Lepidopteran transcriptome analysis following infection by phylogenetically unrelated polydnaviruses highlights differential and common responses

Provost, Bertille; Jouan, Véronique; Hilliou, Frédérique; Delobel, Pierre; Bernardo, Pauline; Ravallec, Marc; François, Clément; Wajnberg, Éric; Darboux, Isabelle; Fournier, Philippe; Strand, Michael R.; Volkoff, Anne Nathalie

doi:10.1016/j.ibmb.2011.03.010

Cited by 23 publications

(21 citation statements)

References 59 publications

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“…Transcriptomic analyses of these particular host-parasitoid interactions have so far focused on host genes (26,27) or on specific virulence genes or multigenic families and have rarely given a global vision of PDV transcription during these interactions (3,5,28). Recently, an extensive BV transcriptome profile was reported, which concerned Microplitis demolitor BV (MdBV) expression in Pseudoplusia includens, where the spatial and temporal expressions of most predicted open reading frames (ORFs) of this BV were analyzed by reverse transcription-PCR (RT-PCR) (29).…”

Section: Importancementioning

confidence: 99%

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Chevignon

Thézé

Cambier

et al. 2014

J Virol

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Bracoviruses (BVs) from the Polydnaviridae family are symbiotic viruses used as biological weapons by parasitoid wasps to manipulate lepidopteran host physiology and induce parasitism success. BV particles are produced by wasp ovaries and injected along with the eggs into the caterpillar host body, where viral gene expression is necessary for wasp development. Recent sequencing of the proviral genome of Cotesia congregata BV (CcBV) identified 222 predicted virulence genes present on 35 proviral segments integrated into the wasp genome. To date, the expressions of only a few selected candidate virulence genes have been studied in the caterpillar host, and we lacked a global vision of viral gene expression. In this study, a large-scale transcriptomic analysis by 454 sequencing of two immune tissues (fat body and hemocytes) of parasitized Manduca sexta caterpillar hosts allowed the detection of expression of 88 CcBV genes expressed 24 h after the onset of parasitism. We linked the expression profiles of these genes to several factors, showing that different regulatory mechanisms control viral gene expression in the host. These factors include the presence of signal peptides in encoded proteins, diversification of promoter regions, and, more surprisingly, gene position on the proviral genome. Indeed, most genes for which expression could be detected are localized in particular proviral regions globally producing higher numbers of circles. Moreover, this polydnavirus (PDV) transcriptomic analysis also reveals that a majority of CcBV genes possess at least one intron and an arthropod transcription start site, consistent with an insect origin of these virulence genes. IMPORTANCEBracoviruses (BVs) are symbiotic polydnaviruses used by parasitoid wasps to manipulate lepidopteran host physiology, ensuring wasp offspring survival. To date, the expressions of only a few selected candidate BV virulence genes have been studied in caterpillar hosts. We performed a large-scale analysis of BV gene expression in two immune tissues of Manduca sexta caterpillars parasitized by Cotesia congregata wasps. Genes for which expression could be detected corresponded to genes localized in particular regions of the viral genome globally producing higher numbers of circles. Our study thus brings an original global vision of viral gene expression and paves the way to the determination of the regulatory mechanisms enabling the expression of BV genes in targeted organisms, such as major insect pests. In addition, we identify sequence features suggesting that most BV virulence genes were acquired from insect genomes.

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Section: Importancementioning

confidence: 99%

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Chevignon

Thézé

Cambier

et al. 2014

J Virol

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“…Recent studies, using micro-arrays [48,49] or RNAseq [26 ], have demonstrated changes in transcript levels of host genes after IV injection. Following HdIV infection, S. frugiperda genes potentially involved in the immune response (galectin 3, hemocyte protease 4) were upregulated while genes encoding for collagens were down-regulated [48,49].…”

Section: Role Of IV Virulence Genes In Parasitism Of Insect Hostsmentioning

confidence: 99%

“…Following HdIV infection, S. frugiperda genes potentially involved in the immune response (galectin 3, hemocyte protease 4) were upregulated while genes encoding for collagens were down-regulated [48,49]. Similarly, differentially expressed genes were identified in P. xylostella parasitized by D. semiclausum, including a number of antimicrobial peptides (gloverin, cecropin E and lysozyme) that were upregulated following parasitism [26 ].…”

Section: Role Of IV Virulence Genes In Parasitism Of Insect Hostsmentioning

confidence: 99%

Specificities of ichnoviruses associated with campoplegine wasps: genome, genes and role in host–parasitoid interaction

Dorémus

Darboux

Cusson

et al. 2014

Current Opinion in Insect Science

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“…RNA-Seq has been widely used to investigate the molecular mechanisms of the interactions between pathogens and their insect hosts [8–11]. In this study, RNA-Seq was applied to polyadenylate-enriched mRNAs from A .…”

Section: Introductionmentioning

confidence: 99%

Transcriptome Analysis of the Midgut of the Chinese Oak Silkworm Antheraea pernyi Infected with Antheraea pernyi Nucleopolyhedrovirus

Wang

Sun

et al. 2016

PLoS ONE

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The Antheraea pernyi nucleopolyhedrovirus (ApNPV) is an exclusive pathogen of A. pernyi. The intense interactions between ApNPV and A. pernyi cause a series of physiological and pathological changes to A. pernyi. However, no detailed report exists regarding the molecular mechanisms underlying the interactions between ApNPV and A. pernyi. In this study, four cDNA libraries of the A. pernyi midgut, including two ApNPV-infected groups and two control groups, were constructed for transcriptomic analysis to provide new clues regarding the molecular mechanisms that underlie these interactions. The transcriptome of the A. pernyi midgut was de novo assembled using the Trinity platform because of the lack of a genome resource for A. pernyi. Compared with the controls, a total of 5,172 differentially expressed genes (DEGs) were identified, including 2,183 up-regulated and 2,989 down-regulated candidates, of which 2,965 and 911 DEGs were classified into different GO categories and KEGG pathways, respectively. The DEGs involved in A. pernyi innate immunity were classified into several categories, including heat-shock proteins, apoptosis-related proteins, serpins, serine proteases and cytochrome P450s. Our results suggested that these genes were related to the immune response of the A. pernyi midgut to ApNPV infection via their essential roles in regulating a variety of physiological processes. Our results may serve as a basis for future research not only on the molecular mechanisms of ApNPV invasion but also on the anti-ApNPV mechanism of A. pernyi.

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Lepidopteran transcriptome analysis following infection by phylogenetically unrelated polydnaviruses highlights differential and common responses

Cited by 23 publications

References 59 publications

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Specificities of ichnoviruses associated with campoplegine wasps: genome, genes and role in host–parasitoid interaction

Transcriptome Analysis of the Midgut of the Chinese Oak Silkworm Antheraea pernyi Infected with Antheraea pernyi Nucleopolyhedrovirus

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