Molecular and Functional Characterization of Three Odorant-Binding Protein from Periplaneta americana

Abstract

The American cockroach, Periplaneta americana, is a vector of many pathogenic organisms associated with human diseases. Olfaction plays a crucial role in guiding cockroach behaviors and contributes to their ability to transmit pathogens. Odorant binding proteins (OBPs), abundant in the insect olfactory sensilla, are important for insect olfaction. In this study, three OBP genes, PameOBP1, 2 and 3, were cloned from P. americana. Sequence alignment and phylogenetic analysis revealed that PameOBP1, 2 and 3 belong to the Minus-C OBP, Classic OBP, and Plus-C OBP subfamilies, respectively. Expression pattern and ligand-binding analysis showed that PameOBP1 and 2 were specifically expressed in antennae, and exhibited high binding affinities (Ki < 2 μM) to farnesene, farnesol, 2-tridecanone, and tetradecane, suggesting roles in volatile perception. Conversely, PameOBP3 was ubiquitously expressed in most of the tissues examined at high levels and displayed very weak binding affinities (Ki > 40 μM) for all 87 ligands tested. Our study provides insights into the functional diversity of PameOBP genes and provides some volatiles that can potentially be used in behavioral interference of P. americana.

Identification of odorant‐binding and chemosensory protein genes and the ligand affinity of two of the encoded proteins suggest a complex olfactory perception system in Periplaneta americana

“…migratoria OBP1, which may be involved in detecting plant volatiles, has been investigated so far (Zheng et al ., ; Li et al ., ). PameOBP1 and PameOBP2 may participate in general odorant reception, having been shown to have affinities with some plant volatiles in vitro (Li et al ., ). Thus, we propose that PameOBP1 and PameOBP2 may have dual roles, one in detecting pheromone components of both sexes and another as host odorants.…”

“…However, in P. americana , the putative PBPs, OBP1 and OBP2, showed the highest expression in female antennae amongst all 60 OBPs based on the RPKM values. This finding suggests that OBP1 and OBP2 can detect not only sex pheromone components but also other odorants from food or plant sources, such as farnesene, farnesol, 2‐tridecanone and tetradecane, which presented higher affinities [displacement constant (Ki) <2 μM] in our earlier study (Li et al ., ). PameOBP4 , 24 , 38 and 49 were expressed equally in the antennae of both sexes, indicating that they play roles in perceiving general host volatiles, similar to the GOBPs of moths (Zhou et al ., ; Li et al ., ).…”

“…5). We first determined the placement of the pheromone-binding proteins (PBPs) (Li et al, 2017). Thus, we propose that PameOBP1 and PameOBP2 may have dual roles, one in detecting pheromone components of both sexes and another as host odorants.…”

“…OBPs are considered as transporters that bind chemical odorant molecules to sensory dendrites, where they activate odorant receptors located on the membrane surface through odorant molecules alone or OBP/odorant complexes (Laughlin et al ., ; Gomez‐Diaz et al ., ; Pelosi et al ., ; Benton, ). OBPs have been identified in many insect species (Xu et al ., ; He et al ., ; Liu et al ., ; Li et al ., ). Because of their functions and different ligands, OBPs, especially those in Lepidoptera moths, have been classified as pheromone‐binding proteins, which bind sex pheromone components, and general odorant‐binding proteins (GOBPs), which bind general plant volatiles (Liu et al ., ; Vogt et al ., ; Zhu et al ., ).…”

“…However, little is known about the chemosensory mechanisms of this species. In previous studies, we identified three OBPs (OBP1-3) and three CSPs (CSP2, 3 and 10) using expressed sequence tags (Xu et al, 2009) and characterized the odorant affinities of OBP1-3 (Li et al, 2017). Besides the antennae, two major paired external sensory appendages (maxillary and labial palps) in the mouthparts of P. americana were also found to contain a variety of chemosensory sensilla and sensory nerves (Wieczorek, 1978;Boeckh & Ernst, 1987).…”