Oligomerization and Photo-Deoligomerization of HOOKLESS1 Controls Plant Differential Cell Growth

Apical hook curvature is crucial for buried seedling survival and a superb model for dissecting differential cell growth. HOOKLESS1 (HLS1) is essential for apical hook formation, acting as a hub integrating various external and internal signals. However, its functional mechanism remains unclear. Here, we demonstrate that HLS1 protein is present as an oligomer in the nucleus of dark-grown seedlings. Oligomerization is required for HLS1 activation, as the mutated HLS1 protein abolishing self-association exists as nonfunctional monomers. Upon light exposure, photoreceptor phyB translocates into the nucleus and interacts with HLS1, disrupting the self-association and oligomerization of HLS1 to initiate hook unfolding. Remarkably, genetic expression of nuclear-localized phyB is sufficient to inactivate HLS1, resulting in compromised hook curvature in etiolated seedlings. Together, we conclude that HLS1 protein is active as oligomeric form in darkness and achieves allosteric photo-deactivation upon light, providing intriguing mechanistic insight into the molecular switch for developmental transition. [Display omitted] •HLS1 interacts with itself to assemble an oligomer in dark-grown seedlings•The oligomer is the active form of HLS1 in maintaining apical hook curvature•Photoreceptor phyB directly interacts with HLS1 to disrupt HLS1 self-association•Allosteric photo-deactivation of HLS1 imposed by phyB initiates hook unfolding The apical hook that protects the fragile shoot meristem of seedlings underground forms in darkness and opens upon exposure to light. Lyu et al. show that hook formation and unfolding are controlled by the assembly and light-dependent disassembly of HLS1 oligomers, revealing how a photo-switchable oligomerization controls a developmental transition.