Skip to main content
Log in

Molecular characterization of a new species of begomovirus associated with yellow vein mosaic of bhendi (Okra) in Bhubhaneswar, India

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Yellow vein mosaic disease of okra is major constraint for the production of okra in India. It is caused by whitefly transmitted begomoviruses and results in severe economic losses of the crop. In the present study a new begomovirus (OYBHU isolate) infecting okra showing yellow vein symptoms from Bhubhaneswar, India was characterized. The complete genome sequence (homologous to DNA-A) was determined and it comprised 2757 nucleotides. Attempts to amplify DNA- B were not successful. However, the association of a betasatellite suggests that the isolate is monopartite and typical of the begomoviruses infecting malvaceous hosts in the Old World. The genome organization is characteristic of begomoviruses, encoding seven ORFs with two ORFs [AV1 (CP) and AV2] in virion sense strand and five ORFs (AC1-AC5) in complementary strand. Comparisons of the virus genome sequence with other known begomoviruses suggests that OYBHU virus isolate is distinct, with Croton yellow vein mosaic virus being its nearest relative, sharing the 81.4 to 86.1 % sequence identity. This is further supported by phylogenetic analyses with clustering of BYVBV on a well supported branch separated from all other begomoviruses. The name Bhendi yellow vein Bhubhaneswar virus (BYVBV) is proposed for virus isolate OYBHU with the additional descriptor [India: Bhubhaneswar:OYBHU:06]. Recombination analyses with BYVBV suggest that it is a recombinant and may have originated by the exchange of genomic segments between the begomoviruses Croton yellow vein mosaic virus, Bhendi yellow vein mosaic virus, Cotton leaf curl multan virus and Mesta yellow vein mosaic virus.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Banks, G. K., Colvin, J., Chowda Reddy, R. V., Maruthi, M. N., Muniyappa, V., Venkatesh, H. M., et al. (2001). First report of the Bemisia tabaci B biotype in India and an associated tomato leaf curl virus disease epidemic. Plant Disease, 85, 231.

    Article  Google Scholar 

  • Berrie, L. C., Rybicki, E. P., & Rey, M. E. C. (2001). Complete nucleotide sequence and host range of South African cassava mosaic virus: further evidence for recombinations amongst begomoviruses. Jounalof General Virology, 82, 53–58.

    CAS  Google Scholar 

  • Briddon, R. W., & Stanley, J. (2006). Subviral agents associated with plant single-stranded DNA viruses. Virology, 344, 198–210.

    Article  CAS  Google Scholar 

  • Briddon, R. W., Bull, S. E., Mansoor, S., Amin, I., & Markham, P. G. (2002). Universal primers for the PCR-mediated amplification of DNA-: a molecule associated with some monopartite begomoviruses. Molecular Biotechnology, 20, 315–318.

    Article  PubMed  CAS  Google Scholar 

  • Briddon, R. W., Bull, S. E., Amin, I., Idris, A. M., Mansoor, S., Bedford, I. D., et al. (2003). Diversity of DNA beta: a satellite molecule associated with some monopartitebegomoviruses. Virology, 312, 106–121.

    Article  PubMed  CAS  Google Scholar 

  • Briddon, R. W., Bull, S. E., Amin, I., Mansoor, S., Bedford, I. D., Rishi, N., et al. (2004). Diversity of DNA 1; a satellite-like molecule associated with monopartite begomovirus-DNA β complexes. Virology, 324(4), 62–474.

    Google Scholar 

  • Chakraborty, S., Pandey, P. K., Banerjee, M. K., Kalloo, G., & Fauquet, C. M. (2003). Tomato leaf curl Gujarat virus, a new begomovirus species causing a severe leaf curl disease of tomato in Varanasi, India. Phytopathology, 93, 1485–1495.

    Article  CAS  Google Scholar 

  • Chatchawankanphanich, O., & Maxwell, D. P. (2002). Tomato leaf curl Karnataka virus from Bangalore, India, appears to be a recombinant begomovirus. Phytopathology, 92, 637–645.

    Article  PubMed  Google Scholar 

  • Chatterjee, A., & Ghosh, S. K. (2007). A new monopartite begomovirus isolated from Hibiscus cannabinus L. in India. Archives of Virology, 152, 2113–2118.

    Article  PubMed  CAS  Google Scholar 

  • Doyle, J. J., & Doyle, J. L. (1990). Isolation of plant DNA from fresh tissue. Focus, 12, 13–15.

    Google Scholar 

  • Fauquet, C. M., Briddon, R. W., Brown, J. K., Moriones, E., Stanley, J., Zerbini, M., et al. (2008). Geminivirus strain demarcation and nomenclature. Archives of Virology, 153, 783–821.

    Article  PubMed  CAS  Google Scholar 

  • Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • Hanley-Bowdoin, L., Settlage, S. B., Orozco, B. M., Nagar, S., & Robertson, D. (2000). Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Critical Review in Biochemistry and Molecular Biology, 35(2), 105–140.

    CAS  Google Scholar 

  • Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23, 254–267.

    Article  PubMed  CAS  Google Scholar 

  • Jeanmougin, F., Thompson, J. D., Gouy, M., Higgins, D. G., & Gibson, T. J. (1998). Multiple sequence alignment with Clustal X. Trends in Biochemical Science, 23, 403–405.

    Article  CAS  Google Scholar 

  • Jeske, H., Lutgemeier, M., & Preiss, W. (2001). DNA forms indicate rolling circle and recombination-dependent replication of Abutilon mosaic virus. European Molecular Biology Journal, 20, 6158–6167.

    CAS  Google Scholar 

  • Kirthi, N., Maiya, S. P., Murthy, M. R. N., & Savitri, H. S. (2002). Evidence of recombination among the tomato leaf curl virus strains/species from Bangalore, India. Archives of Virology, 147, 255–272.

    Article  PubMed  CAS  Google Scholar 

  • Krishnareddy, M. (2010). Climate change and virus diseases of Horticultural crops. In H. P. Singh, J. P. Singh, & S. S. Lal (Eds.), Challenges of climate change – Indian Horticulture (pp. 153–165). New Delhi, India: Westville Publishing house. 209P.

    Google Scholar 

  • Kumari, P., Singh, A. K., Chattopadhyay, B., & Chakraborty, S. (2010). Molecular characterization of a new species of Begomovirus and betasatellite causing leaf curl disease of tomato in India. Virus Research, 152, 19–29.

    Article  PubMed  CAS  Google Scholar 

  • Lazarowitz, S. G. (1992). Geminiviruses: genome structure and gene function. Critical Review in Plant Science, 11, 327–349.

    CAS  Google Scholar 

  • Lefeuvre, P., Martin, D. P., Hoareau, M., Naze, F., Delatte, H., Thierry, M., et al. (2007). Begomovirus ‘melting pot’ in the southwest Indian Ocean islands: molecular diversity and evolution through recombination. Journal of General Virology, 88, 3458–3468.

    Article  PubMed  CAS  Google Scholar 

  • Mansoor, S., Khan, S. H., Bashir, A., Saeed, M., Zafar, Y., Malik, K. A., et al. (1999). Identification of a novel circular single-stranded DNA associated with cotton leaf curl disease in Pakistan. Virology, 259, 190–199.

    Article  PubMed  CAS  Google Scholar 

  • Martin, D. P., Lemey, P., Lott, M., Vincent, M., Posada, D., & Lefeuvre, P. (2010). RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics, 26(19), 2462–2463.

    Article  PubMed  CAS  Google Scholar 

  • Nawaz-ul-Rehman, M. S., Nahid, N., Mansoor, S., Briddon, R. W., & Fauquet, C. M. (2010). Post-transcriptional gene silencing suppressor activity of the alpha-Rep of non-pathogenic alphasatellites associated with begomoviruses. Virology, 405, 300–308.

    Article  PubMed  CAS  Google Scholar 

  • Padidam, M., Sawyer, S., & Fauquet, C. M. (1999). Possible emergence of new geminiviruses by frequent recombination. Virology, 265, 218–225.

    Article  PubMed  CAS  Google Scholar 

  • Pandey, P., Mukhopadhya, S., Naqvi, A. R., Mukherjee, S. K., Shekhawat, G. S., & Choudhury, N. R. (2010). Molecular characterization of two distinct monopartite begomoviruses infecting tomato in India. Virology Journal, 7, 337.

    Article  PubMed  Google Scholar 

  • Polston, J. E., & Anderson, P. L. (1997). The emergence of whitefly transmitted geminiviruses in tomato in the Western Hemisphere. Plant Disease, 81, 1358–1369.

    Article  Google Scholar 

  • Prasanna, H. C., & Rai, M. (2007). Detection and frequency of recombination in tomato infecting begomoviruses of South and Southeast Asia. Virology Journal, 4, 111. doi:10.1186/1743-422X-4-111.

    Article  PubMed  CAS  Google Scholar 

  • Rekha, A. R., Maruthi, M. N., Muniyappa, V., & Colvin, J. (2005). Occurrence of three genotypic clusters of Bemisia tabaci and the rapid spread of the B biotype in south India. Entomologia Experimentaliset Applicata, 117, 221–233.

    Article  Google Scholar 

  • Rojas, M. R., Gilbertson, R. L., Russel, D. R., & Maxwell, D. P. (1993). Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted geminiviruses. Plant Disease, 77, 340–347.

    Article  CAS  Google Scholar 

  • Rojas, M. R., Hagen, C., Lucas, W. J., & Gilbertson, R. L. (2005). Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Annuals Review of Phytopathology, 43, 361–394.

    Article  CAS  Google Scholar 

  • Sanz, A. I., Fraile, A., GarciaArenal, F., Zhou, X. P., Robinson, D. J., Khalid, S., et al. (2000). Multiple infection, recombination and genome relationships among begomovirus isolates found in cotton and other plants in Pakistan. Journal of General Virology, 81, 1839–1849.

    PubMed  CAS  Google Scholar 

  • Sastry, K. S. M., & Singh, S. J. (1974). Effect of yellow vein mosaic virus infection on growth and yield of okra crop. Indian Phytopathology, 27, 294–297.

    Google Scholar 

  • Saunders, K., & Stanley, J. (1999). A nanovirus-like component associated with yellow vein disease of Ageratum conyzoides: evidence for interfamilial recombination between plant DNA viruses. Virology, 264, 142–152.

    Article  PubMed  CAS  Google Scholar 

  • Saunders, K., Bedford, I. D., Briddon, R. W., Markham, P. G., Wong, S. M., & Stanley, J. (2000). A novel virus complex causes Ageratum yellow vein disease. Proceedings of the National Academy of Sciences of the United States of America, 97, 6890–6895.

    Article  PubMed  CAS  Google Scholar 

  • Schnippenkoetter, W. H., Martin, D. P., Willment, J. A., & Rybicki, E. P. (2001). Forced recombination between distinct strains of Maize streak virus. Journal of General Virology, 82, 3081–3090.

    PubMed  CAS  Google Scholar 

  • Seal, S. E., Vandenbosch, F., & Jeger, M. J. (2006). Factors influencing begomovirus evolution and their increasing global significance: implications for sustainable control. Critical Reviews in Plant Sciences, 25, 23–46.

    Article  Google Scholar 

  • Shankarappa, K. S., Rangaswamy, K. T., Aswathanarayana, D. S., Rekha, A. R., Raghavendra, N., Reddy, C. N. L., et al. (2007). Development and optimization of silverleaf assay, protein and nucleic acid based diagnostic techniques for quick and reliable detection and monitoring biotype B of Bemisia tabaci in India. Bulletin of Entomological Research, 97, 503–513.

    Article  PubMed  CAS  Google Scholar 

  • Sinha, S. N., & Chakrabarthi, A. K. (1978). Effect of yellow vein mosaic virus infection on okra seed production. Seed Research, 6, 67–70.

    Google Scholar 

  • Stanley, J., Bisaro, D. M., Briddon, R. W., Brown, J. K., Fauquet, C. M., & Harrison, B. D. (Eds.). (2005). Virus taxonomy, VIIIth report of the ICTV (pp. 301–326). London: Elsevier/Academic Press.

    Google Scholar 

  • 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. Molecular Biology and Evolution. doi:10.1093/molbev/msr 121.

    Google Scholar 

  • Varma, A., & Malathi, V. G. (2003). Emerging geminivirus problems: a serious threat to crop production. Annuals of Applied Biology, 142, 145–164.

    Article  CAS  Google Scholar 

  • Venkataravanappa, V., Reddy, C. N. L., Swaranalatha, P., Jalali, S., Briddon, R. W., & Krishna Reddy, M. (2011). Diversity and phylogeography of begomovirus-associated beta satellites of okra in India. Virology Journal, 8, 555. doi:10.1186/1743-422X-8-555.

    Article  PubMed  CAS  Google Scholar 

  • Venkataravanappa, V., Reddy, C. N. L., Jalali, S., & Krishna Reddy, M. (2012a). Molecular characterization of distinct bipartite begomovirus infecting bhendi (Abelmoschus esculentus L.) in India. Virus Genes, 44, 522–535. doi:10.1007/s11262-012-0732-y.

    Article  PubMed  CAS  Google Scholar 

  • Venkataravanappa, V., Lakshminarayana Reddy, C. N., Jalali, S., Swarnalatha, C. N., Devaraju, P., et al. (2012b). Molecular evidence for association of Cotton leaf curl Alabad virus with yellow vein mosaic disease of okra in North India. Archives of Phytopathology and Plant Protection, 45, 2095–2113. doi:10.1080/03235408.2012.721682. Corrigendum, 2013. 46, 127.

    Article  Google Scholar 

  • Zhou, X. P., Liu, Y. L., Calvert, L., Munoz, C., Otim-Nape, G. W., Robinson, D. J., et al. (1997). Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. Journal of General Virology, 78, 2101–2111.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The research was supported by ICAR NETWORK project on development of diagnostics to emerging plant viruses, Indian Council of Agricultural Research, Government of India, New Delhi, India.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to C. N. Lakshminarayana Reddy or M. Krishna Reddy.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Venkataravanappa, V., Reddy, C.N.L., Jalali, S. et al. Molecular characterization of a new species of begomovirus associated with yellow vein mosaic of bhendi (Okra) in Bhubhaneswar, India. Eur J Plant Pathol 136, 811–822 (2013). https://doi.org/10.1007/s10658-013-0209-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-013-0209-4

Keywords

Navigation