Inter-organelle communication dynamically orchestrates juvenile hormone biosynthesis and female reproduction

ABSTRACT Inter-organelle communication coordinates cellular homeostasis and function. Juvenile hormone (JH) is produced in the corpora allata (CA) and acts as a gonadotrophic hormone in most insects. Using transcriptomic, biochemical, molecular, and genetic analyses, here we investigated the underlying mechanism of how inter-organelle communication dynamically orchestrates JH biosynthesis and female reproduction in the American cockroach, Periplaneta americana. The extracellular stimuli insulin and allatostatin act through their membrane receptors and antagonistically regulate RyR-mediated Ca2+ release from the endoplasmic reticulum in CA cells. Ca2+-activated CaMKII stimulates energy metabolism in the mitochondria partially via SLC25A6, and induces the expression of JH biosynthetic genes HMGR, Jhamt, and Cyp15a1 through activating transcription factor CREB, which recruits CBP for histone acetylation in the nucleus. Additionally, mitochondria interact with CREB-CBP through mitonuclear communication to regulate JH biosynthesis. From the perspective of inter-organelle communication, this comprehensive study significantly advanced our understanding of hormone biosynthesis and reproductive biology in insects.