Dataset Information

Genome-Wide Profiling of Diadegma semiclausum Ichnovirus Integration in Parasitized Plutella xylostella Hemocytes Identifies Host Integration Motifs and Insertion Sites.

ABSTRACT: Polydnaviruses (PDVs), classified into two genera, bracoviruses (BVs) and ichnoviruses (IVs), are large, double-stranded DNA viruses, which are beneficial symbionts of parasitoid wasps. PDVs do not replicate in their infected lepidopteran hosts. BV circles have been demonstrated to be integrated into host genomic DNA after natural parasitization. However, the integrations of IV circles in vivo remain largely unknown. Here, we analyzed the integration of Diadegma semiclausum ichnovirus (DsIV) in the genomic DNA of parasitized Plutella xylostella hemocytes. We found that DsIV circles are present in host hemocytes with non-integrated and integrated forms. Moreover, DsIV integrates its DNA circles into the host genome by two distinct strategies, conservatively, and randomly. We also found that four conserved-broken circles share similar motifs containing two reverse complementary repeats at their breaking sites, which were host integration motifs (HIMs). We also predicted HIMs of eight circles from other ichnoviruses, indicating that a HIM-mediated specific mechanism was conserved in IV integrations. Investigation of DsIV circle insertion sites of the host genome revealed the enrichment of microhomologies between the host genome and the DsIV circles at integration breakpoints. These findings will deepen our understanding of the infections of PDVs, especially IVs.

SUBMITTER: Wang ZH

PROVIDER: S-EPMC7843510 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Genome-Wide Profiling of Diadegma semiclausum Ichnovirus Integration in Parasitized Plutella xylostella Hemocytes Identifies Host Integration Motifs and Insertion Sites.

Wang Ze-Hua ZH Zhou Yue-Nan YN Yang Jing J Ye Xi-Qian XQ Shi Min M Huang Jian-Hua JH Chen Xue-Xin XX

Frontiers in microbiology 20210115

Polydnaviruses (PDVs), classified into two genera, bracoviruses (BVs) and ichnoviruses (IVs), are large, double-stranded DNA viruses, which are beneficial symbionts of parasitoid wasps. PDVs do not replicate in their infected lepidopteran hosts. BV circles have been demonstrated to be integrated into host genomic DNA after natural parasitization. However, the integrations of IV circles in vivo remain largely unknown. Here, we analyzed the integration of Diadegma semiclausum ichnovi ...[more]

PMID: 33519757

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Project description:BackgroundParasitoid insects manipulate their hosts' physiology by injecting various factors into their host upon parasitization. Transcriptomic approaches provide a powerful approach to study insect host-parasitoid interactions at the molecular level. In order to investigate the effects of parasitization by an ichneumonid wasp (Diadegma semiclausum) on the host (Plutella xylostella), the larval transcriptome profile was analyzed using a short-read deep sequencing method (Illumina). Symbiotic polydnaviruses (PDVs) associated with ichneumonid parasitoids, known as ichnoviruses, play significant roles in host immune suppression and developmental regulation. In the current study, D. semiclausum ichnovirus (DsIV) genes expressed in P. xylostella were identified and their sequences compared with other reported PDVs. Five of these genes encode proteins of unknown identity, that have not previously been reported.ResultsDe novo assembly of cDNA sequence data generated 172,660 contigs between 100 and 10000 bp in length; with 35% of > 200 bp in length. Parasitization had significant impacts on expression levels of 928 identified insect host transcripts. Gene ontology data illustrated that the majority of the differentially expressed genes are involved in binding, catalytic activity, and metabolic and cellular processes. In addition, the results show that transcription levels of antimicrobial peptides, such as gloverin, cecropin E and lysozyme, were up-regulated after parasitism. Expression of ichnovirus genes were detected in parasitized larvae with 19 unique sequences identified from five PDV gene families including vankyrin, viral innexin, repeat elements, a cysteine-rich motif, and polar residue rich protein. Vankyrin 1 and repeat element 1 genes showed the highest transcription levels among the DsIV genes.ConclusionThis study provides detailed information on differential expression of P. xylostella larval genes following parasitization, DsIV genes expressed in the host and also improves our current understanding of this host-parasitoid interaction.

Project description:Polydnaviruses (PDVs) exhibit species-specific mutualistic relationships with endoparasitoid wasps. PDVs can be categorized into bracoviruses and ichnoviruses, which have independent evolutionary origins. In our previous study, we identified an ichnovirus of the endoparasitoid Diadegma fenestrale and named it DfIV. Here, DfIV virions from the ovarian calyx of gravid female wasps were characterized. DfIV virion particles were ellipsoidal (246.5 nm × 109.0 nm) with a double-layered envelope. Next-generation sequencing of the DfIV genome revealed 62 non-overlapping circular DNA segments (A1-A5, B1-B9, C1-C15, D1-D23, E1-E7, and F1-F3); the aggregate genome size was approximately 240 kb, and the GC content (43%) was similar to that of other IVs (41%-43%). A total of 123 open reading frames were predicted and included typical IV gene families such as repeat element protein (41 members), cysteine motif (10 members), vankyrin (9 members), polar residue-rich protein (7 members), vinnexin (6 members), and N gene (3 members). Neuromodulin N (2 members) was found to be unique to DfIV, along with 45 hypothetical genes. Among the 62 segments, 54 showed high (76%-98%) sequence similarities to the genome of Diadegma semiclausum ichnovirus (DsIV). Three segments, namely, D22, E3, and F2, contained lepidopteran host genome integration motifs with homologous regions of about 36-46 bp between them (Diadegma fenestrale ichnovirus, DfIV and lepidopteran host, Plutella xylostella). Most of the DfIV genes were expressed in the hymenopteran host and some in the lepidopteran host (P. xylostella), parasitized by D. fenestrale. Five segments (A4, C3, C15, D5, and E4) were differentially expressed at different developmental stages of the parasitized P. xylostella, and two segments (C15 and D14) were highly expressed in the ovaries of D. fenestrale. Comparative analysis between DfIV and DsIV revealed that the genomes differed in the number of segments, composition of sequences, and internal sequence homologies.

Project description:BackgroundIn nature, insects have evolved behavioural and physiological adaptations to cope with short term exposure to extreme temperatures. Extreme heat events may increase as a result of climate change; this in turn will affect insect population dynamics. We examined the effect of abrupt and ecologically relevant gradual exposure to high temperatures on the survival and hsp70 gene expression in diamondback moth (DBM) adults and the parasitoid Diadegma insulare, as well as in parasitized and non-parasitized DBM larvae.Principal findingsTolerance to high temperatures in DBM adults was higher than in D. insulare adults. There was no difference in the survival of DBM adults between abrupt and ramped increases from 25 to 38°C; however, at 40°C survival was higher when the temperature increased gradually. In contrast, more D. insulare adults survived when the temperature was ramped rather than shifted abruptly to both 38 and 40°C. There was no heat stress effect of up to 40°C on the survival of either parasitized or non-parasitized DBM larvae. In adults of both species, more hsp70 expression was observed when temperatures increased abruptly to 38°C compared to ramping. In contrast, at 40°C significantly more expression was found in insects exposed to the ramping rather than the abrupt regime. Hsp70 expression level was in agreement with adult survival data and appears to be a good indicator of stress levels. In parasitized and non-parasitized larvae, hsp70 expression was significantly higher after abrupt shifts compared to ramping at both temperatures.Conclusions/significanceHsp70 gene expression was responsive to extreme temperatures in both DBM and D. insulare, which may underlie the ability of these insects to survive in extreme temperatures. Survival and hsp70 expression upon abrupt changes are distinctly different from those after ramping indicating that experimental protocol must be considered before extrapolating laboratory results to natural field situations.

Dataset Information

Genome-Wide Profiling of Diadegma semiclausum Ichnovirus Integration in Parasitized Plutella xylostella Hemocytes Identifies Host Integration Motifs and Insertion Sites.

Publications

Genome-Wide Profiling of <i>Diadegma semiclausum</i> Ichnovirus Integration in Parasitized <i>Plutella xylostella</i> Hemocytes Identifies Host Integration Motifs and Insertion Sites.

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