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PCH1 regulates light, temperature, and circadian signaling as a structural component of phytochrome B-photobodies in Arabidopsis

He Huang,Katrice E. McLoughlin,Maria L. Sorkin,Maria L. Sorkin,E. S. Burgie,Rebecca K. Bindbeutel,R. Vierstra,Dmitri A. Nusinow

Published 2019 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance In Arabidopsis, phytochrome B (phyB) perceives light and temperature signals to regulate various fundamental morphogenic processes in plants through its interconversion between its active Pfr and inactive Pr states. On photoconversion from Pr to Pfr, phyB forms subnuclear foci called photobodies, whose compositions and molecular functions are unclear. We show here that the phyB-interacting protein PCH1 is a structural component of phyB photobodies that protects Pfr from thermal reversion back to Pr, thereby helping to maintain phyB signaling. Loss of PCH1 compromises photobody formation, which disrupts a number of downstream events, including photomorphogenesis and thermal perception and signaling into the circadian clock. These results demonstrate that the formation of PCH1-dependent phyB photobodies is an essential step connecting light and temperature to controls on plant morphogenesis. The members of the phytochrome (phy) family of bilin-containing photoreceptors are major regulators of plant photomorphogenesis through their unique ability to photointerconvert between a biologically inactive red light-absorbing Pr state and an active far-red light-absorbing Pfr state. While the initial steps in Pfr signaling are unclear, an early event for the phyB isoform after photoconversion is its redistribution from the cytoplasm into subnuclear foci known as photobodies (PBs), which dissipate after Pfr reverts back to Pr by far-red irradiation or by temperature-dependent nonphotochemical reversion. Here we present evidence that PHOTOPERIODIC CONTROL OF HYPOCOTYL 1 (PCH1) functions both as an essential structural component of phyB-containing PBs and as a direct regulator of thermal reversion that is sufficient to stabilize phyB as Pfr in vitro. By examining the genetic interaction between a constitutively active phyBY276H-YFP allele (YHB-YFP) and PCH1, we show that the loss of PCH1 prevents YHB from coalescing into PBs without affecting its nuclear localization, whereas overexpression of PCH1 dramatically increases PB levels. Loss of PCH1, presumably by impacting phyB-PB assembly, compromises a number of events elicited in YHB-YFP plants, including their constitutive photomorphogenic phenotype, red light-regulated thermomorphogenesis, and input of phyB into the circadian clock. Conversely, elevated levels of both phyB and PCH1 generate stable, yet far-red light–reversible PBs that persisted for days. Collectively, our data demonstrate that the assembly of PCH1-containing PBs is critical for phyB signaling to multiple outputs and suggest that altering PB dynamics could be exploited to modulate plant responses to light and temperature.

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