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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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
Aragao FJL, Faria JC (2009) First transgenic geminivirus-resistant plant in the field. Nat Biotechnol 27:1086–1088
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
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
Briddon RW, Markham PG (2000) Cotton leaf curl virus disease. Virus Res 71:151–159
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
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
Chowda-Reddy RV, Colvin J, Muniyappa V, Seal SE (2005) Diversity and distribution of begomoviruses infecting tomato in India. Arch Virol 150:845–867
Czosnek H, Laterrot H (1997) A worldwide survey of tomato yellow leaf curl viruses. Arch Virol 142:1391–1406
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
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
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
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
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
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
Idris AM, Brown JK (2002) Molecular analysis of Cotton leaf curl virus-Sudan reveals an evolutionary history of recombination. Virus Genes 24:249–256
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
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
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
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
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
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
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
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
McCouch S (2004) Diversifying selection in plant breeding. PLoS Biol 2:e347
Moffat AS (1999) Geminiviruses emerge as serious crop threat. Science 286:1835
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
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
Nariani TK (1956) Leaf curl of papaya. Indian Phytopathol 9:151–155
Nawaz-ul-Rehman MS, Fauquet CM (2009) Evolution of geminiviruses and their satellites. FEBS Lett 583:1825–1832
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
Padidam M, Sawyer S, Fauquet CM (1999) Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225
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
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
Polston JE, Anderson PL (1997) The emergence of whitefly transmitted geminiviruses in tomato in the Western Hemisphere. Plant Dis 81:1358–1369
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
Posada D, Crandall K (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Prasanna HC, Rai M (2007) Detection and frequency of recombination in tomato-infecting begomoviruses of South and Southeast Asia. Virol J 4:111
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
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
Rybicki EP, Pietersen G (1999) Plant virus disease problems in the developing world. Adv Virus Res 53:127–175
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
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
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
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
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
Singh P (2011) Molecular characterization and serological detection of putative begomoviruses infecting papaya from Delhi and Haryana. Dissertation, University of Delhi
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
Thomas KM, Krishnaswami CS (1939) Leaf crinkle—a transmissible disease of papaya. Curr Sci 8:316
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
Vanderschuren H, Stupak MFJ, Gruissem W, Zhang P (2007) Engineer resistance to geminiviruses—review and perspectives. Plant Biotechnol J 5:207–220
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
Varma A, Malathi VG (2003) Emerging geminivirus problems. A serious threat to crop production. Ann Appl Biol 142:145–164
Wang X, Xie Y, Zhou X (2004) Molecular characterization of two distinct begomoviruses from papaya in China. Virus Genes 29:303–309
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
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
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
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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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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DOI: https://doi.org/10.1007/s00705-012-1287-x