Male-derived phospholipase A2 enhances WD46 expression and increases fertility in Ophraella communa.

Abstract

Successful bisexual reproduction requires interactions between males and females. Male-derived seminal fluid proteins (SFPs) transferred to females during mating profoundly affect females from pre- to post-mating, and the subsequent shift in female physiology enhances their fertility. SFPs have important evolutionary implications for the fitness of many insects. However, little is known about how females respond to male SFPs. In this study, we identified a male-derived SFP-phospholipase A2 (PLA2) in Ophraella communa. PLA2 is a vital enzyme in eicosanoid biosynthesis; however, it has not been identified as an insect SFP. We found that OcPLA2 is specifically expressed in males, especially in the male accessory glands (MAGs); it is transferred to the female during mating and functions as an SFP to enhance fertility. The expression of a female-derived gene encoding the WD repeat-containing protein 46 (WD46) was upregulated when OcPLA2 entered the female reproductive tract, and this contributed to female egg production by increasing triacylglycerol lipase (TGL) gene expression and the triglyceride (TG) content. This is the first study to identify PLA2 as an SFP in insects. Our findings also shed light on the regulatory role of OcPLA2 in beetle reproduction; the expression of OcPLA2 is initially correlated with female WD46 expression and later with the decline in TGL gene expression and the TG content. This represents a unique mechanism of reproductive regulation by an SFP.