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Phylogenetic relationships, recombination analysis, and genetic variability among diverse variants of tomato yellow leaf curl virus in Iran and the Arabian Peninsula: further support for a TYLCV center of diversity

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Abstract

The discovery of five strains of TYLCV in Iran, including the most well-known and widespread, TYLCV-IL, spurred a detailed study of the full-length genomes of additional TYLCV field isolates and an in-depth analysis of phylogenetic relationships, extent of recombination, and genetic variability of TYLCV isolates within Iran and throughout the Arabian Peninsula. Phylogenetic analysis of complete genome sequences of TYLCV isolates from Iran and other countries revealed four monophyletic clusters could be differentiated based on geographical origin, indicating that recent dispersal of these populations (by the vector or by humans) from these four regions has occurred minimally, or not at all. Genetic analysis revealed that TYLCV-IL isolates from southern Iran possessed greater genetic variability than the northeastern isolates, a pattern that may be reflective of evolution driven by geographically dependent isolation. Similarly, isolates of TYLCV-OM originating from Oman showed greater genetic variability than TYLCV-OM variants from Iran. Major recombination events, which were detected in all strains of TYLCV had breakpoints initiating in the C1, C1/C4, C2/C3 and V1 open reading frames (ORFs) and ending at the non-coding region and the C1, C1/C2 and C3 ORFs. Hence, these regions have consistently served as hot spots for recombination worldwide during the evolution of all currently recognized isolates and strains of TYLCV.

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References

  1. Moriones E, Navas-Castillo J (2000) Tomato yellow leaf curl virus, an emerging virus complex causing epidemics worldwide. Virus Res 71:123–134

    Article  CAS  PubMed  Google Scholar 

  2. Czosnek H, Laterrot H (1997) A worldwide survey of tomato yellow leaf curl viruses. Arch Virol 142:1391–1406

    Article  CAS  PubMed  Google Scholar 

  3. Diaz-Pendon JA, Canizares MC, Moriones E, Bejarano ER, Czosnek H, Navas-Castillo J (2010) Tomato yellow leaf curl viruses: menage a trois between the virus complex, the plant and the whitefly vector. Mol Plant Pathol 11:441–450

    Article  CAS  PubMed  Google Scholar 

  4. Brown J, Fauquet C, Briddon R, Zerbini M, Moriones E, Navas-Castillo J (2012) Family Geminiviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: classification and nomenclature of viruses-ninth report of the international committee on taxonomy of viruses. Elsevier Academic Press, USA, pp 351–373

    Google Scholar 

  5. Brown JK (2010) Phylogenetic biology of the Bemisia tabaci sibling species group. In: Stansly PA, Naranjo SE (eds) Bemisia: bionomics and management of a global pest. Dordrecht-Springer, Amsterdam, pp 31–67

    Google Scholar 

  6. Brown J, Frohlich D, Rosell R (1995) The sweet potato or silver leaf white flies: biotypes of Bemisia tabaci or a species complex? Ann Rev Entomol 40:511–534

    Article  CAS  Google Scholar 

  7. Gill RJ, Brown JK (2010) Systematics of Bemisia and Bemisia relatives: can molecular techniques solve the Bemisia tabaci complex conundrum–A taxonomist’s viewpoint. In: Stansly PA, Naranjo SE (eds) Bemisia: bionomics and management of a global pest. Dordrecht-Springer, Amsterdam, pp 5–29

    Google Scholar 

  8. Brown J (2007) The Bemisia tabaci complex: genetic and phenotypic variation and relevance to TYLCV-vector interactions. In: Czosnek H (ed) Tomato yellow leaf curl virus––disease management, molecular biology, and breeding for resistance. Springer, The Netherlands, pp 25–56

    Google Scholar 

  9. Brown JK, Czosnek H (2002) Whitefly transmission of plant viruses. In: Plumb RT (ed) Advances in botanical research. Academic Press, New York, pp 65–100

    Google Scholar 

  10. Brown JK (2007) The Bemisia tabaci complex: genetic and phenotypic variability drives begomovirus spread and virus diversification. Online, APSnet Features. http://www.apsnet.org/online/feature/btabaci/

  11. Garcia-Andres S, Accotto GP, Navas-Castillo J, Moriones E (2007) Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the tomato yellow leaf curl disease in the mediterranean basin. Virology 359:302–312

    Article  CAS  PubMed  Google Scholar 

  12. Mansoor S, Amin I, Iram S, Hussain M, Zafar Y, Malik K, Briddon R (2003) Breakdown of resistance in cotton to cotton leaf curl disease in Pakistan. Plant Pathol 52:784

    Article  Google Scholar 

  13. García-Arenal F, Fraile A, Malpica JM (2001) Variability and genetic structure of plant virus populations. Ann Rev Phytopathol 39:157–186

    Article  Google Scholar 

  14. García-Arenal F, McDonald BA (2003) An analysis of the durability of resistance to plant viruses. Phytopathology 93:941–952

    Article  PubMed  Google Scholar 

  15. Gibbs AJ, Keese PL, Gibbs MJ, Garcia-Arenal F (1999) Plant virus evolution: past, present and future. In: Domingo E, Webster R, Holland J (eds) Origin and evolution of viruses. Academic Press, New York, pp 263–285

    Chapter  Google Scholar 

  16. Isnard M, Granier M, Frutos R, Reynaud B, Peterschmitt M (1998) Quasispecies nature of three maize streak virus isolates obtained through different modes of selection from a population used to assess response to infection of maize cultivars. J Gen Virol 79:3091–3099

    CAS  PubMed  Google Scholar 

  17. Ge L, Zhang J, Zhou X, Li H (2007) Genetic structure and population variability of tomato yellow leaf curl China virus. J Virol 81:5902–5907

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  19. Pita J, Fondong V, Sangare A, Otim-Nape G, Ogwal S, Fauquet C (2001) Recombination, pseudo-recombination and synergism of gemini viruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda. J Gen Virol 82:655–665

    CAS  PubMed  Google Scholar 

  20. Preiss W, Jeske H (2003) Multitasking in replication is common among gemini viruses. J Virol 77:2972–2980

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Seal S, vanden Bosch F, Jeger M (2006) Factors influencing begomovirus evolution and their increasing global significance: implications for sustainable control. Crit Rev Plant Sci 25:23–46

    Article  Google Scholar 

  22. Moya A, Holmes EC, González-Candelas F (2004) The population genetic sand evolutionary epidemiology of RNA viruses. Nat Rev Microbiol 2(4):279–288

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Idris AM, Brown JK (2005) Evidence for interspecific-recombination for three monopartite begomoviral genomes associated with the tomato leaf curl disease from central Sudan. Arch Virol 150:1003–1012

    Article  CAS  PubMed  Google Scholar 

  25. Bananej K, Kheyr-Pour A, Salekdeh GH, Ahoonmanesh A (2004) Complete nucleotide sequence of Iranian tomato yellow leaf curl virus isolate: further evidence for natural recombination amongst begomoviruses. Brief report. Arch Virol 149:1435–1443

    Article  CAS  PubMed  Google Scholar 

  26. Khan AJ, Idris AM, Al-Saady NA, Al-Mahruki MS, Al-Subhi AM, Brown JK (2008) A divergent isolate of Tomato yellow leaf curl virus from Oman with an associated DNA beta satellite: an evolutionary link between Asian and the Middle Eastern virus-satellite complexes. Virus Gen 36:169–176

    Article  CAS  Google Scholar 

  27. Lefeuvre P, Martin DP, Harkins G, Lemey P, Gray AJ, Meredith S, Lakay F, Lett JM, Monjane A, Varsani A, Heydarnejad J (2010) The spread of Tomato yellow leaf curl virus from the Middle East to the world. PLoS Pathog 6:e1001164

    Article  PubMed Central  PubMed  Google Scholar 

  28. Pakniat A, Behjatnia SAA, Kharazmi S, Shahbazi M, Izadpanah K (2010) Molecular characterization and construction of an infectious clone of a new strain of tomato yellow leaf curl virus in southern Iran. Iran J Plant Pathol 46:101–115

    Google Scholar 

  29. Bird J, Idris A, Rogan D, Brown J (2001) Introduction of the exotic Tomato yellow leaf curl virus-Israel in tomato to Puerto Rico. Plant Dis 85:1028

    Article  Google Scholar 

  30. Brown J, Idris A (2006) Introduction of the exotic monopartite Tomato yellow leaf curl virus into west coast Mexico. Plant Dis 90:1360

    Article  Google Scholar 

  31. Idris A, Guerrero J, Brown J (2007) Two distinct isolates of Tomato yellow leaf curl virus threaten tomato production in Arizona and Sonora, Mexico. Plant Dis 91:910

    Article  Google Scholar 

  32. Isakeit T, Idris A, Sunter G, Black M, Brown J (2007) Tomato yellow leaf curl virus in tomato in Texas, originating from transplant facilities. Plant Dis 91:466

    Article  Google Scholar 

  33. Navas-Castillo J, Sanchez-Campos S, Noris E, Louro D, Accotto GP, Moriones E (2000) Natural recombination between Tomato yellow leaf curl virus-Is and Tomato leaf curl virus. J Gen Virol 81:2797–2801

    CAS  PubMed  Google Scholar 

  34. Ooi K, Ohshita S, Ishii I, Yahara T (1997) Molecular phylogeny of gemini virus infecting wild plants in Japan. J Plant Res 110:247–257

    Article  CAS  Google Scholar 

  35. Yahara T, Ooi K, Oshita S, Ishii I, Ikegami M (1998) Molecular evolution of a host-range gene in gemini viruses infecting asexual populations of Eupatorium makinoi. Gen Genet Sys 73:137–141

    Article  CAS  Google Scholar 

  36. Sanz AI, Fraile A, Gallego JM, Malpica JM, García-Arenal F (1999) Genetic variability of natural populations of cotton leaf curl gemini virus, a single-stranded DNA virus. J Mol Evol 49:672–681

    Article  CAS  PubMed  Google Scholar 

  37. Sanchez-Campos S, Diaz JA, Monci F, Bejarano ER, Reina J, Navas-Castillo J, Aranda MA, Moriones E (2002) High genetic stability of the begomovirus Tomato yellow leaf curl Sardinia virus in southern Spain over an 8-year period. Phytopathology 92:842–849

    Article  CAS  PubMed  Google Scholar 

  38. Fazeli R, Heydarnejad J, Massumi H, Shaabanian M, Varsani A (2009) Genetic diversity and distribution of tomato-infecting begomoviruses in Iran. Virus Gen 38:311–319

    Article  CAS  Google Scholar 

  39. Bananej K, Vahdat A, Hosseini Salekdeh G (2009) Begomoviruses associated with yellow leaf curl disease of tomato in Iran. J Phytopathol 157:243–247

    Article  Google Scholar 

  40. Silva S, Castillo-Urquiza G, Hora-Júnior B, Assunção I, Lima G, Pio-Ribeiro G, Zerbini F, Mizubuti E (2012) Species diversity, phylogeny and genetic variability of begomovirus populations infecting leguminous weeds in Northeastern Brazil. Plant Pathol 61:457–467

    Article  Google Scholar 

  41. Antignus Y, Cohen S (1994) Complete nucleotide sequence of an infectious clone of a mild isolate of tomato yellow leaf curl virus (TYLCV). Phytopathology 84:707–712

    Article  CAS  Google Scholar 

  42. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bulletin 19:11–15

    Google Scholar 

  43. Cullings KW (1992) Design and testing of a plant-specific PCR primer for ecological and evolutionary studies. Mol Ecol 1:233–240

    Article  CAS  Google Scholar 

  44. Lapidot M (2002) Screening common bean (Phaseolus vulgaris) for resistance to Tomato yellow leaf curl virus. Plant Dis 86:429–432

    Article  Google Scholar 

  45. Azizi A, Shams-Bakhsh M, Mozafari J, Montazeri-Hedesh R (2012) Complete genomic sequence of a strain of Tomato yellow leaf curl virus from Iran. Iran J Virol 5:18–27

    Google Scholar 

  46. Rojas MR, Gilbertson RL, Russell DR, Maxwell DP (1993) Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted gemini viruses. Plant Dis 77:340–347

    Article  CAS  Google Scholar 

  47. Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG (2002) Universal primers for the PCR-mediated amplification of DNA β, a molecule associated with some monopartite begomoviruses. Mol Biotechnol 20:315–318

    Article  CAS  PubMed  Google Scholar 

  48. Inoue-Nagata AK, Albuquerque LC, Rocha WB, Nagata T (2004) A simple method for cloning the complete begomovirus genome using the bacteriophage Ø29 DNA polymerase. J Virol Meth 116:209–211

    Article  CAS  Google Scholar 

  49. Sambrook JR, Russel D (2001) Molecular cloning: a laboratory manual. CSHL Press, Cold Spring Harbor

    Google Scholar 

  50. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Bao Y, Chetvernin V, Tatusova T (2012) Pairwise sequence comparison (PASC) and its application in the classification of Filo viruses. Viruses 4:1318–1327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  52. 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 Central  PubMed  Google Scholar 

  53. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  54. Berrie LC, Rybicki EP, Rey ME (2001) Complete nucleotide sequence and host range of South African cassava mosaic virus: further evidence for recombination amongst begomoviruses. J Gen Virol 82:53–58

    CAS  PubMed  Google Scholar 

  55. Lefeuvre P, Lett JM, Reynaud B, Martin DP (2007) Avoidance of protein fold disruption in natural virus recombinants. PLoS Pathog 3:e181

    Article  PubMed Central  PubMed  Google Scholar 

  56. Lefeuvre P, Martin DP, Hoareau M, Naze F, Delatte H, Thierry M, Varsani A, Reynaud B, Becker N, Lett JM (2007) Begomovirus ‘melting pot’ in the south-west Indian Ocean islands: molecular diversity and evolution through recombination. J Gen Virol 88:3458–3468

    Article  CAS  PubMed  Google Scholar 

  57. Garcia-Andres S, Tomas DM, Sanchez-Campos S, Navas-Castillo J, Moriones E (2007) Frequent occurrence of recombinants in mixed infections of tomato yellow leaf curl disease-associated begomoviruses. Virology 365:210–219

    Article  CAS  PubMed  Google Scholar 

  58. Idris AM, Brown JK (2002) Molecular analysis of Cotton leaf curl virus-Sudan reveals an evolutionary history of recombination. Virus Gen 24:249–256

    Article  CAS  Google Scholar 

  59. Duffy S, Holmes EC (2008) Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus tomato yellow leaf curl virus. J Virol 82:957–965

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Polston JE, Anderson PK (1997) The emergence of whitefly-transmitted gemini viruses in tomato in the Western hemisphere. Plant Dis 81:1358–1369

    Article  Google Scholar 

  61. Polston J, McGovern R, Brown L (1999) Introduction of tomato yellow leaf curl virus in Florida and implications for the spread of this and other Gemini viruses of tomato. Plant Dis 83:984–988

    Article  Google Scholar 

  62. Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D (2000) Gemini viruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Biochem Mol Biol 35:105–140

    CAS  PubMed  Google Scholar 

  63. Garcia-Andres S, Monci F, Navas-Castillo J, Moriones E (2006) Begomovirus genetic diversity in the native plant reservoir Solanum nigrum: evidence for the presence of a new virus species of recombinant nature. Virology 350:433–442

    Article  CAS  PubMed  Google Scholar 

  64. Monci F, Sanchez-Campos S, Navas-Castillo J, Moriones E (2002) A natural recombinant between the gemini viruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 303:317–326

    Article  CAS  PubMed  Google Scholar 

  65. Idris AM, Abdullah N, Brown J (2012) Leaf curl diseases of two solanaceous species in Southwest Arabia are caused by a monopartite begomovirus evolutionarily most closely related to a species from the Nile Basin and unique suite of beta satellites. Virus Res 169:296–300

    Article  CAS  PubMed  Google Scholar 

  66. Huang A, Hogan JW, Istrail S, DeLong A, Katzenstein DA, Kantor R (2012) Global analysis of sequence diversity within HIV-1 subtypes across geographic regions. Fut Virol 7:505–517

    Article  CAS  Google Scholar 

  67. Duffy S, Holmes EC (2007) Multiple introductions of the old world begomovirus Tomato yellow leaf curl virus into the new world. Appl Environ Microbiol 73:7114–7117

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

The authors wish to thank Siobain Duffy, Department of Ecology, Evolution and Natural Resources, School of Environmental and Biological Sciences, Rutgers University, USA, for generous and informative technical advice. This report is a component of the Ph.D. dissertation of the first author.

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Authors and Affiliations

  1. Plant Pathology Department, Faculty of Agriculture, Tarbiat Modares University, Tehran, Iran

    Mohammad Reza Hosseinzadeh & Masoud Shams-Bakhsh

  2. Department of Plant Sciences, Faculty of Biological Sciences, Tarbiat Modares University, Tehran, Iran

    Shahrokh Kazempour Osaloo

  3. School of Plant Sciences, The University of Arizona, Tucson, AZ, 85721, USA

    Judith K. Brown

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  1. Mohammad Reza Hosseinzadeh
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  2. Masoud Shams-Bakhsh
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Correspondence to Masoud Shams-Bakhsh.

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Hosseinzadeh, M.R., Shams-Bakhsh, M., Osaloo, S.K. et al. Phylogenetic relationships, recombination analysis, and genetic variability among diverse variants of tomato yellow leaf curl virus in Iran and the Arabian Peninsula: further support for a TYLCV center of diversity. Arch Virol 159, 485–497 (2014). https://doi.org/10.1007/s00705-013-1851-z

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