Abstract Seasonal polyphenism enables organisms to adapt to environmental challenges by increasing phenotypic diversity. Cacopsylla chinensis exhibits remarkable seasonal polyphenism, specifically in the form of summer-form and winter-form, which have distinct morphological phenotypes. Previous research has shown that low temperature and the temperature receptor CcTRPM regulate the transition from summer-form to winter-form in C. chinensis by impacting cuticle content and thickness. However, the underling neuroendocrine regulatory mechanism remains largely unknown. Bursicon, also known as the tanning hormone, is responsible for the hardening and darkening of the insect cuticle. In this study, we report for the first time on the novel function of Bursicon and its receptor in the transition from summer-form to winter-form in C. chinensis . Firstly, we identified CcBurs- α and CcBurs- β as two typical subunits of Bursicon in C. chinensis , which were regulated by low temperature (10°C) and CcTRPM . Subsequently, CcBurs- α and CcBurs- β formed a heterodimer that mediated the transition from summer-form to winter-form by influencing the cuticle chitin contents and cuticle thickness. Furthermore, we demonstrated that CcBurs-R acts as the Bursicon receptor and plays a critical role in the up-stream signaling of the chitin biosyntheis pathway, regulating the transition from summer-form to winter-form. Finally, we discovered that miR-6012 directly targets CcBurs-R , contributing to the regulation of Bursicon signaling in the seasonal polyphenism of C. chinensis . In summary, these findings reveal the novel function of neuroendocrine regulatory mechanism underlying seasonal polyphenism and provide critical insights into insect Bursicon and its receptor.

The fascinating role of neuropeptide Bursicon and its receptor in shaping insect seasonal polyphenism