Genome‐wide characterization and transcriptomic analyses of neuropeptides and their receptors in an endoparasitoid wasp, Pteromalus puparum

Abstract

In insects, neuropeptides constitute a group of signaling molecules that act in regulation of multiple physiological and behavioral processes by binding to their corresponding receptors. On the basis of the bioinformatic approaches, we screened the genomic and transcriptomic data of the parasitoid wasp, Pteromalus puparum, and annotated 36 neuropeptide precursor genes and 33 neuropeptide receptor genes. Compared to the number of precursor genes in Bombyx mori (Lepidoptera), Chilo suppressalis (Lepidoptera), Drosophila melanogaster (Diptera), Nilaparvata lugens (Hemiptera), Apis mellifera (Hymenoptera), and Tribolium castaneum (Coleoptera), P. puparum (Hymenoptera) has the lowest number of neuropeptide precursor genes. This lower number may relate to its parasitic life cycle. Transcriptomic data of embryos, larvae, pupae, adults, venom glands, salivary glands, ovaries, and the remaining carcass revealed stage‐, sex‐, and tissue‐specific expression patterns of the neuropeptides, and their receptors. These data provided basic information about the identity and expression profiles of neuropeptides and their receptors that are required to functionally address their biological significance in an endoparasitoid wasp.

Identification of Neuropeptides and Their Receptors in the Ectoparasitoid, Habrobracon hebetor

“…Taken together, these results indicate that some neuropeptides are generally missing in wasps. We did identify natalisin (NTL), FMRFamide (FMRF), and leucokinin (LK) in H. hebetor ( Table 1 ), which had not been annotated in N. vitripennis (Hauser et al, 2010 ) or P. puparum (Xu et al, 2020 ), however, they were also found in other Braconidae wasps. For example, NTL was annotated in D. alloeum, F. arisanus , and M. demolitor .…”

“…Using both Nr-annotation and homology searches, we newly annotated 34 candidate neuropeptide genes in H. hebetor ( Table 1 , Supplementary Material File 1 ). When compared with other insects, such as P. puparum (Xu et al, 2020 ), A. mellifera (Hummon et al, 2006 ), D. melanogaster (Hewes and Taghert, 2001 ), B. mori (Roller et al, 2008 ), T. castaneum (Li et al, 2008 ), N. lugens (Tanaka et al, 2014 ), and Chilo suppressalis (Xu et al, 2016 ), evidently H. hebetor has the fewest neuropeptide precursor genes ( Supplementary Table 1 ), and also slightly fewer types of neuropeptides. Then, by using the RNA-Seq and genomic data of Cotesia vestalis (Wei et al, 2010 ), D. alloeum (Lowe and Eddy, 1997 ), Diadromus collaris (Li et al, 2015 ), Fopius arisanus (Lowe and Eddy, 1997 ), Macrocentrus cingulum (Yin et al, 2018 ) , Microplitis demolitor (Burke et al, 2014 ), and Trichogramma pretiosum (Lowe and Eddy, 1997 ), we were able to identify their neuropeptide precursor genes using the same method ( Table 2 ).…”

“…Unlike C. vestalis, D. alloeum, D. collaris, F. arisanus, M. cingulum, M. demolitor, T. pretiosum, N. vitripennis (Hauser et al, 2010 ) and P. puparum (Xu et al, 2020 ), neither allatotropin (AT), inotocin, CCHamide (CCHa), neuropeptide F (NPF) nor pigment dispersing factor (PDF) were found in the transcriptome databases of H. hebtor ( Tables 1 , 2 , Supplementary Table 1 ). Both allatostatin C (AstC) and allatostatin B (AstB) were missing in several wasp species analyzed in this study, namely P. puparum, N. vitripennis, A. mellifera , and H. hebetor , but the two were present in D. melanogaster, B. mori , and T. castaneum ( Table 2 , Supplementary Table 1 ).…”

“…In this study, we identified two receptors in H. hebetor that belonged to the RTKs ( Figure 8 ), both being orthologs of the ILP receptor (InR). A phylogenetic analysis indicated that the NP receptor and InR are closely related (Xu et al, 2020 ).…”

“…With the development of next-generation sequencing technology, here we identified a complete set of neuropeptide genes and interrelated receptor genes via genomic and transcriptomic sequencing of H. hebetor . Building on this, we then compared them with those annotated in representative species of different insect orders, including the wasp parasitoids Nasonia vitripennis (Hauser et al, 2010 ) and Pteromalus puparum (Xu et al, 2020 ), the bee Apis mellifera (Hummon et al, 2006 ), the fly Drosophila melanogaster (Broeck, 2001 ), the moth Bombyx mori (Roller et al, 2008 ), the beetle Tribolium castaneum (Li et al, 2008 ), and an hemipteran insect: Nilaparvata lugens (Tanaka et al, 2014 ). In this study, we identified 34 neuropeptide candidate genes and 44 neuropeptide candidate receptor genes in H. hebetor .…”