Identification and expression profiles of gustatory receptor genes in Bactrocera minax larvae (Diptera: Tephritidae): Role of BminGR59f in larval growth

Abstract

Insects employ various types of gustatory receptors (GRs) to identify nutrient‐rich food and avoid toxic substances. The larval gustatory system is the critical checkpoint for food acceptance or rejection. As a specialist herbivore, the larvae of Bactrocera minax feed only on unripe citrus fruits. However, how larvae use GRs to check and adapt to the secondary metabolites in unripe citrus fruits remains unknown. In this study, we first performed developmental expression profiles showing that most BminGRs genes were highly expressed in 1st and 2nd instar larvae and that tissue‐specific expression indicated high expression of most BminGRs genes in the mouthparts of 2nd instar larvae. Furthermore, we found that silencing BminGR59f by RNA interference (RNAi) affected the growth of 2nd instar B. minax larvae. Hesperidin and naringin were screened as ligands of BminGR59f via RNAi and cell calcium imaging, and the combination of these two flavones increased the body weight of larvae. In summary, we identified a novel gustatory perception pattern in B. minax for detecting hesperidin and naringin, which boosted the growth of B. minax larvae. These results shed light on how specialist herbivores detect and adapt to host metabolites in adverse environments depending on larval GRs.

Role of Genes in Regulating Host Plants Expansion in Tephritid Fruit Flies (Diptera) and Potential for RNAi-Based Control

“…The GR (gustatory receptor) family is another type of chemosensory protein that is a ligand-gated ion channel broadly expressed in gustatory receptor neurons in taste organs and is mainly involved in taste recognition of CO 2 , sugar, and bitterness (Li et al 2020, Zhang et al 2022. When receiving taste signals, GR genes are involved in identifying taste and ingestion.…”

“…OR13a and OR82 expression are higher in antennae in B. dorsalis in response to 1-octen-3-ol and geranyl acetate, respectively, which are major volatile components of its host fruits, mango (Mangifera indica) and almond fruit (Terminalia catappa) (Miyazaki et al 2018). For B. minax, increasing the expression levels of several GR genes (BminGR66a, BminGR32aa, BminGR64a and b, and BminGR59f) regulate the taste process in response to different chemosensory stimuli of hosts (Zhang et al 2022).…”

“…However, functional genes related to host plant adaptation are also target genes in RNAi control methods for tephritids. For example, the vision-related gene R6 or gustation gene GR59f of B. minax (Wang et al 2019, Zhang et al 2022, digestion-related genes try1, try2, try4, and try5 of B. dorsalis (Li et al 2017), olfactory Orco gene of B. oleae (Tsoumani et al 2020), CSP2 gene of B. dorsalis (Yi et al 2014), anddetoxification genes CYP6A41 andCYP6EK1 of B. dorsalis (Huang et al 2012) are associated with host adaptation functional genes, and all of these genes possess an exploitable potential as target genes to control fruit flies.…”

The temporal–spatial expression and functional analysis of three gustatory receptor genes in Solenopsis invicta using sweet and bitter compounds

“…In mulberry leaves, isoquercetin induces feeding behavior in B. mori; no preference for isoquercetin was detected in BmGR63 knockdown B. mori (Zhang et al, 2022a). In Bactrocera minax, BminGR59f boosted larval growth through the detection of naringin and hesperidin (Zhang et al, 2022b). On the other hand, GRs are also involved in the detection of CO 2 , such as GR3 in Aedes aegypti (McMeniman et al, 2014).…”

“…Similarly, broad expression profiles of TchiGR64f1 and TchiGR64f2 have been detected in T. chilonsis, and these GRs perform different functions (Liu et al, 2020b). Previously, it has been stated that the expression patterns of GRs in different tissues gives us clues about their functions (Li et al, 2022;Zhang et al, 2022b). GR genes are mainly expressed in gustatory tissues that have gustatory sensilla, such as antennae, foreleg tarsi, wings, ovipositor, and mouthparts (Montell, 2009).…”