Protein feeding mediates sex pheromone biosynthesis in an insect

Abstract

Protein feeding is critical for male reproductive success in many insect species. However, how protein affects the reproduction remains largely unknown. Using Bactrocera dorsalis as the study model, we investigated how protein feeding regulated sex pheromone synthesis. We show that protein ingestion is essential for sex pheromone synthesis in male. While protein feeding or deprivation did not affect Bacillus abundance, transcriptome analysis revealed that sarcosine dehydrogenase (Sardh) in protein-fed males regulates the biosynthesis of sex pheromones by increasing glycine and threonine (sex pheromone precursors) contents. RNAi-mediated loss-of-function of Sardh decreases glycine, threonine and sex pheromone contents and results in decreased mating ability in males. The study links male feeding behavior with discrete patterns of gene expression that plays role in sex pheromone synthesis, which in turn translate to successful copulatory behavior of the males.

Reproductive behavior of fruit flies: courtship, mating, and oviposition

“…In B. dorsalis, proteins can be converted into precursors for sex pheromone synthesis; therefore, a protein deficiency can affect this process. 100 This was also observed in Ceratitis capitata and B. tryoni, where the amount of protein intake is directly related to the intensity of sex pheromone release. 226,227 Protein intake also makes A. obliqua more sensitive to sex pheromones.…”

“…33 Further studies have shown that both are synthesized in the rectum by Bacillus using glucose, threonine, and glycine as substrates. 99,100 Based on studies of Zhang et al, 101 and Gui et al, 100 the TMP and TTMP synthesis pathway in the B. dorsalis rectum is proposed (Fig. 1).…”

“…34,99,100 In B. dorsalis, sarcosine dehydrogenase (SARDH) is integral for the conversion of supplemental proteins to sex pheromones. 100 For B. dorsalis females, several spiroacetals in the body can attract males, however the mechanism of their synthesis has not been reported. 30 Gonçalves et al 102 found that the volatile compounds released by Ceratitis capitata males are also present in salivary gland extracts, suggesting that the salivary gland is the storage and possibly the synthesis site of these compounds, but the exact associated mechanism needs to be demonstrated through detailed biosynthetic and histological studies on the salivary gland.…”

“…126 Although some fruit fly females can mate multiple times, most do not, as in Ceratitis capitata, with only 5% of females mating more than once in the wild. 127 Thus, mating behavior between males and females and 101 and Gui et al 100 whether females will engage in multiple mating events is influenced by various factors.…”

The effects of circularly polarized light on mating behavior and gene expression in Anomala corpulenta (Coleoptera: Scarabaeidae)

“…Furthermore, some amino acid metabolic pathways that regulate insect reproduction were also found to be significantly enriched. Recent studies indicate that phenylalanine metabolism regulates reproduction and mating behavior in flies and mosquitos (Proline et al, 2014;Arya et al, 2021), while glycine, serine, and threonine metabolism are involved in sex pheromone biosynthesis in the oriental fruit fly (Gui et al, 2023). Overall, when A. corpulenta beetles were subjected to LCP light stress, not only was the expression of insect environmental signaling pathway-related genes affected, but that of amino acid metabolism pathways related to insect reproduction was also affected.…”