Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects

Abstract

Odorant-binding proteins (OBPs) and chemosensory proteins (CSPs) are regarded as carriers of pheromones and odorants in insect chemoreception. These proteins are typically located in antennae, mouth organs and other chemosensory structures; however, members of both classes of proteins have been detected recently in other parts of the body and various functions have been proposed. The best studied of these non-sensory tasks is performed in pheromone glands, where OBPs and CSPs solubilise hydrophobic semiochemicals and assist their controlled release into the environment. In some cases the same proteins are expressed in antennae and pheromone glands, thus performing a dual role in receiving and broadcasting the same chemical message. Several reports have described OBPs and CSPs in reproductive organs. Some of these proteins are male specific and are transferred to females during mating. They likely carry semiochemicals with different proposed roles, from inhibiting other males from approaching mated females, to marking fertilized eggs, but further experimental evidence is still needed. Before being discovered in insects, the presence of binding proteins in pheromone glands and reproductive organs was widely reported in mammals, where vertebrate OBPs, structurally different from OBPs of insects and belonging to the lipocalin superfamily, are abundant in rodent urine, pig saliva and vaginal discharge of the hamster, as well as in the seminal fluid of rabbits. In at least four cases CSPs have been reported to promote development and regeneration: in embryo maturation in the honeybee, limb regeneration in the cockroach, ecdysis in larvae of fire ants and in promoting phase shift in locusts. Both OBPs and CSPs are also important in nutrition as solubilisers of lipids and other essential components of the diet. Particularly interesting is the affinity for carotenoids of CSPs abundantly secreted in the proboscis of moths and butterflies and the occurrence of the same (or very similar CSPs) in the eyes of the same insects. A role as a carrier of visual pigments for these proteins in insects parallels that of retinol-binding protein in vertebrates, a lipocalin structurally related to OBPs of vertebrates. Other functions of OBPs and CSPs include anti-inflammatory action in haematophagous insects, resistance to insecticides and eggshell formation. Such multiplicity of roles and the high success of both classes of proteins in being adapted to different situations is likely related to their stable scaffolding determining excellent stability to temperature, proteolysis and denaturing agents. The wide versatility of both OBPs and CSPs in nature has suggested several different uses for these proteins in biotechnological applications, from biosensors for odours to scavengers for pollutants and controlled releasers of chemicals in the environment.

Genome‐wide analysis of odorant‐binding proteins and chemosensory proteins in the sweet potato whitefly, Bemisia tabaci

“…The number of OBPs detected in B. tabaci (eight) is substantially lower than that detected in Drosophila melanogaster (52), Anopheles gambiae (69), Bombyx mori (44), Tribolium castaneum (50) and Apis mellifera (21) (Table S4) (Lynch & Conery, ; Zhou, ; Vieira & Rozas, ; Xue et al ., ; Benoit et al ., ; Mesquita et al ., ; Pelosi et al ., ). The relatively low number of OBPs in B. tabaci has several possible explanations.…”

Functional Characterization of Odorant Binding Protein 27 (RproOBP27) From Rhodnius prolixus Antennae

“…Although the genome predicts 27 genes which encode OBPs (Mesquita et al, 2015), only 17 OBPs were found to be expressed in adult antennae (Oliveira et al, 2017), which suggests that several genes belonging to the OBP family may not be directly involved in odor transport, as observed in other insects (Pelosi et al, 2018). Moreover, amongst the 11 OBP transcripts identified in antenna, leg, proboscis, and head from adults ( Figure 1 ), four had already been described in the midgut transcriptome: RproOBP1 , RproOBP11 , RproOBP14 , and RproOBP24 (Ribeiro et al, 2014).…”

“…New cases due to vector transmission were estimated to 29,925/year (WHO, 2015). Several proteins participate in insect chemosensation, including odorant binding proteins (OBPs), which transports odor molecules through the sensillum lymph to odorant receptors (ORs) (Fan et al, 2011; Leal, 2012; Brito et al, 2016; Pelosi et al, 2018); ORs located in the membrane of olfactory sensorial neurons (Benton, 2006), which recognize volatile odorant molecules (de Bruyne and Baker, 2008); and ionotropic receptors (IRs), which detect diverse chemical ligands from the environment (Benton et al, 2009). OBPs represent the first contact between semiochemicals from the environment and the olfactory sensory system since they are responsible for transporting hydrophobic ligands to their specific ORs (Wojtasek and Leal, 1999; Fan et al, 2011).…”

“…OBPs represent the first contact between semiochemicals from the environment and the olfactory sensory system since they are responsible for transporting hydrophobic ligands to their specific ORs (Wojtasek and Leal, 1999; Fan et al, 2011). OBPs are small soluble proteins secreted by accessory cells into the antenna sensillar lymph surrounding the olfactory sensory neurons (Brito et al, 2016; Pelosi et al, 2018). Initially, OBPs were identified and characterized at molecular level in Drosophila melanogaster (Brito et al, 2016).…”

Evolution and functional analysis of odorant‐binding proteins in three rice planthoppers: Nilaparvata lugens, Sogatella furcifera, and Laodelphax striatellus

“…A sensitive and delicate olfactory system is vital for insects to communicate with their external environment, including host seeking, mating, and avoiding predators . Antennae are the major olfactory organ, with many hair‐like structures called sensilla.…”