Molecular elements involved in locust olfaction : gene families in the desert locust Schistocerca gregaria
Xingcong Jiang
Abstract
Xingcong Jiang
Abstract
Locusts are remarkable insects due to their unique and potentially devastating phenotypic plasticity based on the local population density. While solitarious phase locusts avoid one another, gregarious locusts can form dense and highly mobile swarms, which have been feared as agricultural pests since ancient history. For this reason alone, locust biology has long been the object of intense scientific studies; moreover, from a purely scientific perspective it is of great interest to unravel the mystery underlying the phenotypic plasticity. The unique phase transition including the behavioral plasticity heavily relies on chemical communication by means of critical volatiles. It is therefore important to elucidate the mechanisms underlying locust chemosensory communication, including the identification of molecular elements involved in recognizing odorous compounds. Towards this goal, the desert locust Schistocerca gregaria, as a representative locust species, was investigated in this study. \nOne of the key elements for recognizing odorous compounds are odorant binding proteins (OBPs). To gain insight into the repertoire of locust OBPs, genomic sequences encoding candidate OBPs from Schistocerca gregaria together with those from three other locust species were subjected to thorough comparative analyses. The results indicated that locust OBPs could be classified into several categories, namely, classic OBPs, plus-C OBPs, minus-C OBPs and atypical OBPs which reside in four major phylogenetic families (I to IV). With the aim to uncover distinct features of the various OBP types, the initial studies were concentrating on the conserved subfamilies I-A and II-A which comprise classic OBPs. The sequence analyses provided evidence for both common and subfamily-specific motifs as well as evolutionary clues based on the calculation of coden substitution rates, which suggested the effect of purifying selection pressure. The subfamily I-A comprised a much higher number of orthologous OBPs than subfamily II-A, which resulted in a distinct re-clustering patterns for subfamily I-A and subfamily II-A. Exploring the topographic expression pattern on the antennae revealed that OBPs of subfamily I-A were selectively expressed in sensilla basiconica and sensilla trichodea, whereas OBPs of subfamily II-A were restricted to sensilla coeloconica. Furthermore, cells expressing the subtype OBP1 were present in almost all sensilla basiconica and trichodea, whereas other subtypes were only present in subpopulations. The OBPs of subfamily II-A, were expressed in distinct subpopulations of sensilla coeloconica. Analyses of representative OBPs from the remaining phylogenetic subfamilies revealed that representative subtypes from subfamily III-A and III-B were expressed in sensilla chaetica, similarly the two representatives of subfamily I-B were also expressed in this sensillum type. The selective expression of these OBPs in sensilla chaetica was substantiated by analyzing the antennal tip, which comprises numerous sensilla chaetica. The atypical OBP OBP12, a representative of subfamily IV-A was found to be selectively expressed in a distinct subpopulation of sensilla coeloconica, while plus-C OBP OBP9, from subfamily IV-B, showed a unique expression pattern and seemed to be associate with all four sensillum types. The diversity and complex sensilla- and cellular-specific distribution implies distinct functional implications of OBP subtypes in the process of chemoreception. \n
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Locusts are remarkable insects due to their unique and potentially devastating phenotypic plasticity based on the local population density. While solitarious phase locusts avoid one another, gregarious locusts can form dense and highly mobile swarms, which have been feared as agricultural pests since ancient history. For this reason alone, locust biology has long been the object of intense scientific studies; moreover, from a purely scientific perspective it is of great interest to unravel the mystery underlying the phenotypic plasticity. The unique phase transition including the behavioral plasticity heavily relies on chemical communication by means of critical volatiles. It is therefore important to elucidate the mechanisms underlying locust chemosensory communication, including the identification of molecular elements involved in recognizing odorous compounds. Towards this goal, the desert locust Schistocerca gregaria, as a representative locust species, was investigated in this study. \nOne of the key elements for recognizing odorous compounds are odorant binding proteins (OBPs). To gain insight into the repertoire of locust OBPs, genomic sequences encoding candidate OBPs from Schistocerca gregaria together with those from three other locust species were subjected to thorough comparative analyses. The results indicated that locust OBPs could be classified into several categories, namely, classic OBPs, plus-C OBPs, minus-C OBPs and atypical OBPs which reside in four major phylogenetic families (I to IV). With the aim to uncover distinct features of the various OBP types, the initial studies were concentrating on the conserved subfamilies I-A and II-A which comprise classic OBPs. The sequence analyses provided evidence for both common and subfamily-specific motifs as well as evolutionary clues based on the calculation of coden substitution rates, which suggested the effect of purifying selection pressure. The subfamily I-A comprised a much higher number of orthologous OBPs than subfamily II-A, which resulted in a distinct re-clustering patterns for subfamily I-A and subfamily II-A. Exploring the topographic expression pattern on the antennae revealed that OBPs of subfamily I-A were selectively expressed in sensilla basiconica and sensilla trichodea, whereas OBPs of subfamily II-A were restricted to sensilla coeloconica. Furthermore, cells expressing the subtype OBP1 were present in almost all sensilla basiconica and trichodea, whereas other subtypes were only present in subpopulations. The OBPs of subfamily II-A, were expressed in distinct subpopulations of sensilla coeloconica. Analyses of representative OBPs from the remaining phylogenetic subfamilies revealed that representative subtypes from subfamily III-A and III-B were expressed in sensilla chaetica, similarly the two representatives of subfamily I-B were also expressed in this sensillum type. The selective expression of these OBPs in sensilla chaetica was substantiated by analyzing the antennal tip, which comprises numerous sensilla chaetica. The atypical OBP OBP12, a representative of subfamily IV-A was found to be selectively expressed in a distinct subpopulation of sensilla coeloconica, while plus-C OBP OBP9, from subfamily IV-B, showed a unique expression pattern and seemed to be associate with all four sensillum types. The diversity and complex sensilla- and cellular-specific distribution implies distinct functional implications of OBP subtypes in the process of chemoreception. \n
Key concepts: Desert locust, Schistocerca, Locust, Olfaction, Biology, Evolutionary biology, Ecology