Thermosensory TRPV Heterotetramers Drive Seasonal Polyphenism: Molecular Basis of CcIav/CcNan-PKCα-AKH/AKHR Signaling in Pear Psyllid Morph Transition.

Temperature critically governs seasonal polyphenism, shaping species distribution and invasion dynamics. Although vanilloid-type transient receptor potential (TRPV) channels are conserved thermal sensors, their mechanistic role in orchestrating seasonal polyphenism remains unresolved. The pear psyllid Cacopsylla chinensis exhibits striking temperature-dependent transitions: warm spring temperature triggers winter-form adult females to oviposit and irreversibly transform into summer-forms, providing a model to dissect this phenomenon. Here, how TRPV-mediated thermal sensing regulates this process. It is demonstrated that exposure to 25 °C - a critical ecological threshold-induces an orchestrated shift in energy metabolism, follicular epithelium remodeling, and ovarian maturation, culminating in phenotypic transformation. Central to this process is the assembly of functional heterotetrameric TRPV channels comprising interdependent subunits CcIav and CcNan, which directly perceive the 25 °C thermal signal. Mechanistically, CcIav/CcNan activation triggers a phosphorylation cascade via protein kinase CcPKCα, subsequently potentiating adipokinetic hormone signaling through CcAKHR. This axis synchronizes energy metabolism reprogramming with reproductive tissue reorganization to drive polyphenic switching. Significantly, the evolutionary conservation of this TRPV is validated heterotetramer-dependent thermosensation mechanism across three phylogenetically diverse insect species. This work delineates a previously unrecognized CcIav/CcNan-CcPKCα-AKH/CcAKHR signaling module essential for insect seasonal adaptation and pioneers a receptor-targeted strategy for disrupting psyllid population cycles in agroecosystems.