Transcription Factor CcFoxO Mediated the Transition from Summer Form to Winter Form in Cacopsylla chinensis

Amid global climate change featuring erratic temperature fluctuations, insects adapt via seasonal polyphenism, essential for population sustainability and reproductive success. <i>Cacopsylla chinensis</i>, influenced by environment variations, displays a distinct summer form and winter form distinguished by significant morphological variations. Previous studies have highlighted the role of temperature receptor <i>CcTPRM</i> in orchestrating the transition in response to 10 °C temperature. Nevertheless, the contribution of the transcription factor <i>FoxO</i> in this process has remained ambiguous. Here, we aimed to explore the correlation between <i>C. chinensis</i> FoxO (<i>CcFoxO</i>) and cold stress responses, while identifying potential energetic substances for monitoring physiological shifts during this transition from summer to winter form under cold stress by using RNAi. Initially, <i>CcFoxO</i> emerges as responsive to low temperatures (10 °C) and is regulated by <i>CcTRPM</i>. Subsequent investigations reveal that <i>CcFoxO</i> facilitates the accumulation of triglycerides and glycogen, thereby influencing the transition from summer form to winter form by affecting cuticle pigment content, cuticle chitin levels, and cuticle thickness. Thus, the knockdown of <i>CcFoxO</i> led to high mortality and failed transition. Overall, our findings demonstrate that <i>CcFoxO</i> governs seasonal polyphenism by regulating energy storage. These insights not only enhance our comprehension of <i>FoxO</i> functionality but also offer avenues for environmentally friendly management strategies for <i>C. chinensis</i>.