Involvement of integument‐rich CYP4G19 in hydrocarbon biosynthesis and cuticular penetration resistance in Blattella germanica (L.)

Abstract

BACKGROUND Cuticle penetration plays an important role as a mechanism of insecticide resistance, but the underlying molecular mechanism remains poorly understood. In Blattella germanica, the cytochrome P450 gene, CYP4G19, is overexpressed in a pyrethroid‐resistant strain. Here, we investigated whether CYP4G19 is involved in the biosynthesis of hydrocarbons and further contributes to cuticular penetration resistance in B. germanica. RESULTS Compared with the susceptible strain, pyrethroid‐resistant cockroaches showed lower cuticular permeability with Eosin Y staining. Removal of epicuticular lipids, mainly nonpolar hydrocarbons, with a hexane wash intensified the cuticular permeability and decreased the resistance index of the resistant strain. CYP4G19 was predominately expressed in the abdominal integument and could be upregulated by desiccation stress or short exposure to beta‐cypermethrin. Overexpression of CYP4G19 in the resistant strain was positively correlated with a higher level of cuticular hydrocarbons (CHCs). RNAi‐mediated knockdown of CYP4G19 significantly decreased its expression and caused a reduction in CHCs. Meanwhile, CYP4G19 suppression resulted in a non‐uniform array of the lipid layer, enhanced cuticle permeability, and compromised insecticide tolerance. CONCLUSION Our findings confirm that CYP4G19 is involved in hydrocarbon production and appears to contribute to hydrocarbon‐based penetration resistance in B. germanica. This study highlights the lipid‐based penetration resistance, advancing our understanding of the molecular mechanism underlying P450‐mediated cuticular penetration resistance in insects. © 2019 Society of Chemical Industry

Climate change and the genetics of insecticide resistance

“…Together, these two studies showed that resistance to pyrethroid insecticides can be due to the overexpression of CYP4G genes in diverse insect species, leading to an increase in CHC levels and reduced penetration of these insecticides. The B. germanica study also showed that the overexpression of Cyp4g19 can be induced by desiccation stress, which may lead to lower penetration of beta‐cypermethrin in B. germanica . The functional link between susceptibility to desiccation and increased insecticide penetration was established in a recent study in the brown planthopper, Nilaparvata lugens .…”

“…The B. germanica study also showed that the overexpression of Cyp4g19 can be induced by desiccation stress, which may lead to lower penetration of beta-cypermethrin in B. germanica. 39 The functional link between susceptibility to desiccation and increased insecticide penetration was established in a recent study in the brown Figure 3. Either adaptation to a more arid environment or response to insecticide usage could lead to an increase in cuticular hydrocarbon (CHC) production, leading to a thicker epicuticle and both desiccation resistance and decreased insecticide penetration.…”

“…In a probable case of parallel evolution, a CYP4G homolog, Cyp4g19 , was also overexpressed in a pyrethroid‐resistant strain of the German cockroach, Blattella germanica , which showed decreased cuticular permeability to insecticides . The expression of Cyp4g19 was knocked down using RNAi, resulting in loss of CHCs and enhanced cuticular permeability, as well as increased mortality when treated with the insecticide beta‐cypermethrin.…”

“…38 In a probable case of parallel evolution, a CYP4G homolog, Cyp4g19, was also overexpressed in a pyrethroid-resistant strain of the German cockroach, Blattella germanica, which showed decreased cuticular permeability to insecticides. 39 The expression of Cyp4g19 was knocked down using RNAi, resulting in loss of CHCs and enhanced cuticular permeability, as well as increased mortality when treated with the insecticide beta-cypermethrin. Together, these two studies showed that resistance to pyrethroid insecticides can be due to the overexpression of CYP4G genes in diverse insect species, leading to an increase in CHC levels and reduced penetration of these insecticides.…”

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

“…Early studies in the triatomine Triatoma infestans and other species have shown that removal of cuticle HCs by solvent extraction or inhibition of their biosynthesis affects their desiccation tolerance and facilitates the penetration of insecticides through the cuticle (Motoyama et al, 1992;Juárez, 1994a). Conversely, larger amounts of cuticle HCs together with a diminished insecticide penetration have been shown to be associated with insecticide resistance in T. infestans (Pedrini et al, 2009;Juárez et al, 2010;Calderón-Fernández et al, 2011), the mosquito Anopheles gambiae (Balabanidou et al, 2016), and more recently in the cockroach Blattella germanica (Chen et al, 2019).…”