The bark beetle, Ips typographus (L.), is a major pest of Norway spruce, Picea abies (L.), causing enormous economic losses globally. The adult stage of the I. typographus has a complex life cycle (callow and sclerotized); the callow beetles feed ferociously, whereas sclerotized male beetles are more aggressive and pioneers in establishing new colonies. We conducted a comparative proteomics study to understand male and female digestion and detoxification processes in callow and sclerotized beetles. Proteome profiling was performed using high-throughput liquid chromatography-mass spectrometry. A total of >3000 proteins were identified from the bark beetle gut, and among them, 539 were differentially abundant (fold change ±2, FDR <0.05) between callow and sclerotized beetles. The differentially abundant proteins (DAPs) mainly engage with binding, catalytic activity, anatomical activity, hydrolase activity, metabolic process, and carbohydrate metabolism, and hence may be crucial for growth, digestion, detoxification, and signalling. We validated selected DAPs with RT-qPCR. Gut enzymes such as NADPH-cytochrome P450 reductase (CYC), glutathione S-transferase (GST), and esterase (EST) play a crucial role in the I. typographus for detoxification and digesting of host allelochemicals. We conducted enzyme activity assays with them and observed a positive correlation of CYC and GST activities with the proteomic results, whereas EST activity was not fully correlated. Furthermore, our investigation revealed that callow beetles had an upregulation of proteins associated with juvenile hormone (JH) biosynthesis and chitin metabolism, whereas sclerotized beetles exhibited an upregulation of proteins linked to fatty acid metabolism and the TCA cycle. These distinctive patterns of protein regulation in metabolic and functional processes are specific to each developmental stage, underscoring the adaptive responses of I. typographicus in overcoming conifer defences and facilitating their survival. Taken together, it is the first gut proteomic study comparing males and females of callow and sclerotized I. typographus, shedding light on the adaptive ecology at the molecular level. Furthermore, the information about bark beetle handling of nutritionally limiting and defence-rich spruce phloem diet can be utilized to formulate RNAi-mediated beetle management.

Comparative gut proteomics study revealing adaptive physiology of Eurasian spruce bark beetle, Ips typographus (Coleoptera: Scolytinae)

Nilaparvata lugens proclotting enzymes (NlPCEs) belong to the clip domain serine protease (clip-SP) family, which is a characteristic protease family in arthropods. NlPCE3 was previously reported to regulate egg production and development in female N. lugens, but its role in male N. lugens is unclear. In the present study, qPCR analysis showed that NlPCE3 was expressed in three different tissues (gut, testis and fat body). RNAi revealed that dsNlPCE3 injection made the male vas deferens thinner and reduced the oviposition level of the females that mated with dsNlPCE3-treated males, causing eggs not to hatch. Furthermore, immunofluorescence staining showed that NlPCE3 was widely expressed in the male internal genitalia. However, after dsNlPCE3 injection, expression of NlPCE3 was diffuse in the male internal genitalia, whose peripheral cells seemed degraded. Overall, these results indicate that NlPCE3 is important for reproduction in male N. lugens.

PCE3 Plays a Role in the Reproduction of Male Nilaparvata lugens.

BACKGROUND
Previous studies of brown planthopper (BPH), Nilaparvata lugens, showed that carrying the plant pathogenic virus, rice ragged stunt virus (RRSV), enhanced the lethality of the entomopathogenic fungus, Metarhizium anisopliae (YTTR). The underlying mechanism for this was not established but a serine protease cascade was hypothesized to be involved.


RESULTS
Two immune response genes, NlKPI and NlVenomase, were identified and shown to be involved. Synthesized dsRNA techniques used in this study to explore gene function revealed that treatment with dsRNA to silence either gene led to a higher BPH mortality from M. anisopliae infection than the dsRNA control treatment. NlKPI and NlVenomase play vital roles in BPH immunity to defend against alien pathogens. And both genes participate in the immune response process of BPHs against co-infection with RRSV and M. anisopliae YTTR by regulating the expression of antimicrobial peptides and phenoloxidase activity.


CONCLUSION
Our study provided new targets for BPH biocontrol and laid a solid foundation for further research on the interaction of "plant virus- insect vector- entomopathogenic fungus". This article is protected by copyright. All rights reserved.

The immune response mechanism of Nilaparvata lugens against a combined infection of rice ragged stunt virus and Metarhizium anisopliae.

Plant viruses and entomopathogenic fungi (EPF) can both elicit immune responses in insects. This study was designed to clarify whether plant viruses could affect the efficacy of EPF and explore the immune responses of brown planthopper (BPH), Nilaparvata lugens, in response to different pathogen infections. In this study, a strain of Metarhizium anisopliae YTTR with high pathogenicity against BPH was selected and explored whether rice ragged stunt virus (RRSV) could affect its lethality against BPH. RNA-seq was used to detect the inner responses of BPH in response to RRSV and M. anisopliae YTTR infection. Results showed that M. anisopliae YTTR has strong lethality against BPH (RRSV-carrying and RRSV-free). RRSV invasion did not affect the susceptibility of BPH against M. anisopliae YTTR at all concentrations. At 1 × 108 spores/mL, M. anisopliae YTTR caused a cumulative mortality of 80% to BPH at 7 days post-treatment. The largest numbers of differentially expressed genes (DEGs) was obtained in BPH treated with the two pathogens than in other single pathogen treatment. In addition, KEGG enrichment analysis showed that the DEGs were mostly enriched in immune and physiological mechanisms-related pathways. Both RRSV and M. anisopliae YTTR could induce the expression changes of immune-related genes. However, most of the immune genes had varying expression patterns in different treatment. Our findings demonstrated that RRSV invasion did not have any significant effect on the pathogenicity of M. anisopliae YTTR, while the co-infection of M. anisopliae YTTR and RRSV induced more immune and physiological mechanisms -related genes’ responses. In addition, the presence of RRSV could render the interplay between BPH and M. anisopliae YTTR more intricate. These findings laid a basis for further elucidating the immune response mechanisms of RRSV-mediated BPH to M. anisopliae infection.

/pdf/immune-responses-and-transcriptomic-analysis-of-nilaparvata-gvllex1u.pdf

Immune Responses and Transcriptomic Analysis of Nilaparvata lugens against Metarhizium anisopliae YTTR Mediated by Rice Ragged Stunt Virus

Trypsin is one of the most diverse and widely studied protease hydrolases. However, the diversity and characteristics of the Trypsin superfamily of genes have not been well understood, and their role in insecticide resistance is yet to be investigated. In this study, a total of 342 Trypsin genes were identified and classified into seven families based on homology, characteristic domains and phylogenetics in Anopheles sinensis, and the LY-Domain and CLECT-Domain families are specific to the species. Four Trypsin genes, (Astry2b, Astry43a, Astry90, Astry113c) were identified to be associated with pyrethroid resistance based on transcriptome analyses of three field resistant populations and qRT-PCR validation, and the knock-down of these genes significantly decrease the pyrethroid resistance of Anopheles sinensis based on RNAi. The activity of Astry43a can be reduced by five selected insecticides (indoxacarb, DDT, temephos, imidacloprid and deltamethrin); and however, the Astry43a could not directly metabolize these five insecticides, like the trypsin NYD-Tr did in earlier reports. This study provides the overall information frame of Trypsin genes, and proposes the role of Trypsin genes to insecticide resistance. Further researches are necessary to investigate the metabolism function of these trypsins to insecticides. 

Characteristics of Trypsin genes and their roles in insecticide resistance based on omics and functional analyses in the malaria vector Anopheles sinensis

Clip domain serine proteases play vital roles in various innate immune functions and in embryonic development. Nilaparvata lugens proclotting enzymes (NlPCEs) belong to this protease family. NlPCE1 was reported to be involved in innate immunity, whereas the role of other NlPCEs is unclear. In the present study, N. lugens proclotting enzyme-3 (NlPCE3) was cloned and characterized. NlPCE3 contains a signal peptide, a clip domain, and a trypsin-like serine protease domain. NlPCE3 was expressed in all tissues examined (gut, fat body, and ovary), and at all developmental stages. Immunofluorescence staining showed that NlPCE3 was mainly expressed in the cytoplasm and cytomembrane of follicular cells. Double stranded NlPCE3 RNA interference clearly inhibited the expression of NlPCE3, resulting in abnormal egg formation and obstruction of ovulation. These results indicate that NlPCE3 plays an important role in egg production in N. lugens.

https://www.mdpi.com/2075-4450/10/11/378/pdf

A Clip Domain Serine Protease Involved in Egg Production in Nilaparvata lugens: Expression Patterns and RNA Interference

Simple Summary The brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae), is a destructive insect pest of rice. It causes reductions in rice yield and great economic losses. In this study, we used RNAi to explore the function of the inter-alpha-trypsin inhibitor heavy chain 4 (ITIH4) gene in the development and reproduction of the brown planthopper. Our results revealed that ITIH4 influences the survival, ovarian development, egg production, and egg hatching of this insect, indicating that ITIH4 plays important roles in development and reproduction. Considering the importance of ITIH4 in the brown planthopper, it may be a potential target for pest management. Abstract The brown planthopper, Nilaparvata lugens, is a difficult-to-control insect pest affecting rice yields in Asia. As a structural component of the inter-alpha-trypsin inhibitor (ITI), the inter-alpha-trypsin inhibitor heavy chain (ITIH) has been reported to be involved in various inflammatory or malignant disorders, ovarian development, and ovulation. To reveal the function of ITIH4 in N. lugens, the gene encoding N. lugens ITIH4 (NlITIH4) was cloned and characterized. NlITIH4 contains a signal peptide, a vault protein inter-alpha-trypsin domain, and a von Willebrand factor type A domain. qPCR analysis showed that NlITIH4 was expressed at all developmental stages and in all tissues (fat body, ovary, and gut), with the highest expression in the fat body. Double stranded NlITIH4 (dsNlITIH4) injection clearly led to an RNAi-mediated inhibition of the expression of NlITIH4 and resulted in reduced survival, delayed ovarian development, and reduced egg production and egg hatching. These results indicate that NlITIH4 plays an important role in the development and reproduction of N. lugens.

/pdf/inter-alpha-trypsin-inhibitor-heavy-chain-4-plays-an-1yr1a2k1.pdf

Inter-Alpha-Trypsin Inhibitor Heavy Chain 4 Plays an Important Role in the Development and Reproduction of Nilaparvata lugens

SLC26A10 is a member of the SLC26 gene family, but its role in insects is still unclear. We cloned the SLC26A10 gene of Nilaparvata lugens (NlSLC26A10) and found NlSLC26A10 contained 11 transmembrane regions and a STAS domain. Expression pattern analysis showed NlSLC26A10 expression was more upregulated in adults than in nymphs, highest in the ovary. After injection of double-stranded RNA (dsRNA) of NlSLC26A10, the mRNA level of NlSLC26A10 significantly decreased and, consequently, the ovarian development of adult females was hindered; the amount and the hatchability of eggs and yeast-like symbionts in mature oocytes decreased. Further study showed that NlSLC26A10 might result in decreased juvenile hormone level and vitellogenin expression. These results indicate that NlSLC26A10 plays an essential role in the reproduction of N. lugens.

/pdf/molecular-characterization-and-rna-interference-analysis-of-1c2yrpcd.pdf

Molecular Characterization and RNA Interference Analysis of SLC26A10 From Nilaparvata lugens (Stål)

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A Clip Domain Serine Protease Involved in Egg Production in Nilaparvata lugens: Expression Patterns and RNA Interference

PCE3 Plays a Role in the Reproduction of Male Nilaparvata lugens.

Inter-Alpha-Trypsin Inhibitor Heavy Chain 4 Plays an Important Role in the Development and Reproduction of Nilaparvata lugens

Molecular Characterization and RNA Interference Analysis of SLC26A10 From Nilaparvata lugens (Stål)