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Proteo-Transcriptomic Characterization of Sirex nitobei (Hymenoptera: Siricidae) Venom.

ABSTRACT: The wood-boring woodwasp Sirex nitobei is a native pest in Asia, infecting and weakening the host trees in numerous ecological and commercial coniferous forest plantations. In China, hosts of S. nitobei are diverse, so the pest has spread to several provinces of China, resulting in considerable economic and ecological damage. During female oviposition, S. nitobei venom along with arthrospores of the symbiotic fungus Amylostereum areolatum or A. chaetica is injected into host trees, and the combination of these two biological factors causes the death of xylem host trees. The presence of venom alone causes only the yellowing and wilting of needles. In this study, we constructed the venom gland transcriptome of S. nitobei for the first time and a total of 15,036 unigenes were acquired. From the unigenes, 11,560 ORFs were identified and 537 encoding protein sequences with signal peptides at the N-terminus. Then, we used the venomics approach to characterize the venom composition of female S. nitobei and predicted 1095 proteins by liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis. We focused on seven proteins that were both highly expressed in the venom gland transcriptome and predicted in the crude venom proteome. These seven proteins are laccase-2, laccase-3, a protein belonging to the Kazal family, chitooligosaccharidolytic β-N-acetylglucosaminidase, beta-galactosidase, icarapin-like protein, and waprin-Thr1-like protein. Using quantitative real-time PCR (qRT-PCR), we also proved that the genes related to these seven proteins are specifically expressed in the venom glands. Finally, we revealed the functional role of S. nitobei venom in the physiological response of host trees. It can not only promote the colonization of symbiotic fungus but contribute to the development of eggs and larvae. This study provides a deeper understanding of the molecular mechanism of the woodwasp-pine interaction.

SUBMITTER: Gao C

PROVIDER: S-EPMC8402507 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe woodwasp Sirex noctilio Fabricius is a major quarantine pest worldwide that was first discovered in China in 2013 and mainly harms Pinus sylvestris var. mongolica Litv.. S. nitobei Matsumura is a native species in China and is closely related to S. noctilio. Recently, the two woodwasps species were found attacking the P. sylvestris var. mongolica Litv in succession. The olfactory system is the foundation of insect behavior. Olfactory genes were identified through antennal transcriptome analysis. The expression profiles odorant binding proteins (OBPs) were analyzed with RT-qPCR.ResultsFrom our transcriptome analysis, 16 OBPs, 7 chemosensory proteins (CSPs), 41 odorant receptors (ORs), 8 gustatory receptors (GRs), 13 ionotropic receptors (IRs), and one sensory neuron membrane protein (SNMP) were identified in S. noctilio, while 15 OBPs, 6 CSPs, 43 ORs, 10 GRs, 16 IRs, and 1 SNMP were identified in S. nitobei. Most of the olfactory genes identified in two species were homologous. However, some species-specific olfactory genes were identified from the antennal transcriptomes, including SnocOBP13, SnocCSP6, SnocOR26, SnocGR2, SnocIR7 in S. noctilio and SnitGR9, SnitGR11, SnitIR17 in S. nitobei. In total, 14 OBPs were expressed primarily in the antennae. SnocOBP9 and SnitOBP9, identified as PBP homologues, were sex-biased expression in two siricid, but with different pattern. SnocOBP11 and SnitOBP11 were highly expressed in antennae and clearly expressed in external genitalia. SnocOBP7 and SnitOBP7 were highly expressed in male genitalia. SnocOBP3 and SnocOBP10 were highly expressed in female genitalia and male heads, while SnitOBP3 and SnitOBP10 did not show obvious tissue bias.ConclusionWe analyzed 86 and 91 olfactory genes from S. noctilio and S. nitobei, respectively. Most of the olfactory genes identified were homologous, but also some species-specific olfactory genes were identified, which indicated the similarities and differences of the molecular mechanisms between the two closely-related species. Different expression in the antennae, external genitals or heads, exhibiting an obvious sex bias, suggested their different role in recognizing sex pheromones or plant volatiles. Species-specific expression for several OBPs genes may suggest that they strengthened or lost their original function during species differentiation, resulting in olfactory differences between the two species.

Project description:The European woodwasp, Sirex noctilio Fabricius, is a major invasive quarantine pest that attacks and kills pine trees outside of its native range. Insect gut structure and gut microbiota play crucial roles in various life activities. Despite a few reports in nutrition and survival, an extensive study on the S. noctilio larval gut microbiome is lacking. We studied the gut structure using a stereo microscope and used high throughput sequencing of the bacterial 16S rRNA genes and fungal internal transcribed spacer 2 (ITS2) regions to investigate gut microbiota in different developmental stages of S. noctilio, including larvae, adults, and larval frass. We used PICRUSt2 to predict the functional profiles. The larval gut was thin and thread-like from the oral cavity to the anus, carrying few xylem particles in the crop. Pseudomonas, Ralstonia, and Burkholderia s.l were the dominant bacteria in the guts of larvae, adults, and frass, respectively. Even though Pseudomonas was the most abundant among all bacteria, Zoogloea, Ruminobacter, and Nitrosospira, which might be involved in degrading organic matter and fixing nitrogen occurred exclusively in the larval gut indicating their possible role in the growth and development of larvae in pine tree xylem. Fungal communities did not change significantly across different developmental stages or the frass. Amylostereum was dominant in the woodwasp's larval gut. Functional prediction of bacterial and fungal communities revealed that they may encod enzymes involved in degrading lignocellulose and fixing nitrogen. Ours is the first study that compares gut microbial communities present in S. noctilio larvae, adults, and frass. This study could provide an understanding of larval nutrient acquisition in nutrient-deficient host xylem to some extent. Our study may unlock novel strategies for the development of pest management approaches based on interfering with the gut microbiota and restricting their role in larval survival and development.

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Proteo-Transcriptomic Characterization of Sirex nitobei (Hymenoptera: Siricidae) Venom.

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