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Spatial and temporal diversity of begomoviral complexes in papayas with leaf curl disease

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Abstract

Old World, monopartite begomoviruses associated with satellite DNA β were observed in papaya showing symptoms of leaf curl disease sampled randomly over five years from within a radius of 250 km in north-central India. Three groups of DNA A sequences were evident. One group resembled chili leaf curl virus infecting tomatoes (ChiLCuV). Another group resembled tomato leaf curl New Delhi virus (ToLCuNDV). The third group was novel (tentatively named papaya leaf crumple virus, PaLCrV), with less than 89% identity to known begomovirus sequences in the GenBank database. At least seven DNA A sequences were putative recombinants. The AC4-encoding regions exhibited highest numbers of non-synonymous substitutions. Most DNA β sequences resembled tomato leaf curl virus–associated DNA βs. A few DNA β sequences were similar to that of croton yellow vein mosaic virus–associated DNA β (CroYVMVβ). One DNA β sequence was novel and showed <65% similarity to its counterparts. Mixed infections and sequence diversity among 25 cloned av1 genes indicated that papayas grown in plantations, kitchen gardens and feral patches in the region are vulnerable to disease outbreak. No geographic or temporal patterns were discernable in the distribution of these viruses.

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References

  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  2. Aragao FJL, Faria JC (2009) First transgenic geminivirus-resistant plant in the field. Nat Biotechnol 27:1086–1088

    Article  PubMed  CAS  Google Scholar 

  3. Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X, Fauquet CM (2008) Recommendations for the classification and nomenclature of the DNA-β satellites of begomoviruses. Arch Virol 153:763–781

    Article  PubMed  CAS  Google Scholar 

  4. 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 monopartite begomoviruses. Mol Biotechnol 20:315–318

    Article  PubMed  CAS  Google Scholar 

  5. Briddon RW, Markham PG (2000) Cotton leaf curl virus disease. Virus Res 71:151–159

    Article  PubMed  CAS  Google Scholar 

  6. Bull SE, Tsai W-S, Briddon RW, Markham PG, Stanley J, Green SK (2004) Diversity of begomovirus DNA β satellites of non-malvaceous plants in east and south-east Asia. Arch Virol 149:1193–1200

    Article  PubMed  CAS  Google Scholar 

  7. Chandra KJ, Samuel LDK (1999) Viral and phytoplasmal diseases of papaya in India. In: Verma LR, Sharma RC (eds) Diseases of horticultural crops-fruits. Indus Publishing Company, New Delhi, pp 493–515

    Google Scholar 

  8. Chowda-Reddy RV, Colvin J, Muniyappa V, Seal SE (2005) Diversity and distribution of begomoviruses infecting tomato in India. Arch Virol 150:845–867

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  10. 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  PubMed  CAS  Google Scholar 

  11. Etessami P, Saunders K, Watts J, Stanley J (1991) Mutational analysis of complementary-sense genes of African cassava mosaic virus DNA A. J Gen Virol 72:1005–1012

    Article  PubMed  CAS  Google Scholar 

  12. Fauquet CM, Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X (2008) Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821

    Article  PubMed  CAS  Google Scholar 

  13. Fauquet CM, Sawyer S, Idris AM, Brown JK (2005) Sequence analysis and classification of apparent recombinant begomoviruses infecting tomato in the Nile and Mediterranean Basins. Phytopathology 95:549–555

    Article  PubMed  CAS  Google Scholar 

  14. Fondong VN, Chowda Reddy RV, Lu C, Hankoua B, Felton C, Czymmek K, Achenjang F (2007) The consensus N-Myristoylation motif of a Geminivirus AC4 protein is required for membrane binding and pathogenicity. Mol Plant Microbe Interact 20:380–391

    Article  PubMed  CAS  Google Scholar 

  15. Ha C, Coombs S, Revill P, Harding R, Vu M, Dale J (2008) Molecular characterization of begomoviruses and DNA satellites from Vietnam: additional evidence that the New World geminiviruses were present in the Old World prior to continental separation. J Gen Virol 89:312–326

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  17. 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

    PubMed  CAS  Google Scholar 

  18. Jupin I, De Kouchkovsky F, Jouanneau F, Gronenborn B (1994) Movement of tomato yellow leaf curl geminivirus (TYLCV): involvement of the protein encoded by ORF C4. Virology 204:82–90

    Article  PubMed  CAS  Google Scholar 

  19. Kosakovsky Pond SL, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. In: Nielsen R (ed) Statistical methods in molecular evolution. Springer, ISBN:0-387-22333-9

  20. Kosakovsky Pond SL, Poon AFY, Frost SDW (2007) Estimating selection pressures on alignments of coding sequences. In: Lemey P, Salemi M, Vandamme A-M (eds) The phylogenetic handbook, 2nd edn. Cambridge University Press, ISBN:978-0521730716

  21. Legg JP (1999) Emergence, spread and strategies for controlling the pandemic of cassava mosaic virus disease in east and central Africa. Crop Prot 18:627–637

    Article  Google Scholar 

  22. Mansoor S, Briddon RW, Bull SE, Bedford ID, Bashir A, Hussain M, Saeed M, Zafar Y, Malik KA, Fauquet C, Markham PG (2003) Cotton leaf curl disease is associated with multiple monopartite begomoviruses supported by single DNA β. Arch Virol 148:1969–1986

    Article  PubMed  CAS  Google Scholar 

  23. Martin DP, Lerney 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 

  24. Maruthi MN, Rekha AR, Mirza SH, Alam SN, Colvin J (2007) PCR-based detection and partial genome sequencing indicate high genetic diversity in Bangladeshi begomoviruses and their whitefly vector, Bemisia tabaci. Virus Genes 34:373–385

    Article  PubMed  CAS  Google Scholar 

  25. McCouch S (2004) Diversifying selection in plant breeding. PLoS Biol 2:e347

    Article  PubMed  Google Scholar 

  26. Moffat AS (1999) Geminiviruses emerge as serious crop threat. Science 286:1835

    Article  CAS  Google Scholar 

  27. Monci F, Sánchez-Campos S, Navas-Castillo J, Moriones E (2002) A natural recombinant between the geminiviruses 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  PubMed  CAS  Google Scholar 

  28. Muse SV, Gaut BS (1994) A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol Biol Evol 11:715–724

    PubMed  CAS  Google Scholar 

  29. Nariani TK (1956) Leaf curl of papaya. Indian Phytopathol 9:151–155

    Google Scholar 

  30. Nawaz-ul-Rehman MS, Fauquet CM (2009) Evolution of geminiviruses and their satellites. FEBS Lett 583:1825–1832

    Article  PubMed  CAS  Google Scholar 

  31. Noris E, Vaira AM, Caciagli P, Masenga V, Gronenborn B, Accotto GP (1998) Amino acids in the capsid protein of tomato yellow leaf curl virus that are crucial for systemic infection, particle formation, and insect transmission. J Virol 72:10050–10057

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  33. Paximadis M, Muniyappa V, Rey MEC (2001) A mixture of begomoviruses in leaf curl-affected tobacco in Karnataka, South India. Ann Appl Biol 139:101–109

    Article  CAS  Google Scholar 

  34. Pita JS, Fondong VN, Sangaré A, Otim-Nape GW, Ogwal S, Fauquet CM (2001) Recombination, pseudorecombination and synergism of geminiviruses are determinant keys to the epidemic of severe cassava mosaic disease in Uganda. J Gen Virol 82:655–665

    PubMed  CAS  Google Scholar 

  35. Polston JE, Anderson PL (1997) The emergence of whitefly transmitted geminiviruses in tomato in the Western Hemisphere. Plant Dis 81:1358–1369

    Article  Google Scholar 

  36. Poon AFY, Frost SDW, Kosakovsky Pond SL (2009) Detecting signatures of selection from DNA sequences using Datamonkey. In: Posada D (ed) Bioinformatics for DNA sequences analysis, methods in molecular biology. Humana Press, a part of Springer Science+Business Media, pp 163–183

  37. Posada D, Crandall K (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  38. Prasanna HC, Rai M (2007) Detection and frequency of recombination in tomato-infecting begomoviruses of South and Southeast Asia. Virol J 4:111

    Article  PubMed  CAS  Google Scholar 

  39. Praveen S, Dasgupta A, Varma A (2004) Phylogenetic analysis and homologies of the Replicase of tomato leaf curl geminiviruses: implications for obtaining pathogen derived resistance. Virus Genes 28:195–199

    Article  PubMed  CAS  Google Scholar 

  40. Raj SK, Snehi SK, Khan MS, Singh R, Khan AA (2008) Molecular evidence for association of Tomato leaf curl New Delhi virus with leaf curl disease of papaya (Carica papaya L.) in India. Aust Plant Dis Notes 3:152–155

    Article  CAS  Google Scholar 

  41. Rybicki EP, Pietersen G (1999) Plant virus disease problems in the developing world. Adv Virus Res 53:127–175

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  43. Sanz AI, Fraile A, García-Arenal F, Zhou X, Robinson DJ, Khalid S, Butt T, Harrison B (2000) Multiple infection, recombination and genome relationships among begomovirus isolates found in cotton and other plants in Pakistan. J Gen Virol 81:1839–1849

    PubMed  CAS  Google Scholar 

  44. Saxena S, Hallan V, Singh BP, Sane PV (1998) Nucleotide sequence and intergeminiviral homologies of the DNA A of papaya leaf curl geminivirus from India. Biochem Mol Biol Int 45:101–113

    PubMed  CAS  Google Scholar 

  45. Sen PK, Ganguli BD, Malik PC (1946) A note on a leaf curl disease of papaya (Carica papaya L.). Indian J Hortic 3:38–40

    Google Scholar 

  46. Sharma AD, Gill PK, Singh P (2002) DNA isolation from dry and fresh samples of polysaccharide-rich plants. Plant Mol Biol Rep 20:415a–415f

    Article  Google Scholar 

  47. Singh P (2011) Molecular characterization and serological detection of putative begomoviruses infecting papaya from Delhi and Haryana. Dissertation, University of Delhi

  48. 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 

  49. Thomas KM, Krishnaswami CS (1939) Leaf crinkle—a transmissible disease of papaya. Curr Sci 8:316

    Google Scholar 

  50. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acid Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  51. Vanderschuren H, Stupak MFJ, Gruissem W, Zhang P (2007) Engineer resistance to geminiviruses—review and perspectives. Plant Biotechnol J 5:207–220

    Article  PubMed  CAS  Google Scholar 

  52. Vanitharani R, Chellappan P, Pita JS, Fauquet CM (2004) Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. J Virol 78:9487–9498

    Article  PubMed  CAS  Google Scholar 

  53. Varma A, Malathi VG (2003) Emerging geminivirus problems. A serious threat to crop production. Ann Appl Biol 142:145–164

    Article  CAS  Google Scholar 

  54. Wang X, Xie Y, Zhou X (2004) Molecular characterization of two distinct begomoviruses from papaya in China. Virus Genes 29:303–309

    Article  PubMed  CAS  Google Scholar 

  55. Zhou X, Liu Y, Calvert L, Munoz C, Otim-Nape GW, Robinson DJ, Harrison BD (1997) Evidence that DNA A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. J Gen Virol 78:2101–2111

    PubMed  CAS  Google Scholar 

  56. Zhou X, Liu Y, Robinson DJ, Harrison BD (1998) Four DNA A variants among Pakistani isolates of cotton leaf curl virus and their affinities to DNA A of geminivirus isolates from okra. J Gen Virol 79:915–923

    PubMed  CAS  Google Scholar 

  57. Zhou XP, Xie Y, Tao XR, Zhang ZK, Li ZH, Fauquet CM (2003) Characterization of DNA β associated with begomoviruses in China and evidence for co-evolution with their cognate viral DNA A. J Gen Virol 84:237–247

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Drs. C. Fauquet and E. Rybicki are thanked for encouraging comments on preliminary poster presentations of this study. Drs. V. Calhoun and L. Bao of GenBank and NCBI are thanked for their advice during sequence submissions. PS acknowledges a PhD-ship from CSIR (Council of Scientific and Industrial Research), Government of India. SM-L thanks Dr. D. Gonsalves for an introduction into the world of papaya viruses. Equipment support from Bio-Rad (India) Inc. is gratefully acknowledged. This work was supported in part by funds from University Grants Commission for strengthening R&D at Delhi University. No virus isolates from this study were grown or maintained at any site away from their site of origin.

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Correspondence to S. Mazumdar-Leighton.

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Nucleotide sequence data reported are available in the GenBank database under accession numbers DQ376036-37, EU126822-24, DQ376038-39, HM134220-37, DQ989325-26, HM140364-71, EU126825-26, HM143901-11.

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Singh-Pant, P., Pant, P., Mukherjee, S.K. et al. Spatial and temporal diversity of begomoviral complexes in papayas with leaf curl disease. Arch Virol 157, 1217–1232 (2012). https://doi.org/10.1007/s00705-012-1287-x

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