Guangdong Provincial Key Laboratory of Insect Developmental Biology and Applied Technology, Institute of Insect Science and Technology, School of Life Sciences, South China Normal University, Guangzhou, China.
State Key Laboratory of Crop Stress Biology for Arid Areas, and Key Laboratory of Integrated Pest Management on the Loess Plateau of Ministry of Agriculture, Northwest A&F University, Yangling, China.
Nat Ecol Evol. 2022 Aug;6(8):1180-1190. doi: 10.1038/s41559-022-01808-w. Epub 2022 Jul 4.
Sex differentiation and hormones are essential for the development of sexual signals in animals, and the regulation of sexual signals involves complex gene networks. However, it is unknown whether a core gene is able to connect the upstream regulators for controlling sexual signal outputs and behavioural consequences. Here, we identify a single gene that integrates both sex differentiation and hormone signalling with sexual attractiveness in an insect model. CYP4PC1 in the German cockroach, Blattella germanica, controls the rate-limiting step in producing female-specific contact sex pheromone (CSP) that stimulates male courtship. As revealed by behavioural, biochemical, molecular, genetic and bioinformatic approaches, in sexually mature females, CYP4PC1 expression and CSP production are coordinately induced by sex differentiation genes and juvenile hormone (JH) signalling. In adult males, direct inhibition of CYP4PC1 expression by doublesex binding in gene promoter and lack of the gonadotropic hormone JH prevent CSP production, thus avoiding male-male attraction. By manipulating the upstream regulators, we show that wild-type males prefer to court cockroaches with higher CYP4PC1 expression and CSP production in a dose-dependent manner, regardless of their sex. These findings shed light on how sex-specific and high sexual attractiveness is conferred in insects.
性别的分化和激素对动物性信号的发育至关重要，而性信号的调节涉及复杂的基因网络。然而，目前尚不清楚是否有一个核心基因能够将控制性信号输出和行为后果的上游调节剂联系起来。在这里，我们在昆虫模型中鉴定出一个单一的基因，该基因将性别分化和激素信号与性吸引力联系起来。德国蟑螂 Blattella germanica 中的 CYP4PC1 控制着产生雌性特有的接触性性信息素（CSP）的限速步骤，该性信息素刺激雄性求偶。通过行为学、生物化学、分子生物学、遗传学和生物信息学方法揭示，在性成熟的雌性中，CYP4PC1 的表达和 CSP 的产生受到性别分化基因和保幼激素（JH）信号的协调诱导。在成年雄性中，双性结合蛋白直接抑制基因启动子中 CYP4PC1 的表达，并缺乏促性腺激素 JH，从而阻止 CSP 的产生，从而避免雄性间的吸引力。通过操纵上游调节剂，我们表明，无论其性别如何，野生型雄性更喜欢与 CYP4PC1 表达和 CSP 产生水平较高的蟑螂求偶，且这种偏好呈剂量依赖性。这些发现阐明了昆虫中如何赋予性别特异性和高性吸引力。
