BMC Evolutionary Biology | |
Evolutionary mechanisms driving the evolution of a large polydnavirus gene family coding for protein tyrosine phosphatases | |
Jean-Michel Drezen3  Elisabeth Huguet3  Catherine Dupuy3  François Héricourt2  Elfie Perdereau3  Stéphane Dupas1  Céline Serbielle3  | |
[1] IRD, Institut de Recherche pour le Développement, UR 072, Laboratoire Evolution, Génomes et Spéciation, UPR 9034, Centre National de la Recherche Scientifique (CNRS), 91198 Gif sur Yvette Cedex, France et Université Paris-Sud 11, 91405, Orsay Cedex, France;Present address: INRA, USC1328, Arbres et Réponses aux Contraintes Hydriques et Environnementales (ARCHE), BP 6759, 45067, Orléans Cedex 2, France;Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 7261, Faculté des Sciences et Techniques, Université F. Rabelais, Parc de Grandmont, 37200, Tours, France | |
关键词: Positive selection; Gene duplication; Protein tyrosine phosphatase; Bracovirus; Polydnavirus; | |
Others : 1130525 DOI : 10.1186/1471-2148-12-253 |
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received in 2012-07-18, accepted in 2012-12-11, 发布年份 2012 | |
【 摘 要 】
Background
Gene duplications have been proposed to be the main mechanism involved in genome evolution and in acquisition of new functions. Polydnaviruses (PDVs), symbiotic viruses associated with parasitoid wasps, are ideal model systems to study mechanisms of gene duplications given that PDV genomes consist of virulence genes organized into multigene families. In these systems the viral genome is integrated in a wasp chromosome as a provirus and virus particles containing circular double-stranded DNA are injected into the parasitoids’ hosts and are essential for parasitism success. The viral virulence factors, organized in gene families, are required collectively to induce host immune suppression and developmental arrest. The gene family which encodes protein tyrosine phosphatases (PTPs) has undergone spectacular expansion in several PDV genomes with up to 42 genes.
Results
Here, we present strong indications that PTP gene family expansion occurred via classical mechanisms: by duplication of large segments of the chromosomally integrated form of the virus sequences (segmental duplication), by tandem duplications within this form and by dispersed duplications. We also propose a novel duplication mechanism specific to PDVs that involves viral circle reintegration into the wasp genome. The PTP copies produced were shown to undergo conservative evolution along with episodes of adaptive evolution. In particular recently produced copies have undergone positive selection in sites most likely involved in defining substrate selectivity.
Conclusion
The results provide evidence about the dynamic nature of polydnavirus proviral genomes. Classical and PDV-specific duplication mechanisms have been involved in the production of new gene copies. Selection pressures associated with antagonistic interactions with parasitized hosts have shaped these genes used to manipulate lepidopteran physiology with evidence for positive selection involved in adaptation to host targets.
【 授权许可】
2012 Serbielle et al.; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Arguello JR, Chen Y, Yang S, Wang W, Long M: Origination of an X-linked testes chimeric gene by illegitimate recombination in Drosophila. PLoS Genet 2006, 2:e77.
- [2]Katju V, Lynch M: The structure and early evolution of recently arisen gene duplicates in the Caenorhabditis elegans genome. Genetics 2003, 165:1793-1803.
- [3]Hasselmann M, Lechner S, Schulte C, Beye M: Origin of a function by tandem gene duplication limits the evolutionary capability of its sister copy. Proc Natl Acad Sci U S A 2010, 107:13378-13383.
- [4]Moleirinho A, Carneiro J, Matthiesen R, Silva R, Amorim A, Azevedo L: Gains, losses and changes of function after gene duplication: study of the metallothionein family. PLoS One 2011, 6:e18487.
- [5]Casewell N, Wagstaff S, Harrison R, Renjifo C, Wüster W: Domain loss facilitates accelerated evolution and neofunctionalization of duplicate snake venom metalloproteinase toxin genes. Mol Biol Evol 2011, 28:1157-1172.
- [6]Desjardins C, Gundersen-Rindal D, Hostetler J, Tallon L, Fadrosh D, Fuester R, Pedroni M, Haas B, Schatz M, Jones K, et al.: Comparative genomics of mutualistic viruses of Glyptapanteles parasitic wasps. Genome Biol 2008, 9:R183. BioMed Central Full Text
- [7]Belle E, Beckage NE, Rousselet J, Poirie M, Lemeunier F, Drezen J-M: Visualization of polydnavirus sequences in a parasitoid wasp chromosome. J Virol 2002, 76:5793-5796.
- [8]Fleming JGW, Summers MD: Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proc Natl Acad Sci U S A 1991, 88:9770-9774.
- [9]Asgari S, Hellers M, Schmidt O: Host haemocyte inactivation by an insect parasitoid: transient expression of a polydnavirus gene. J Gen Virol 1996, 77:2653-2662.
- [10]Beckage NE, Gelman DB: Wasp parasitoid disruption of host development: implications for new biologically based strategies of pest control. Annu Rev Entomol 2004, 49:299-330.
- [11]Tanaka K, Tsuzuki S, Matsumoto H, Hayakawa Y: Expression of Cotesia kariyai polydnavirus genes in lepidopteran hemocytes and Sf9 cells. J Insect Physiol 2000, 49:433-440.
- [12]Whitfield JB: Molecular and morphological data suggest a single origin of the polydnaviruses among braconid wasps. Naturwissenschaften 1997, 84:502-507.
- [13]Espagne E, Dupuy C, Huguet E, Cattolico L, Provost B, Martins N, Poirie M, Periquet G, Drezen JM: Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 2004, 306:286-289.
- [14]Dupuy C, Gundersen-Rindal D, Cusson M: Genomics and replication of polydnaviruses. In Parasitoid Viruses: Symbionts and Pathogens. Edited by Beckage NE, Drezen JM. San Diego, CA: Elsevier; 2011:47-58.
- [15]Webb BA, Strand MR, Dickey SE, Beck MH, Hilgarth RS, Barney WE, Kadash K, Kroemer JA, Lindstrom KG, Rattanadechakul W, et al.: Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 2006, 347:160-174.
- [16]Desjardins C, Gundersen-Rindal D, Hostetler J, Tallon L, Fuester R, Schatz M, Pedroni M, Fadrosh D, Haas B, Toms B, et al.: Structure and evolution of a proviral locus of Glyptapanteles indiensis bracovirus. BMC Microbiol 2007, 7:1-17. BioMed Central Full Text
- [17]Lapointe R, Tanaka K, Barney WE, Whitfield JB, Banks JC, Béliveau C, Stoltz D, Webb B, Cusson M: Genomic and morphological features of a banchine polydnavirus: comparison with bracovirus and ichnovirus. J Virol 2007, 81:6491-6501.
- [18]Moreau S, Huguet E, Drezen J-M: Polydnaviruses as tools to deliver wasp virulence factors to impair lepidopteran host immunity. In Insect Infection and Immunity evolution, ecology and mechanisms. Edited by Reynolds S, Rolff J. Oxford: Oxford University Press; 2009:137-158.
- [19]Chen Y, Gao F, Ye X-q, Wei S, Shi M, Zheng H-j, Chen X: Deep sequencing of Cotesia vestalis reveals the complexity of a polydnavirus genome. Virology 2011, 414:42-50.
- [20]Bezier A, Herbiniere J, Serbielle C, Lesobre J, Wincker P, Huguet E, Drezen JM: Bracovirus gene products are highly divergent from insect proteins. Arch Insect Biochem Physiol 2008, 67:172-187.
- [21]Serbielle C, Chowdhury S, Pichon S, Dupas S, Lesobre J, Purisima EO, Drezen JM, Huguet E: 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.
- [22]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, 47:378-395.
- [23]Whitfield JB: Estimating the age of the polydnavirus/braconid wasp symbiosis. Proc Natl Acad Sci U S A 2002, 99:7508-7513.
- [24]Bezier A, Annaheim M, Herbiniere J, Wetterwald C, Gyapay G, Bernard-Samain S, Wincker P, Roditi I, Heller M, Belghazi M, et al.: Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 2009, 323:926-930.
- [25]Drezen JM, Herniou E, Bézier A: Evolutionary progenitors of Bracoviruses. In Parasitoid Viruses: Symbionts and Pathogens. Edited by Beckage NE, Drezen JM. San Diego, CA: Elsevier; 2011:15-31.
- [26]Drezen JM, Bézier A, Lesobre J, Huguet E, Cattolico L, Periquet G, Dupuy C: The few virus like genes of Cotesia congregata bracovirus. Insect Biochem Physiol 2006, 61:110-122.
- [27]Dupuy C, Periquet G, Serbielle C, Bezier A, Louis F, Drezen JM: Transfer of a chromosomal Maverick to endogenous bracovirus in a parasitoid wasp. Genetica 2011, 139:489-496.
- [28]Andersen JN, Mortensen OH, Peters GH, Drake PG, Iversen LF, Olsen OH, Jansen PG, Andersen HS, Tonks NK, Moller NPH: Structural and evolutionary relationships among protein tyrosine phosphatase domains. Mol Cell Biol 2001, 21:7117-7136.
- [29]Provost B, Varricchio P, Arana E, Espagne E, Falabella P, Huguet E, La Scaleia R, Cattolico L, Poirie M, Malva C, et al.: Bracoviruses contain a large multigene family coding for protein tyrosine phosphatases. J Virol 2004, 78:13090-13103.
- [30]Gundersen-Rindal DE, Pedroni MJ: Characterization and transcriptional analysis of protein tyrosine phosphatase genes and an ankyrin repeat gene of the parasitoid Glyptapanteles indiensis polydnavirus in the parasitized host. J Gen Virol 2006, 87:311-322.
- [31]Ibrahim AMA, Choi JY, Je YH, Kim Y: Protein tyrosine phosphatases encoded in Cotesia plutellae bracovirus: Sequence analysis, expression profile, and a possible biological role in host immunosuppression. Dev Comp Immunol 2007, 31:978-990.
- [32]Pruijssers AJ, Strand MR: PTP-H2 and PTP-H3 from Microplitis demolitor Bracovirus localize to focal adhesions and are antiphagocytic in insect immune cells. J Virol 2007, 81:1209-1219.
- [33]Bitra K, Zhang S, Strand M: Transcriptomic profiling of Microplitis demolitor bracovirus reveals host, tissue and stage-specific patterns of activity. J Gen Virol 2011, 92:2060-2071.
- [34]Ibrahim AMA, Kim Y: Transient expression of protein tyrosine phosphatases encoded in Cotesia plutellae bracovirus inhibits insect cellular immune responses. Naturwissenschaften 2008, 95:25-32.
- [35]Eum J-H, Bottjen R, Pruijssers A, Clark K, Strand M: Characterization and kinetic analysis of protein tyrosine phosphatase-H2 from Microplitis demolitor bracovirus. Insect Biochem Mol Biol 2010, 40:690-698.
- [36]DeVinney I, Steele-Mortimer I, Finlay BB: Phosphatases and kinases delivered to the host cell by bacterial pathogens. Trends Microbiol 2000, 8:29-33.
- [37]Choi JY, Roh JY, Kang JN, Shim HJ, Woo SD, Jin BR, Li MS, Je YH: Genomic segments cloning and analysis of Cotesia plutellae polydnavirus using plasmid capture system. Biochem Biophys Res Commun 2005, 332:487-493.
- [38]Michel-Salzat A, Whitfield JB: Preliminary evolutionnary relationships within the parasitoids wasp genus Cotesia (Hymenoptera: Braconidae: Microgastrinae): combined analysis of four genes. Syst Entomol 2004, 29:371-382.
- [39]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, 85:11685-11696.
- [40]Gundersen-Rindal DE, Lynn DE: Polydnavirus integration in lepidopteran host cells in vitro. J Insect Physiol 2003, 49:453-462.
- [41]Innan H, Kondrashov F: The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 2010, 11:97-108.
- [42]Puius YA, Zhao Y, Sullivan M, Lawrence DS, Almo SC, Zhang ZY: Identification of a second aryl phosphate-binding site in protein-tyrosine phosphatase 1B: A paradigm for inhibitor design. Proc Natl Acad Sci U S A 1997, 94:13420-13425.
- [43]Salmeen A, Andersen JN, Myers MP, Tonks NK, Barford D: Molecular basis for the dephosphorylation of the activation segment of the insulin receptor by protein tyrosine phosphatase 1B. Mol Cell 2000, 6:1401-1412.
- [44]Peters GH, Iversen LF, Andersen HS, Moller NPH, Olsen OH: Residue 259 in protein-tyrosine phosphatase PTPlB and PTP alpha determines the flexibility of glutamine 262. Biochemistry 2004, 43:8418-8428.
- [45]Bailey JA, Eichler EE: Primate segmental duplications: crucibles of evolution, diversity and disease. Nat Rev Genet 2006, 7:552-564.
- [46]Gundersen-Rindal D, Dougherty EM: Evidence for integration of Glyptapanteles indiensis polydnavirus DNA into the chromosome of Lymantria dispar in vitro. Virus Res 2000, 66:27-37.
- [47]Gundersen-Rindal D: Integration of polydnaviruses DNA into host cellulargenomic DNA. In Parasitoid Viruses: Symbionts and Pathogens. Edited by Beckage NE, Drezen JM. San Diego, CA: Elsevier; 2011:99-113.
- [48]Savary S, Beckage NE, Tan F, Periquet G, Drezen JM: Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastinae) at potential recombinase binding sites. J Gen Virol 1997, 78:3125-3134.
- [49]Fan C, Chen Y, Long M: Recurrent tandem gene duplication gave rise to functionally divergent genes in Drosophila. Mol Biol Evol 2008, 25:1451-1458.
- [50]Ganko EW, Meyers BC, Vision TJ: Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol 2007, 10:2298-2309.
- [51]Hoffmann FG, Opazo JC, Storz JF: Rapid rates of lineage-specific gene duplication and deletion in the α-Globin gene family. Mol Biol Evol 2008, 25:591-602.
- [52]Hooper SD, Berg OG: On the nature of gene innovation: duplication patterns in microbial genomes. Mol Biol Evol 2003, 20:945-954.
- [53]Kaessmann H, Vinckenbosch N, Long MY: RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet 2009, 10:19-31.
- [54]Espagne E, Douris V, Lalmanach G, Provost B, Cattolico L, Lesobre J, Kurata S, Iatrou K, Drezen JM, Huguet E: A virus essential for insect host-parasite interactions encodes cystatins. J Virol 2005, 79:9765-9776.
- [55]Strand MR: Polydnavirus gene expression profiling: What we know now. In Parasitoid Viruses: Symbionts and Pathogens. Edited by Beckage NE, Drezen JM. San Diego, CA: Elsevier; 2011:139-147.
- [56]Nei M, Rooney AP: Concerted and birth and death evolution families. Annu Rev Genet 2005, 39:121-152.
- [57]Babushok D, Ostertag E, Kazazian H: Current topics in genome evolution: molecular mechanisms of new gene formation. Cell Mol Life Sci 2007, 64:542-554.
- [58]McBride CS: Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia. Proc Natl Acad Sci U S A 2007, 104:4996-5001.
- [59]Smith MA, Rodriguez JJ, Whitfield JB, Deans AR, Janzen DH, Hallwachs W, Hebert PDN: Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proc Natl Acad Sci U S A 2008, 105:12359-12364.
- [60]Ohno S: Evolution by gene duplication. New York: Springer; 1970.
- [61]Force A, Lynch M, Pickett FB, Amores A, Yan Y-l, Postlethwait J: Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545.
- [62]Des Marais DL, Rausher MD: Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature 2008, 454(7205):762-765.
- [63]Conant GC, Wolfe KH: Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 2008, 9:938-950.
- [64]Francino MP: An adaptive radiation model for the origin of new gene functions. Nat Genet 2005, 37:573-578.
- [65]Falabella P, Caccialupi P, Varricchio P, Malva C, Pennacchio F: Protein tyrosine phosphatases of Toxoneuron nigriceps Bracovirus as potential disrupters of host prothoracic gland function. Arch Insect Biochem Physiol 2006, 61:157-169.
- [66]Kamita SG, Nagasaka K, Chua JW, Shimada T, Mita K, Kobayashi M, Maeda S, Hammock BD: A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proc Natl Acad Sci U S A 2004, 102:2584-2589.
- [67]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, 25:4876-4882.
- [68]Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000, 17:540-552.
- [69]Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
- [70]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
- [71]Guindon S, Gascuel O: A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
- [72]Yang Z: PAML: A program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997, 13:555-556.
- [73]Yang Z, Nielsen R: Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 2002, 19:908-917.
- [74]Zhang J, Nielsen R, Yang Z: Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 2005, 22:2472-2479.
- [75]Swanson WJ, Nielsen R, Yang Q: Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 2003, 20:18-20.