Modulation of fatty acid elongation in cockroaches sustains sexually dimorphic hydrocarbons and female attractiveness

Abstract

Insect cuticular hydrocarbons (CHCs) serve as important intersexual signaling chemicals and generally show variation between the sexes, but little is known about the generation of sexually dimorphic hydrocarbons (SDHCs) in insects. In this study, we report the molecular mechanism and biological significance that underlie the generation of SDHC in the German cockroach Blattella germanica. Sexually mature females possess more C29 CHCs, especially the contact sex pheromone precursor 3,11-DimeC29. RNA interference (RNAi) screen against the fatty acid elongase family members combined with heterologous expression of the genes in yeast revealed that both BgElo12 and BgElo24 were involved in hydrocarbon (HC) production, but BgElo24 is of wide catalytic activities and is able to provide substrates for BgElo12, and only the female-enriched BgElo12 is responsible for sustaining female-specific HC profile. Repressing BgElo12 masculinized the female CHC profile, decreased contact sex pheromone level, and consequently reduced the sexual attractiveness of female cockroaches. Moreover, the asymmetric expression of BgElo12 between the sexes is modulated by sex differentiation cascade. Specifically, male-specific BgDsx represses the transcription of BgElo12 in males, while BgTra is able to remove this effect in females. Our study reveals a novel molecular mechanism responsible for the formation of SDHCs and also provide evidences on shaping of the SDHCs by sexual selection, as females use them to generate high levels of contact sex pheromone.

Melanin synthesis genes BgTH and BgDdc affect body color and cuticle permeability in Blattella germanica

“…In D. melanogaster, Marican et al (2004) showed that dopamine influences the production of female flies' pheromonal hydrocarbon primarily by functioning in its last differential steps. RNAi of a HC biosynthesis gene CYP4G79 decreases the CHC contents in Harmonia axyridis, resulting in abnormal cuticular pigmentation and key melanin genes' upregulation in transcriptional analysis (Zhang et al, 2021). Thus, the correlation between TH or DDC and hydrocarbons in B. germanica needs to be further explored.…”

Evolutionary History of Sexual Differentiation Mechanism in Insects

“…Genes under dsx control in males are dsx -free in females of I. senegalensis ( Takahashi et al 2021 ), Bl. germanica ( Wexler et al 2019 ; Pei et al 2021 ), and Ni. lugens ( Zhuo et al 2018 ).…”

Evaluation of Reference Genes for Transcriptional Profiling in Two Cockroach Models

“…The Mus musculus lymphotoxin A gene ( Muslta ) not found in B. germanica served as an unrelated control for RNAi [ 28 ]. DsRNA synthesis and purification were performed using a T7 RiboMAX Express RNAi System (Promega, Madison, WI, USA) as described in our previous study [ 28 , 33 ]. Cockroaches were anesthetized with carbon dioxide, and 2 µL of dsRNA was injected into the hemocoel at a dose of 6 µg per cockroach.…”

“…Assessment of gene function by silencing gene expression (e.g., highly efficient RNAi in cockroaches) and accurate measurement of gene expression are needed for successful functional genomics. Hitherto, only actin has been used historically and extensively as a reference gene for qPCR normalization in these two species [ 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 28 , 31 , 32 , 33 ]. However, its stability under specific experimental conditions was not empirically validated, yet there is no stable reference gene quantification system for B. germanica and P. americana .…”