1887

Journal of General Virology header logo

Volume 83, Issue 6

Molecular evolution of : evidence of host adaptation, genetic recombination and geographical spread Free

Abstract

(TuMV), a species of the genus , occurs worldwide. Seventy-six isolates of TuMV were collected from around the world, mostly from and crops, but also from several non-brassica species. Host tests grouped the isolates into one or other of two pathotypes; (B) and (BR). The nucleotide sequences of the first protein (P1) and coat protein (CP) genes of the isolates were determined. One-tenth of the isolates were found to have anomalous and variable phylogenetic relationships as a result of recombination. The 5′-terminal 300 nt of the P1 gene of many isolates was also variable and phylogenetically anomalous, whereas the 380 nt 3′ terminus of the CP gene was mostly conserved. Trees calculated from the remaining informative parts of the two genes of the non-recombinant sequences by neighbour-joining, maximum-likelihood and maximum-parsimony methods were closely similar, and so these parts of the sequences were concatenated and trees calculated from the resulting 1150 nt. The isolates fell into four consistent groups; only the relationships of these groups with one another and with the outgroup differed. The ‘basal-B’ cluster of eight B-pathotype isolates was most variable, was not monophyletic, and came from both brassicas and non-brassicas from southwest and central Eurasia. Closest to it, and forming a monophyletic subgroup of it in most trees, and similarly variable, was the ‘basal-BR’ group of eight BR pathotype Eurasian isolates. The third and least variable group, the ‘Asian-BR’ group, was of 22 BR-pathotype isolates, all from brassicas, mostly , and all from east Asia mostly Japan. The fourth group of 36 isolates, the ‘world-B’ group, was from all continents, most were isolated from brassicas and most were of the B-pathotype. The simplest of several possible interpretations of the trees is that TuMV originated, like its brassica hosts, in Europe and spread to the other parts of the world, and that the BR pathotype has recently evolved in east Asia.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-6-1511
2002-06-01
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/6/0831511a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-6-1511&mimeType=html&fmt=ahah

References

  1. Aleman-Verdaguer M.-E., Goudou-Urbino C., Dubern J., Beachy R. N., Fauquet C. 1997; Analysis of the sequence diversity of the P1, HC, P3, NIb and CP genomic regions of several yam mosaic potyvirus isolates: implications for the intraspecies molecular diversity of potyviruses. Journal of General Virology 78:1253–1264
     [Google Scholar]
  2. Bateson M. F., Henderson J., Chaleeprom W., Gibbs A. J., Dale J. L. 1994; Papaya ringspot potyvirus: isolate variability and the origin of PRSV type P (Australia. Journal of General Virology 75:3547–3553
     [Google Scholar]
  3. Bousalem M., Douzery E. J. P., Fargette D. 2000; High genetic diversity, distant phylogenetic relationships and intraspecies recombination events among natural populations of Yam mosaic virus : a contribution to understanding potyvirus evolution. Journal of General Virology 81:243–255
     [Google Scholar]
  4. Clark M. F., Adams A. N. 1977; Characteristic of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology 34:475–483
     [Google Scholar]
  5. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
     [Google Scholar]
  6. Felsenstein J. 1993 PHYLIP (Phylogeny Interference Package), version 3.5 Department of Genetics, University of Washington; Seattle, USA:
     [Google Scholar]
  7. Fraile A., Aranda M. A., García-Arenal F. 1995; Evolution of the tobamoviruses. In Molecular Basis of Virus Evolution pp 338–350 Edited by Gibbs A., Calisher C. H., García-Arenal F. Cambridge: Cambridge University Press;
     [Google Scholar]
  8. Fraile A., Escriu F., Aranda M. A., Malpica J. M., Gibbs A. J., García-Arenal F. 1997; A century of tobamovirus evolution in an Australian population of Nicotiana glauca . Journal of Virology 71:8316–8320
     [Google Scholar]
  9. Fuji S., Nakamae H. 1999; Complete nucleotide sequence of the genomic RNA of a Japanese yam mosaic virus, a new potyvirus in Japan. Archives of Virology 144:231–240
     [Google Scholar]
  10. Gal-On A., Meiri E., Raccah B., Gaba V. 1998; Recombination of engineered defective RNA species produces infective potyvirus in planta. Journal of Virology 72:5268–5270
     [Google Scholar]
  11. Gao F., Bailes E., Robertson D. L., Chen Y., Rodenburg C. M., Michael S. F., Cummins L. B., Arthur L. O., Peeters M., Shaw G. M., Sharp P. M., Hahn B. H. 1999; Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes . Nature 397:436–441
     [Google Scholar]
  12. Gibbs M. J., Armstrong J. S., Gibbs A. J. 2000; Sister-Scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582
     [Google Scholar]
  13. Gibbs M. J., Armstrong J. S., Gibbs A. J. 2001; Recombination in the hemagglutinin gene of the 1918 ‘Spanish Flu′. Science 293:1842–1845
     [Google Scholar]
  14. Gubler U., Hoffman B. J. 1983; A simple and very efficient method for generating cDNA libraries. Gene 25:263–269
     [Google Scholar]
  15. Holland J., Domingo E. 1998; Origin and evolution of viruses. Virus Genes 16:13–21
     [Google Scholar]
  16. Jeanmougin F., Thompson J. D., Gouy M., Higgins D. G., Gibson T. J. 1998; Multiple sequence alignment with Clustal X. Trends in Biochemical Sciences 23:403–405
     [Google Scholar]
  17. Kimura M. 1980; A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequence. Journal of Molecular Evolution 16:111–120
     [Google Scholar]
  18. Lehmann P., Petrzik K., Jenner C., Greenland A., Špak J., Kozubek E., Walsh J. A. 1997; Nucleotide and amino acid variation in the coat protein coding region of turnip mosaic virus isolates and possible involvement in the interaction with the brassica resistance gene TuRBO1. Physiological and Molecular Plant Pathology 51:195–208
     [Google Scholar]
  19. McCutchan F. E., Salminen M. O., Carr J. K., Burke D. S. 1996; HIV-1 genetic diversity. AIDS 10: Supplement 313–20
     [Google Scholar]
  20. Masuta C., Ueda S., Suzuki M., Uyeda I. 1998; Evolution of a quadripartite hybrid virus by interspecific exchange and recombination between replicase components of two related tripartite RNA viruses. Proceedings of the National Academy of Sciences, USA 95:10487–10492
     [Google Scholar]
  21. Nicolas O., Laliberté J.-F. 1992; The complete nucleotide sequence of turnip mosaic potyvirus RNA. Journal of General Virology 73:2785–2793
     [Google Scholar]
  22. Ohshima K., Tanaka M., Sako N. 1996; The complete nucleotide sequence of turnip mosaic virus RNA Japanese strain. Archives of ViroIogy 141:1991–1997
     [Google Scholar]
  23. Padidam M., Sawyer S., Fauquet C. M. 2000; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225
     [Google Scholar]
  24. Page R. D. 1996; TreeView: an application to display phylogenetic trees on personal computer. Computer Applications in the Biosciences 12:357–358
     [Google Scholar]
  25. Provvidenti R. 1996; Turnip mosaic potyvirus. In Viruses of Plants pp 1340–1343 Edited by Brunt A. A., Crabtree K., Dallwitz M. J., Gibbs A. J., Watson L. Wallingford, UK: CAB International;
     [Google Scholar]
  26. Reid A. H., Fanning T. G., Hultin J. V., Taubenberger J. K. 1999; Origin and evolution of the 1918 ‘Spanish′ influenza virus hemagglutinin gene. Proceedings of the National Academy of Sciences, USA 96:1651–1656
     [Google Scholar]
  27. Revers F., Le Gall O., Candresse T., Le Romancer M., Dunez J. 1996; Frequent occurrence of recombinant potyvirus isolates. Journal of General Virology 77:1953–1965
     [Google Scholar]
  28. Revers F., Lot H., Souche S., Le Gall O., Candresse T., Dunez J. 1997; Biological and molecular variability of lettuce mosaic virus isolates. Phytopathology 87:397–403
     [Google Scholar]
  29. Riechmann J. L., Laín S., García J. A. 1992; Highlights and prospects of potyvirus molecular biology. Journal of General Virology 73:1–16
     [Google Scholar]
  30. Robertson D. L., Sharp P. M., McCutchan F. E., Hahn B. H. 1995; Recombination in HIV-1. Nature 374:124–126
     [Google Scholar]
  31. Roossinck M. 1997; Mechanisms of plant virus evolution. Annual Review of Phytopathology 35:191–209
     [Google Scholar]
  32. Roossinck M. J., Lee Z., Hellwald K.-H. 1999; Rearrangements in the 5′ nontranslated region and phylogenetic analyses of cucumber mosaic virus RNA 3 indicate radial evolution of three subgroups. Journal of Virology 73:6752–6758
     [Google Scholar]
  33. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4:406–425
     [Google Scholar]
  34. Sanz A. I., Fraile A., García-Arenal F., Zhou X., Robinson D. J., Khalid S., Butt T., Harrison B. D. 2000; Multiple infection, recombination and genome relationships among begomovirus isolates found in cotton and other plants in Pakistan. Journal of General Virology 81:1839–1849
     [Google Scholar]
  35. Schneider W. L., Roossinck M. J. 2000; Evolutionarily related Sindbis-like plant viruses maintain different levels of population diversity in a common host. Journal of Virology 74:3130–3134
     [Google Scholar]
  36. Sevilla N., Domingo E. 1996; Evolution of a persistent aphthovirus in cytolytic infections: partial reversion of phenotypic traits accompanied by genetic diversification. Journal of Virology 70:6617–6624
     [Google Scholar]
  37. Shukla D. D., Ward C. W., Brunt A. A. 1994; Introduction. In The Potyviridae pp 1–26 Edited by Shukla D. D., Ward C. W., Brunt A. A. Wallingford, UK: CAB International;
     [Google Scholar]
  38. Simon A. E., Bujarski J. J. 1994; RNA–RNA recombination and evolution in virus-infected plants. Annual Review of Phytopathology 32:337–362
     [Google Scholar]
  39. Smith G. R., Borg Z., Lockhart B. E., Braithwaite K. S., Gibbs M. J. 2000; Sugarcane yellow leaf virus: a novel member of the Luteoviridae that probably arose by inter-species recombination. Journal of General Virology 81:1865–1869
     [Google Scholar]
  40. Strimmer K., von Haeseler A. 1996; Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13:964–969
     [Google Scholar]
  41. Strimmer K., Goldman N., von Haeseler A. 1997; Bayesian probabilities and quartet puzzling. Molecular Biology and Evolution 14:210–211
     [Google Scholar]
  42. Swofford D. L. 1998 PAUP. Phylogenetic analysis using parsimony. Version 4 Sinauer Associates; Sunderland, MA, USA:
     [Google Scholar]
  43. Thompson J. D., Higgins D. G., Gibson T. J. 1994; CLUSTAL W. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22:4673–4680
     [Google Scholar]
  44. Tordo V. M.-J., Chachulska A. M., Fakhfakh H., Le Romancer M., Robaglia C., Astier-Manifacier S. 1995; Sequence polymorphism in the 5′ NTR and in the P1 coding region of potato virus Y genomic RNA. Journal of General Virology 76:939–949
     [Google Scholar]
  45. Van der Vlugt R. A. A., Leunissen J., Goldbach R. 1993; Taxonomic relationships between distinct potato virus Y isolates based on detailed comparisons of the viral coat proteins and 3′-nontranslated regions. Archives of Virology 131:361–375
     [Google Scholar]
  46. Ward C. W., Weiller G. F., Shukla D. D., Gibbs A. 1995; Molecular systematics of the Potyviridae, the largest plant virus family. In Molecular Basis of Virus Evolution pp 477–500 Edited by Gibbs A., Calisher C. H., García-Arenal F. Cambridge: Cambridge University Press;
     [Google Scholar]
  47. Weiller G. F. 1998; Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Molecular Biology and Evolution 15:326–335
     [Google Scholar]
  48. Weiller G. F., Gibbs A. 1995; DIPLOMO: the tool for a new type of evolutionary analysis. Computer Applications in the Biosciences 11:535–540
     [Google Scholar]
  49. Worobey M. 2000; Extensive homologous recombination among widely divergent TT viruses. Journal of Virology 74:7666–7670
     [Google Scholar]
  50. Zylstra P., Rothenfluh H. S., Weiller G. S., Blanden R. V., Steele E. J. 1998; PCR amplification of murine immunoglobulin germline V genes: strategies for minimization of recombination artefacts. Immunology and Cell Biology 76:395–405
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-6-1511
Loading
Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread
J. Gen. Virol. 83, 1511 (2002); https://doi.org/10.1099/0022-1317-83-6-1511
/content/journal/jgv/10.1099/0022-1317-83-6-1511
/content/journal/jgv/10.1099/0022-1317-83-6-1511
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error