Skip to main content

Role of Genetic Recombination in the Molecular Architecture of Papaya ringspot virus

Biochemical Genetics volume 46, pages 835–846 (2008)Cite this article

Abstract

Papaya ringspot virus (PRSV) has a single-stranded RNA genome and causes severe economic losses both in cucurbits and papaya worldwide. The extent to which the genome of PRSV is shaped by recombination provides an understanding of the molecular evolution of PRSV and helps in studying features such as host specificity, geographic distribution, and its emergence as new epidemics. The PRSV-P-Indian isolate was completely sequenced and compared with 14 other isolates reported from the rest of the world for their phylogenetic survey of recombination events. Cistron-by-cistron sequence comparison and phylogenetic analysis based on full-genome polyprotein showed two distinct groupings of Asian and American isolates, although PRSV-P and W-India clustered along with the American isolates. Recombination sites were found throughout the genomes, except in the small 6K1 protein gene. A significant proportion of recombination hotspots was found in the P1 gene, followed by P3, cylindrical inclusion (CI), and helper component proteinase (HcPro). Correlations between the presence of recombination sites, geographic distribution, and phylogenetic relationship provide an opportunity to establish the molecular evolution and geographic route of PRSV.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  • Bag S, Agarwal S, Jain RK (2007) Sequence diversity in the coat proteins of Papaya ringspot virus isolates originating from different locations in India. Indian Phytopath 60(2):244–250

    CAS  Google Scholar 

  • Bateson MF, Henderson J, Chaleeprom W, Gibbs AG, Dale JL (1994) Papaya ringspot potyvirus: isolate variability and the origin of PRSV type (Australia). J Gen Virol 75:3547–3553

    PubMed  Article  CAS  Google Scholar 

  • Bateson MF, Lines RE, Revill P, Chaleepron W, Ha VC, Gibbs AJ, Dale JL (2002) On the evolution and molecular epidemiology of potyvirus Papaya ringspot virus. J Gen Virol 83:2575–2585

    PubMed  CAS  Google Scholar 

  • Bujarski JJ, Kaesberg P (1986) Genetic recombination between RNA components of a multipartite plant virus. Nature 321:528–531

    PubMed  Article  CAS  Google Scholar 

  • Chare ER, Holmes EC (2006) A phylogenetic survey of recombination frequency in plant RNA viruses. Arch Virol 151:933–946

    PubMed  Article  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fernandez-Rodriguez T, Rubio L, Carballo O, Marys E (2008) Genetic variation of papaya ringspot virus in Venezuela. Arch Virol 153:343–349

    PubMed  Article  CAS  Google Scholar 

  • Gonsalves D (1998) Control of papaya ringspot virus in papaya: a case study. Annu Rev Phytopathol 36:415–437

    PubMed  Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis programs for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hon C-C, Lam T-Y, Shi Z-L, Drummond AJ, Yip C-W, Zeng F, Lam P-Y, Leung FC-C (2008) Evidence of the recombinant origin of a bat severe acute respiratory syndrome (SARS)-like coronavirus and its implications on the direct ancestor of SARS coronavirus. J Virol 82(4):1819–1826

    PubMed  Article  CAS  Google Scholar 

  • Inoue-Nagata AK, Franco CM, Martin DP, Rezende JA, Ferreira GB, Dutra LS, Nagata T (2007) Genome analysis of a severe and a mild isolate of Papaya ringspot virus-type W found in Brazil. Virus Genes 35:881–882

    Article  CAS  Google Scholar 

  • Jain RK, Pappu HR, Pappu SS, Varma A, Ram RD (1998) Molecular characterization of Papaya ringspot potyvirus isolates from India. Ann Appl Biol 132:413–425

    Article  CAS  Google Scholar 

  • Jain RK, Sharma J, Sivakumar AS, Sharma PK, Byadgi AS, Verma AK, Varma A (2004) Variability in the coat protein gene of Papaya ringspot virus isolates from multiple locations in India. Arch Virol 149:2435–2442

    PubMed  Article  CAS  Google Scholar 

  • Klein PG, Klein RR, Rodriguez-Cerezo E, Hunt AG, Shaw JG (1994) Mutational analysis of the Tobacco vein mottling virus genome. Virology 204:759–769

    PubMed  Article  CAS  Google Scholar 

  • Lai MMC (1992) RNA recombination in animal and plant viruses. Microbiol Rev 56:61–79

    PubMed  CAS  Google Scholar 

  • Noa-Carrazana JC, Gonzalez-De-Leon D, Silva-Rosales L (2007) Molecular characterization of a severe isolate of Papaya ringspot virus in Mexico and its relationship with other isolates. Virus Genes 35:109–117

    PubMed  Article  CAS  Google Scholar 

  • Ohshima K, Yamaguchi Y, Hirota R, Hamamoto T, Tomimura K, Tan Z, Sano T, Azuhata F, Walsh JA et al (2002) Molecular evolution of Turnip mosaic virus: evidence of host adaptation, genetic recombination and geographical spread. J Gen Virol 83:1511–1521

    PubMed  CAS  Google Scholar 

  • Ohshima K, Tomitaka Y, Wood JT, Minematsu Y, Kajiyama H, Tomimura K, Gibbs AJ (2007) Pattern of recombination in Turnip mosaic virus genomic sequences indicates hotspots of recombination. J Gen Virol 88:298–315

    PubMed  Article  CAS  Google Scholar 

  • Parameswari B, Mangrauthia SK, Praveen S, Jain RK (2007) Complete genome sequence of an isolate of Papaya ringspot virus from India. Arch Virol 152(4):843–845

    PubMed  Article  CAS  Google Scholar 

  • Posada D, Crandall KA, Holmes EC (2002) Recombination in evolutionary genomics. Annu Rev Genet 36:75–97

    PubMed  Article  CAS  Google Scholar 

  • Praveen S, Kushwaha CM, Mishra AK, Singh V, Jain RK, Varma A (2005) Engineering tomato for resistance to tomato leaf curl disease using viral rep gene sequences. Plant Cell Tissue Organ Cult 83:311–318

    Article  Google Scholar 

  • Purcifull DE, Edwardson JR, Hiebert E, Gonsalves D (1984) Papaya ringspot virus. CMI/AAB description of plant viruses. No. 292. CAB International, Wallingford, UK

    Google Scholar 

  • Ramesh SV, Mishra AK, Praveen S (2007) Hairpin RNA mediated strategies for silencing of Tomato leaf curl virus AC1 and AC4 genes for effective resistance in plants. Oligonucleotide 17:251–257

    Article  CAS  Google Scholar 

  • Reichmann JL, Lain S, Garcia JA (1992) Highlights and prospects of potyvirus molecular biology. J Gen Virol 73:1–16

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Roy G, Jain RK, Bhat AI, Varma A (1999) Comparative host range and serological studies of Papaya ringspot potyvirus isolates. Indian Phytopath 62:14–17

    Google Scholar 

  • Salvador B, Saénz P, Yangüez E, Quiot JB, Quiot L, Delgadillo MO, García JA, Simón-Mateo C (2008) Host-specific effect of P1 exchange between two potyviruses. Mol Plant Path 9(2):147–155

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Urcuqui-Inchima S, Haenni AL, Bernardi F (2001) Potyvirus proteins: a wealth of functions. Virus Res 74:157–175

    PubMed  Article  CAS  Google Scholar 

  • 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 88:1016–1028

    PubMed  Article  CAS  Google Scholar 

  • Varma A (1988) The economic impact of filamentous plant virus—the Indian subcontinent. In: Milne RG (ed) The plant viruses, vol 4. Plenum Press, New York, pp 371–376

    Google Scholar 

  • Verchot J, Carrington JC (1995a) Debilitation of plant potyvirus infectivity by P1 proteinase-inactivating mutations and restoration by second-site modifications. J Virol 69:1582–1590

    PubMed  CAS  Google Scholar 

  • Verchot J, Carrington JC (1995b) Evidences that the potyvirus P1 proteinase functions in trans as an accessory factor for genome amplification. J Virol 69:3668–3674

    PubMed  CAS  Google Scholar 

  • Worobey M, Holmes EC (1999) Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80:2535–2543

    PubMed  CAS  Google Scholar 

  • Yang LJ, Hidaka M, Masaki H, Uozumi T (1998) Detection of Potato virus Y P1 protein in infected cells and analysis of its cleavage sites. Biosci Biotechnol Biochem 62:380–382

    PubMed  Article  CAS  Google Scholar 

  • Yeh SD, Jan FJ, Chiang CH, Doong TJ, Chen MC, Chung PH, Bau HJ (1992) Complete nucleotide sequence and genetic organization of Papaya ringspot virus RNA. J Gen Virol 73:2531–2541

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgment

Satendra K. Mangrauthia was supported by a fellowship from the Council of Scientific and Industrial Research, New Delhi.

Author information

Affiliations

  1. Division of Biochemistry, Indian Agricultural Research Institute, New Delhi, 110012, India

    Satendra K. Mangrauthia

  2. Division of Plant Pathology, Indian Agricultural Research Institute, New Delhi, 110012, India

    B. Parameswari, R. K. Jain & Shelly Praveen

Authors
  1. Satendra K. Mangrauthia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Parameswari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. K. Jain
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shelly Praveen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shelly Praveen.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Mangrauthia, S.K., Parameswari, B., Jain, R.K. et al. Role of Genetic Recombination in the Molecular Architecture of Papaya ringspot virus . Biochem Genet 46, 835–846 (2008). https://doi.org/10.1007/s10528-008-9198-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-008-9198-y

Keywords

  • Potyvirus
  • Genome diversity
  • P1
  • PRSV-P-India