Obligate Heterodimerization ofArabidopsisPhytochromes C and E and Interaction with the PIF3 Basic Helix-Loop-Helix Transcription Factor

Abstract

Phytochromes are dimeric chromoproteins that regulate plant responses to red (R) and far-red (FR) light. The Arabidopsis thaliana genome encodes five phytochrome apoproteins: type I phyA mediates responses to FR, and type II phyB-phyE mediate shade avoidance and classical R/FR-reversible responses. In this study, we describe the complete in vivo complement of homodimeric and heterodimeric type II phytochromes. Unexpectedly, phyC and phyE do not homodimerize and are present in seedlings only as heterodimers with phyB and phyD. Roles in light regulation of hypocotyl length, leaf area, and flowering time are demonstrated for heterodimeric phytochromes containing phyC or phyE. Heterodimers of phyC and chromophoreless phyB are inactive, indicating that phyC subunits require spectrally intact dimer partners to be active themselves. Consistent with the obligate heterodimerization of phyC and phyE, phyC is made unstable by removal of its phyB binding partner, and overexpression of phyE results in accumulation of phyE monomers. Following a pulse of red light, phyA, phyB, phyC, and phyD interact in vivo with the PHYTOCHROME INTERACTING FACTOR3 basic helix-loop-helix transcription factor, and this interaction is FR reversible. Therefore, most or all of the type I and type II phytochromes, including heterodimeric forms, appear to function through PIF-mediated pathways. These findings link an unanticipated diversity of plant R/FR photoreceptor structures to established phytochrome signaling mechanisms.