Plants use a collection of photoreceptors to entrain their growth, development, and reproduction with the ambient light environment. One influential class are the phytochromes (Phys), a family of dimeric bilin-bound chromoproteins that signal by reversibly transitioning from a dark-adapted Pr state to a red light-activated Pfr state. To understand how Phys convert light into interpretable signals we have employed structure-based approaches using tractable bacterial and plant models. Based on X-ray crystallographic models of the photosensory module (PSM) harboring the bilin along with cryo-EM models of the full-length dimer, we have identified a cascade of events, starting with a light-induced ZZZssa-to-ZZEssa isomerization of the bilin that rotates the D-pyrrole ring. This flip forces sliding of the bilin in its binding pocket followed by a b-stranded to a-helical reconfiguration of a unique anti-parallel hairpin loop that induces rotation strain within the PSM. Whereas this strain translates into an output module in microbial versions, it impacts the architecture of a large dimeric platform in plant Phys that ultimately appears to allow differential interactions with various downstream partners including the family of PIF transcriptional repressors. Interestingly, plants encode a family of Phy isoforms with overlapping and distinct roles in photomorphogenesis. Comparison models of Arabidopsis PhyA and PhyB, which help sense low and high fluence light environments, respectively, revealed that these distinctions are underpinned by unique biophysical properties driven by slightly different photoreceptor architectures. Collectively, these structural characterizations illuminated how Phys signal and ultimately diversified to extend light and temperature perception in plants.