, in which PHYB condensation confers the co-occurrence and competition of two antagonistic phase-separated PHYB signaling actions—PIF5 stabilization in PBs and PIF5 degradation in the surrounding nucleoplasm— thereby enabling an environmentally-sensitive counterbalancing mechanism to titrate nucleoplasmic PIF5 and its transcriptional output. This PB-enabled signaling mechanism provides a framework for regulating a plethora of PHYB-interacting signaling molecules in diverse plant environmental responses.