Skip to main content
Log in

Phylogenetic analysis and signature of recombination hotspots in sugarcane mosaic virus infecting sugarcane in India

  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

Sugarcane mosaic virus (SCMV) one of the causative viruses of mosaic disease in sugarcane occurs in sugarcane growing countries worldwide. India is the second largest sugarcane producing country and genome of SCMV from India has not been characterized so far. Hence detailed studies were carried out to characterize the virus isolates based on its complete genome. Comparative genome analyses of five new isolates were performed with previously reported SCMV full genome sequences of isolates infecting sugarcane, maize, sorghum and Canna. Sequence identity matrix and phylogenetic analyses clearly represented that Indian isolates are closely related to sugarcane infecting isolates reported from Australia, Argentina, China and Iran and they diverged as a separate subgroup from other reported maize infecting isolates from Mexico, China, Ohio, Spain, Germany, Iran, Ethiopia, Kenya and Eucador. Selection pressure analysis clearly depicted the predomination of strong purifying selection throughout the viral genome, and strongest in CI and HC-Pro gene. Evidence for few positively selected sites was identified in all the cistrons except in 6 K1 and Nib rep. Among the genomic region, CI gene has exhibited comparatively more recombination hotspots followed by HC-Pro unlike other reported isolates. As the cultivation of sugarcane first originated in India, our results from the recombination events strongly suggest that Indian SCMV populations contribute for the emergence of upcoming new recombinant SCMV isolates not only within the sugarcane isolates but also with maize infecting isolates of SCMV in other countries irrespective of geographic origin and host type.

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

  • Achon, M. A., Serrano, L., Alonso-Duenas, N., & Porta, C. (2007). Complete genome sequences of Maize dwarf mosaic and Sugarcane mosaic virus isolates coinfecting maize in Spain. Archives of Virology, 152, 2073–2078.

    Article  CAS  PubMed  Google Scholar 

  • Adams, I. P., Harju, V. A., Hodges, T., Hany, U., Skelton, A., Rai, S., Deka, M. K., Smith, J., Fox, A., Uzayisenga, B., Ngaboyisonga, C., Uwumukiza, B., Rutikanga, A., Rutherford, M., Ricthis, B., Phiri, N., & Boonham, N. (2014). First report of maize lethal necrosis disease in Rwanda. New Disease Reports, 29, 22.

    Article  Google Scholar 

  • Barber, C. A. (1921). The mosaic mottling disease of the sugarcane. International Sugar Journal, 23, 12–19.

    Google Scholar 

  • Bernreiter, A., Garcia Teijeiro, R., Jarrin, D., Garrido, P., & Ramos, L. (2017). First report of Maize yellow mosaic virus infecting maize in Ecuador. New Disease Reports, 36, 11.

    Article  Google Scholar 

  • Blanc, S., Ammar, E. D., Garcıa-Lampasona, S., Dolja, V. V., Llave, C., Baker, J., & Pirone, T. P. (1998). Mutations in the potyvirus helper component protein: Effects on interactions with virions and aphid stylets. Journal of General Virology, 79, 3119–3122.

    Article  CAS  PubMed  Google Scholar 

  • Cavatorta, J. R., Savage, A. E., Yeam, I., Gray, S. M., & Jahn, M. M. (2008). Positive Darwinian selection at single amino acid sites conferring plant virus resistance. Journal of Molecular Evolution, 67, 551–559.

    Article  CAS  PubMed  Google Scholar 

  • Chaves-Bedoya, G., Espejel, F., Alcala-Briseno, R. I., Hernandez-Vela, J., & Silva-Rosales, L. (2011). Short distance movement of genomic negative strands in a host and nonhost for sugarcane mosaic virus (SCMV). Virology Journal, 8, 15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, J., Chen, J., & Adams, M. (2002). Characterisation of potyviruses from sugarcane and maize in China. Archives of Virology, 147, 1237–1246.

  • Chona, B. L., & Rafay, S. A. (1950). Studies on the sugarcane disease in India. Indian Journal of Agricultural Sciences, 20, 39–50.

    Google Scholar 

  • Costa, A.S., &Muller, G.W.(1982). General evaluation of the impacts of viral diseases of economic crops on the development of Latin American countries. Proceedings of the first international conference on the impact of viral diseases in developing Latin American and Carribbean countries, Rio De Janeiro.

  • Daniels, J., & Roach, B. T. (1987). Taxonomy and evolution. In J. Heinz (Ed.), Sugarcane improvement through breeding (Vol. 1, pp. 7–84). Amsterdam: Elsevier.

    Chapter  Google Scholar 

  • Delport, W., Poon, A., Frost, S. D., & Kosakovsky Pond, S. L. (2010). Datamonkey: A suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics, 26, 2455–2457.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Etherington, G. J., Dicks, J., & Roberts, I. N. (2005). Recombination analysis tool (RAT): A program for the high-throughput detection of recombination. Bioinformatics, 21, 278–281.

    Article  CAS  PubMed  Google Scholar 

  • Fan, Z. F., Chen, H. Y., Liang, X. M., & Li, H. F. (2003). Complete sequence of the genomic RNA of the prevalent strain of a potyvirus infecting maize in China. Archives of Virology, 148, 773–782.

    Article  CAS  PubMed  Google Scholar 

  • Fauconnier, R. (1993). Sugar cane (pp. 1–40). UK: Macmillan Press Ltd London.

    Google Scholar 

  • Gao, B., Cui, X. W., Li, X. D., Zhang, C. Q., & Miao, H. Q. (2011). Complete genomic sequence analysis of a highly virulent isolate revealed a novel strain of sugarcane mosaic virus. Virus Genes, 43, 390–397.

    Article  CAS  PubMed  Google Scholar 

  • Goodman, B.S. (1999). A study of South African strains of sugarcane mosaic potyvirus (SCMV) identified by sequence analysis of the 5’ region of the coat protein gene. M.Sc thesis, Department of Biotechnology, Durban University of Technology, Durban, South Africa, 136 pp.

  • Grisham, M.P. (2000). A guide to sugarcane diseases. CIRAD-ISSCT, CIRAD publication services, Montpellier. (pp. 249–254).

  • 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 

  • Hughes, A. L., & Hughes, M. A. (2005). Patterns of nucleotide difference in overlapping and non-overlapping reading frames of papillomavirus genomes. Virus Research, 113, 81–88.

    Article  CAS  PubMed  Google Scholar 

  • Hughes, A. L., & Hughes, M. A. (2007). Coding sequence polymorphism in avian mitochondrial genomes reflects population histories. Molecular Ecology, 16, 1369–1376.

    Article  CAS  PubMed  Google Scholar 

  • Koike, H., Gillespie, A. G.(1989). Mosaic. In Ricaud, BT Egan, AG Gillespie, CG Hughes (Ed.), Disease of sugarcane – major diseases (pp. 301–322).

  • Kong, P., & Steinbiss, H. H. (1998). Complete nucleotide sequence and analysis of the putative polyprotein of maize dwarf mosaic virus genomic RNA (Bulgarian isolate). Archives of Virology, 143, 1791–1799.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., Li, M., Knyas, C., & Tamura, K. (2018). Mega X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35, 1574–1549.

    Google Scholar 

  • Lai, M. M. C. (1992). RNA recombination in animal and plant viruses. Microbiological Reviews, 56, 61–79.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li, L., Wang, X., & Zhou, G. (2007). Analyses of maize embryo invasion by Sugarcane mosaic virus. Plant Science, 172, 131–138.

    Article  CAS  Google Scholar 

  • Mahuku, G., Wangai, A., Sadessa, K., Teklewold, A., Wegary, D., Ayalneh, D., Adams, I., Smith, J., Bottomley, E., Bryce, S., Braidwood, L., Feyissa, B., Regassa, B., Wanjala, B., Kimunye, J. N., Mugambi, C., Monjero, K., & Prasanna, M. (2015). First Report of maize chlorotic mottle virus and maize lethal necrosis on Maize in Ethiopia. Plant Disease, 99, 1870.

    Article  Google Scholar 

  • Mangrauthia, S. K., Parameswari, B., Jain, R. K., & Praveen, S. (2008). Role of genetic recombination in the molecular architecture of Papaya ringspot virus. Biochemical Genetics, 46, 835–846.

    Article  CAS  PubMed  Google Scholar 

  • Martin, D. P., Murrell, B., Michael, G., Khoosal, A., & Muhire, B. (2015). RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evolution, 1(1), vev003. https://doi.org/10.1093/ve/vev003.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moradi, Z., Mehrvar, M., Nazifi, E., & Mohammad, Z. (2016). The complete genome sequences of two naturally occurring recombinant isolates of Sugarcane mosaic virus from Iran. Virus Genes, 52, 270–280.

    Article  CAS  PubMed  Google Scholar 

  • Moury, B., Morel, C., Johansen, E., & Jacquemond, M. (2002). Evidence for diversifying selection in potato virus Y and in the coat protein of other potyviruses. Journal of General Virology, 83, 2563–2573.

    Article  CAS  PubMed  Google Scholar 

  • Oertel, U., Fuchs, E., & Hohmann, F. (1999). Differentiation of isolates of sugarcane mosaic potyvirus (SCMV) on the basis of molecular, serological and biological investigations. Z PflKrankh Pfl Schutz, 106, 304–313.

    Google Scholar 

  • Ohshima, K., Tomitaka, Y., Wood Jeffery, T., Minematsu, Y., Kajiyama, H., Tomimura, K., & Gibbs Adrian, J. (2007). Patterns of recombination in turnip mosaic virus genomic sequences indicate hotspots of recombination. Journal of General Virology, 88, 298–315.

    Article  CAS  PubMed  Google Scholar 

  • Pond, S. L. K., & Frost, S. (2005). Datamonkey: Rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics, 21, 2531–2533.

    Article  CAS  PubMed  Google Scholar 

  • Simon-Loriere, E., & Holmes, E. C. (2011). Why do RNA viruses recombine? Natural Reviews Microbiology, 9, 617–626.

    Article  CAS  PubMed  Google Scholar 

  • Stewart, L. R., Bouchard, R., Redinbaugh, M. G., & Meulia, T. (2012). Complete sequence and development of a full-length infectious clone of an Ohio isolate of maize dwarf mosaic virus (MDMV). Virus Research, 165, 219–224.

    Article  CAS  PubMed  Google Scholar 

  • Tang, W., Yan, Z. Y., Zhu, T. S., Xu, X. J., Li, X. D., & Tian, Y. P. (2018). The complete genomic sequence of Sugarcane mosaic virus from Canna spp. in China. Virology Journal, 15, 147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viswanathan, R. (2016). Varietal degeneration in sugarcane and its management in India. Sugar Tech, 18, 1–7.

    Article  Google Scholar 

  • Viswanathan, R., & Balamuralikrishnan, M. (2005). Impact of mosaic infection on growth and yield of sugarcane. Sugar Tech, 7, 61–65.

    Article  CAS  Google Scholar 

  • Viswanathan, R., & Karuppaiah, R. (2010). Distribution pattern of RNA viruses causing mosaic symptoms and yellow leaf in Indian sugarcane varieties. Sugar Cane International, 28, 202–205.

    Google Scholar 

  • Viswanathan, R., & Rao, G. P. (2011). Disease scenario and management of major sugarcane diseases in India. Sugar Tech, 13, 336–353.

    Article  CAS  Google Scholar 

  • Viswanathan, R., Balamuralikrishnan, M., & Karuppaiah, R. (2007). Sugarcane mosaic in India: A cause of combined infection of Sugarcane mosaic virus and Sugarcane streak mosaic virus. Sugar Cane International, 25, 6–14.

    CAS  Google Scholar 

  • Viswanathan, R., Balamuralikrishnanan, M., & Karuppaiah, R. (2008). Sugarcane mosaic complex in India: Cause of different viruses/strains. Indian Journal of Virology, 19, 94–94.

    Google Scholar 

  • Viswanathan, R., Karuppaiah, R., & Balamuralikrishnan, M. (2009). Identification of new variants of SCMV causing sugarcane mosaic in India and assessing their genetic diversity in relation to SCMV type strains. Virus Genes, 39, 375–386.

    Article  CAS  PubMed  Google Scholar 

  • Viswanathan, R., Karuppaiah, R., & Balamuralikrishnan, M. (2010). Detection of three major RNA viruses infecting sugarcane by multiplex reverse transcription polymerase chain reaction (multiplex RT PCR). Australasian Plant Pathology, 39, 79–84.

    Article  CAS  Google Scholar 

  • Viswanathan, R., Ganesh Kumar, V., Karuppaiah, R., Scindiya, M., & Chinnaraja, C. (2013). Development of duplex immunocapture (duplex IC) RT-PCR for the detection of Sugarcane streak mosaic virus and Sugarcane mosaic virus in sugarcane. Sugar Tech, 15, 399–405.

    Article  CAS  Google Scholar 

  • Wamaitha, M. J., Nigam, D., Maina, S., Stomeo, F., Wangai, A., Njuguna, J. N., Holton, T. A., Wanjala, B. W., Wamalwa, M., Lucas, T., Djikeng, A., & Ruiz, H. G. (2018). Metagenomic analysis of viruses associated with maize lethal necrosis in Kenya. Virology Journal, 15, 90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia, X. C., Melchinger, A. E., Kuntze, L., & Lubberstedt, T. (1999). Quantitative trait loci mapping of resistance to Sugarcane mosaic virus in maize. Phytopathology, 89, 660–667.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z. N., & Mirkov, T. E. (1997). Sequence and relationships of sugarcane mosaic and sorghum mosaic virus strains and development of RT-PCR–based RFLPs for strain discrimination. Phytopathology, 87, 932–939.

    Article  CAS  PubMed  Google Scholar 

  • Zhong, Y., Guo, A., Li, C., Zhuang, B., Lai, M., Wei, C., Luo, J., & Li, Y. (2005). Identification of a naturally occurring recombinant isolate of sugarcane mosaic virus causing maize dwarf mosaic disease. Virus Genes, 30, 75–83.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The financial support received from the Department of Biotechnology, New Delhi (BTPR4978-AGR-36712-2012) is greatly acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Viswanathan.

Ethics declarations

Conflict of interest

The authors declared that there is no conflict of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 30 kb)

ESM 2

(DOCX 14 kb)

ESM 3

(XLSX 58 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bagyalakshmi, K., Parameswari, B. & Viswanathan, R. Phylogenetic analysis and signature of recombination hotspots in sugarcane mosaic virus infecting sugarcane in India. Phytoparasitica 47, 275–291 (2019). https://doi.org/10.1007/s12600-019-00726-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-019-00726-1

Keywords

Navigation