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Genetic structure of rice black-streaked dwarf virus populations in China

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Abstract

Rice black-streaked dwarf virus (RBSDV) is a double-stranded RNA (dsRNA) virus belonging to the genus Fijivirus in the family Reoviridae. The genome of RBSDV consists of ten dsRNA segments. Although RBSDV has caused significant economic losses to rice and maize production in the past few years in China, its molecular diversity and evolution remain largely unknown. To elucidate the factor(s) underlying the evolution of RBSDV, we determined segment 8 (S8; carrying ORF8 encoding the minor core capsid protein) sequences of 101 samples and segment 10 (S10; carrying ORF10 encoding the major capsid protein) sequences of 103 samples. The results show that both ORF8 and ORF10 are under negative selection. The S8 of three isolates and S10 of two isolates are recombinants. The RBSDV population in China can be classified into three groups according to S8 sequences or into two groups according to S10 sequences, irrespective of host or geographical origin. Of the RBSDV isolates with both S8 and S10 sequences available, 17 are between-group reassortants and 30 are between-subgroup reassortants. The RBSDV subpopulations from different geographical regions and hosts show frequent gene flow within or between subpopulations. The RBSDV population from maize is in a state of expansion. In this study, no new emergent population was detected. Taken together, the results indicate that, in addition to recombination and negative selection, reassortment and gene flow are important factors that drive evolution of RBSDV in China.

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References

  1. Bai FW, Qu ZC, Yan J, Zhang HW, Xu J, Ye MM, Wu HL, Liao XG, Shen DL (2001) Identification of rice black streaked dwarf virus in different cereal crops with dwarfing symptoms in China. Acta Virol 45:335–339

    PubMed  CAS  Google Scholar 

  2. Bermingham E, Moritz C (1998) Comparative phylogeography: concepts and application. Mol Ecol 7:367–369

    Article  Google Scholar 

  3. Bonnet J, Fraile A, Sacristan S, Malpica JM, Garcia-Arenal F (2005) Role of recombination in the evolution of natural populations of Cucumber mosaic virus, a tripartite RNA plant virus. Virology 332:359–368

    Article  PubMed  CAS  Google Scholar 

  4. Chare ER, Holmes EC (2005) A phylogenetic survey of recombinant frequency in plant RNA viruses. Arch Virol 151:933–946

    Article  PubMed  Google Scholar 

  5. Chen J, Zhu QQ, Yuan CY, Sun ZW, Li XD, Zhou T, Fan ZF (2008) Molecular characterization of Rice black-streaked dwarf virus isolates causing maize rough dwarf disease in Shandong. Acta Phytopathol Sin 38:540–543

    Google Scholar 

  6. Drake JW, Holland JJ (1999) Mutation rates among RNA viruses. Proc Natl Acad Sci USA 96:13910–13913

    Article  PubMed  CAS  Google Scholar 

  7. Fraile A, Alonso-Prados JL, Aranda MA, Bernal JJ, Malpica JM, Garcia-Arenal F (1997) Genetic exchange by recombination or reassortment is infrequent in natural populations of a tripartite RNA plant virus. J Virol 71:934–940

    PubMed  CAS  Google Scholar 

  8. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  Google Scholar 

  9. Garcia-Arenal F, Fraile A, Malpica JM (2003) Variation and evolution of plant virus populations. Int Microbiol 6:225–232

    Article  PubMed  Google Scholar 

  10. Glasa M, Palkovics L, Kominek P, Labonne G, Pittnerova S, Kudela O, Candresse T, Subr Z (2004) Geographically and temporally distant natural recombinant isolates of Plum pox virus (PPV) are genetically very similar and form a unique PPV subgroup. J Gen Virol 85:2671–2681

    Article  PubMed  CAS  Google Scholar 

  11. Holmes EC (2009) The Evolutionary Genetics of Emerging Viruses. Annu Rev Ecol Evol Syst 40:353–372

    Article  Google Scholar 

  12. Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014

    PubMed  CAS  Google Scholar 

  13. Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting geographic subdivision. Mol Biol Evol 9:138–151

    PubMed  CAS  Google Scholar 

  14. Isogai M, Uyeda I, Lee BC (1998) Detection and assignment of proteins encoded by rice black streaked dwarf fijivirus S7, S8, S9 and S10. J Gen Virol 79:1487–1494

    PubMed  CAS  Google Scholar 

  15. Li W-H (1993) Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol 36:96–99

    Article  PubMed  CAS  Google Scholar 

  16. Li Y, Jia M, Jiang Z, Zhou T, Fan Z (2012) Molecular variation and recombination in RNA segment 10 of rice black-streaked dwarf virus isolated from China during 2007–2010. Arch Virol 157:1351–1356

    Article  PubMed  CAS  Google Scholar 

  17. Lin H-X, Rubio L, Smythe AB, Falk BW (2004) Molecular population genetics of Cucumber mosaic virus in California: evidence for founder effects and reassortment. J Virol 78:6666–6675

    Article  PubMed  CAS  Google Scholar 

  18. Liu H, Wei C, Zhong Y, Li Y (2007) Rice black-streaked dwarf virus minor core protein P8 is a nuclear dimeric protein and represses transcription in tobacco protoplasts. FEBS Lett 581:2534–2540

    Article  PubMed  CAS  Google Scholar 

  19. Liu H, Wei C, Zhong Y, Li Y (2007) Rice black-streaked dwarf virus outer capsid protein P10 has self-interactions and forms oligomeric complexes in solution. Virus Res 127:34–42

    Article  PubMed  CAS  Google Scholar 

  20. Manrubia SC, Escarmís C, Domingo E, Lázaro E (2005) Contribution of recombination and selection to molecular evolution of Citrus tristeza virus. J Gen Virol 90:1527–1538

    Google Scholar 

  21. Martin S, Sambade A, Rubio L, Vives MC, Moya P, Guerri J, Elena SF, Moreno P (2009) Contribution of recombination and selection to molecular evolution of Citrus tristeza virus. J Gen Virol 90:1527–1538

    Article  PubMed  CAS  Google Scholar 

  22. Martin DP, 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

    Article  PubMed  CAS  Google Scholar 

  23. Nagy PD (2008) Recombination in plant RNA viruses. In: Roossinck (MJ) Plant virus evolution. Springer, Berlin, pp 133–156

  24. Ohshima K, Tomitaka Y, Wood JT, Minematsu Y, Kajiyama H, Tomimura K, Gibbs AJ (2007) Patterns of recombination in turnip mosaic virus genomic sequences indicate hotspots of recombination. J Gen Virol 88:298–315

    Article  PubMed  CAS  Google Scholar 

  25. Oliver JE, Vigne E, Fuch M (2010) Genetic structure and molecular variability of Grapevine fanleaf virus populations. Virus Res 152:30–40

    Article  PubMed  CAS  Google Scholar 

  26. Pamilo P, Bianchi NO (1993) Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol Biol Evol 10:271–281

    PubMed  CAS  Google Scholar 

  27. Roossinck MJ (1997) Mechanisms of plant virus evolution. Annu Rev Phytopathol 35:191–209

    Article  PubMed  CAS  Google Scholar 

  28. Roossinck MJ (2008) Plant virus evolution. Springer, Berlin

  29. Rozas J (2009) DNA sequence polymorphism analysis using DnaSP. Methods Mol Biol 537:337–350

    Article  PubMed  CAS  Google Scholar 

  30. Ruan YL, Chen SX, Lin RF, Jiang DL, Jin DD (1984) Researches on rice black-streaked dwarf disease. J Zhejiang Agric Sci: 185–187

  31. Shikata E, Kitagawa Y (1977) Rice black-streaked dwarf virus: its properties, morphology and intracellular localization. Virology 77:826–842

    Article  PubMed  CAS  Google Scholar 

  32. Simon-Loriere E, Holmes EC (2011) Why do RNA viruses recombine? Nat Rev Microbiol 9(8):617–626

    Article  PubMed  CAS  Google Scholar 

  33. Stenger DC, Sisterson MS, French R (2010) Population genetics of Homalodisca vitripennis reovirus validates timing and limited introduction to California of its invasive insect host, the glassy-winged sharpshooter. Virology 407:53–59

    Article  PubMed  CAS  Google Scholar 

  34. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  35. Thompson JD, Higgins DG, Gibson TJ (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  36. Tomimura K, Gibbs AJ, Jenner CE, Walsh JA, Ohshima K (2003) The phylogeny of Turnip mosaic virus; comparisons of 38 genomic sequences reveal a Eurasian origin and a recent ‘emergence’ in East Asia. Mol Ecol 12:2099–2111

    Article  PubMed  CAS  Google Scholar 

  37. Tomitaka Y, Ohshima K (2006) A phylogeographical study of the Turnip mosaic virus population in East Asia reveals an ‘emergent’ lineage in Japan. Mol Ecol 15:4437–4457

    Article  PubMed  CAS  Google Scholar 

  38. Traore O, Sorho F, Pinel A, Banwo O, Maley J, Hebrad E, Winter S, Sere Y, Konate G, Fargettr D (2005) Processes of diversification and dispersion of Rice yellow mottle virus inferred from largescale and high-resolution phylogeographical studies. Mol Ecol 14:2097–2110

    Article  PubMed  CAS  Google Scholar 

  39. Tsompana M, Abad J, Purugganan M, Moyer JW (2005) The molecular population genetics of the Tomata spotted wilt virus (TSWV) genome. Mol Ecol 14:55–63

    Google Scholar 

  40. Uyeda I, Ando Y, Murao K, Kimura I (1995) High resolution genome typing and genomic reassortment events of rice dwarf Phytoreovirus. Virology 212:724–727

    Article  PubMed  CAS  Google Scholar 

  41. Valli A, Lopez-Moya JJ, Garcia JA (2007) Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. J Gen Virol 88:1016–1028

    Article  PubMed  CAS  Google Scholar 

  42. van der Walt E, Rybicki EP, Varsani A, Polston JE, Billharz R, Donaldson L, Monjane AL, Martin DP (2009) Rapid host adaptation by extensive recombination. J Gen Virol 90:734–746

    Article  PubMed  Google Scholar 

  43. Wang ZH, Fang SG, Xu JL, Sun LY, Li DW, Yu JL (2003) Sequence analysis of the complete genome of Rice black-streaked dwarf virus isolated from maize with rough dwarf disease. Virus Genes 27:163–168

    Article  PubMed  Google Scholar 

  44. Wei TY, Wang H, Lin HX, Wu ZJ, Lin QY, Xie LH (2003) Sequence analysis of RNA3 of Rice stripe virus isolates found in China: evidence for reassortment in Tenuivirus. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai). Acta Bioch Bioph Sin 35:97–103

    CAS  Google Scholar 

  45. Wei TY, Yang JG, Liao FR, Gao FL, Lu LM, Zhang XT, Li F, Wu ZJ, Lin QY, Xie LH, Lin HX (2009) Genetic diversity and population structure of rice stripe virus in China. J Gen Virol 90:1025–1034

    Article  PubMed  CAS  Google Scholar 

  46. Wright S (1951) The genetical structure of populations. Ann Eugenics 15:323–354

    Google Scholar 

  47. Yin X, Xu FF, Zheng FQ, Li XD, Liu BS, Zhang CQ (2011) Molecular characterization of segments S7 to S10 of a southern rice black-streaked dwarf virus isolate from maize in northern China. Virol Sin 26:47–53

    Article  PubMed  CAS  Google Scholar 

  48. Yin X, Zhu QQ, Xu FF, Liu ZQ, Zhang GM, Li XD (2013) Optimization of RT-PCR detection system for rice black-streaked dwarf virus and detection of its natural hosts. Acta Phytopathol Sin 43 (5): (in press)

  49. Zhang CL, Gao R, Wang J, Zhang GM, Li XD, Liu HT (2011) Molecular variability of Tobacco vein banding mosaic virus populations. Virus Res 158:188–198

    Article  PubMed  CAS  Google Scholar 

  50. Zhang HM, Chen JP, Adams MJ (2001) Molecular characterisation of segments 1 to 6 of Rice black-streaked dwarf virus from China provides the complete genome. Arch Virol 146:2331–2339

    Article  PubMed  CAS  Google Scholar 

  51. Zhang HM, Chen JP, Lei JL, Adams MJ (2001) Sequence analysis shows that a dwarfing disease on rice, wheat and maize in China is caused by rice black-streaked dwarf virus. Eur J Plant Pathol 107:563–567

    Article  CAS  Google Scholar 

  52. Zhang HY, Diao YG, Yang HB, Zhao Y, Zhang XX, Zhai BP (2011) Population dynamics and migration characteristics of the small brown planthopper in spring in Jining, Shandong Province. Chin J Appl Entomol 48:1298–1308

    Google Scholar 

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Acknowledgments

This study was supported by grant for Shandong Innovative Research Team for Maize, Modern Agricultural Industry Technology System, Program for Science and Technology Development of Shandong Province (2009GG10009021), and Special Research Funds for Doctoral Program (SRFDP, 20123702110013) from Ministry of Education, China.

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Authors and Affiliations

  1. Laboratory of Plant Virology, Department of Plant Pathology, College of Plant Protection, Shandong Agricultural University, Tai’an, 271018, Shandong, China

    Xiao Yin, Wei Tang, Qin-Qin Zhu, Xiang-Dong Li, Guang-Min Zhang & Huan-Ting Liu

  2. Department of Entomology, College of Plant Protection, Shandong Agricultural University, Tai’an, 271018, Shandong, China

    Fang-Qiang Zheng

  3. Department of Crop Genetics and Breeding Science, College of Agronomy, Shandong Agricultural University, Tai’an, 271018, Shandong, China

    Bao-Shen Liu

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  1. Xiao Yin
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Correspondence to Xiang-Dong Li.

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X. Yin, F.-Q. Zheng, W. Tang are contributed equally.

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Yin, X., Zheng, FQ., Tang, W. et al. Genetic structure of rice black-streaked dwarf virus populations in China. Arch Virol 158, 2505–2515 (2013). https://doi.org/10.1007/s00705-013-1766-8

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