Identification and characterization of soluble binding proteins associated with host foraging in the parasitoid wasp Diachasmimorpha longicaudata

Abstract

The communication and reproduction of insects are driven by chemical sensing. During this process, chemical compounds are transported across the sensillum lymph to the sensory neurons assisted by different types of soluble binding proteins: odorant-binding proteins (OBPs); chemosensory proteins (CSPs); some members of ML-family proteins (MD-2 (myeloid differentiation factor-2)-related Lipid-recognition), also known as NPC2-like proteins. Potential transcripts involved in chemosensing were identified by an in silico analysis of whole-body female and male transcriptomes of the parasitic wasp Diachasmimorpha longicaudata. This analysis facilitated the characterization of fourteen OBPs (all belonging to the Classic type), seven CSPs (and two possible isoforms), and four NPC2-like proteins. A differential expression analysis by qPCR showed that eleven of these proteins (CSPs 2 and 8, OBPs 2, 3, 4, 5, 6, 9, 10, and 11, and NPC2b) were over-expressed in female antenna and two (CSP 1 and OBP 12) in the body without antennae. Foraging behavior trials (linked to RNA interference) suggest that OBPs 9, 10, and 11 are potentially involved in the female orientation to chemical cues associated with the host. OBP 12 seems to be related to physiological processes of female longevity regulation. In addition, transcriptional silencing of CSP 3 showed that this protein is potentially associated with the regulation of foraging behavior. This study supports the hypothesis that soluble binding proteins are potentially linked to fundamental physiological processes and behaviors in D. longicaudata. The results obtained here contribute useful information to increase the parasitoid performance as a biological control agent of fruit fly pest species.

Identification of candidate genes associated with host-seeking behavior in the parasitoid wasp Diachasmimorpha longicaudata

“…We annotated the putative sensory gene repertoire of D. longicaudata antennae including ten sensory-related gene families. The number of sequences identi ed was similar to that observed for other hymenopteran species, see Table 1 [11,19,20,25,[49][50][51]. Although our results suggested that most of the sensory genes expressed in the antenna of sexually mature and mated D. longicaudata females and males were identi ed (see above), sensory genes with a very low expression, such as gustatory receptors or genes expressed under speci c physiological conditions, may not have been included in our transcriptome.…”

“…In comparison with the odorant-molecule carriers previously identi ed in our whole-body transcriptome of D. longicaudata [25], we found 12 of the 14 OBPs expressed in the antenna previously identi ed in the whole-body, and a new OBP, DlonOBP11LK (Additional File 5: Supplementary Figure S2). Further, we identi ed ve of the nine CSPs (including the ones suggested as possible isoforms) previously identi ed in whole-body, and three of the four NPC2-like receptors found in the mentioned transcriptome [25]. In addition, four new CSPs, as follows, DlonCSP3, DlonCSP4, DlonCSP6 and DlonCSP7 were identi ed based on our assembly (Additional File 5: Supplementary Figure S2), and the sequences previously designated as OBPs 10 and 11, CSPs 3, 10 and 11 and NPC2b [25], were not identi ed in the present work.…”

“…By focusing on highly and differentially expressed genes in the female antennae, it has been possible to identify candidate chemosensory-related genes associated with female host-seeking behavior for oviposition in parasitoid species such as Cotesia vestalis Haliday (Hymenoptera: Braconidae) and Microplitis mediator Haliday (Hymenoptera: Braconidae) [14-16, 18, 19]. Functional studies, such as RNA interference, molecular docking and competitive uorescence binding assays (including attractant VOCs for female parasitoids), have given further evidence of the role of speci c ORs and OBPs in host detection in parasitoid wasps [20][21][22][23][24][25].…”

“…Further, speci c VOCs have been identi ed to act as attractants to females [3]. However, a deeper understanding of the sensory-related gene repertoire of this parasitoid wasp is still necessary; only ORs, OBPs and CSPs, among other proteins, have been identi ed for this species [25,47]. Further, functional assays to identify receptors associated with host-seeking behavior for oviposition have been conducted only for a few OBPs and CSPs [25].…”

“…Favret gv-IABIMO, Instituto Nacional de Tecnología Industrial (INTA) and Consejo Nacional de Investigaciones Cientí cas y Técnicas (CONICET). D. longicaudata individuals were obtained from a colony named IGEAF_D.longicaudata-Af, reared on Anastrepha fraterculus Wiedemann for 30 generations[25]. This colony was established from D. longicaudata wasps reared on Ceratitis capitata Wiedemann for ~ 200 generations, named IGEAF_D.longicaudata-Ca_colony, which was established with parasitoids provided by Fundación Miguel Lillo-CIRPON[75].…”