Photobodies enable the phase-separation and counterbalance of phytochrome B mediated PIF5 degradation and stabilization

Abstract

Photoactivation 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 show that PHYB condensation enables the co-occurrence and competition of two antagonistic phase-separated signaling actions. We found that PHYB recruits PHYTOCHROME-INTERACTING FACTOR5 (PIF5) to PBs and, surprisingly, that 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. Our results support a model in which PHYB condensation stabilizes PIF5 in PBs to counteract 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. We propose that this function of PBs represents a general function of biomolecular condensates to allow distinct variations of a cellular process or signaling pathway to coexist and interact to generate dynamically adjustable integrated outputs within a single subcellular space.