An expanded odorant-binding protein mediates host cue detection in the parasitic wasp Baryscapus dioryctriae basis of the chromosome-level genome assembly analysis

Abstract

Background: Baryscapus dioryctriae (Chalcidodea: Eulophidae) is a parasitic wasp that parasitizes the pupae of many Pyralidae members and has been used as a biological control agent against Dioryctria pests of pinecones.

Results: This B. dioryctriae assembly has a genome size of 485.5 Mb with a contig N50 of 2.17 Mb, and scaffolds were assembled onto six chromosomes using Hi-C analysis, significantly increasing the scaffold N50 to 91.17 Mb, with more than 96.13% of the assembled bases located on chromosomes, and an analysis revealed that 94.73% of the BUSCO gene set. A total of 54.82% (279.27 Mb) of the assembly was composed of repetitive sequences and 24,778 protein-coding genes were identified. Comparative genomic analysis demonstrated that the chemosensory perception, genetic material synthesis, and immune response pathways were primarily enriched in the expanded genes. Moreover, the functional characteristics of an odorant-binding protein (BdioOBP45) with ovipositor-biased expression identified from the expanded olfactory gene families were investigated by the fluorescence competitive binding and RNAi assays, revealing that BdioOBP45 primarily binds to the D. abietella-induced volatile compounds, suggesting that this expanded OBP is likely involved in locating female wasp hosts and highlighting a direction for future research.

Conclusions: Taken together, this work not only provides new genomic sequences for the Hymenoptera systematics, but also the high-quality chromosome-level genome of B. dioryctriae offers a valuable foundation for studying the molecular, evolutionary, and parasitic processes of parasitic wasps.

Keywords: Baryscapus dioryctriae; Hi‐C; Odorant-binding protein; Parasitic wasp.

Fig. 1

Life cycle of the parasitoid wasp B. dioryctriae on its alternative host Galleria mellonella. Female wasps lay eggs in the host chrysalis

Fig. 2

Comprehensive genomic insights and chromosomal synteny of B. dioryctriae in comparison with C. cunea and N. vitripennis. A Genome landscape of the parasitoid wasp B. dioryctriae. From the outer to inner circles: (a) six chromosomes at the Mb scale; (b, c, and d) TE density, SSR density, and gene density across the genome; (e) CG contents across the genome. B Karyograms of B. dioryctriae. C Chromosome synteny based on CDS pairwise alignment between B. dioryctriae, C. cunea, and N. vitripennis. The colored lines indicate shared syntenic blocks

Fig. 3

Comparative genomic analysis of the parasitoid wasp B. dioryctriae. A A maximum-likelihood phylogenetic tree is shown for B. dioryctriae with 13 hymenopteran insects. The phylogenetic tree was based on 1265 single-copy proteins. A. rosae was used as the outgroup. The bootstrap value of all nodes is supported at 100/100. The numbers of expanded (green) and contracted (pink) gene families are shown on the branches. B The GO and KEGG enrichment results of B. dioryctriae difficile-expanded genes are summarized and visualized as scatter plots

Fig. 4

Genome-wide analysis of odorant-binding proteins and gene expression patterns in B. dioryctriae with a focus on OG0000305 and OG000696. A Odorant-binding proteins in the B. dioryctriae genome. B Gene expression of OG0000305. C Gene expression of OG000696. FA and MA: female and male antennae; FH and MH: female and male heads without antennae; Fab: female abdomens without ovipositors and digestive tracts; Fov: female ovipositors; Mge: male genitalia; Mab: male abdomens without genitalia and digestive tracts; T: male and female thoraxes; L: male and female legs

Fig. 5

Binding analysis of recombinant BdioOBP45 to candidate ligands. A The binding curve of 1-NPN to recombinant BdioOBP45 and the Scatchard plot. B Binding curves for BdioOBP45 binding to four ligands

Fig. 6

In vivo functional investigation of BdioOBP45. A Behavioral experiment device diagram for B. dioryctriae. B Behavioral responses of B. dioryctriae adults to three ligands of BdioOBP45. C Relative expression levels of BdioOBP45 at 12 h, 24 h, 36 h, and 48 h after microinjection of double-stranded RNA (dsRNA) into wasps. Asterisks on the top portion of the bars show that the values differed significantly; that is, columns labeled with different letters are significantly different (P < 0.05). D Behavioral response of B. dioryctriae BdioOBP45-silenced adult wasps to g-terpinene and α-pinene