Systematic phylogenetic analysis of influenza A virus reveals many novel mosaic genome segments

Infection, Genetics and Evolution

Volumn 18, Issue , 2013, Pages 367-378

  Lam, Tommy Tsan Yuk ^a   Chong, Yee Ling ^b   Shi, Mang ^c   Hon, Chung Chau ^d   Li, Jun ^e   Martin, Darren P ^f   Tang, Julian Wei Tze ^g   Mok, Chee Keng ^h   Shih, Shin Ru ^h   Yip, Chi Wai ^e   Jiang, Jingwei ^e   Hui, Raymond Kin Hei ^e   Pybus, Oliver G ^a   Holmes, Edward C ^c,i   Leung, Frederick Chi Ching ^e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITI MALAYSIA SARAWAK   (Malaysia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d INSTITUT PASTEUR   (France)

^e UNIVERSITY OF HONG KONG   (Hong Kong)

^f UNIVERSITY OF CAPE TOWN   (South Africa)

^g UNIVERSITY OF ALBERTA   (Canada)

^h CHANG GUNG UNIVERSITY   (Taiwan)

ⁱ NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Influenza A virus; Mosaic pattern; Mosaic screening protocol; Recombination

Indexed keywords

ARTICLE; CHROMOSOME BREAKAGE; CHRONOLOGY; CONTROLLED STUDY; GENE IDENTIFICATION; GENE SEQUENCE; GEOGRAPHY; INFLUENZA VIRUS A; MOSAICISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SIMULATION; VIRUS GENOME; VIRUS RECOMBINANT;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE; RNA VIRUSES;

INFLUENZA A VIRUS; MOSAIC PATTERN; MOSAIC SCREENING PROTOCOL; RECOMBINATION;

ANIMALS; BIRDS; DATABASES, GENETIC; GENOME, VIRAL; GENOMICS; HUMANS; INFLUENZA A VIRUS; INFLUENZA IN BIRDS; INFLUENZA, HUMAN; LINEAR MODELS; MOSAICISM; PHYLOGENY; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, RNA;

EID: 84880816395     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2013.03.015     Document Type: Article

References (56)

1. Anisimova M., Nielsen R., Yang Z. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 2003, 164:1229-1236.
2. Bao Y., Bolotov P., Dernovoy D., Kiryutin B., Zaslavsky L., Tatusova T., Ostell J., Lipman D. The influenza virus resource at the National Center for Biotechnology Information. J. Virol. 2008, 82:596-601.
3. Boni M.F., de Jong M.D., van Doorn H.R., Holmes E.C. Guidelines for identifying homologous recombination events in influenza A virus. PLoS ONE 2010, 5:e10434.
4. Boni M.F., Posada D., Feldman M.W. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 2007, 176:1035-1047.
5. Boni M.F., Zhou Y., Taubenberger J.K., Holmes E.C. Homologous recombination is very rare or absent in human influenza A virus. J. Virol. 2008, 82:4807-4811.
6. Boni M.F., Smith G.J.D., Holmes E.C., Vijaykrishna D. No evidence for intra-segment recombination of 2009 H1N1 influenza virus in swine. Gene 2012, 494:242-245.
7. Brown I.H., Harris P.A., McCauley J.W., Alexander D.J. Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. J. Gen. Virol. 1998, 79(Pt 12):2947-2955.
8. Cauthen A.N., Swayne D.E., Schultz-Cherry S., Perdue M.L., Suarez D.L. Continued circulation in China of highly pathogenic avian influenza viruses encoding the hemagglutinin gene associated with the 1997 H5N1 outbreak in poultry and humans. J. Virol. 2000, 74:6592-6599.
9. Chare E.R., Gould E.A., Holmes E.C. Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. J. Gen. Virol. 2003, 84:2691-2703.
10. Chen H., Deng G., Li Z., Tian G., Li Y., Jiao P., Zhang L., Liu Z., Webster R.G., Yu K. The evolution of H5N1 influenza viruses in ducks in southern China. Proc. Natl. Acad. Sci. USA 2004, 101:10452-10457.
11. Chen R., Holmes E.C. Avian influenza virus exhibits rapid evolutionary dynamics. Mol. Biol. Evol. 2006, 23:2336-2341.
12. de Silva A., Messer W. Arguments for live flavivirus vaccines. Lancet 2004, 364:500.
13. Dugan V.G., Chen R., Spiro D.J., Sengamalay N., Zaborsky J., Ghedin E., Nolting J., Swayne D.E., Runstadler J.A., Happ G.M., Senne D.A., Wang R., Slemons R.D., Holmes E.C., Taubenberger J.K. The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog. 2008, 4:e1000076.
14. Edgar R.C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 2004, 5:113.
15. Emerson B.C., Paradis E., Thébaud C. Revealing the demographic histories of species using DNA sequences. Trends Ecol. Evol. 2001, 16:707-716.
16. Galli A., Lai A., Corvasce S., Saladini F., Riva C., Deho L., Caramma I., Franzetti M., Romano L., Galli M., Zazzi M., Balotta C. Recombination analysis and structure prediction show correlation between breakpoint clusters and RNA hairpins in the pol gene of human immunodeficiency virus type 1 unique recombinant forms. J. Gen. Virol. 2008, 89:3119-3125.
17. Ghedin E., Fitch A., Boyne A., Griesemer S., DePasse J., Bera J., Zhang X., Halpin R.A., Smit M., Jennings L., St George K., Holmes E.C., Spiro D.J. Mixed infection and the genesis of influenza virus diversity. J. Virol. 2009, 83:8832-8841.
18. Guan Y., Peiris M., Kong K.F., Dyrting K.C., Ellis T.M., Sit T., Zhang L.J., Shortridge K.F. H5N1 influenza viruses isolated from geese in Southeastern China: evidence for genetic reassortment and interspecies transmission to ducks. Virology 2002, 292:16-23.
19. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
20. He C.Q., Han G.Z., Wang D., Liu W., Li G.R., Liu X.P., Ding N.Z. Homologous recombination evidence in human and swine influenza A viruses. Virology 2008, 380:12-20.
21. He C.Q., Xie Z.X., Han G.Z., Dong J.B., Wang D., Liu J.B., Ma L.Y., Tang X.F., Liu X.P., Pang Y.S., Li G.R. Homologous recombination as an evolutionary force in the avian influenza A virus. Mol. Biol. Evol. 2009, 26:177-187.
22. Hofacker I.L., Fontana W., Stadler P.F., Bonhoeffer L.S., Tacker M., Schuster P. Fast folding and comparison of RNA secondary structures. Monatsh. Chem. 1994, 167-188.
23. Hoffmann E., Stech J., Leneva I., Krauss S., Scholtissek C., Chin P.S., Peiris M., Shortridge K.F., Webster R.G. Characterization of the influenza A virus gene pool in avian species in southern China: was H6N1 a derivative or a precursor of H5N1?. J. Virol. 2000, 74:6309-6315.
24. Holmes E.C., Worobey M., Rambaut A. Phylogenetic evidence for recombination in dengue virus. Mol. Biol. Evol. 1999, 16:405-409.
25. Jenkins G.M., Rambaut A., Pybus O.G., Holmes E.C. Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J. Mol. Evol. 2002, 54:156-165.
26. Judo M.S., Wedel A.B., Wilson C. Stimulation and suppression of PCR-mediated recombination. Nucleic Acids Res. 1998, 26:1819-1825.
27. Kou Z., Lei F.M., Yu J., Fan Z.J., Yin Z.H., Jia C.X., Xiong K.J., Sun Y.H., Zhang X.W., Wu X.M., Gao X.B., Li T.X. New genotype of avian influenza H5N1 viruses isolated from tree sparrows in China. J. Virol. 2005, 79:15460-15466.
28. Krasnitz M., Levine A.J., Rabadan R. Anomalies in the influenza virus genome database: new biology or laboratory errors?. J. Virol. 2008, 82:8947-8950.
29. Lam T.Y., Hon C.C., Wang Z., Hui R.K., Zeng F., Leung F.C. Evolutionary analyses of European H1N2 swine influenza A virus by placing timestamps on the multiple reassortment events. Virus Res. 2008, 131:271-278.
30. Li C., Yu K., Tian G., Yu D., Liu L., Jing B., Ping J., Chen H. Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology 2005, 340:70-83.
31. Liu J.H., Okazaki K., Shi W.M., Wu Q.M., Mweene A.S., Kida H. Phylogenetic analysis of neuraminidase gene of H9N2 influenza viruses prevalent in chickens in China during 1995-2002. Virus Genes 2003, 27:197-202.
32. Lole K.S., Bollinger R.C., Paranjape R.S., Gadkari D., Kulkarni S.S., Novak N.G., Ingersoll R., Sheppard H.W., Ray S.C. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J. Virol. 1999, 73:152-160.
33. Martin D., Rybicki E. RDP: detection of recombination amongst aligned sequences. Bioinformatics 2000, 16:562-563.
34. Martin D.P., Williamson C., Posada D. RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 2005, 21:260-262.
35. Meyerhans A., Vartanian J.P., Wain-Hobson S. DNA recombination during PCR. Nucleic Acids Res. 1990, 18:1687-1691.
36. Padidam M., Sawyer S., Fauquet C.M. Possible emergence of new geminiviruses by frequent recombination. Virology 1999, 265:218-225.
37. Parrish C.R., Kawaoka Y. The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu. Rev. Microbiol. 2005, 59:553-586.
38. Poon A.F., Frost S.D., Pond S.L. Detecting signatures of selection from DNA sequences using Datamonkey. Methods Mol. Biol. 2009, 537:163-183.
39. Posada D. Unveiling the molecular clock in the presence of recombination. Mol. Biol. Evol. 2001, 18:1976-1978.
40. Posada D., Crandall K.A. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc. Natl. Acad. Sci. USA 2001, 98:13757-13762.
41. Posada D., Crandall K.A., Holmes E.C. Recombination in evolutionary genomics. Annu. Rev. Genet. 2002, 36:75-97.
42. Scheffler K., Martin D.P., Seoighe C. Robust inference of positive selection from recombining coding sequences. Bioinformatics 2006, 22:2493-2499.
43. Schierup M.H., Hein J. Consequences of recombination on traditional phylogenetic analysis. Genetics 2000, 156:879-891.
44. Schierup M.H., Hein J. Recombination and the molecular clock. Mol. Biol. Evol. 2000, 17:1578-1579.
45. Shafikhani S. Factors affecting PCR-mediated recombination. Environ. Microbiol. 2002, 4:482-486.
46. Shimodaira H., Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 1999, 16:1114-1116.
47. Shriner D., Nickle D.C., Jensen M.A., Mullins J.I. Potential impact of recombination on sitewise approaches for detecting positive natural selection. Genet. Res. 2003, 81:115-121.
48. Simon-Loriere E., Galetto R., Hamoudi M., Archer J., Lefeuvre P., Martin D.P., Robertson D.L., Negroni M. Molecular mechanisms of recombination restriction in the envelope gene of the human immunodeficiency virus. PLoS Pathog. 2009, 5:e1000418.
49. Simon-Loriere E., Holmes E.C. Why do RNA viruses recombine?. Nat. Rev. Microbiol. 2011, 9:617-626.
50. Smith G.J., Fan X.H., Wang J., Li K.S., Qin K., Zhang J.X., Vijaykrishna D., Cheung C.L., Huang K., Rayner J.M., Peiris J.S., Chen H., Webster R.G., Guan Y. Emergence and predominance of an H5N1 influenza variant in China. Proc. Natl. Acad. Sci. USA 2006, 103:16936-16941.
51. Smith J.M. Analyzing the mosaic structure of genes. J. Mol. Evol. 1992, 34:126-129.
52. Swofford D.L. PAUP*. Phylogenetic Analysis Using Parsimony 2003, Sinauer Associates, Sunderland, Massachusetts, (*and Other Methods). Version fourth ed.
53. Webster R.G., Bean W.J., Gorman O.T., Chambers T.M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 1992, 56:152-179.
54. Worobey M., Holmes E.C. Evolutionary aspects of recombination in RNA viruses. J. Gen. Virol. 1999, 80(Pt 10):2535-2543.
55. Worobey M., Rambaut A., Pybus O.G., Robertson D.L. Questioning the evidence for genetic recombination in the 1918 "Spanish flu" virus. Science 2002, 296:211. discussion 211.
56. Xu K.M., Smith G.J., Bahl J., Duan L., Tai H., Vijaykrishna D., Wang J., Zhang J.X., Li K.S., Fan X.H., Webster R.G., Chen H., Peiris J.S., Guan Y. The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J. Virol. 2007, 81:10389-10401.