1887

Abstract

The genetic variation and population structure of (SMV) in Iran was analysed through the characterization of a set of isolates collected in the soybean-growing provinces of Iran. The partial nucleotide sequence of these isolates showed a single, undifferentiated population with low genetic diversity, highly differentiated from other SMV world populations. These traits are compatible with a population bottleneck associated with the recent introduction of SMV in Iran. Phylogenetic analyses suggest that SMV was introduced into Iran from East Asia, with at least three introduction events. The limited genetic diversification of SMV in Iran may be explained by strong negative selection in most viral genes eliminating the majority of mutations, together with recombination purging deleterious mutations. The pathogenicity of Iranian SMV isolates was typified on a set of soybean differential lines either susceptible or carrying different resistance genes or alleles to SMV. Two pathotypes were distinguished according to the ability to overcome 4 resistance in line V94-5152. Amino acid sequence comparisons of virulent and avirulent isolates on V94-5152 (4), plus site-directed mutagenesis in a biologically active cDNA clone, identified mutation S1053N in the P3 protein as the determinant for virulence on V94-5152. Codon 1053 was shown to be under positive selection, and S1053N-determined 4-virulence occurred in isolates with different genealogies. The V94-5152 (4)-virulence determinant in Iranian isolates maps into a different amino acid position in the P3 protein than those previously reported, indicating different evolutionary pathways towards resistance breaking that might be conditioned by sequence context.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.055434-0
2013-11-01
2020-01-27
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/11/2557.html?itemId=/content/journal/jgv/10.1099/vir.0.055434-0&mimeType=html&fmt=ahah

References

  1. Adams M. J., Antoniw J. F., Fauquet C. M.. ( 2005;). Molecular criteria for genus and species discrimination within the family Potyviridae.. Arch Virol 150:, 459–479. [CrossRef][PubMed]
    [Google Scholar]
  2. Amirshahi M. C.. ( 1976;). Soybean production and research in Iran. . INTSOY Ser 10:, 236.
    [Google Scholar]
  3. Anonymous ( 2011;). FAO statistics. http://faostat.fao.org/
    [Google Scholar]
  4. Chao L.. ( 1990;). Fitness of RNA virus decreased by Muller’s ratchet. . Nature 348:, 454–455. [CrossRef][PubMed]
    [Google Scholar]
  5. Chare E. R., Holmes E. C.. ( 2004;). Selection pressures in the capsid genes of plant RNA viruses reflect mode of transmission. . J Gen Virol 85:, 3149–3157. [CrossRef][PubMed]
    [Google Scholar]
  6. Chare E. R., Holmes E. C.. ( 2006;). A phylogenetic survey of recombination frequency in plant RNA viruses. . Arch Virol 151:, 933–946. [CrossRef][PubMed]
    [Google Scholar]
  7. Chen P., Ma G., Buss G. R., Gunduz I., Roane C. W., Tolin S. A.. ( 2001;). Inheritance and allelism tests of Raiden soybean for resistance to Soybean mosaic virus.. J Hered 92:, 51–55. [CrossRef][PubMed]
    [Google Scholar]
  8. Cho E. K., Goodman R. M.. ( 1979;). Strains of Soybean mosaic virus classification based on virulence in resistanct soybean cultivars. . Phytopathology 69:, 467–470. [CrossRef]
    [Google Scholar]
  9. Choi B. K., Koo J. M., Ahn H. J., Yum H. J., Choi C. W., Ryu K. H., Chen P., Tolin S. A.. ( 2005;). Emergence of Rsv-resistance breaking Soybean mosaic virus isolates from Korean soybean cultivars. . Virus Res 112:, 42–51. [CrossRef][PubMed]
    [Google Scholar]
  10. Chowda-Reddy R. V., Sun H., Chen H., Poysa V., Ling H., Gijzen M., Wang A.. ( 2011a;). Mutations in the P3 protein of Soybean mosaic virus G2 isolates determine virulence on Rsv4-genotype soybean. . Mol Plant Microbe Interact 24:, 37–43. [CrossRef][PubMed]
    [Google Scholar]
  11. Chowda-Reddy R. V., Sun H., Hill J. H., Poysa V., Wang A.. ( 2011b;). Simultaneous mutations in multi-viral proteins are required for Soybean mosaic virus to gain virulence on soybean genotypes carrying different R genes. . PLoS ONE 6:, e28342. [CrossRef][PubMed]
    [Google Scholar]
  12. Chung B. Y., Miller W. A., Atkins J. F., Firth A. E.. ( 2008;). An overlapping essential gene in the Potyviridae. . Proc Natl Acad Sci U S A 105:, 5897–5902. [CrossRef][PubMed]
    [Google Scholar]
  13. Cuevas J. M., Delaunay A., Visser J. C., Bellstedt D. U., Jacquot E., Elena S. F.. ( 2012;). Phylogeography and molecular evolution of Potato virus Y.. PLoS ONE 7:, e37853. [CrossRef][PubMed]
    [Google Scholar]
  14. Domier L. L., Steinlage T. A., Hobbs H. A., Wang Y., Herrera-Rodriguez G., Haudenshield J. S., McCoppin N. K., Hartman G. L.. ( 2007;). Similarities in seed and aphid transmission among Soybean mosaic virus isolates. . Plant Dis 91:, 546–550. [CrossRef]
    [Google Scholar]
  15. Duarte E. A., Clarke D. K., Moya A., Domingo E., Holland J. J.. ( 1992;). Rapid fitness losses in mammalian RNA virus clones due to Muller’s ratchet. . Proc Natl Acad Sci U S A 89:, 6015–6019. [CrossRef][PubMed]
    [Google Scholar]
  16. Eggenberger A. L., Hajimorad M. R., Hill J. H.. ( 2008;). Gain of virulence on Rsv1-genotype soybean by an avirulent Soybean mosaic virus requires concurrent mutations in both P3 and HC-Pro. . Mol Plant Microbe Interact 21:, 931–936. [CrossRef][PubMed]
    [Google Scholar]
  17. Elena S. F., Sanjuán R.. ( 2005;). Adaptive value of high mutation rates of RNA viruses: separating causes from consequences. . J Virol 79:, 11555–11558. [CrossRef][PubMed]
    [Google Scholar]
  18. Eskandari F.. ( 1978;). Studies on soybean mosaic in Iran. . Z Pflanzenkr Pflanzenschutz 85:, 686–688.
    [Google Scholar]
  19. Excoffier L., Laval G., Schneider S.. ( 2005;). ARLEQUIN ver. 3.0: an integrated software package for population genetics data analysis. . Evol Bioinform Online 1:, 47–50. [PubMed]
    [Google Scholar]
  20. Farzadfar Sh., Golnaraghi A. R., Pourrahim R.. ( 2002;). Plant Viruses of Iran. Tehran:: Saman;.
    [Google Scholar]
  21. 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.. J Virol 71:, 8316–8320.[PubMed]
    [Google Scholar]
  22. Gagarinova A. G., Babu M., Poysa V., Hill J. H., Wang A.. ( 2008a;). Identification and molecular characterization of two naturally occurring Soybean mosaic virus isolates that are closely related but differ in their ability to overcome Rsv4 resistance. . Virus Res 138:, 50–56. [CrossRef][PubMed]
    [Google Scholar]
  23. Gagarinova A. G., Babu M., Strömvik M. V., Wang A.. ( 2008b;). Recombination analysis of Soybean mosaic virus sequences reveals evidence of RNA recombination between distinct pathotypes. . Virol J 5:, 143. [CrossRef][PubMed]
    [Google Scholar]
  24. García-Arenal F., Fraile A., Malpica J. M.. ( 2001;). Variability and genetic structure of plant virus populations. . Annu Rev Phytopathol 39:, 157–186. [CrossRef][PubMed]
    [Google Scholar]
  25. Gibbs A. J., Ohshima K., Phillips M. J., Gibbs M. J.. ( 2008;). The prehistory of potyviruses: their initial radiation was during the dawn of agriculture. . PLoS ONE 3:, e2523. [CrossRef][PubMed]
    [Google Scholar]
  26. Gibbs A. J., Fargette D., García-Arenal F., Gibbs M. J.. ( 2010;). Time–the emerging dimension of plant virus studies. . J Gen Virol 91:, 13–22. [CrossRef][PubMed]
    [Google Scholar]
  27. Guindon S., Gascuel O.. ( 2003;). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. . Syst Biol 52:, 696–704. [CrossRef][PubMed]
    [Google Scholar]
  28. Gunduz I., Buss G. R., Chen P., Tolin S. A.. ( 2002;). Characterization of SMV resistance genes in Tousan 140 and Hourei soybean. . Crop Sci 42:, 90–95. [CrossRef][PubMed]
    [Google Scholar]
  29. Gunduz I., Buss G. R., Chen P., Tolin S. A.. ( 2004;). Genetic and phenotypic analysis of Soybean mosaic virus resistance in PI 88788 soybean. . Phytopathology 94:, 687–692. [CrossRef][PubMed]
    [Google Scholar]
  30. Hajimorad M. R., Hill J. H.. ( 2001;). Rsv1-mediated resistance against Soybean mosaic virus-N is hypersensitive response-independent at inoculation site, but has the potential to initiate a hypersensitive response-like mechanism. . Mol Plant Microbe Interact 14:, 587–598. [CrossRef][PubMed]
    [Google Scholar]
  31. Hajimorad M. R., Eggenberger A. L., Hill J. H.. ( 2003;). Evolution of Soybean mosaic virus-G7 molecularly cloned genome in Rsv1-genotype soybean results in emergence of a mutant capable of evading Rsv1-mediated recognition. . Virology 314:, 497–509. [CrossRef][PubMed]
    [Google Scholar]
  32. Hajimorad M. R., Eggenberger A. L., Hill J. H.. ( 2008;). Adaptation of Soybean mosaic virus avirulent chimeras containing P3 sequences from virulent strains to Rsv1-genotype soybeans is mediated by mutations in HC-Pro. . Mol Plant Microbe Interact 21:, 937–946. [CrossRef][PubMed]
    [Google Scholar]
  33. Hajimorad M. R., Wen R. H., Eggenberger A. L., Hill J. H., Maroof M. A.. ( 2011;). Experimental adaptation of an RNA virus mimics natural evolution. . J Virol 85:, 2557–2564. [CrossRef][PubMed]
    [Google Scholar]
  34. Hartman G. L., West E. D., Herman T. K.. ( 2011;). Crops that feed the World 2. Soybean-worldwide production, use, and constraints caused by pathogens and pests. . Food Sec 3:, 5–17. [CrossRef]
    [Google Scholar]
  35. Hayes A. J., Ma G., Buss G. R., Maroof M. A.. ( 2000;). Molecular marker mapping of Rsv4, a gene conferring resistance to all known strains of Soybean mosaic virus. . Crop Sci 40:, 1434–1437. [CrossRef]
    [Google Scholar]
  36. Hayes A. J., Jeong S. C., Gore M. A., Yu Y. G., Buss G. R., Tolin S. A., Maroof M. A.. ( 2004;). Recombination within a nucleotide-binding-site/leucine-rich-repeat gene cluster produces new variants conditioning resistance to Soybean mosaic virus in soybeans. . Genetics 166:, 493–503. [CrossRef][PubMed]
    [Google Scholar]
  37. Hjulsager C. K., Olsen B. S., Jensen D. M., Cordea M. I., Krath B. N., Johansen I. E., Lund O. S.. ( 2006;). Multiple determinants in the coding region of Pea seed-borne mosaic virus P3 are involved in virulence against sbm-2 resistance. . Virology 355:, 52–61. [CrossRef][PubMed]
    [Google Scholar]
  38. Hughes A. L., Hughes M. A.. ( 2007;). More effective purifying selection on RNA viruses than in DNA viruses. . Gene 404:, 117–125. [CrossRef][PubMed]
    [Google Scholar]
  39. Jayaram C. H., Hill J. H., Miller W. A.. ( 1992;). Complete nucleotide sequences of two Soybean mosaic virus strains differentiated by response of soybean containing the Rsv resistance gene. . J Gen Virol 73:, 2067–2077. [CrossRef][PubMed]
    [Google Scholar]
  40. Jenkins G. M., Rambaut A., Pybus O. G., Holmes E. C.. ( 2002;). Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. . J Mol Evol 54:, 156–165. [CrossRef][PubMed]
    [Google Scholar]
  41. Jenner C. E., Tomimura K., Ohshima K., Hughes S. L., Walsh J. A.. ( 2002;). Mutations in Turnip mosaic virus P3 and cylindrical inclusion proteins are separately required to overcome two Brassica napus resistance genes. . Virology 300:, 50–59. [CrossRef][PubMed]
    [Google Scholar]
  42. Jenner C. E., Wang X., Tomimura K., Ohshima K., Ponz F., Walsh J. A.. ( 2003;). The dual role of the potyvirus P3 protein of Turnip mosaic virus as a symptom and avirulence determinant in brassicas. . Mol Plant Microbe Interact 16:, 777–784. [CrossRef][PubMed]
    [Google Scholar]
  43. Karimi A., Noaparast F.. ( 1989;). Soybean mosaic virus in Iran. . In Proceedings of the 9th Plant Protection Congress Iran, 171.
    [Google Scholar]
  44. Khatabi B., Fajolu O. L., Wen R.-H., Hajimorad M. R.. ( 2012;). Evaluation of North American isolates of Soybean mosaic virus for gain of virulence on Rsv-genotype soybeans with special emphasis on resistance-breaking determinants on Rsv4. . Mol Plant Pathol 13:, 1077–1088. [CrossRef][PubMed]
    [Google Scholar]
  45. Kim B. M., Suehiro N., Natsuaki T., Inukai T., Masuta C.. ( 2010;). The P3 protein of Turnip mosaic virus can alone induce hypersensitive response-like cell death in Arabidopsis thaliana carrying TuNI.. Mol Plant Microbe Interact 23:, 144–152. [CrossRef][PubMed]
    [Google Scholar]
  46. Kimura M.. ( 1980;). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. . J Mol Evol 16:, 111–120. [CrossRef][PubMed]
    [Google Scholar]
  47. Li W. H.. ( 1993;). Unbiased estimation of the rates of synonymous and nonsynonymous substitution. . J Mol Evol 36:, 96–99. [CrossRef][PubMed]
    [Google Scholar]
  48. Li K., Yang Q. H., Zhi H. J., Gai J. Y.. ( 2010;). Identification and distribution of Soybean mosaic virus strains in Southern China. . Plant Dis 94:, 351–357. [CrossRef]
    [Google Scholar]
  49. Ma G., Chen P., Buss G. R., Tolin S. A.. ( 2003;). Genetic study of a lethal necrosis to Soybean mosaic virus in PI 507389 soybean. . J Hered 94:, 205–211. [CrossRef][PubMed]
    [Google Scholar]
  50. Martin D. P., Lemey P., Lott M., Moulton V., Posada D., Lefeuvre P.. ( 2010;). RDP3: a flexible and fast computer program for analyzing recombination. . Bioinformatics 26:, 2462–2463. [CrossRef][PubMed]
    [Google Scholar]
  51. Moreno I. M., Malpica J. M., Díaz-Pendón J. A., Moriones E., Fraile A., García-Arenal F.. ( 2004;). Variability and genetic structure of the population of Watermelon mosaic virus infecting melon in Spain. . Virology 318:, 451–460. [CrossRef][PubMed]
    [Google Scholar]
  52. Ohshima K., Yamaguchi Y., Hirota R., Hamamoto T., Tomimura K., Tan Z., Sano T., Azuhata F., Walsh J. A.. & other authors ( 2002;). Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. . J Gen Virol 83:, 1511–1521.[PubMed]
    [Google Scholar]
  53. Ohshima K., Tomitaka Y., Wood J. T., Minematsu Y., Kajiyama H., Tomimura K., Gibbs A. J.. ( 2007;). Patterns of recombination in turnip mosaic virus genomic sequences indicate hotspots of recombination. . J Gen Virol 88:, 298–315. [CrossRef][PubMed]
    [Google Scholar]
  54. Pamilo P., Bianchi N. O.. ( 1993;). Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. . Mol Biol Evol 10:, 271–281.[PubMed]
    [Google Scholar]
  55. Peakall R., Smouse P. E.. ( 2012;). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research–an update. . Bioinformatics 28:, 2537–2539. [CrossRef][PubMed]
    [Google Scholar]
  56. Pinel-Galzi A., Rakotomalala M., Sangu E., Sorho F., Kanyeka Z., Traoré O., Sérémé D., Poulicard N., Rabenantoandro Y.. & other authors ( 2007;). Theme and variations in the evolutionary pathways to virulence of an RNA plant virus species. . PLoS Pathog 3:, e180. [CrossRef][PubMed]
    [Google Scholar]
  57. Poulicard N., Pinel-Galzi A., Traoré O., Vignols F., Ghesquière A., Konaté G., Hébrard E., Fargette D.. ( 2012;). Historical contingencies modulate the adaptability of Rice yellow mottle virus.. PLoS Pathog 8:, e1002482. [CrossRef][PubMed]
    [Google Scholar]
  58. Saghai Maroof M. A., Tucker D. M., Skoneczka J. A., Bowman B. C., Tripathy S., Tolin S. A.. ( 2010;). Fine mapping and candidate gene discovery of the Soybean mosaic virus resistance gene, Rsv4. . Plant Genome 3:, 14–22. [CrossRef][PubMed]
    [Google Scholar]
  59. Seo J.-K., Lee S.-H., Kim K.-H.. ( 2009a;). Strain-specific cylindrical inclusion protein of Soybean mosaic virus elicits extreme resistance and a lethal systemic hypersensitive response in two resistant soybean cultivars. . Mol Plant Microbe Interact 22:, 1151–1159. [CrossRef][PubMed]
    [Google Scholar]
  60. Seo J.-K., Ohshima K., Lee H.-G., Son M., Choi H.-S., Lee S.-H., Sohn S.-H., Kim K.-H.. ( 2009b;). Molecular variability and genetic structure of the population of Soybean mosaic virus based on the analysis of complete genome sequences. . Virology 393:, 91–103. [CrossRef][PubMed]
    [Google Scholar]
  61. Shurtleff W., Aoyagi A.. ( 2008;). History of Soybeans and Soyfoods in the Middle East (1909–2007): Bibliography and Sourcebook. . Lafayette, CA:: Soyinfo Center;. http://www.soyinfocenter.com/pdf/117/AsMe.pdf
  62. Suh S. J., Bowman B. C., Jeong N., Yang K., Kastl C., Tolin S. A., Maroof M. A. S., Jeong S. C.. ( 2011;). The Rsv3 locus conferring resistance to Soybean mosaic virus is associated with a cluster of coiled coil nucleotide-binding leucine-rich repeat genes. . Plant Genome 4:, 55–64. [CrossRef]
    [Google Scholar]
  63. Takahashi K., Tanaka T., Iida W., Tsuda Y.. ( 1980;). Studies on virus disease and causal viruses of soybean in Japan. . Bull Tohoku Natl Agric Exp Stn 62:, 1–130.
    [Google Scholar]
  64. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S.. ( 2011;). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28:, 2731–2739. [CrossRef][PubMed]
    [Google Scholar]
  65. Tomimura K., Spak J., Katis N., Jenner C. E., Walsh J. A., Gibbs A. J., Ohshima K.. ( 2004;). Comparisons of the genetic structure of populations of Turnip mosaic virus in West and East Eurasia. . Virology 330:, 408–423. [CrossRef][PubMed]
    [Google Scholar]
  66. Urcuqui-Inchima S., Haenni A.-L., Bernardi F.. ( 2001;). Potyvirus proteins: a wealth of functions. . Virus Res 74:, 157–175. [CrossRef][PubMed]
    [Google Scholar]
  67. Wen R. H., Hajimorad M. R.. ( 2010;). Mutational analysis of the putative pipo of Soybean mosaic virus suggests disruption of PIPO protein impedes movement. . Virology 400:, 1–7. [CrossRef][PubMed]
    [Google Scholar]
  68. Wen R. H., Khatabi B., Ashfield T., Maroof M. A. S., Hajimorad M. R.. ( 2013;). The HC-Pro and P3 cistrons of an avirulent Soybean mosaic virus are recognized by different resistance genes at the complex Rsv1 locus. . Mol Plant Microbe Interact 26:, 203–215. [CrossRef][PubMed]
    [Google Scholar]
  69. Zhang C., Hajimorad M. R., Eggenberger A. L., Tsang S., Whitham S. A., Hill J. H.. ( 2009;). Cytoplasmic inclusion cistron of Soybean mosaic virus serves as a virulence determinant on Rsv3-genotype soybean and a symptom determinant. . Virology 391:, 240–248. [CrossRef][PubMed]
    [Google Scholar]
  70. Zheng C., Chen P., Gergerich R.. ( 2005;). Characterization of resistance to Soybean mosaic virus in diverse soybean germplasm. . Crop Sci 45:, 2503–2509. [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.055434-0
Loading
/content/journal/jgv/10.1099/vir.0.055434-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF

Most cited articles

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