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Genetic evolutionary analysis of soybean mosaic virus populations from three geographic locations in China based on the P1 and CP genes

  • Lei Zhang
  • Jing ShangEmail author
  • Qi Jia
  • Kai Li
  • Hui Yang
  • Huanhuan Liu
  • Zhongqin Tang
  • Xiaoli Chang
  • Min Zhang
  • Wenming Wang
  • Wenyu YangEmail author
Original Article

Abstract

Soybean mosaic virus (SMV) is one of the major pathogens causing serious soybean losses. Little is known about the genetic structure and evolutionary biology of the SMV population in southwestern China. In this study, 29 SMV isolates were obtained from Sichuan Province, and the genomic regions encoding the first protein (P1) and coat protein (CP) were sequenced. Combined with SMV isolates from the southeastern and northeastern regions of China, the genetic and molecular evolution of SMV was studied. Recombination analysis revealed that intraspecific and interspecific recombination had occurred in the SMV population. A phylogenetic tree based on the P1 gene reflected the geographic origin of the non-interspecific recombinant SMV (SMV-NI), while a tree based on the CP gene did not. Though frequent gene flow of the SMV-NI populations was found between the southeastern and northeastern populations, the southwestern population was relatively independent. Genetic differentiation was significant between the SMV interspecific recombinant (SMV-RI) and the non-interspecific recombinant (SMV-NI) populations. It was interesting to note that there was an almost identical recombination breakpoint in SMV-RI and Watermelon mosaic virus (WMV). Population dynamics showed that SMV-RI might be in an expanding state, while the SMV-NI population is relatively stable.

Abbreviations

SMV

Soybean mosaic virus

BCMV

Bean common mosaic virus

WMV

Watermelon mosaic virus

SMV-RI

Interspecific recombination of SMV

SMV-NI

Non-interspecific recombination of SMV

P1

First protein

CP

Coat protein

NE

Northeast

SE

Southeast

SW

Southwest

Notes

Funding

This study was supported by grants from the National Key Research and Development Plan, Project No. 2017YFD0301704, 2018YFD0200700, and 2018YFD0201006; Sichuan Provincial Science and Technology Project, Project No. 2016NYZ0053; Research Foundation of Sichuan Provincial Education Department (035Z1038); and Scientific Research Foundation of Sichuan Provincial Science and Technology Department (2015NZ0040).

Compliance with ethical standards

Conflict of interest

We have no conflict of interest to declare.

Supplementary material

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Supplementary material 1 (JPEG 1287 kb)
705_2019_4165_MOESM2_ESM.doc (112 kb)
Supplementary material 2 (DOC 112 kb)

References

  1. 1.
    Achtman M, Wagner M (2008) Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6:431–440Google Scholar
  2. 2.
    Ahangaran A, Habibi MK, Mohammadi GHM, Winter S, Garcia-Arenal F (2013) Analysis of Soybean mosaic virus genetic diversity in Iran allows the characterization of a new mutation resulting in overcoming Rsv4-resistance. J Gen Virol 94:2557–2568Google Scholar
  3. 3.
    Anandalakshmi R, Pruss GJ, Ge X, Marathe R, Mallory AC, Smith TH, Vance VB (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci 95:13079–13084Google Scholar
  4. 4.
    Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165Google Scholar
  5. 5.
    Bashalkhanov S, Pandey M, Rajora OP (2009) A simple method for estimating genetic diversity in large populations from finite sample sizes. BMC Genet 10:1–10Google Scholar
  6. 6.
    Chen J, Zheng HY, Lin L, Adams MJ, Antoniw JF, Zhao MF, Shang YF, Chen JP (2004) A virus related to Soybean mosaic virus from Pinellia ternata in China and its comparison with local soybean SMV isolates. Arch Virol 149:349–363Google Scholar
  7. 7.
    Chen Y, Wu M, Ma F, Chen J, Wang B (2017) Complete nucleotide sequences of seven soybean mosaic viruses (SMV), isolated from wild soybeans (Glycine soja) in China. Arch Virol 162:901–904Google Scholar
  8. 8.
    Cho EK, Chung BJ (1976) Studies on identification and classification of soybean virus diseases in Korea I. Preliminary studies on a soybean virus disease. Genet Sel Evol 22:273–277Google Scholar
  9. 9.
    Cho EK, Goodman RM (1979) Strains of soybean mosaic virus: classification based on virulence in resistant soybean cultivars. Phytopathology 69:467–470Google Scholar
  10. 10.
    Choi BK, Koo JM, Ahn HJ, Yum HJ, Choi CW, Ryu KH, Chen P, Tolin SA (2005) Emergence of Rsv-resistance breaking Soybean mosaic virus isolates from Korean soybean cultivars. Virus Res 112:42–51Google Scholar
  11. 11.
    Chowda-Reddy RV, Sun H, Chen H, Poysa V, Ling H, Gijzen M, Wang A (2011) Mutations in the P3 protein of Soybean mosaic virus G2 isolates determine virulence on Rsv4-genotype soybean. Mol Plant Microbe Interact 24:37–43Google Scholar
  12. 12.
    Chung BY, Miller WA, Atkins JF, Firth AE (2008) An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci USA 105:5897–5902Google Scholar
  13. 13.
    Desbiez C, Lecoq H (2004) The nucleotide sequence of Watermelon mosaic virus (WMV, Potyvirus) reveals interspecific recombination between two related potyviruses in the 5’ part of the genome. Arch Virol 149:1619–1632Google Scholar
  14. 14.
    Domier LL, Latorre IJ, Steinlage TA, McCoppin N, Hartman GL (2003) Variability and transmission by Aphis glycines of North American and Asian Soybean mosaic virus isolates. Arch Virol 148:1925–1941Google Scholar
  15. 15.
    Du J, Han T, Gai J, Yong T, Sun X, Wang X, Yang F, Liu J, Shu K, Liu W, Yang W (2018) Maize-soybean strip intercropping: achieved a balance between high productivity and sustainability. J Integr Agric 17:747–754Google Scholar
  16. 16.
    Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797Google Scholar
  17. 17.
    Eggenberger AL, Hajimorad MR, Hill JH (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 21:931–936Google Scholar
  18. 18.
    Fu Y, Li W (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709Google Scholar
  19. 19.
    Gagarinova AG, Babu M, Strömvik MV, Wang A (2008) Recombination analysis of Soybean mosaic virus sequences reveals evidence of RNA recombination between distinct pathotypes. Virol J 5:143Google Scholar
  20. 20.
    Gao F, Zou W, Xie L, Zhan J (2017) Adaptive evolution and demographic history contribute to the divergent population genetic structure of Potato virus Y between China and Japan. Evol Appl 10:379–390Google Scholar
  21. 21.
    Gao L, Sun S, Li K, Wang L, Hou W, Wu C, Zhi H, Han T (2018) Spatio-temporal characterisation of changes in the resistance of widely grown soybean cultivars to Soybean mosaic virus across a century of breeding in China. Crop Pasture Sci 69:395Google Scholar
  22. 22.
    Gao L, Zhai R, Zhong YK, Karthikeyan A, Ren R, Zhang K, Li K, Zhi HJ (2015) Screening Isolates of Soybean mosaic virus for Infectivity in a Model Plant, Nicotiana benthamiana. Plant Dis 99:442–446Google Scholar
  23. 23.
    Gibbs AJ, Trueman JWH, Gibbs MJ (2008) The bean common mosaic virus lineage of potyviruses: where did it arise and when? Arch Virol 153:2177–2187Google Scholar
  24. 24.
    Hill JH, Whitham SA (2014) Control of virus diseases in soybeans. Adv Virus Res 90:355–390Google Scholar
  25. 25.
    Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014Google Scholar
  26. 26.
    Hudson RR, Boos DD, Kaplan NL (1992) A statistical test for detecting geographic subdivision. Mol Biol Evol 9:138–151Google Scholar
  27. 27.
    Hymowitz T, Newell CA (1981) Taxonomy of the genus glycine, domestication and uses of soybeans. Econ Bot 35:272–288Google Scholar
  28. 28.
    Ivanov KI, Eskelin K, Lohmus A, Makinen K (2014) Molecular and cellular mechanisms underlying potyvirus infection. J Gen Virol 95:1415–1429Google Scholar
  29. 29.
    Ivanov KI, Mäkinen K (2012) Coat proteins, host factors and plant viral replication. Curr Opin Virol 2:712–718Google Scholar
  30. 30.
    Jayaram C, Hill JH, Miller WA (1992) Complete nucleotide sequences of two soybean mosaic virus strains differentiated by response of soybean containing the Rsv resistance gene. J Gen Virol 73:2067–2077Google Scholar
  31. 31.
    Jiang H, Li K, Dou D, Gai J (2017) Characterization of a soybean mosaic virus variant causing different diseases in Glycine max and Nicotiana benthamiana. Arch Virol 162:549–553Google Scholar
  32. 32.
    Jossey S, Hobbs HA, Domier LL (2013) Role of soybean mosaic virus-encoded proteins in seed and aphid transmission in soybean. Phytopathology 103:941Google Scholar
  33. 33.
    Kim MJ, Kao C (2001) Factors regulating template switch in vitro by viral RNA-dependent RNA polymerases: implications for RNA-RNA recombination. Proc Natl Acad Sci USA 98:4972–4977Google Scholar
  34. 34.
    Lee GA, Crawford GW, Liu L, Sasaki Y, Chen X (2011) Archaeological soybean (Glycine max) in East Asia: does size matter? PLoS One 6:e26720Google Scholar
  35. 35.
    Li K, Yang QH, Zhi HJ, Gai JY (2010) Identification and distribution of Soybean mosaic virus strains in Southern China. Plant Dis 94:351–357Google Scholar
  36. 36.
    Li M, Kim J, Seo E, Hong SM, Hwang E, Moon J, Domier LL, Hammond J, Youn Y, Lim H (2014) Sequence variability in the HC-Pro coding regions of Korean soybean mosaic virus isolates is associated with differences in RNA silencing suppression. Arch Virol 159:1373–1383Google Scholar
  37. 37.
    Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452Google Scholar
  38. 38.
    Lin J (2016) Pathogenicity and biological characteristics of recombinant Soybean mosaic virus in the Huang-Huai-Hai. Hebei Agricultural University, HebeiGoogle Scholar
  39. 39.
    Liu J, Fang Y, Pang H (2016) The Current Status of the Soybean-Soybean Mosaic Virus (SMV) Pathosystem. Front Microbiol 7:1906Google Scholar
  40. 40.
    Maliogka VI, Salvador B, Carbonell A, Sã EP, Leã NDS, Oliveros JC, Delgadillo MO, Garcã AJA, Simón‐Mateo CA (2012) Virus variants with differences in the P1 protein coexist in a Plum pox virus population and display particular host-dependent pathogenicity features. Mol Plant Pathol 13:877–886Google Scholar
  41. 41.
    Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evolution 1:v3Google Scholar
  42. 42.
    Mayo MA, Pringle CR (1998) Virus taxonomy-1997. J Gen Virol 79:649–657Google Scholar
  43. 43.
    Mengual-Chuliá B, Bedhomme S, Lafforgue G, Elena SF, Bravo IG (2016) Assessing parallel gene histories in viral genomes. BMC Evol Biol 16:32Google Scholar
  44. 44.
    Revers F, García JA (2015) Molecular biology of potyviruses. Adv Virus Res 92:101–199Google Scholar
  45. 45.
    Ross JP (1977) Effect of aphid-transmitted soybean mosaic virus on yields of closely related resistant and susceptible soybean lines. Crop Sci 17:869–872Google Scholar
  46. 46.
    Salvador B, Saénz P, Yangüez E, Quiot JB, Quiot L, Delgadillo M, García J, Simón-Mateo C (2008) Host-specific effect of P1 exchange between two potyviruses. Mol Plant Pathol 9:147–155Google Scholar
  47. 47.
    Seo J, Kan S, Seo BY, Jung JK, Kim K (2010) Mutational analysis of interaction between coat protein and helper component-proteinase of Soybean mosaic virus involved in aphid transmission. Mol Plant Pathol 11:265–276Google Scholar
  48. 48.
    Seo J, Ohshima K, Lee H, Son M, Choi H, Lee S, Sohn S, Kim K (2009) Molecular variability and genetic structure of the population of Soybean mosaic virus based on the analysis of complete genome sequences. Virology 393:91–103Google Scholar
  49. 49.
    Seo JK, Vo Phan MS, Kang SH, Choi HS, Kim KH (2013) The charged residues in the surface-exposed C-terminus of the Soybean mosaic virus coat protein are critical for cell-to-cell movement. Virology 446:95–101Google Scholar
  50. 50.
    Shang J, Xi D, Huang Q, Xu M, Yuan S, Wang S, Jia S, Cao S, Zhou Z, Lin H (2009) Effect of two satellite RNAs on Nicotiana glutinosa infected with Cucumber mosaic virus (CMV). Physiol Mol Plant 74:184–190Google Scholar
  51. 51.
    Shi Y, Chen J, Hong X, Chen J, Adams MJ (2007) A potyvirus P1 protein interacts with the Rieske Fe/S protein of its host. Mol Plant Pathol 8:785–790Google Scholar
  52. 52.
    Shukla DD, Ward CW, Brunt AA (1994) The potyviridae. CAB International, WallingfordGoogle Scholar
  53. 53.
    Simonloriere E, Holmes EC (2011) Why do RNA viruses recombine? Nat Rev Microbiol 9:617–626Google Scholar
  54. 54.
    Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595Google Scholar
  55. 55.
    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 28:2731–2739Google Scholar
  56. 56.
    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 15:4437–4457Google Scholar
  57. 57.
    Urcuquiinchima S, Haenni AL, Bernardi F (2001) Potyvirus proteins: a wealth of functions. Virus Res 74:157–175Google Scholar
  58. 58.
    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 88:1016–1028Google Scholar
  59. 59.
    Valli AA, Gallo A, Rodamilans B, López-Moya JJ, García JA (2018) The HCPro from thePotyviridae family: an enviable multitasking Helper Component that every virus would like to have. Mol Plant Pathol 19:744–763Google Scholar
  60. 60.
    Wang Y, Hajimorad MR (2016) Gain of virulence by Soybean mosaic virus on Rsv4-genotype soybeans is associated with a relative fitness loss in a susceptible host. Mol Plant Pathol 17:1154–1159Google Scholar
  61. 61.
    Wang Y, Khatabi B, Hajimorad MR (2015) Amino acid substitution in P3 of Soybean mosaic virus to convert avirulence to virulence on Rsv4-genotype soybean is influenced by the genetic composition of P3. Mol Plant Pathol 16:301–307Google Scholar
  62. 62.
    Wen RH, Hajimorad MR (2010) Mutational analysis of the putative pipo of soybean mosaic virus suggests disruption of PIPO protein impedes movement. Virology 400:1–7Google Scholar
  63. 63.
    Whitlock M, McCauley D (1999) Indirect measures of gene flow and migration: FST ≠ 1/(4Nm + 1). Heredity 82:117–125Google Scholar
  64. 64.
    Yang Y, Gong J, Li H, Li C, Wang D, Li K, Zhi H (2011) Identification of a novel Soybean mosaic virus isolate in China that contains a unique 5’ terminus sharing high sequence homology with Bean common mosaic virus. Virus Res 157:13–18Google Scholar
  65. 65.
    Yang Y, Lin J, Zheng G, Zhang M, Zhi H (2014) Recombinant soybean mosaic virus is prevalent in Chinese soybean fields. Arch Virol 159:1793–1796Google Scholar
  66. 66.
    Yoon Y, Lim S, Yun WJ, Kim BS, Bae DH, Maharjan R, Yi H, Bae S, Lee Y, Lee B (2017) First report of Soybean mosaic virus and Soybean yellow mottle mosaic virus in Vigna angularis. Plant Dis 102:689Google Scholar
  67. 67.
    Zhan J, McDonald BA (2013) Experimental measures of pathogen competition and relative fitness. Annu Rev Phytopathol 51:131–153Google Scholar
  68. 68.
    Zhan J, Thrall PH, Papaix J, Xie L, Burdon JJ (2015) Playing on a pathogen’s weakness: using evolution to guide sustainable plant disease control strategies. Annu Rev Phytopathol 53:19–43Google Scholar
  69. 69.
    Zhou G, Shao Z, Ma F, Wu P, Wu X, Xie Z, Yu D, Cheng H, Liu Z, Jiang Z, Chen Q, Wang B, Chen J (2015) The evolution of soybean mosaic virus: An updated analysis by obtaining 18 new genomic sequences of Chinese strains/isolates. Virus Res 208:189–198Google Scholar
  70. 70.
    Zhou G, Wu X, Zhang Y, Wu P, Wu X, Liu L, Wang Q, Hang Y, Yang J, Shao Z, Wang B, Chen J (2014) A genomic survey of thirty soybean-infecting bean common mosaic virus (BCMV) isolates from China pointed BCMV as a potential threat to soybean production. Virus Res 191:125–133Google Scholar

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© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Sichuan Engineering Research Center for Crop Strip Intercropping System and Key Laboratory of Crop Eco‑physiology and Farming System in Southwest ChinaSichuan Agricultural UniversityChengduChina
  2. 2.College of Agronomy and Key Laboratory for Major Crop DiseasesSichuan Agricultural UniversityChengduChina
  3. 3.National Center for Soybean Improvement, National Key Laboratory for Crop Genetics and Germplasm Enhancement, Key Laboratory of Biology and Genetic Improvement of Soybean, Ministry of AgricultureNanjing Agricultural UniversityNanjingChina

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