European Journal of Plant Pathology

, Volume 153, Issue 1, pp 289–297 | Cite as

Occurrence of Apple stem grooving virus on Rubus ellipticus, a perennial weed in India

  • Pooja BhardwajEmail author
  • Vipin Hallan


Rubus ellipticus, widely distributed in the Himalayas, was found to display severe virus-like symptoms (chlorosis, chlorotic mosaic, leaf deformation, necrotic and chlorotic spots on leaves). It was found growing abundantly in the campus of CSIR- IHBT Palampur, an important area for apple nursery development. Therefore to understand the status of this weed in terms of Apple stem grooving virus, leaf samples were tested. Seven samples from a total of thirty samples were found positive by DAS-ELISA, NASH and RT-PCR, confirming the presence of ASGV infection in 23% of the samples. Four of the positive samples (with positive signal in NASH) were characterized at coat protein (CP) gene. Phylogenetically, the CP sequences of the four isolates clustered with apple isolate (Ap-RC) from India, sharing 98.7–99.1% (aa) and 99.4–99.7% homology (nt). The rubus isolates shared an overall identity of 92.4–99.1% at (aa) and 86.6–99.5% at (nt) level with rest of the isolates from different hosts and geographical regions. R. ellipticus, might act as a reservoir host for ASGV, due to its widespread presence in the Himalayas.





The authors are thankful to the Director, CSIR-Institute of Himalayan Bioresource Technology Palampur, HP (India), for providing necessary facilities. Department of Biotechnology (DBT), (grant no. BT/PR/11001PBD/16/803/2008), Govt. of India is duly acknowledged for financial support. Academy of Scientific and Innovative Research (AcSIR) New Delhi is also acknowledged. This is CSIR-IHBT publication number 3844.

Compliance with ethical standards

Conflict of interest

The authors declare that they do not have conflicts of interest.

Human and animal rights and informed consent

This research does not involve Human Participants and/or animals.

Both of the authors give their consent for this publication.


  1. Arora, R.K., & Pandey, A. (1996). Wild edible plants of India. Diversity, Conservation and use. Indian Council of Agricultural Research. National Bureau of Plant Genetic Resources, New Delhi.Google Scholar
  2. Bhardwaj, P., Ram, R., Zaidi, A. A., & Hallan, V. (2014). Characterization of Apple stem grooving virus infecting Actinidia deliciosa (Kiwi) in India. Scientia Horticulturae, 176, 105–111.CrossRefGoogle Scholar
  3. Bhardwaj, P., Ram, R., Zaidi, A. A., & Hallan, V. (2016). Apple stem grooving virus naturally infects Himalayan wild cherry (Prunus cerasoides D. Don). Forest Pathology, 46, 116–121.CrossRefGoogle Scholar
  4. Birisik, N., Hassan, M., & Baloglu, S. (2008). A preliminary account on apple viruses in Mediterranean region of Turkey. Acta Horticulturae, 781, 125–130.CrossRefGoogle Scholar
  5. Clark, M. F., & Adams, A. N. (1977). Characteristics of the microplate method of enzyme linked immunosorbent assay for the detection of plant viruses. Journal of General Virology, 34, 475–483.CrossRefGoogle Scholar
  6. Clover, G. R. G., Pearson, M. N., Elliot, D. R., Tang, Z., Smales, T. E., & Alexander, B. J. R. (2003). Characterization of a strain of Apple stem grooving virus in Actinidia chinesis from China. Plant Pathology, 52, 371–378.CrossRefGoogle Scholar
  7. Daubeny, H. A. (1996). Brambles. In J. Janick & J. N. Moore (Eds.), Fruit Breeding (Vol. II Vine and small fruit crops, pp. 109–190). New York: John Wiley & Sons, Inc..Google Scholar
  8. De Sequeira, O. A. (1967). Studies on a virus causing stem grooving and graft-union abnormalities in Virginia crab apple. Annals of Applied Biology, 60, 59–66.CrossRefGoogle Scholar
  9. Ferretti, L., Hallan, V., Rana, T., Ram, R., Dhir, S., Negi, A., Lakshmi, V., Thockchom, T., Zaidi, A. A., Barba, M. (2010). Nucleotide analysis of pome fruit virus isolates detected in apple and pear samples from Italy and India. 21st international conference on virus and other graft transmissible diseases of fruit crops. Julius-Kühn-Archiv, 427.Google Scholar
  10. Finn, C. E. (2008). Rubus spp., blackberry. In J. Janick & R. E. Paull (Eds.), The encyclopedia of fruits and nuts (pp. 348–351). Cambridge: Centre for Agriculture and Biosciences International (CABI).Google Scholar
  11. Fulton, R. W. (1966). Mechanical transmission of viruses of woody plants. Annual Review of Phytopathology, 4, 79–98.CrossRefGoogle Scholar
  12. Garnsey, S. M. (1964). Detection of Tatter leaf virus of citrus in Florida. Proceedings of the Florida state of horticultural Society, 77, 106–109.Google Scholar
  13. GRIN (Germplasm Resources Information Network). (2003). Online Database United States Department of Agriculture, Agricultural Research Service, National Germplasm Resources Laboratory, Beltsville, MD. Available: Accessed 27 Mar 2003.
  14. Hooker, J. D. (1879). The Flora of British India. II. Ashford, Kent, England: L. Reeve and Co. Ltd., NR.Google Scholar
  15. Hunter, J. A., Chamberlain, E. F., & Atkinson, J. D. (1958). Note on the transmission of apple mosaic by natural root grafting. New Zealand Journal of Agricultural Research, 1, 80–82.Google Scholar
  16. Inouye, N., Maeda, T., & Mitsuhata, K. (1979). Citrus tatter leaf virus isolated from lily. Annals of the Phytopathological Society of Japan, 45, 712–720.CrossRefGoogle Scholar
  17. Ito, T., Ieki, H., & Ozaki, K. (2002). Simultaneous detection of six citrus viroids and Apple stem Grooving virus from citrus plants by multiplex reverse transcription polymerase chain reaction. Journal of Virological Methods, 106, 235–239.CrossRefGoogle Scholar
  18. James, D. (1999). A simple and reliable protocol for the detection of Apple stem grooving virus by RT-PCR and in a multiplex PCR assay. Journal of Virological Methods, 83, 1–9.CrossRefGoogle Scholar
  19. Lister, R. M., Bancroft, J. B., & Nadakavukaren, M. J. (1965). Some sap-transmissible viruses from apple. Phytopathology, 55, 859–870.Google Scholar
  20. Liu, P., Zang, L., Zang, H., Jiao, H., & Wu, Y. (2013). Detection and molecular variability of Apple stem grooving virus in Shaanxi, China. Journal of Phytopathology, 161, 445–449.CrossRefGoogle Scholar
  21. Lovisolo, O., Accotto, G. P., Masenga, V., & Colariccio, A. (2003). An isolate of Apple stem grooving virus associated with Cleopatra mandarin fruit intumescence. Fitopatologia Brasileira, 28, 54–58.CrossRefGoogle Scholar
  22. McGavin, W. J., McMenemy, L. S., & MacFarlane, S. A. (2010). The complete sequence of a UK strain of Black raspberry necrosis virus. Archives of Virology, 155, 1897–1899.CrossRefGoogle Scholar
  23. Menzel, W., Jelkmann, W., & Maiss, E. (2002). Detection of four apple viruses by multiplex RT-PCR assays with co amplification of plant m RNA as internal control. Journal of Virological Methods, 99, 81–92.CrossRefGoogle Scholar
  24. Misra, L. P., & Sharma, V. K. (1970). Preliminary investigations on the control of weeds in the apple orchard. Indian Science Congress Proceedings, 57, 540–541.Google Scholar
  25. Misra, P., & Singh, M. M. (1972). Efficacy of certain herbicides on the control of Rosa moschata and Rubus ellipticus in temperate fruits. Indian Journal of Weed Science, 4, 81–87.Google Scholar
  26. Motoshima, S., Kato, M., Nishio, T., & Kobayashi, T. (1983). Sap-transmissible viruses detected from imported pear plants. Research Bulletin of the Plant Protection Service Japan, 19, 29–37.Google Scholar
  27. Muthaiyan, M. C. (Ed.). (2009). Principles and practices of plant quarantine. New Delhi: Allied Publishers Pvt. Ltd ISBN: 978–81–8424-407-6.Google Scholar
  28. Narayanasamy, P. (2011). Microbial plant pathogens-detection and disease diagnosis: Viral and viroid pathogens (Vol. 3). Netherlands: Springer Science+Business Media.CrossRefGoogle Scholar
  29. Negi, A., Rana, T., Kumar, Y., Hallan, V., & Zaidi, A. A. (2009). First report of Apple stem grooving virus from pome and stone fruits in India. Journal of Plant Pathology, 91(2), 499–505.Google Scholar
  30. Negi, A., Rana, T., Kumar, Y., Ram, R., Hallan, V., & Zaidi, A. A. (2010). Analysis of the coat protein gene of Indian strain of Apple stem grooving virus. Journal of Plant Biochemistry and Biotechnology, 19(1), 91–94.CrossRefGoogle Scholar
  31. Nemeth, M. (1986). Virus, mycoplasma and rickettsia diseases of fruit trees (p. 841). Budapest.: Akademiai Kiado.Google Scholar
  32. Nickel, O., Fajardo, T. V. M., Jelkmann, W., & Kuhn, G. B. (2001). Sequence analysis of the capsid protein gene of an isolate of Apple stem grooving virus, and its survey in southern Brazil. Fitopatologia Brasileira, 26(3), 655–659.CrossRefGoogle Scholar
  33. Rodoni, B. C., & Constable, F. E. (2008). The incidence and strain variation of Apple stem grooving and Apple stem pitting viruses in Australian pome fruit. Acta Horticulturae, 781, 167–174.CrossRefGoogle Scholar
  34. Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning. A laboratory manual (2nd ed.). New York: Cold Spring Harbor Laboratory Press.Google Scholar
  35. Sastry, K.S. (2013). Plant virus and viroid diseases in the tropics. Volume 1: Introduction of plant viruses and sub-viral agents, classification, assessment of loss, transmission and diagnosis. Dordrecht Heidelberg: Springer science+Business media B.V. SpringerGoogle Scholar
  36. Shim, H., Min, Y., Hong, S., Kwon, M., Kim, D., Kim, H., Choi, Y., Lee, S., & Yang, J. (2004). Nucleotide sequences of a Korean isolate of Apple stem grooving virus associated with black necrotic leaf spot disease on pear (Pyrus pyrifolia). Molecular Cell, 18, 192–199.Google Scholar
  37. Starr, F., Starr, K., & Loope, L. (2003). Rubus ellipticus Yellow Himalayan raspberry Rosaceae United States Geological Survey. Biological resources division Haleakala field station, Maui, Hawaii.Google Scholar
  38. Takahashi, T., Saito, N., Goto, M., Kawai, A., Namba, S., & Yamashita, S. (1990). Apple stem grooving virus isolated from Japanese apricot (Prunus mume) imported from China. Research Bulletin of the Plant Protection Service Japan, 26, 15–21.Google Scholar
  39. Tang, J., Olson, J. D., Ochoa-Corona, F. M., & Clover, G. R. G. (2010). Nandina domestica, a new host of Apple stem grooving virus and Alternanthera mosaic virus. Australasian Plant Disease Notes, 5, 25–27.CrossRefGoogle Scholar
  40. van Regenmortel, M. H. V., Fauquet, C.M., Bishop, D. H. L., Carstens, E. B., Estes, M. K., Lemon, S. M., Maniloff, J., Mayo, M. A., McGeoch, D. J., Pringle, C. R., Wickner, R. B. (2000). Virus taxonomy. Seventh report of the International Committee on Taxonomy of Viruses. San Diego: Academic Press, pp. 1162.Google Scholar
  41. Wagner, W.L., Herbst, D.R.., Sohmer, S.H. (1999). Manual of the Flowering Plants of Hawaii, 2 Vols. Bishop Museum Special Publication 83. Honolulu: University of Hawai'i and Bishop Museum Press.Google Scholar
  42. Waterworth, H. E., & Gilmer, R. M. (1969). Dark green epinasty of Chenopodium quinoa, a syndrome induced by a virus latent in apple and pear. Phytopathology, 59, 334–338.Google Scholar
  43. Welsh, M. F., & Van der Meer, F. A. (1989). Apple stem grooving virus. In: W. A. Pullman (Ed.), Virus and virus-like disease of pome fruits and simulating noninfectious disorders (pp. 253–267). College of Agriculture and Home Economics Washington State University.Google Scholar
  44. Yoshikawa, N. (2000). Apple stem grooving virus. CMI/AAB descriptions of plant viruses no. 376. Egham: CABI Bioscience.Google Scholar
  45. Youssef, S. A., Moawad, S. M., Nosseir, F. M., Shalaby, A. A. (2010). Detection and identification of Apple stem pitting virus and Apple stem grooving virus affecting apple and pear trees in Egypt. Julius-Kuhn-Archiv, 427, 248–2452.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  1. 1.Academy of Scientific and Innovative Research (AcSIR)New DelhiIndia
  2. 2.Plant Virology LabCSIR-Institute of Himalayan Bioresource TechnologyPalampurIndia

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