Skip to main content
SpringerLink
Log in

Genetic diversity of potato virus Y (PVY): sequence analyses reveal ten novel PVY recombinant structures

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

The potato virus Y (PVY) complex includes five non-recombinant strains and a growing number of recombinants. Up to now, the bulk of these PVY recombinants were found to be composed of genome segments coming from only two “parental” genomes, PVYO and PVYEu-N, with a small minority including segments from other parents, e.g. PVYC, PVYNA-N, and a segment of the recombinant strain PVY-NE11. Here, comprehensive analyses of 396 whole genomes of PVY isolates from 34 countries and a variety of hosts revealed 28 isolates to be rare or novel recombinants. When subjected to a thorough recombination analysis, these 28 PVY isolates were found to represent 25 poorly sampled PVY recombinant structures, ten of which had not been recognized previously. Nine of the ten novel structures carried parental sequences from PVYNA-N or PVY-NE11 strains recombined with PVYO and PVYEu-N sequences, while seven of the new structures contained sequences from three different parents. The number of known PVY recombinant patterns now stands at thirty six. These recombinant structures present a challenge for PVY strain typing, but may shed light on interactions between PVY and host resistance genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Abdel El-Mohsen NMA, Gamal El-Dinn AS, Sohair IE-A, Sadik AS, Abdelmaksoud HM (2003) Characterization of potato virus Y strain ‘N-Egypt’. Ann Agric Sci 48:485–504

    Google Scholar 

  2. Adams MJ, Zerbini FM, French R, Rabenstein F, Stenger DC, Valkonen JPT (2012) Family Potyviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Ninth report of the international committee on taxonomy of viruses. Elsevier, Amsterdam, pp 1069–1089

  3. Bahrami Kamangar S, Smagghe G, Maes M, De Jonghe K (2014) Potato virus Y (PVY) strains in Belgian seed potatoes and first molecular detection of the N-Wi strain. J Plant Dis Protect 121:10–19

    Article  Google Scholar 

  4. Beczner L, Horvath H, Romhanyi L, Forster H (1984) Etiology of tuber ringspot disease in potato. Potato Res 27:339–351

    Article  Google Scholar 

  5. Benedict C, McMoran D, Inglis D, Karasev AV (2015) Tuber symptoms associated with recombinant strains of Potato virus Y in specialty potatoes under northwestern Washington growing conditions. Am J Potato Res 92:593–602

    Article  CAS  Google Scholar 

  6. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2005) GenBank. Nucl Acids Res 33(database issue):D34–D38. doi:10.1093/nar/gki063

  7. Chen X, Liu J, Xu L, Jiang F, Xie X, Zhu C, Wen F (2010) Inhibiting virus infection by RNA interference of the eight functional genes of the Potato virus Y genome. J Phytopathol 158:776–784. doi:10.1111/j.1439-0434.2010.01701.x

    Article  CAS  Google Scholar 

  8. Chikh-Ali M, Alruwaili H, Vander Pol D, Karasev AV (2016) Molecular characterization of recombinant strains of Potato virus Y from Saudi Arabia. Plant Dis 100:292–297

    Article  CAS  Google Scholar 

  9. Chikh-Ali M, Bosque-Perez N, Vander Pol D, Sembel D, Karasev AV (2016) Occurrence and molecular characterization of recombinant Potato virus Y NTN (PVYNTN) isolates from Sulawesi, Indonesia. Plant Dis 100:269–275

    Article  CAS  Google Scholar 

  10. Chikh-Ali M, Gray SM, Karasev AV (2013) An improved multiplex IC-RT-PCR assay distinguishes nine strains of Potato virus Y. Plant Dis 97:1370–1374

    Article  CAS  Google Scholar 

  11. Chikh-Ali M, Rowley JS, Kuhl JC, Gray SM, Karasev AV (2014) Evidence of a monogenic nature of the Nz gene conferring resistance against Potato virus Y strain Z (PVYZ) in potato. Am J Potato Res 91:649–654

    Article  CAS  Google Scholar 

  12. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Elwan EA, Aleem EEA, Fattouh FA, Green KJ, Tran LT, Karasev AV (2017) Occurrence of diverse recombinant strains of Potato virus Y circulating in potato fields in Egypt. Plant Dis. doi:10.1094/PDIS-02-17-0275-RE (in press)

    Google Scholar 

  14. Fanigliulo A, Comes S, Pacella R, Harrach B, Martin DP, Crescenzi A (2005) Characterisation of Potato virus Y nnp strain inducing veinal necrosis in pepper: a naturally occurring recombinant strain of PVY. Arch Virol 150:709–720

    Article  CAS  PubMed  Google Scholar 

  15. Funke CN, Nikolaeva OV, Green KJ, Tran LT, Chikh-Ali M, Quintero-Ferrer A, Cating R, Frost KE, Hamm PB, Olsen N, Pavek MJ, Gray SM, Crosslin JM, Karasev AV (2017) Strain-specific resistance to Potato virus Y (PVY) in potato and its effect on the relative abundance of PVY strains in commercial potato fields. Plant Dis 101:20–28

    Article  Google Scholar 

  16. Galvino-Costa SB, Figueira A, Camargos VV, Geraldino PS, Hu X, Nikolaeva OV, Kerlan C, Karasev AV (2012) A novel type of Potato virus Y recombinant genome, determined for the genetic strain PVYE. Plant Pathol 61:388–398

    Article  CAS  Google Scholar 

  17. Galvino-Costa SBF, Figueira AR, Rabelo-Filho FAC, Moraes FHR, Nikolaeva OV, Karasev AV (2012) Molecular typing of Potato virus Y isolates from Brazil reveals a diverse set of recombinant strains. Plant Dis 96:1451–1458

    Article  CAS  Google Scholar 

  18. Gao F, Chang F, Shen J, Shi F, Xie L, Zhan J (2014) Complete genome analysis of a novel recombinant isolate of Potato virus Y from China. Arch Virol 159:3439–3442

    Article  CAS  PubMed  Google Scholar 

  19. Gibbs A, Ohshima K (2010) Potyviruses and the digital revolution. Ann Rev Phytopathol 48:205–223

    Article  CAS  Google Scholar 

  20. Gibbs A, Ohshima K, Yasaka R, Mohammadi M, Gibbs MJ, Jones RAC (2017) The phylogenetics of the global population of Potato virus Y and its necrogenic recombinants. Virus Evol 3:vex002. doi:10.1093/ve/vex002

    Article  PubMed  PubMed Central  Google Scholar 

  21. Gibbs MJ, Armstrong JS, Gibbs AJ (2000) Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582

    Article  CAS  PubMed  Google Scholar 

  22. Glais L, Tribodet M, Kerlan C (2002) Genomic variability in Potato potyvirus Y (PVY): evidence that PVYNW and PVYNTN variants are single to multiple recombinants between PVYO and PVYN isolates. Arch Virol 147:363–378

    Article  CAS  PubMed  Google Scholar 

  23. Gray S, De Boer S, Lorenzen J, Karasev A, Whitworth J, Nolte P, Singh R, Boucher A, Xu H (2010) Potato virus Y: an evolving concern for potato crops in the United States and Canada. Plant Dis 94:1384–1397

    Article  Google Scholar 

  24. Green KJ, Brown CJ, Gray SM, Karasev AV (2017) Phylogenetic study of recombinant strains of Potato virus Y. Virology 507:40–52

    Article  CAS  PubMed  Google Scholar 

  25. Green KJ, Chikh-Ali M, Hamasaki RT, Melzer MJ, Karasev AV (2017) Potato virus Y (PVY) isolates from Physalis peruviana are unable to systemically infect potato or pepper and form a distinct new lineage within the PVYC strain group. Phytopathology. doi:10.1094/PHYTO-04-17-0147-R (published on-line)

    Google Scholar 

  26. Hataya T, Inoue AK, Ohshima K, Shikata E (1994) Characterization and strain identification of a Potato virus Y isolate non-reactive with monoclonal antibodies specific to the ordinary and necrotic strains. Intervirology 37:12–19

    Article  CAS  PubMed  Google Scholar 

  27. Hu X, Karasev AV, Brown CJ, Lorenzen JH (2009) Sequence characteristics of Potato virus Y recombinants. J Gen Virol 90:3033–3041

    Article  CAS  PubMed  Google Scholar 

  28. Jones RAC (1990) Strain group specific and virus specific hypersensitive reactions to infection with potyviruses in potato cultivars. Ann Appl Biol 117:93–105

    Article  Google Scholar 

  29. Karasev AV, Gray SM (2013) Continuous and emerging challenges of Potato virus Y in potato. Annu Rev Phytopathol 51:571–586

    Article  CAS  PubMed  Google Scholar 

  30. Karasev AV, Hu X, Brown CJ, Kerlan C, Nikolaeva OV, Crosslin JM, Gray SM (2011) Genetic diversity of the ordinary strain of Potato virus Y (PVY) and origin of recombinant PVY strains. Phytopathology 101:778–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Karasev AV, Nikolaeva OV, Hu X, Sielaff Z, Whitworth J, Lorenzen JH, Gray SM (2010) Serological properties of ordinary and necrotic isolates of Potato virus Y: a case study of PVYN misidentification. Am J Pot Res 87:1–9

    Article  Google Scholar 

  32. Kehoe MA, Jones RAC (2016) Improving Potato virus Y strain nomenclature: lessons from comparing isolates obtained over a 73-year period. Plant Pathol 65:322–333

    Article  CAS  Google Scholar 

  33. Kerlan C (2006) Potato virus Y. Descriptions of plant viruses no 414. Association of applied biologists, UK. http://www.dpvweb.net/dpv/showdpv.php?dpvno=414. Accessed 1 July 2017

  34. Kerlan C, Nikolaeva OV, Hu X, Meacham T, Gray SM, Karasev AV (2011) Identification of the molecular make-up of the Potato virus Y strain PVYZ: genetic typing of PVYZ-NTN. Phytopathology 101:1052–1060

    Article  CAS  PubMed  Google Scholar 

  35. Le Romancer M, Kerlan C, Nedellec M (1994) Biological characterization of various geographical isolates of Potato virus Y including superficial necrosis on potato tubers. Plant Pathol 43:138–144

    Article  Google Scholar 

  36. Lorenzen JH, Meacham T, Berger PH, Shiel PJ, Crosslin JM, Hamm PB, Kopp H (2006) Whole genome characterization of Potato virus Y isolates collected in the western USA and their comparison to isolates from Europe and Canada. Arch Virol 151:1055–1074

    Article  CAS  PubMed  Google Scholar 

  37. Lorenzen JH, Piche LM, Gudmestad NC, Meacham T, Shiel P (2006) A multiplex PCR assay to characterize Potato virus Y isolates and identify strain mixtures. Plant Dis 90:935–940

    Article  CAS  Google Scholar 

  38. Lorenzen J, Nolte P, Martin D, Pasche JS, Gudmestad NC (2008) NE-11 represents a new strain variant class of Potato virus Y. Arch Virol 153:517–525

    Article  CAS  PubMed  Google Scholar 

  39. 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  CAS  PubMed  PubMed Central  Google Scholar 

  40. Martin DP, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563

    Article  CAS  PubMed  Google Scholar 

  41. Minin V, Abdo Z, Joyce P, Sullivan J (2003) Performance-based selection of likelihood models for phylogeny estimation. Syst Biol 52:674–683

    Article  PubMed  Google Scholar 

  42. Moodley V, Ibaba JD, Naidoo R, Gubba A (2014) Full-genome analyses of a Potato virus Y (PVY) isolate infecting pepper (Capsicum annuum L.) in the Republic of South Africa. Virus Genes 49:466–476

    Article  CAS  PubMed  Google Scholar 

  43. Moury B, Caromel B, Johansen E, Simon V, Chauvin L, Jacquot E, Kerlan C, Lefebvre V (2011) The helper component proteinase cistron of Potato virus Y induces hypersensitivity and resistance in potato genotypes carrying dominant resistance genes on chromosome IV. Mol Plant Microbe Interact 24:787–797

    Article  CAS  PubMed  Google Scholar 

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

    Chapter  Google Scholar 

  45. Nagy PD, Simon AE (1997) New insights into the mechanisms of RNA recombination. Virology 235:1–9

    Article  CAS  PubMed  Google Scholar 

  46. Nikolaeva OV, Roop D, Galvino-Costa SFB, Figueira AR, Gray SM, Karasev AV (2012) Epitope mapping for monoclonal antibodies recognizing tuber necrotic strains of Potato virus Y. Am J Potato Res 89:121–128

    Article  CAS  Google Scholar 

  47. Ogawa T, Nakagawa A, Hataya T, Ohshima K (2012) The genetic structure of populations of Potato virus Y in Japan; based on the analysis of 20 full genomic sequences. J Phytopathol 160:661–673

    Article  Google Scholar 

  48. Padidam M, Sawyer S, Fauquet CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225

    Article  CAS  PubMed  Google Scholar 

  49. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98:13757–13762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Quenouille J, Vassilakos N, Moury B (2013) Potato virus Y: a major crop pathogen that has provided major insights into the evolution of viral pathogenicity. Mol Plant Pathol 14:439–452

    Article  CAS  PubMed  Google Scholar 

  51. Quintero-Ferrer A, Robles-Hernandez L, Gonzalez-Franco AC, Kerlan C, Karasev AV (2014) Molecular and biological characterization of a recombinant isolate of Potato virus Y from Mexico. Arch Virol 159:1781–1785. doi:10.1007/s00705-013-1968-0

    Article  CAS  PubMed  Google Scholar 

  52. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16:276–277

    Article  CAS  PubMed  Google Scholar 

  53. Robaglia C, Durand-Tardif M, Tronchet M, Boudazin G, AstierManifacier S, Casse-Delbart F (1989) Nucleotide sequence of potato virus Y (N strain) genomic RNA. J Gen Virol 70:935–947

    Article  CAS  PubMed  Google Scholar 

  54. Roossinck MJ (2003) Plant RNA virus evolution. Curr Opin Microbiol 6:406–409

    Article  CAS  PubMed  Google Scholar 

  55. Salminen MO, Carr JK, Burke DS, McCutchan FE (1995) Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retrovir 11:1423–1425

    Article  CAS  PubMed  Google Scholar 

  56. Schubert J, Fomitcheva V, Sztangret-Wiśniewska J (2007) Differentiation of Potato virus Y strains using improved sets of diagnostic PCR-primers. J Virol Methods 140:66–74

    Article  CAS  PubMed  Google Scholar 

  57. Schubert J, Thieme T, Thieme R, Ha CV, Hoang GT (2015) Molecular and biological characterization of Potato virus Y isolates from Vietnam. J Phytopathol 163:620–631. doi:10.1111/jph.12362

    Article  Google Scholar 

  58. Simon AE, Bujarski JJ (1994) RNA-RNA Recombination and evolution in virus-infected plants. Ann Rev Phytopathol 32:337–362

    Article  CAS  Google Scholar 

  59. Singh RP, Valkonen JPT, Gray SM, Boonham N, Jones RAC, Kerlan C, Schubert J (2008) Discussion paper: the naming of Potato virus Y strains infecting potato. Arch Virol 153:1–13

    Article  CAS  PubMed  Google Scholar 

  60. Smith JM (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126–129

    CAS  PubMed  Google Scholar 

  61. Sokal R, Michener C (1958) A statistical method for evaluating systematic relationships. Univ Kansas Sci Bull 38:1409–1438

    Google Scholar 

  62. Sukumaran J, Holder MT (2010) A Python library for phylogenetic computing. Bioinformatics 26:1569–1571

    Article  CAS  PubMed  Google Scholar 

  63. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Tian YP, Valkonen JP (2013) Genetic determinants of Potato virus Y required to overcome or trigger hypersensitive resistance to PVY strain group O controlled by the gene Ny in potato. Mol Plant Microbe Interact 26:297–305. doi:10.1094/MPMI-09-12-0219-R

    Article  CAS  PubMed  Google Scholar 

  65. Tian Y-P, Valkonen JPT (2015) Recombination of strain O segments to HCpro–encoding sequence of strain N of Potato virus Y modulates necrosis induced in tobacco and in potatoes carrying resistance genes Ny or Nc. Mol Plant Pathol 16:735–747

    Article  CAS  PubMed  Google Scholar 

  66. Vassilakos N, Simon V, Tzima A, Johansen E, Moury M (2016) Genetic determinism and evolutionary reconstruction of a host jump in a plant virus. Mol Biol Evol 33:541–553. doi:10.1093/molbev/msv222

    Article  CAS  PubMed  Google Scholar 

  67. Wang B, Jia JL, Wang XQ, Wang ZY, Yang BH, Li XD, Zhu XP (2012) Molecular characterization of two recombinant potato virus Y isolates from China. Arch Virol 157:401–403

    Article  CAS  PubMed  Google Scholar 

  68. Wylie SJ, Adams M, Chalam C, Kreuze J, López-Moya JJ, Ohshima K, Praveen S, Rabenstein F, Stenger D, Wang A, Zerbini FM (2017) ICTV Virus Taxonomy Profile: Potyviridae. J Gen Virol 98:352–354

    Article  PubMed  Google Scholar 

  69. Zimnoch-Guzowska E, Yin Z, Chrzanowska M, Flis B (2013) Sources and effectiveness of potato PVY resistance in IHAR’s breeding research. Am J Potato Res 90:21–27

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of PSES, University of Idaho, Moscow, ID, 83844-2339, USA

    Kelsie J. Green & Alexander V. Karasev

  2. Bioinformatics and Computational Biology Program, University of Idaho, Moscow, ID, USA

    Kelsie J. Green, Celeste J. Brown & Alexander V. Karasev

  3. Department of Biological Sciences, University of Idaho, Moscow, ID, USA

    Celeste J. Brown

Authors
  1. Kelsie J. Green
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Celeste J. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander V. Karasev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander V. Karasev.

Ethics declarations

Funding

This work was funded in part through grants from the United States Department of Agriculture (USDA)-NIFA-NRI (2009-35600-05025), USDA-NIFA-SCRI (2009-51181-05894 and 2014-51181-22373), USDA-ARS (58-5354-7-540, 58-5354-2-345, and 58-1907-8-870), Northwest Potato Research Consortium, Idaho Potato Commission, by the USDA-NIFA-Hatch project IDA01560 and by the Idaho Agricultural Experiment Station.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Handling Editor: F. Murilo Zerbini.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 27 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Green, K.J., Brown, C.J. & Karasev, A.V. Genetic diversity of potato virus Y (PVY): sequence analyses reveal ten novel PVY recombinant structures. Arch Virol 163, 23–32 (2018). https://doi.org/10.1007/s00705-017-3568-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-017-3568-x

Search

Navigation