Recurrent Domestication by Lepidoptera of Genes from Their Parasites Mediated by Bracoviruses

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Eukaryotes are generally thought to evolve mainly through the modification of existing genetic information. However, evidence of horizontal gene transfer (HGT) in eukaryotes-the accidental acquisition of a novel gene from another species, allowing acquisition of novel traits—is now recognized as an important factor in their evolution. We show here that in several lineages, lepidopteran genomes have acquired genes from a bracovirus that is symbiotically used by parasitic wasps to inhibit caterpillar host immune defences. Integration of parts of the viral genome into host caterpillar DNA strongly suggests that integration can sporadically occur in the germline, leading to the production of lepidopteran lineages that harbor bracovirus sequences. Moreover, some of the transferred bracovirus genes reported here originate from the wasp genome, demonstrating that a gene flux exists between the two insect orders Hymenoptera and Lepidoptera that diverged ≈300 MYA. As bracovirus gene organisation has evolved to allow expression in Lepidoptera, these transferred genes can be readily domesticated. Additionally, we present functional analyses suggesting that some of the acquired genes confer to caterpillars a protection toward baculovirus, a very common pathogen in the field. This phenomenon may have implications for understanding how caterpillars acquire resistance against baculoviruses used in biological control.

Vyšlo v časopise: Recurrent Domestication by Lepidoptera of Genes from Their Parasites Mediated by Bracoviruses. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005470
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005470

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1. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature. (2000);405:299–304. 10830951

2. Keeling PJ, Palmer JD. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. (2008);9:605–18. doi: 10.1038/nrg2386 18591983

3. Syvanen M. Evolutionary implications of horizontal gene transfer. Annu Rev Genet. (2012);46:341–58. doi: 10.1146/annurev-genet-110711-155529 22934638

4. Boto L. Horizontal gene transfer in the acquisition of novel traits by metazoans. Proc Biol Sci. (2014);281:20132450. doi: 10.1098/rspb.2013.2450 24403327

5. Crisp A, Boschetti C, Perry M, Tunnacliffe A, Micklem G. Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biol. (2015);16:50. doi: 10.1186/s13059-015-0607-3 25785303

6. Gilbert C, Chateigner A, Ernenwein L, Barbe V, Bézier A, Herniou EA, et al. Population genomics supports baculoviruses as vectors of horizontal transfer of insect transposons. Nat Commun. (2014);5:3348. doi: 10.1038/ncomms4348 24556639

7. Kondo N, Nikoh N, Ijichi N, Shimada M, Fukatsu T. Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci U S A. (2002);99:14280–5. 12386340

8. Dunning Hotopp JC, Clark ME, Oliveira DC, Foster JM, Fischer P, Munoz Torres MC, et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science. (2007);317:1753–6. 17761848

9. Serbus LR, Sullivan W. A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog. (2007);3:e190. 18085821

10. Sun BF, Xiao JH, He SM, Liu L, Murphy RW, Huang DW. Multiple ancient horizontal gene transfers and duplications in lepidopteran species. Insect Mol Biol. (2013);22:72–87. doi: 10.1111/imb.12004 23211014

11. Murphy N, Banks JC, Whitfield JB, Austin AD. Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. Mol Phylogenet Evol. (2008);47:378–95. doi: 10.1016/j.ympev.2008.01.022 18325792

12. Bézier A, Annaheim M, Herbinière J, Wetterwald C, Gyapay G, Bernard-Samain S, et al. Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science. (2009);323:926–30. doi: 10.1126/science.1166788 19213916

13. Herniou EA, Huguet E, Thézé J, Bézier A, Periquet G, Drezen J-M. When parasitc wasps hijacked viruses: genomic and functionnal evolution of polydnaviruses. Phil Transac R Soc B. (2013);368:1–13.

14. Strand MR, Burke GR. Polydnavirus-wasp associations: evolution, genome organization, and function. Curr Opin Virol. (2013);3:587–94. doi: 10.1016/j.coviro.2013.06.004 23816391

15. Gundersden-Rindal D, Dupuy C, Huguet E, Drezen J-M. Parasitoid Polydnaviruses: Evolution, Pathology and Applications. Biocontrol Science and Technology (2013);23:1–61.

16. Strand MR. Polydnavirus gene products that interact with the host immune system. In: Beckage NE, Drezen J-M, editors. Parasitoid viruses symbionts and pathogens. San Diego: Elsevier; 2012. p. 149–61.

17. Beckage NE. Polydnaviruses as endocrine regulators. In: Beckage NE, Drezen J-M, editors. Parasitoid viruses symbionts and pathogens. San Diego: Elsevier; 2012. p. 163–8.

18. Bézier A, Louis F, Jancek S, Periquet G, Thézé J, Gyapay G, et al. Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata: insights into the evolutionary dynamics of bracoviruses. Philos Trans R Soc Lond B Biol Sci. (2013);368:20130047. doi: 10.1098/rstb.2013.0047 23938757

19. Louis F, Bézier A, Periquet G, Ferras C, Drezen JM, Dupuy C. The bracovirus genome of the parasitoid wasp Cotesia congregata is amplified within 13 replication units, including sequences not packaged in the particles. J Virol. (2013);87:9649–60. doi: 10.1128/JVI.00886-13 23804644

20. Burke GR, Walden KK, Whitfield JB, Robertson HM, Strand MR. Widespread genome reorganization of an obligate virus mutualist. PLoS Genet. (2014);10:e1004660. doi: 10.1371/journal.pgen.1004660 25232843

21. Desjardins CA, Gundersen-Rindal DE, Hostetler JB, Tallon LJ, Fuester RW, Schatz MC, et al. Structure and evolution of a proviral locus of Glyptapanteles indiensis bracovirus. BMC Microbiol. (2007);7:61. 17594494

22. Chevignon G, Thézé J, Cambier S, Poulain J, Da Silva C, Bézier A, et al. Functional annotation of Cotesia congregata bracovirus: identification of the viral genes expressed in parasitized host immune tissues. J Virol. (2014);88:8795–812. doi: 10.1128/JVI.00209-14 24872581

23. Desjardins CA, Gundersen-Rindal DE, Hostetler JB, Tallon LJ, Fadrosh DW, Fuester RW, et al. Comparative genomics of mutualistic viruses of Glyptapanteles parasitic wasps. Genome Biol. (2008);9:R183. doi: 10.1186/gb-2008-9-12-r183 19116010

24. Bézier A, Herbinière J, Serbielle C, Lesobre J, Wincker P, Huguet E, et al. Bracovirus gene products are highly divergent from insect proteins. Arch Insect Biochem Physiol. (2008);67:172–87. doi: 10.1002/arch.20219 18348209

25. Serbielle C, Chowdhury S, Pichon S, Dupas S, Lesobre J, Purisima EO, et al. Viral cystatin evolution and three-dimensional structure modelling: a case of directional selection acting on a viral protein involved in a host-parasitoid interaction. BMC Biol. (2008);6:38. doi: 10.1186/1741-7007-6-38 18783611

26. Serbielle C, Dupas S, Perdereau E, Héricourt F, Dupuy C, Huguet E, et al. Evolutionary mechanisms driving the evolution of a large polydnavirus gene family coding for protein tyrosine phosphatases. BMC Evol Biol. (2012);12:253. doi: 10.1186/1471-2148-12-253 23270369

27. Beck MH, Zhang S, Bitra K, Burke GR, Strand MR. The encapsidated genome of Microplitis demolitor bracovirus integrates into the host Pseudoplusia includens. J Virol. (2011);85:11685–96. doi: 10.1128/JVI.05726-11 21880747

28. Dushay MS, Beckage NE. Dose-dependent separation of Cotesia congregata associated polydnavirus effects on Manduca sexta larval development and immunity. J Insect Physiol. (1993);39:1029–40.

29. Quicke DLJ. Parasitic wasps. London: Chapman & Hall; 1997.

30. Beckage NE, Tan FF. Development of the braconid wasp Cotesia congregata in a semi-permissive noctuid host, Trichoplusia ni. Journal of Invertebrate Pathology. (2002);81:49–52. 12417213

31. Schneider SE, Thomas JH. Accidental genetic engineers: horizontal sequence transfer from parasitoid wasps to their lepidopteran hosts. PLoS One. (2014);9:e109446. doi: 10.1371/journal.pone.0109446 25296163

32. Zhan S, Merlin C, Boore JL, Reppert SM. The monarch butterfly genome yields insights into long-distance migration. Cell. (2011);147:1171–85. doi: 10.1016/j.cell.2011.09.052 22118469

33. Chevignon G, Cambier S, Da Silva C, Poulain J, Drezen JM, Huguet E, et al. Transcriptomic response of Manduca sexta immune tissues to parasitization by the bracovirus associated wasp Cotesia congregata. Insect Biochem Mol Biol. (2015).

34. Smith DAS, Lushai G, Allen JA. A classification of Danaus butterflies (Lepidoptera: Nymphalidae) based upon data from morphology and DNA. Zool J Linn Soc. (2005);144:191–212.

35. Lushai G, Smith DAS, Goulson D, Allen JA. Mitochondrial DNA clocks and the phylogeny of Danaus butterflies. Insect Sci Applic. (2003);23:309–15.

36. Brower AVZ, Wahlberg N, Ogawa JR, Boppré M, Vane-Wright RI. Phylogenetic relationships among genera of danaine butterflies (Lepidoptera: Nymphalidae) as implied by morphology and DNA sequences. Systematics and Biodiversity. (2010);8:75–89.

37. Abhiman S, Iyer LM, Aravind L. BEN: a novel domain in chromatin factors and DNA viral proteins. Bioinformatics. (2008);24:458–61. doi: 10.1093/bioinformatics/btn007 18203771

38. Park B, Kim Y. Transient transcription of a putative RNase containing BEN domain encoded in Cotesia plutellae bracovirus induces an immunosuppression of the diamondback moth, Plutella xylostella. J Invertebr Pathol. (2010);105:156–63. doi: 10.1016/j.jip.2010.06.003 20600089

39. Dai Q, Ren A, Westholm JO, Serganov AA, Patel DJ, Lai EC. The BEN domain is a novel sequence-specific DNA-binding domain conserved in neural transcriptional repressors. Genes Dev. (2013);27:602–14. doi: 10.1101/gad.213314.113 23468431

40. Pascual L, Jakubowska AK, Blanca JM, Canizares J, Ferre J, Gloeckner G, et al. The transcriptome of Spodoptera exigua larvae exposed to different types of microbes. Insect Biochem Mol Biol. (2012);42:557–70. doi: 10.1016/j.ibmb.2012.04.003 22564783

41. Kergoat GJ, Prowell DP, Le Ru BP, Mitchell A, Dumas P, Clamens AL, et al. Disentangling dispersal, vicariance and adaptive radiation patterns: a case study using armyworms in the pest genus Spodoptera (Lepidoptera: Noctuidae). Mol Phylogenet Evol. (2012);65:855–70. doi: 10.1016/j.ympev.2012.08.006 22939903

42. Ohkawa T, Volkman LE, Welch MD. Actin-based motility drives baculovirus transit to the nucleus and cell surface. J Cell Biol. (2010);190:187–95. doi: 10.1083/jcb.201001162 20660627

43. Volkman LE. Baculovirus infectivity and the actin cytoskeleton. Curr Drug Targets. (2007);8:1075–83. 17979667

44. Glatz R, Schmidt O, Asgari S. Characterization of a novel protein with homology to C-type lectins expressed by the Cotesia rubecula bracovirus in larvae of the lepidopteran host, Pieris rapae. J Biol Chem. (2003):M301396200.

45. Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. (2004);340:783–95. 15223320

46. Yoshiyama M, Tu Z, Kainoh Y, Honda H, Shono T, Kimura K. Possible horizontal transfer of a transposable element from host to parasitoid. Mol Biol Evol. (2001);18:1952–8. 11557800

47. Guo X, Gao J, Li F, Wang J. Evidence of horizontal transfer of non-autonomous Lep1 Helitrons facilitated by host-parasite interactions. Sci Rep. (2014);4:5119. doi: 10.1038/srep05119 24874102

48. Thomas J, Schaack S, Pritham EJ. Pervasive horizontal transfer of rolling-circle transposons among animals. Genome Biol Evol. (2010);2:656–64. doi: 10.1093/gbe/evq050 20693155

49. Pasquier-Barre F, Dupuy C, Huguet E, Monteiro F, Moreau A, Poirie M, et al. Polydnavirus replication: the EP1 segment of the parasitoid wasp Cotesia congregata is amplified within a larger precursor molecule. J Gen Virol. (2002);83:2035–45. 12124468

50. Burke GR, Thomas SA, Eum JH, Strand MR. Mutualistic polydnaviruses share essential replication gene functions with pathogenic ancestors. PLoS Pathog. (2013);9:e1003348. doi: 10.1371/journal.ppat.1003348 23671417

51. Wyder S, Blank F, Lanzrein B. Fate of polydnavirus DNA of the egg-larval parasitoid Chelonus inanitus in the host Spodoptera littoralis. J Insect Physiol. (2003);49:491–500. 12770628

52. Beck MH, Inman RB, Strand MR. Microplitis demolitor bracovirus genome segments vary in abundance and are individually packaged in virions. Virology. (2007);359:179–89. 17034828

53. Burke GR, Strand MR. Deep sequencing identifies viral and wasp genes with potential roles in replication of Microplitis demolitor Bracovirus. J Virol. (2012);86:3293–306. doi: 10.1128/JVI.06434-11 22238295

54. Wurtele H, Little KC, Chartrand P. Illegitimate DNA integration in mammalian cells. Gene Ther. (2003);10:1791–9. 12960968

55. Takasu K, Hoang Le K. The larval parasitoid Microplitis croceipes oviposits in conspecific adults. Naturwissenschaften. (2007);94:200–6. 17124591

56. Virto C, Navarro D, Tellez MM, Herrero S, Williams T, Murillo R, et al. Natural populations of Spodoptera exigua are infected by multiple viruses that are transmitted to their offspring. J Invertebr Pathol. (2014);122:22–7. doi: 10.1016/j.jip.2014.07.007 25128697

57. Cabodevilla O, Villar E, Virto C, Murillo R, Williams T, Caballero P. Intra- and intergenerational persistence of an insect nucleopolyhedrovirus: adverse effects of sublethal disease on host development, reproduction, and susceptibility to superinfection. Appl Environ Microbiol. (2011);77:2954–60. doi: 10.1128/AEM.02762-10 21398487

58. Wilson JW. Notes on the biology of Laphrygma exigua Hübner. Florida Entomol. (1932);16:33–9.

59. Weis WI, Taylor ME, Drickamer K. The C-type lectin superfamily in the immune system. Immunol Rev. (1998);163:19–34. 9700499

60. Lee S, Nalini M, Kim Y. A viral lectin encoded in Cotesia plutellae bracovirus and its immunosuppressive effect on host hemocytes. Comp Biochem Physiol A Mol Integr Physiol. (2008);149:351–61. doi: 10.1016/j.cbpa.2008.01.007 18325805

61. Liu F, Ling E, Wu S. Gene expression profiling during early response to injury and microbial challenges in the silkworm, Bombyx mori. Arch Insect Biochem Physiol. (2009);72:16–33. doi: 10.1002/arch.20320 19557735

62. Pan D, He N, Yang Z, Liu H, Xu X. Differential gene expression profile in hepatopancreas of WSSV-resistant shrimp (Penaeus japonicus) by suppression subtractive hybridization. Dev Comp Immunol. (2005);29:103–12. 15450750

63. Chai LQ, Tian YY, Yang DT, Wang JX, Zhao XF. Molecular cloning and characterization of a C-type lectin from the cotton bollworm, Helicoverpa armigera. Dev Comp Immunol. (2008);32:71–83. 17568670

64. Smits PH, Vlak JM. Biological activity of Spodoptera exigua nuclear polyhedrosis virus against S. exigua larvae. J invertebrate Pathol. (1988);51:107–14.

65. Cory JS, Myers JH. Within and between population variation in disease resistance in cyclic populations of western tent caterpillars: a test of the disease defence hypothesis. J Anim Ecol. (2009);78:646–55. doi: 10.1111/j.1365-2656.2008.01519.x 19220564

66. Jakubowska AK, Vogel H, Herrero S. Increase in gut microbiota after immune suppression in baculovirus-infected larvae. PLoS Pathog. (2013);9:e1003379. doi: 10.1371/journal.ppat.1003379 23717206

67. Kozak CA. The mouse "xenotropic" gammaretroviruses and their XPR1 receptor. Retrovirology. (2010);7:101. doi: 10.1186/1742-4690-7-101 21118532

68. Taylor GM, Gao Y, Sanders DA. Fv-4: identification of the defect in Env and the mechanism of resistance to ecotropic murine leukemia virus. J Virol. (2001);75:11244–8. 11602766

69. Fujino K, Horie M, Honda T, Merriman DK, Tomonaga K. Inhibition of Borna disease virus replication by an endogenous bornavirus-like element in the ground squirrel genome. Proc Natl Acad Sci U S A. (2014);111:13175–80. doi: 10.1073/pnas.1407046111 25157155

70. Abel PP, Nelson RS, De B, Hoffmann N, Rogers SG, Fraley RT, et al. Delay of disease development in transgenic plants that express the tobacco mosaic virus coat protein gene. Science. (1986);232:738–43. 3457472

71. Gottula J, Fuchs M. Toward a quarter century of pathogen-derived resistance and practical approaches to plant virus disease control. Adv Virus Res. (2009);75:161–83. doi: 10.1016/S0065-3527(09)07505-8 20109666

72. Malfavon-Borja R, Feschotte C. Fighting fire with fire: Endogenous retrovirus envelopes as restriction factors. J Virol. (2015);89:4047–50. doi: 10.1128/JVI.03653-14 25653437

73. Yan Y, Buckler-White A, Wollenberg K, Kozak CA. Origin, antiviral function and evidence for positive selection of the gammaretrovirus restriction gene Fv1 in the genus Mus. Proc Natl Acad Sci U S A. (2009);106:3259–63. doi: 10.1073/pnas.0900181106 19221034

74. Bertsch C, Beuve M, Dolja VV, Wirth M, Pelsy F, Herrbach E, et al. Retention of the virus-derived sequences in the nuclear genome of grapevine as a potential pathway to virus resistance. Biol Direct. (2009);4:21. doi: 10.1186/1745-6150-4-21 19558678

75. Flegel TW. Hypothesis for heritable, anti-viral immunity in crustaceans and insects. Biol Direct. (2009);4:32. doi: 10.1186/1745-6150-4-32 19725947

76. Cai Y, Fan J, Sun S, Wang F, Yang K, Li G, et al. Interspecific interaction between Spodoptera exigua multiple nucleopolyhedrovirus and Microplitis bicoloratus (Hymenoptera: Braconidae: Microgastrina) in Spodoptera exigua (Lepidoptera: Noctuidae) larvae. J Econ Entomol. (2012);105:1503–8. 23156143

77. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics. (2009);25:119–20. doi: 10.1093/bioinformatics/btn578 18990721

78. Mason WRM. The polyphyletic nature of Apanteles Foerster (Hymenoptera: Braconidae): a phylogeny and reclassification of Microgastrinae. Memoirs of the Entomological Society of Canada ed: Memoirs of the Entomological Society of Canada; 1981. 147 p.

79. Hernandez-Martinez P, Ferre J, Escriche B. Susceptibility of Spodoptera exigua to 9 toxins from Bacillus thuringiensis. J Invertebr Pathol. (2008);97:245–50. 18082763

80. Hernandez-Martinez P, Naseri B, Navarro-Cerrillo G, Escriche B, Ferre J, Herrero S. Increase in midgut microbiota load induces an apparent immune priming and increases tolerance to Bacillus thuringiensis. Environ Microbiol. (2010);12:2730–7. doi: 10.1111/j.1462-2920.2010.02241.x 20482744

81. Hernandez-Martinez P, Navarro-Cerrillo G, Caccia S, de Maagd RA, Moar WJ, Ferre J, et al. Constitutive activation of the midgut response to Bacillus thuringiensis in Bt-resistant Spodoptera exigua. PLoS One. (2010);5.

82. Park Y, Gonzalez-Martinez RM, Navarro-Cerrillo G, Chakroun M, Kim Y, Ziarsolo P, et al. ABCC transporters mediate insect resistance to multiple Bt toxins revealed by bulk segregant analysis. BMC Biol. (2014);12:46. doi: 10.1186/1741-7007-12-46 24912445

83. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. (2012);9:357–9. doi: 10.1038/nmeth.1923 22388286

84. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. (2009);25:2078–9. doi: 10.1093/bioinformatics/btp352 19505943

85. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. (2008);18:821–9. doi: 10.1101/gr.074492.107 18349386

86. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. (2002);30:3059–66. 8. 12136088

87. Pond SL, Frost SD, Muse SV. HyPhy: hypothesis testing using phylogenies. Bioinformatics. (2005);21:676–9. 15509596

88. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. (2007);24:1586–91. 17483113

89. Hernandez-Rodriguez CS, Ferre J, Herrero S. Genomic structure and promoter analysis of pathogen-induced repat genes from Spodoptera exigua. Insect Mol Biol. (2009);18:77–85. doi: 10.1111/j.1365-2583.2008.00850.x 19076251

90. Kaba SA, Salcedo AM, Wafula PO, Vlak JM, van Oers MM. Development of a chitinase and v-cathepsin negative bacmid for improved integrity of secreted recombinant proteins. J Virol Methods. (2004);122:113–8. 15488628

91. Luckow VA, Lee SC, Barry GF, Olins PO. Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J Virol. (1993);67:4566–79. 8392598

92. WF IJ, van Strien EA, Heldens JG, Broer R, Zuidema D, Goldbach RW, et al. Sequence and organization of the Spodoptera exigua multicapsid nucleopolyhedrovirus genome. J Gen Virol. (1999);80:3289–304. 10567663

93. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. (1997);25:4876–82. 1. 9396791

94. Nicholas KB, Nicholas HBJ, Deerfield DW. GeneDoc: analysis and visualization of genetic variation. EMBNEWNEWS. (1997);4:14.

95. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. (2011);28:2731–9. doi: 10.1093/molbev/msr121 21546353