Two Antenna-Enriched Carboxylesterases Mediate Olfactory Responses and Degradation of Ester Volatiles in the German Cockroach Blattella germanica

Abstract

Insects have evolved an extremely sensitive olfactory system that is essential for a series of physiological and behavioral activities. Some carboxylesterases (CCEs) comprise a major subfamily of odorant-degrading enzymes (ODEs) playing a crucial role in odorant signal inactivation to maintain the odorant receptor sensitivity. In this study, 93 CCEs were annotated in the genome of the German cockroach Blattella germanica, a serious urban pest. Phylogenetic and digital tissue expression pattern analyses identified two antenna-enriched CCEs, BgerCCE021e3 and BgerCCE021d1, as candidate ODEs. RNA interference (RNAi)mediated knockdown of BgerCCE021e3 and BgerCCE021d1 resulted in partial anosmia with experimental insects exhibiting reduced attraction to ester volatile resources and slower olfactory responses than controls. Furthermore, enzymatic conversion of geranyl acetate by crude male antennal extracts from BgerCCE021e3 and BgerCCE021d1 RNAi insects was also significantly reduced. Our results provide evidence for CCE function in German cockroach olfaction and provide a basis for further exploring behavioral inhibitors that target olfactory-related CCEs.

Antennae-enriched expression of candidate odorant degrading enzyme genes in the turnip aphid, Lipaphis erysimi

“…In summary, this study has identified a dataset of CXE, CYP, GST, and UGT genes from L. erysimi , which might be involved in the processes of pheromone and/or plant volatile degradation. Previous studies have found that antennae-enriched ODEs offer great promise in the development of behavioral interference control strategies, in which ODE-silenced insects are expected to exhibit decreased or disordered foraging behaviors ( Yu et al, 2016 ; Wei et al, 2021 ; Wu et al, 2022 ; Ma et al, 2023 ). Examples include RNAi of LmCYP6FD5 , an antennae-specific P450 gene of Locusta migratoria , the EAG responses of locusts to the main volatiles of gramineous plants, including trans-2-Hexen-1-al, cis-3-Hexenyl acetate, and decanal, were significantly diminished ( Wu et al, 2022 ).…”

“…The first ODE identified was ApolSE , a CXE gene that was highly prevalent within the antennae of male silkmoths Antheraea polyphemus ( Vogt and Riddiford, 1981 ); subsequent functional analyses determined that ApolSE functioned as a pheromone degrading enzyme, effectively breaking down the sex pheromone components [(6E, 11Z)-hexadecadienyl acetate, Z11-16:Ac] ( Vogt et al, 1985 ; Ishida and Leal, 2005 ). Since then, several additional antennal CXEs have been functionally identified in various insects, such as the cotton leafworm Spodoptera littoralis ( Durand et al, 2010 ), beet armyworm Spodoptera exigua ( He et al, 2015 ), German cockroach Blattella germanica ( Ma et al, 2023 ), and oriental fruit moth Grapholita molesta ( Wei et al, 2021 ).…”

“…The turnip aphid, Lipaphis erysimi Kaltenbach, poses a significant threat to the cultivation of Brassica vegetables and oilseed crops due to its direct feeding and/or transmission of harmful plant viruses. RNA interference (RNAi) has emerged as a promising strategy for controlling aphids, and antennal ODEs hold great promise as the optimal target genes for disrupting foraging behaviors ( Yu et al, 2014 ; Yu et al, 2016 ; Wei et al, 2021 ; Wu et al, 2022 ; Ma et al, 2023 ). In this study, we aimed to identify antennae-enriched ODE genes of this aphid species by conducting as follows: 1) performing comparative analysis on the antennal and body transcriptomes of L. erysimi ; 2) isolating and in silico analysis of candidate ODE genes; 3) identifying the expression profile of the ODE genes among different tissues and developmental stages.…”

RNAi of yellow‐y, required for normal cuticle pigmentation, impairs courtship behavior and oviposition in the German cockroach (Blattella germanica)

“…We used insects from a permanent colony of B. germanica that we had started from cockroaches that we had collected in 2022 in Guilin city, Guangxi province, China, and subsequently kept in the laboratory at standardized conditions of 27 ± 1°C, 30%–40% relative humidity, a 12 h light:12 h dark regime and without any exposure to insecticides. In brief, the cockroaches were maintained in glass jars, and as food commercial rat chows and fresh water were provided as reported before (He et al, 2021; Ma et al, 2023).…”

An Antenna-Enriched Chemosensory Protein Plays Important Roles in the Perception of Host Plant Volatiles in Bactrocera dorsalis (Diptera: Tephritidae)

“…11 Insects recognize chemical cues through a complex process mediated by different olfactory proteins, including odorant binding proteins (OBPs), chemosensory proteins (CSPs), odorant receptors (ORs), ionotropic receptors (IRs), sensory neuron membrane proteins (SNMPs), and odor degrading enzymes (ODEs). 12,13 In recent years, numerous studies have been conducted to elucidate the molecular mechanisms involved in the perception of host volatiles in B. dorsalis. Nevertheless, most of them focus on OBPs 9,10,14 and ORs.…”