RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in ichneumonid wasps

English version

Autoři: Ange Lorenzi ^aff001; Marc Ravallec ^aff001; Magali Eychenne ^aff001; Véronique Jouan ^aff001; Stéphanie Robin ^aff002; Isabelle Darboux ^aff001; Fabrice Legeai ^aff002; Anne-Sophie Grenet-Gosselin ^aff001; Mathieu Sicard ^aff004; Don Stoltz ^aff005; Anne-Nathalie Volkoff ^aff001
Působiště autorů: DGIMI, INRA, University of Montpellier, Montpellier, France ^aff001; UMR 1349 INRA/Agrocampus Ouest/Université Rennes 1, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Le Rheu, France ^aff002; Université Rennes 1, INRIA, CNRS, IRISA, Rennes, France ^aff003; ISEM, University of Montpellier, CNRS, IRD, EPHE, Montpellier, France ^aff004; Department of Microbiology and Immunology, Dalhousie University, Halifax, Canada ^aff005
Vyšlo v časopise: RNA interference identifies domesticated viral genes involved in assembly and trafficking of virus-derived particles in ichneumonid wasps. PLoS Pathog 15(12): e32767. doi:10.1371/journal.ppat.1008210
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008210

Souhrn

There are many documented examples of viral genes retained in the genomes of multicellular organisms that may in some cases bring new beneficial functions to the receivers. The ability of certain ichneumonid parasitic wasps to produce virus-derived particles, the so-called ichnoviruses (IVs), not only results from the capture and domestication of single viral genes but of almost entire ancestral virus genome(s). Indeed, following integration into wasp chromosomal DNA, the putative and still undetermined IV ancestor(s) evolved into encoding a ‘virulence gene delivery vehicle’ that is now required for successful infestation of wasp hosts. Several putative viral genes, which are clustered in distinct regions of wasp genomes referred to as IVSPERs (Ichnovirus Structural Protein Encoding Regions), have been assumed to be involved in virus-derived particles morphogenesis, but this question has not been previously functionally addressed. In the present study, we have successfully combined RNA interference and transmission electron microscopy to specifically identify IVSPER genes that are responsible for the morphogenesis and trafficking of the virus-derived particles in ovarian cells of the ichneumonid wasp Hyposoter didymator. We suggest that ancestral viral genes retained within the genomes of certain ichneumonid parasitoids possess conserved functions which were domesticated for the purpose of assembling viral vectors for the delivery of virulence genes to parasitized host animals.

Klíčová slova:

Calyx – Cell membranes – Cytoplasm – Nuclear membrane – Pupae – Virions – Wasps – Nucleocapsids

Zdroje

1. Katzourakis A, Gifford RJ. Endogenous viral elements in animal genomes. PLoS Genet. 2010;6. doi: 10.1371/journal.pgen.1001191 21124940

2. Magiorkinis G, Blanco-Melo D, Belshaw R. The decline of human endogenous retroviruses: extinction and survival. Retrovirology. 2015;12 : 8. doi: 10.1186/s12977-015-0136-x 25640971

3. Johnson WE. Origins and evolutionary consequences of ancient endogenous retroviruses. Nat Rev Microbiol. 2019;17 : 355–370. doi: 10.1038/s41579-019-0189-2 30962577

4. Feschotte C, Gilbert C. Endogenous viruses: insights into viral evolution and impact on host biology. Nat Rev Genet. 2012;13 : 283–296. doi: 10.1038/nrg3199 22421730

5. Metegnier G, Becking T, Chebbi MA, Giraud I, Moumen B, Schaack S, et al. Comparative paleovirological analysis of crustaceans identifies multiple widespread viral groups. Mobile DNA. 2015;6. doi: 10.1186/s13100-015-0047-3 26388953

6. Lequime S, Lambrechts L. Discovery of flavivirus-derived endogenous viral elements in Anopheles mosquito genomes supports the existence of Anopheles-associated insect-specific flaviviruses. Virus Evol. 2017;3. doi: 10.1093/ve/vew035 28078104

7. Suzuki Y, Frangeul L, Dickson LB, Blanc H, Verdier Y, Vinh J, et al. Uncovering the repertoire of endogenous flaviviral elements in Aedes mosquito genomes. J Virol. 2017;91. doi: 10.1128/jvi.00571-17 28539440

8. Horst AMT, Nigg JC, Falk BW. Endogenous viral elements are widespread in arthropod genomes and commonly give rise to piRNAs. J Virol. 2018; doi: 10.1128/jvi.02124-18 30567990

9. Antonelli G, Pistello M. Virology: A scientific discipline facing new challenges. Clin Microbiol Infect. 2019;25 : 133–135. doi: 10.1016/j.cmi.2018.12.003 30580032

10. Black SG, Arnaud F, Palmarini M, Spencer TE. Endogenous retroviruses in trophoblast differentiation and placental development. Am J Reprod Immunol. 2010;64 : 255–264. doi: 10.1111/j.1600-0897.2010.00860.x 20528833

11. Ashley J, Cordy B, Lucia D, Fradkin LG, Budnik V, Thomson T. Retrovirus-like Gag protein Arc1 binds RNA and traffics across synaptic boutons. Cell. 2018;172. doi: 10.1016/j.cell.2018.05.048

12. Pastuzyn ED, Day CE, Kearns RB, Kyrke-Smith M, Taibi AV, Mccormick J, et al. The neuronal gene Arc encodes a repurposed retrotransposon Gag protein that mediates intercellular RNA transfer. Cell. 2018;172. doi: 10.1016/j.cell.2018.05.048

13. Parker BJ, Brisson JA. A laterally transferred viral gene modifies aphid wing plasticity. Curr Biol. 2019;29. doi: 10.1016/j.cub.2019.05.041 31178319

14. Strand MR, Burke GR. Polydnaviruses: From discovery to current insights. Virology. 2015;479–480 : 393–402. doi: 10.1016/j.virol.2015.01.018 25670535

15. Krell PJ, Stoltz DB. Unusual baculovirus of the parasitoid wasp Apanteles melanoscelus: Isolation and preliminary characterization. J Virol. 1979;29 : 1118–1130. 16789176

16. Stoltz DB, Guzo D, Belland ER, Lucarotti CJ, Mackinnon EA. Venom promotes uncoating in vitro and persistence in vivo of DNA from a braconid polydnavirus. J Gen Virol. 1988;69 : 903–907. doi: 10.1099/0022-1317-69-4-903

17. Bezier A, Annaheim M, Herbiniere J, Wetterwald C, Gyapay G, Bernard-Samain S, et al. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science. 2009;323 : 926–930. doi: 10.1126/science.1166788 19213916

18. Volkoff A-N, Jouan V, Urbach S, Samain S, Bergoin M, Wincker P, et al. Analysis of virion structural components reveals vestiges of the ancestral ichnovirus genome. PLoS Pathog. 2010;6. doi: 10.1371/journal.ppat.1000923 20523890

19. Burke GR, Thomas SA, Eum JH, Strand MR. Mutualistic polydnaviruses share essential replication gene functions with pathogenic ancestors. PLoS Pathog. 2013;9. doi: 10.1371/journal.ppat.1003348 23671417

20. Béliveau C, Cohen A, Stewart D, Periquet G, Djoumad A, Kuhn L, et al. Genomic and proteomic analyses indicate that Banchine and Campoplegine polydnaviruses have similar, if not identical, viral ancestors. J Virol. 2015;89 : 8909–8921. doi: 10.1128/JVI.01001-15 26085165

21. Norton W. N., Vinson S. B., Stoltz D. B. Nuclear secretory particles associated with the calyx cells of the ichneumonid parasitoid Campoletis sonorensis (Cameron). Cell Tissue Res. 1975; 162 : 195–208. doi: 10.1007/bf00209207 171071

22. Volkoff A-N, Ravallec M, Bossy J-P, Cerutti P, Rocher J, Cerutti M, et al. The replication of Hyposoter didymator polydnavirus: Cytopathology of the calyx cells in the parasitoid. Biol Cell. 1995;83 : 1–13. doi: 10.1016/0248-4900(96)89926-6

23. Djoumad A, Stoltz D, Beliveau C, Boyle B, Kuhn L, Cusson M. Ultrastructural and genomic characterization of a second banchine polydnavirus confirms the existence of shared features within this ichnovirus lineage. J Gen Virol. 2013;94 : 1888–1895. doi: 10.1099/vir.0.052506-0 23658210

24. Herniou EA, Huguet E, Theze J, Bezier A, Periquet G, Drezen J-M. When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Philos Trans R Soc Lond B Biol Sci. 2013;368. doi: 10.1098/rstb.2013.0051 23938758

25. Blissard GW, Rohrmann GF. Baculovirus diversity and molecular biology. Ann Rev Entom. 1990;35 : 127–155. doi: 10.1146/annurev.en.35.010190.001015 2154158

26. Pichon A, Bézier A, Urbach S, Aury J-M, Jouan V, Ravallec M, et al. Recurrent DNA virus domestication leading to different parasite virulence strategies. Sci Adv. 2015;1. doi: 10.1126/sciadv.1501150 26702449

27. Young J, Mackinnon E, Faulkner P. The architecture of the virogenic stroma in isolated nuclei of Spodoptera frugiperda cells in vitro infected by Autographa californica nuclear polyhedrosis virus. J Struct Biol. 1993;110 : 141–153. doi: 10.1006/jsbi.1993.1015

28. Williams GV, Faulkner P. Cytological changes and viral morphogenesis during baculovirus infection. The Baculoviruses. 1997 : 61–107. doi: 10.1007/978-1-4899-1834-5_4

29. Blissard GW, Theilmann DA. Baculovirus entry and egress from insect cells. Ann Rev Virol. 2018;5 : 113–139. doi: 10.1146/annurev-virology-092917-043356 30004832

30. Deng L, Webb BA. Cloning and expression of a gene encoding a Campoletis sonorensis polydnavirus structural protein. Arch Insect Biochem Physiol. 1999;40 : 30–40. doi: 10.1002/(SICI)1520-6327(1999)40 : 1<30::AID-ARCH4>3.0.CO;2-Y 9987819

31. Nagamine T, Kawasaki Y, Matsumoto S. Induction of a subnuclear structure by the simultaneous expression of baculovirus proteins, IE1, LEF3, and P143 in the presence of hr. Virology. 2006;352 : 400–407. doi: 10.1016/j.virol.2006.04.034 16780915

32. Shi Y, Li K, Tang P, Li Y, Zhou Q, Yang K, et al. Three-dimensional visualization of the Autographa californica multiple nucleopolyhedrovirus occlusion-derived virion envelopment process gives new clues as to its mechanism. Virology. 2015;476 : 298–303. doi: 10.1016/j.virol.2014.11.030 25569457

33. Suárez C, Welsch S, Chlanda P, Hagen W, Hoppe S, Kolovou A, et al. Open membranes are the precursors for assembly of large DNA viruses. Cell Microbiol. 2013; doi: 10.1111/cmi.12156 23751082

34. Quemin ER, Corroyer-Dulmont S, Baskaran A, Penard E, Gazi AD, Christo-Foroux E, et al. Complex membrane remodeling during virion assembly of the 30,000-Year-Old mollivirus Sibericum. J Virol. 2019;93. doi: 10.1128/jvi.00388-19 30996095

35. Stoltz DB, Pavan C, Cunha ABD. Nuclear polyhedrosis virus: A possible example of de novo intranuclear membrane morphogenesis. J Gen Virol. 1973;19 : 145–150. doi: 10.1099/0022-1317-19-1-145

36. Sun S, Rao VB, Rossmann MG. Genome packaging in viruses. Curr Opin Struct Biol. 2010;20 : 114–120. doi: 10.1016/j.sbi.2009.12.006 20060706

37. Rohrmann GF. Baculovirus molecular biology. Bethesda, MD: National Library of Medicine, National Center for Biotechnology Information; 2013. Chapter 12, The AcMNPV genome: Gene content, conservation, and function. https://www.ncbi.nlm.nih.gov/books/NBK114592/

38. Marek M, Merten O-W, Galibert L, Vlak JM, Oers MMV. Baculovirus VP80 protein and the F-actin cytoskeleton interact and connect the viral replication factory with the nuclear periphery. J Virol. 2011;85 : 5350–5362. doi: 10.1128/JVI.00035-11 21450830

39. Ohkawa T, Welch MD. Baculovirus actin-based motility drives nuclear envelope disruption and nuclear egress. Curr Biol. 2018;28. doi: 10.1016/j.cub.2017.11.031

40. Deng L, Stoltz DB, Webb BA. A gene encoding a polydnavirus structural polypeptide is not encapsidated. Virology. 2000;269 : 440–450. doi: 10.1006/viro.2000.0248 10753722

41. Oomens A, Blissard G. Requirement for GP64 to drive efficient budding of Autographa californica multicapsid nucleopolyhedrovirus. Virology. 1999;254 : 297–314. doi: 10.1006/viro.1998.9523 9986796

42. Zhou J, Blissard GW. Identification of a GP64 subdomain involved in receptor binding by budded virions of the baculovirus Autographica californica multicapsid nucleopolyhedrovirus. J Virol. 2008;82 : 4449–4460. doi: 10.1128/JVI.02490-07 18287233

43. Visconti V, Eychenne M, Darboux I. Modulation of antiviral immunity by the ichnovirus HdIV in Spodoptera frugiperda. Mol Immunol. 2019;108 : 89–101. doi: 10.1016/j.molimm.2019.02.011 30784767

44. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2012;29 : 15–21. doi: 10.1093/bioinformatics/bts635 23104886

45. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2013;30 : 923–930. doi: 10.1093/bioinformatics/btt656 24227677

46. Robinson MD, Mccarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009;26 : 139–140. doi: 10.1093/bioinformatics/btp616 19910308

47. Robin S, Ravallec M, Frayssinet M, Whitfield J, Jouan V, Legeai F, et al. Evidence for an ichnovirus machinery in parasitoids of coleopteran larvae. Virus Res. 2019;263 : 189–206. doi: 10.1016/j.virusres.2019.02.001 30738799

48. Rasband W.S. ImageJ. National Institutes of Health, Bethesda, Maryland, USA. 1997–2018. http://imagej.nih.gov/ij

49. Dorémus T, Cousserans F, Gyapay G, Jouan V, Milano P, Wajnberg E, et al. Extensive transcription analysis of the Hyposoter didymator ichnovirus genome in permissive and non-permissive lepidopteran host species. PLoS ONE. 2014;9. doi: 10.1371/journal.pone.0104072 25117496

50. Tellmann G. The E-Method: a highly accurate technique for gene-expression analysis. Nat Methods. 2006;3: i–ii. doi: 10.1038/nmeth894

51. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. R Core Team. 2017. URL https://www.R-project.org/.