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Confirmation of Oryctes rhinoceros nudivirus infections in G-haplotype coconut rhinoceros beetles (Oryctes rhinoceros) from Palauan PCR-positive populations.

ABSTRACT: Coconut rhinoceros beetle (CRB), Oryctes rhinoceros, is a pest of palm trees in the Pacific. Recently, a remarkable degree of palm damage reported in Guam, Hawaii, Papua New Guinea and Solomon Islands has been associated with a particular haplotype (clade I), known as "CRB-G". In the Palau Archipelago, both CRB-G and another haplotype (clade IV) belonging to the CRB-S cluster coexist in the field. In this study, more than 75% of pheromone trap-captured adults of both haplotypes were Oryctes rhinoceros nudivirus (OrNV)-positive by PCR. No significant difference in OrNV prevalence between the haplotypes was detected. In PCR-positive CRB-G tissue specimens from Palau, viral particles were observed by electron microscopy. Hemocoel injection of CRB larvae with crude virus homogenates from these tissues resulted in viral infection and mortality. OrNV isolated from Palauan-sourced CRB was designated as OrNV-Palau1. Both OrNV-Palau1 and OrNV-X2B, a CRB biological control isolate released in the Pacific, were propagated using the FRI-AnCu-35 cell line for production of inoculum. However, the OrNV-Palau1 isolate exhibited lower viral production levels and longer larval survival times compared to OrNV-X2B in O. rhinoceros larvae. Full genome sequences of the OrNV-Palau1 and -X2B isolates were determined and found to be closely related to each other. Altogether these results suggest CRB adults in Palau are infected with a less virulent virus, which may affect the nature and extent of OrNV-induced pathology in Palauan populations of CRB.

SUBMITTER: Tanaka S

PROVIDER: S-EPMC8452681 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Oryctes rhinoceros nudivirus (OrNV) is a double-stranded DNA (dsDNA) virus which has been used as a biocontrol agent to suppress the coconut rhinoceros beetle (Oryctes rhinoceros) in Southeast Asia and the Pacific Islands. A new wave of O. rhinoceros incursions in Oceania is thought to be related to the presence of low-virulence isolates of OrNV or virus-tolerant haplotypes of beetles. In this study, chronically infected beetles were collected from Philippines, Fiji, Papua New Guinea (PNG), and the Solomon Islands (SI). RNA sequencing (RNA-seq) was performed to investigate the global viral gene expression profiles and for comparative genomic analysis of structural variations. Maximum likelihood phylogenic analysis indicated that OrNV strains from the SI and Philippines are closely related, while OrNV strains from PNG and Fiji formed a distinct adjacent clade. We detected several polymorphic sites with a frequency higher than 35% in 892 positions of the viral genome. Nonsynonymous mutations were detected in several hypothetical proteins and 15 nudivirus core genes, such as gp034, lef-8, lef-4, and vp91 We found limited evidence of variation in viral gene expression among geographic populations. Only a few genes, such as gp01, gp022, and gp107, were differentially expressed among different strains. Additionally, small RNA sequencing from the SI population suggested that OrNV is targeted by the host RNA interference (RNAi) response with abundant 21-nucleotide small RNAs. Some of these genomic changes are specific to the geographic population and could be related to particular phenotypic characteristics of the strain, such as viral pathogenicity or transmissibility, and this requires further investigation.IMPORTANCE Oryctes rhinoceros nudivirus has been an effective biocontrol agent against the coconut rhinoceros beetle in Southeast Asia and the Pacific Islands for decades. The recent outbreak of these beetles in many South Pacific islands has had a significant impact on livelihoods in the region. It has been suggested that the resurgence and spread of the pest are related to the presence of low-virulence isolates of OrNV or virus-tolerant haplotypes of beetles. We examined viral genomic and transcriptional variations in chronically infected beetles from different geographical populations. A high number of polymorphic sites among several geographical strains of OrNV were identified, but potentially only a few of these variations in the genome are involved in functional changes and can potentially alter the typical function. These findings provide valuable resources for future studies to improve our understanding of the OrNV genetic variations in different geographic regions and their potential link to virus pathogenicity.

Project description:Incursions of the coconut rhinoceros beetle (CRB), Oryctes rhinoceros, into different islands in the South Pacific have been detected in recent years. It has been suggested that this range expansion is related to an O. rhinoceros haplotype reported to show reduced susceptibility to the well-established classical biocontrol agent, Oryctes rhinoceros nudivirus (OrNV). Our understanding of the genetic characteristics which distinguish the population of O. rhinoceros that has recently established in Solomon Islands from other well-established populations across the region is very limited. Here, we hypothesized that the recently established O. rhinoceros population should have greater innate immune responses when challenged by OrNV than those of well-established and native O. rhinoceros populations. We used the RNA sequencing (RNA-Seq) approach to generate gene expression profiles of midgut tissue from OrNV-infected and noninfected individuals collected in the Solomon Islands (recent incursion), Papua New Guinea and Fiji (previously established), and the Philippines (within the native range). The collections included individuals from each of the three major mitochondrial lineages (CRB-G, CRB-PNG, and CRB-S) known to the region, allowing us to explore the specific responses of each haplotype to infection. Although insects from the Philippines and Solomon Islands that were tested belong to the same mitochondrial lineage (CRB-G), their overall responses to infection were different. The number of differentially expressed genes between OrNV-infected and noninfected wild-caught individuals from the four different locations varied from 148 to 252. Persistent OrNV infection caused a high level of induced antimicrobial activity and immune responses in O. rhinoceros, but the direction and magnitude of the responses were population specific. The insects tested from the Solomon Islands displayed extremely high expression of genes which are known to be involved in immune responses (e.g. coleoptericin, cecropin, and serpin). These variations in the host immune system among insects from different geographical regions might be driven by variations in the virulence of OrNV isolates, and this requires further investigation. Overall, our current findings support the importance of immunity in insect pest incursion and an expansion of the pest's geographic range. IMPORTANCE Oryctes rhinoceros nudivirus (OrNV) is a double-stranded DNA (dsDNA) virus which has been used as a biocontrol agent to suppress coconut rhinoceros beetle (CRB) in the Pacific Islands. Recently a new wave of CRB incursions in Oceania is thought to be related to the presence of low-virulence isolates of OrNV or virus-tolerant haplotypes of beetles (CRB-G). Our comparative analysis of OrNV-infected and noninfected CRBs revealed that specific sets of genes were induced by viral infection in the beetles. This induction was much stronger in beetles collected from the Solomon Islands, a newly invaded country, than in individuals collected from within the beetle's native range (the Philippines) or from longer-established populations in its exotic range (Fiji and Papua New Guinea [PNG]). Beetles from the Philippines and the Solomon Islands that were tested in this study all belonged to the CRB-G haplotype, but the country-specific responses of the beetles to OrNV infection were different.

Project description:Recently, incursions of the Coconut rhinoceros beetle (CRB), Oryctes rhinoceros, have been detected in south Pacific countries that were previously free of the pest. It has been suggested that this range expansion is related to an O. rhinoceros haplotype that is reported to show reduced susceptibility to the well-established classical biocontrol agent, Oryctes rhinoceros nudivirus (OrNV). We investigated O. rhinoceros population genetics and the OrNV status of specimens collected in Fiji, New Caledonia, Papua New Guinea (PNG), Samoa, Solomon Islands, Tonga, Vanuatu and the Philippines. Based on the sequence of the mitochondrial CoxI gene, we found three major mitochondrial haplotype groups (CRB-G, CRB-PNG and CRB-S) across the region. Haplotype diversity varied between and within countries and a high incidence of OrNV infection was detected in all haplotypes wherever they occurred. The O. rhinoceros population in some countries was monotypic and all individuals tested belonged to a single haplotype group. However, in Samoa we detected CRB-S and CRB-PNG and in Solomon Islands we detected all three haplotype groups. Genotyping-by-Sequencing (GBS) showed genetic differentiation in the O. rhinoceros nuclear genome across populations on different islands and provided evidence for gene flow, resulting in a well-mixed population, despite the presence of different CoxI haplotypes in Solomon Islands. Evidence of admixture was also detected on both islands of Samoa. The current CoxI based method is not a reliable diagnostic marker for phenotypic traits, especially in countries such as Solomon Islands where the mitochondrial haplotypes have come back into sympatry and are mixed. To identify possible mechanisms of resistance to OrNV, further molecular analyses O. rhinoceros in response to virus infection is required. To improve biological control of O. rhinoceros, such analyses will need to be combined with an improved understanding of the population genetics of the pest and the evolutionary history of OrNV in the region.

Dataset Information

Confirmation of Oryctes rhinoceros nudivirus infections in G-haplotype coconut rhinoceros beetles (Oryctes rhinoceros) from Palauan PCR-positive populations.

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