Deciphering the role of Rhodnius prolixusCYP4G genes in straight and methyl‐branched hydrocarbon formation and in desiccation tolerance

Abstract

Insect cuticle hydrocarbons are involved primarily in waterproofing the cuticle, but also participate in chemical communication and regulate the penetration of insecticides and microorganisms. The last step in insect hydrocarbon biosynthesis is carried out by an insect‐specific cytochrome P450 of the 4G subfamily (CYP4G). Two genes (CYP4G106 and CYP4G107) have been reported in the triatomines Rhodnius prolixus and Triatoma infestans. In this work, their molecular and functional characterization is carried out in R. prolixus, and their relevance to insect survival is assessed. Both genes are expressed almost exclusively in the integument and have an expression pattern dependent on the developmental stage and feeding status. CYP4G106 silencing diminished significantly the straight‐chain hydrocarbon production while a significant reduction – mostly of methyl‐branched chain hydrocarbons – was observed after CYP4G107 silencing. Molecular docking analyses using different aldehydes as hydrocarbon precursors predicted a better fit of straight‐chain aldehydes with CYP4G106 and methyl‐branched aldehydes with CYP4G107. Survival bioassays exposing the silenced insects to desiccation stress showed that CYP4G107 is determinant for the waterproofing properties of the R. prolixus cuticle. This is the first report on the in vivo specificity of two CYP4Gs to make mostly straight or methyl‐branched hydrocarbons, and also on their differential contribution to insect desiccation.

Cuticle Hydrocarbons Show Plastic Variation under Desiccation in Saline Aquatic Beetles

“…They are quite common in terrestrial insect species from dry areas [ 47 ] and the predominant class of CHCs in desert Tenebrionidae, with an exceptionally thick and impermeable epicuticular wax layer, and generally with more carbon atoms than n-alkanes [ 48 ]. In addition, a recent study showed that a gene related to the synthesis of methyl-branched hydrocarbons is a determinant for the waterproofing properties of Rhodnius prolixus cuticle under desiccation [ 49 ].…”

Comparative analysis of detoxification-related gene superfamilies across five hemipteran species

“…It has been suggested that CYP4 family plays a role in insecticide tolerance and resistance in triatomine species, given their higher expression in T. infestans resistant to pyrethroids [ 4 , 21 ]. Moreover, RNAi mediated gene-silencing of some CYP4 family members led to an increased susceptibility to deltamethrin in T. infestans [ 22 ] and R. prolixus [ 23 ].…”

Effect of salivary CYP4EM1 and CYP4EM2 gene silencing on the life span of Chagas disease vector Rhodnius prolixus (Hemiptera, Reduviidae) exposed to sublethal dose of deltamethrin

“…Even in the presence of acetone only (no insecticide), dsCYP4EM1-injected insects presented reduced LT 50 (104 days) compared with dsKer-injected bugs (148 days). Dulbecco et al (2020) showed that two genes also belonging to the CYP4 clade (CYP4G106 and CYP4G107), which are expressed mainly in R. prolixus integument, are related to cuticle formation and dehydration process. Thus, dsCYP4EM1 injection in addition to CY4PEM2 co-silencing could potentially reduce the expression of different CYP4s clade genes (as observed for CYP4EM3).…”