Partial venom gland transcriptome of a Drosophila parasitoid wasp, Leptopilina heterotoma, reveals novel and shared bioactive profiles with stinging Hymenoptera

Abstract

Analysis of natural host-parasite relationships reveals the evolutionary forces that shape the delicate and unique specificity characteristic of such interactions. The accessory long gland-reservoir complex of the wasp Leptopilina heterotoma (Figitidae) produces venom with virus-like particles. Upon delivery, venom components delay host larval development and completely block host immune responses. The host range of this Drosophila endoparasitoid notably includes the highly-studied model organism, Drosophila melanogaster. Categorization of 827 unigenes, using similarity as an indicator of putative homology, reveals that approximately 25% are novel or classified as hypothetical proteins. Most of the remaining unigenes are related to processes involved in signaling, cell cycle, and cell physiology including detoxification, protein biogenesis, and hormone production. Analysis of L. heterotoma's predicted venom gland proteins demonstrates conservation among endo- and ectoparasitoids within the Apocrita (e.g., this wasp and the jewel wasp Nasonia vitripennis) and stinging aculeates (e.g., the honey bee and ants). Enzyme and KEGG pathway profiling predicts that kinases, esterases, and hydrolases may contribute to venom activity in this unique wasp. To our knowledge, this investigation is among the first functional genomic studies for a natural parasitic wasp of Drosophila. Our findings will help explain how L. heterotoma shuts down its hosts' immunity and shed light on the molecular basis of a natural arms race between these insects.

Keywords: A; APIME; Acph/ACPH; Apis mellifera; Asp–Tyr–Asp; C; CBP; CDD; CO(2); CUNY; City University of New York; Conserved Domain Database; DNA; Drosophila; EBI; EC; EST; Enzyme Commission; European Bioinformatics Institute; Expressed Sequence Tags database; FA; Functional genomics; G; GEF; Glu–Cys; IgE; JAK-STAT; JH; Janus kinase-signal transducer and activator of transcription; KAAS; KEGG; KEGG Automatic Annotation Server; Kyoto Encyclopedia of Genes and Genomes; Leptopilina heterotoma; Lh; MAP; MRJP; MUSCLE; Multiple Sequence Comparison by Log-Expectation; N; NCBI; NF-kappa B; NIH; NRI; NSF; National Center for Biotechnology Information; National Institutes of Health; National Research Initiative; National Science Foundation; OBP; ORF; PBP_BOBP; PCR; PDV; PF; PKG; PLB; PRIAM; PSI; PTM; Parasitoid; Pfam accession number; Position-Specific Iterated; Profils pour l'Identification Automatique du Métabolisme; RISE; RNA; RNA Recognition Motif; RRM; Research Initiative for Scientific Enhancement; SMART; STKc-PKA; Ser/Thr; Serine/Threonine Kinase, cAMP-dependent Protein Kinase; Simple Modular Architecture Research Tool; T; TCA; Transcriptome; USDA; United States Department of Agriculture; VLP; Venom gland; acid phosphatase; adenosine; any nucleotide; aspartate–tyrosine–aspartate; base pair; bp; cDNA; cGMP; carbon dioxide; chemosensory-binding protein; complementary deoxyribonucleic acid; cyclic guanosine monophosphate; cyclic guanosine monophosphate-dependent protein kinase; cytidine; dbEST; deoxyribonucleic acid; dir; direct; expressed sequence tag; farnesoic acid; for; foraging gene; glutamate–cysteine; guanine nucleotide exchange factor; guanosine; h; hours; immunoglobulin E; juvenile hormone; kD; kiloDalton; major royal jelly protein; mer; microgram; milliliter; mitogen-activated protein; ml; nanogram; ng; non-redundant; nr; nuclear factor kappa-light-chain-enhancer of activated B cells; odorant-binding protein; open reading frame; pheromone-binding protein/general odorant-binding protein; phospholipase B; poly adenosine monophosphate; polyA; polyDNA virus; polymerase chain reaction; post-translation modification; repeating unit; rev; reverse; ribonucleic acid; serine/threonine; species pluralis; spp.; thymidine; tricarboxylic acid; virus-like particle; w; white; y; yellow; μg.

Figure 1. Sequence classifications using taxonomic binning

Sequences are classified (a) by order, and (b) by species among Apocrita based on highest similarity between proteins

Figure 1. Sequence classifications using taxonomic binning

Sequences are classified (a) by order, and (b) by species among Apocrita based on highest similarity between proteins

Figure 2. Enzymatic function profile

Predicted functionality by Enzyme Commission (E.C.) number. Number descriptions given in Table 1.

Figure 3. KEGG profile

Predicted functionality by KEGG descriptions for the major pathways, systems, and functions. Only those groups with more than three transcripts are shown. (Ub: Ubiquitination; PTM: Post-Translational Modification; Ox: Oxidative).