Two antennae-enriched carboxylesterases mediate olfactory responses and degradation of ester volatiles in the German cockroach Blattella germanica

Authors: MA, YUN-FENG - Guizhou University; GONG, LANG-LANG - Guizhou University; ZHANG, MING-QI - Guizhou University; LIU, XUAN-ZHENG - Guizhou University; GUO, HUAN - Guizhou University; Hull, Joe; LONG, GUI-JUN - Guizhou University; WANG, HONG - Guizhou University; DEWER, YOUSSEF - Agricultural Research Center Of Egypt; ZHANG, FAN - Shandong Normal University; HE, MING - Guizhou University; HE, PENG - Guizhou University

Submitted to: Journal of Agricultural and Food Chemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/1/2023
Publication Date: 3/15/2023
Citation: Ma, Y., Gong, L., Zhang, M., Liu, X., Guo, H., Hull, J.J., Long, G., Wang, H., Dewer, Y., Zhang, F., He, M., He, P. 2023. Two antennae-enriched carboxylesterases mediate olfactory responses and degradation of ester volatiles in the German cockroach Blattella germanica. Journal of Agricultural and Food Chemistry. 71(12):4789-4801. https://doi.org/10.1021/acs.jafc.2c08488.
DOI: https://doi.org/10.1021/acs.jafc.2c08488

Interpretive Summary: Insect olfaction is a highly evolved system for detecting volatile odorants that impact diverse physiological and behavioral activities, including mate and host identification, avoidance of natural enemies, and interspecies communication. The system is predominantly housed in the antenna and is comprised of multiple gene products that function in the recognition and subsequent degradation of diverse odorants. The clearance of odorants is crucial for resetting the olfactory system back to a baseline suitable for detecting the next odorant. Given this important role, targeted disruption of the clearance process has been proposed as a potential pest control strategy. To provide insights into the German cockroach olfaction system, its genome was searched for genes encoding enzymes, such as carboxylesterases, that have been linked to odorant degradation. Two of the genes identified were found to be highly expressed in male cockroach antennae. RNAi-mediated knockdown of the two gene products resulted in reduced olfactory responses to a number of odorants and limited movement to behavioral attractants. These results provide evidence for likely function of the genes in German cockroach olfaction and provide a basis for further exploring behavioral inhibitors that target the encoded enzymes.

Technical 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.