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Virus Genes

, Volume 50, Issue 3, pp 474–486 | Cite as

Studies on differential behavior of cassava mosaic geminivirus DNA components, symptom recovery patterns, and their siRNA profiles

  • Basavaprabhu L. PatilEmail author
  • Claude M. Fauquet
Article

Abstract

Cassava mosaic disease caused by cassava mosaic geminiviruses (CMGs) with bipartite genome organization is a major constraint for production of cassava in the African continent and the Indian sub-continent. Currently, there are eleven recognized species of CMGs, and several diverse isolates represent them, with vast amount of sequence variability, reflecting into diversity of symptom severity/phenotypes. Here, we make a systematic effort to study the infection dynamics of several species of CMGs and their isolates. Further, we try to identify the genomic component of CMGs contributing to the manifestation of diverse patterns of symptoms and the molecular basis for the differential behavior of CMGs. The pseudo-recombination studies carried out by swapping of DNA-A and DNA-B components of the CMGs revealed that the DNA-B component significantly contributes to the symptom severity. Past studies had shown that the DNA-A component of Sri Lankan cassava mosaic virus shows monopartite feature. Thus, the ability of DNA-A component alone, to replicate and move systemically in the host plant with inherent monopartite features was investigated for all the CMGs. Geminiviruses are known to trigger gene silencing and are also its target, resulting in recovery of the host plant from viral infection. In the collection of several different CMG species and isolates we had, there was a vast variability in their recovery and non-recovery phenotypes. To understand the molecular basis of this, the origin and distribution of virus-derived small interfering RNAs were mapped across their genome and across the CMG-infected symptomatic Nicotiana benthamiana.

Keywords

Geminivirus Begomovirus Cassava mosaic virus Symptom recovery Pseudo-recombination siRNA 

Notes

Acknowledgments

The funding was from Monsanto Fund and United States Agency for International Development (USAID). We thank Dr. John Stanley, John Innes Institute (United Kingdom), for providing several clones of CMGs used in this study. We acknowledge Dr. Nigel Taylor and his team for providing tissue cultured cassava plants, Mr. Samuel Amiteye for his help in cloning work, the DDPSC greenhouse staff for excellent care of the plants and Dr. B. Bagewadi for suggestions to improve the manuscript.

Conflict of interest

None.

Supplementary material

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Supplementary material 1 (JPEG 190 kb)
11262_2015_1184_MOESM2_ESM.jpg (83 kb)
Supplementary material 2 (JPEG 83 kb)

References

  1. 1.
    C.M. Fauquet, R.W. Briddon, J.K. Brown, E. Moriones, J. Stanley, M. Zerbini, X. Zhou, Arch. Virol. 153, 783–821 (2008)CrossRefPubMedGoogle Scholar
  2. 2.
    B.L. Patil, C.M. Fauquet, Mol. Plant Pathol. 10, 685–701 (2009)CrossRefPubMedGoogle Scholar
  3. 3.
    B.L. Patil, S. Rajasubramaniam, C. Bagchi, I. Dasgupta, Arch. Virol. 150, 389–397 (2005)CrossRefPubMedGoogle Scholar
  4. 4.
    H. Jeske, Curr. Top. Microbiol. Immunol. 331, 185–226 (2009)PubMedGoogle Scholar
  5. 5.
    J.P. Legg, P. Lava Kumar, T. Makeshkumar, L. Tripathi, M. Ferguson, E. Kanju, P. Ntawuruhunga, W. Cuellar, Adv. Virus Res. 91, 85–142 (2015)PubMedGoogle Scholar
  6. 6.
    S.E. Bull, R.W. Briddon, W.S. Sserubombwe, K. Ngugi, P.G. Markham, J. Stanley, J. Gen. Virol. 87, 3053–3065 (2006)CrossRefPubMedGoogle Scholar
  7. 7.
    E. van der Walt, E.P. Rybicki, A. Varsani, J.E. Polston, R. Billharz, L. Donaldson, A.L. Monjane, D.P. Martin, J. Gen. Virol. 90, 734 (2009)CrossRefPubMedCentralPubMedGoogle Scholar
  8. 8.
    J. Pita, V.N. Fondong, A. Sangaré, G.W. Otim-Nape, S. Ogwal, C.M. Fauquet, J. Gen. Virol. 82, 655–665 (2001)PubMedGoogle Scholar
  9. 9.
    X. Zhou, Y. Liu, L. Calvert, C. Munoz, G.W. Otim-Nape, D.J. Robinson, B.D. Harrison, 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 (1997)PubMedGoogle Scholar
  10. 10.
    R.W. Briddon, B.L. Patil, B.B. Bagewadi, M.S. Nawaz-ul-Rehman, C.M. Fauquet, BMC Evol. Biol. 10, 97 (2010)CrossRefPubMedCentralPubMedGoogle Scholar
  11. 11.
    K. Saunders, N. Salim, V.R. Mali, V.G. Malathi, R. Briddon, P.G. Markham, J. Stanley, Virology 293, 63–74 (2002)CrossRefPubMedGoogle Scholar
  12. 12.
    F.A. Klinkenberg, J. Stanley, J. Gen. Virol. 71, 1409–1412 (1990)CrossRefGoogle Scholar
  13. 13.
    D.M. Bisaro, Virology 344, 158–168 (2006)CrossRefPubMedGoogle Scholar
  14. 14.
    R. Vanitharani, P. Chellappan, C.M. Fauquet, Trends Plant Sci. 10, 144–151 (2005)CrossRefPubMedGoogle Scholar
  15. 15.
    O. Voinnet, Y.M. Pinto, D.C. Baulcombe, Proc. Natl. Acad. Sci. U.S.A. 96, 14147–14152 (1999)CrossRefPubMedCentralPubMedGoogle Scholar
  16. 16.
    P. Chellappan, R. Vanitharani, C.M. Fauquet, J. Virol. 78, 7465–7477 (2004)CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    S.E. Bull, R.W. Briddon, W.S. Sserubombwe, K. Ngugi, P.G. Markham, J. Stanley, J. Gen. Virol. 88, 1624–1633 (2007)CrossRefPubMedGoogle Scholar
  18. 18.
    O.A. Ariyo, G.I. Atiri, A.G. Dixon, S. Winter, J. Virol. Methods 137, 43–50 (2006)CrossRefPubMedGoogle Scholar
  19. 19.
    V.N. Fondong, J.S. Pita, M.E. Rey, A. de Kochko, R.N. Beachy, C.M. Fauquet, J. Gen. Virol. 81, 287–297 (2000)PubMedGoogle Scholar
  20. 20.
    B.L. Patil, C.M. Fauquet, J. Gen. Virol. 91, 1871–1882 (2010)CrossRefPubMedGoogle Scholar
  21. 21.
    F.A. Klinkenberg, S. Ellwood, J. Stanley, J. Gen. Virol. 70, 1837–1844 (1989)CrossRefGoogle Scholar
  22. 22.
    L.C. Berrie, K.E. Palmer, E.P. Rybicki, M.E.C. Rey, Arch. Virol. 143, 2253–2260 (1998)CrossRefPubMedGoogle Scholar
  23. 23.
    B.L. Patil, C.M. Fauquet, Mol. Plant Pathol. (2015). doi: 10.1111/mpp.12205 Google Scholar
  24. 24.
    B.L. Patil, E. Ogwok, H. Wagaba, I.U. Mohammed, J.S. Yadav, B. Bagewadi, N.J. Taylor, T. Alicai, J.F. Kreuze, M.N. Gowda, C.M. Fauquet, Mol. Plant. Pathol. 12, 31–41 (2011)CrossRefPubMedGoogle Scholar
  25. 25.
    P. Chellappan, R. Vanitharani, F. Ogbe, C.M. Fauquet, Plant Physiol. 138, 1828–1841 (2005)CrossRefPubMedCentralPubMedGoogle Scholar
  26. 26.
    T.R. Resmi, S. Nivedhitha, C. Karthikeyan, K. Veluthambi, FEMS Microbiol. Lett. 360, 42–50 (2014)CrossRefPubMedGoogle Scholar
  27. 27.
    J. Legg, C.M. Fauquet, Plant Mol. Biol. 56, 585–599 (2004)CrossRefPubMedGoogle Scholar
  28. 28.
    D. Evans, H. Jeske, Virology 194, 752–757 (1993)CrossRefPubMedGoogle Scholar
  29. 29.
    J. Stanley, P.G. Markham, R.J. Callis, M.S. Pinner, EMBO J. 5, 1761–1767 (1986)PubMedCentralPubMedGoogle Scholar
  30. 30.
    S. Mansoor, R.W. Briddon, Y. Zafar, J. Stanley, Trends Plant Sci. 8, 128–134 (2003)CrossRefPubMedGoogle Scholar
  31. 31.
    S. Chakraborty, R. Vanitharani, B. Chattopadhyay, C.M. Fauquet, J. Gen. Virol. 89, 818–828 (2008)CrossRefPubMedGoogle Scholar
  32. 32.
    A.V. Arnim, J. Stanley, Determinants of tomato golden mosaic virus symptom development located on DNA B. Virology 186, 286–293 (1992)CrossRefGoogle Scholar
  33. 33.
    A.S. Karthikeyan, R. Vanitharani, V. Balaji, S. Anuradha, P. Thillaichidambaram, P.V. Shivaprasad, C. Parameswari, V. Balamani, M. Saminathan, K. Veluthambi, Arch. Virol. 149, 1643–1652 (2004)CrossRefPubMedGoogle Scholar
  34. 34.
    A. Levy, H. Czosnek, Plant Mol. Biol. 53, 789–803 (2003)CrossRefPubMedGoogle Scholar
  35. 35.
    B.L. Patil, I. Dasgupta, Crit. Rev. Plant Sci. 25, 47–64 (2006)CrossRefGoogle Scholar
  36. 36.
    B.L. Patil, N. Dutt, R.W. Briddon, S.E. Bull, D. Rothenstein, B.K. Borah, I. Dasgupta, J. Stanley, H. Jeske, Virus Res. 124, 59–67 (2007)CrossRefPubMedGoogle Scholar
  37. 37.
    C.C. Cheng, M. Ikegami, Ann. Phytopathol. Soc. Jpn. 57, 45–48 (1991)CrossRefGoogle Scholar
  38. 38.
    D.C. Stenger, K.R. Davis, D.M. Bisaro, Mol. Plant Microbe Interact. 5, 525–527 (1992)CrossRefGoogle Scholar
  39. 39.
    O. Akano, O. Dixon, C. Mba, E. Barrera, M. Fregene, Theor. Appl. Genet. 105, 521–525 (2002)CrossRefPubMedGoogle Scholar
  40. 40.
    T. Blevins, R. Rajeswaran, P.V. Shivaprasad, D. Beknazariants, A. Si-Ammour, H.S. Park, F. Vazquez, D. Robertson, F. Meins Jr, T. Hohn, M.M. Pooggin, Nucleic Acids Res. 34, 6233–6246 (2006)CrossRefPubMedCentralPubMedGoogle Scholar
  41. 41.
    R. Akbergenov, A. Si-Ammour, T. Blevins, I. Amin, C. Kutter, H., Vanderschuren, P. Zhang, W. Gruissem, F. Meins Jr., T. Hohn, M.M. Pooggin, Nucleic Acids Res. 34, 462–471 (2006)CrossRefPubMedCentralPubMedGoogle Scholar
  42. 42.
    M.J. Axtell, Annu. Rev. Plant Biol. 64, 137–159 (2013)CrossRefPubMedGoogle Scholar
  43. 43.
    P. Raja, B.C. Sanville, R.C. Buchmann, D.M. Bisaro, J. Virol. 82, 8997–9007 (2008)CrossRefPubMedCentralPubMedGoogle Scholar
  44. 44.
    E.A. Rodriguez-Negrete, J. Carrillo-Tripp, R.F. Rivera-Bustamante, J. Virol. 83, 1332–1340 (2009)CrossRefPubMedCentralPubMedGoogle Scholar
  45. 45.
    B. Ghoshal, H. Sanfaçon, Virology 456–457, 188–197 (2014)CrossRefPubMedGoogle Scholar
  46. 46.
    X. Qi, F.S. Bao, Z. Xie, PLoS ONE 4, 4 (2009)CrossRefGoogle Scholar
  47. 47.
    F.E. Vaistij, L. Jones, Plant Physiol. 149, 1399 (2009)CrossRefPubMedCentralPubMedGoogle Scholar
  48. 48.
    F. Li, C. Huang, Z. Li, X. Zhou, PLoS Pathog. 10, e1003921 (2014)CrossRefPubMedCentralPubMedGoogle Scholar
  49. 49.
    T. Ho, H. Wang, D. Pallett, T. Dalmay, FEBS Lett. 581, 3267–3272 (2007)CrossRefPubMedGoogle Scholar
  50. 50.
    S.I. Rudnick, J. Swaminathan, M. Sumaroka, S. Liebhaber, A.M. Gewirtz, Proc. Natl. Acad. Sci. U.S.A. 105, 13787–13792 (2008)CrossRefPubMedCentralPubMedGoogle Scholar
  51. 51.
    P.V. Shivaprasad, R. Akbergenov, D. Trinks, R. Rajeswaran, K. Veluthambi, T. Hohn, M.M. Pooggin, J. Virol. 79, 8149–8163 (2005)CrossRefPubMedCentralPubMedGoogle Scholar
  52. 52.
    A. Vermeulen, L. Behlen, A. Reynolds, A. Wolfson, W.S. Marshall, J. Karpilow, A. Khvorova, RNA 11, 674–682 (2005)CrossRefPubMedCentralPubMedGoogle Scholar
  53. 53.
    J.F. Kreuze, A. Perez, M. Untiveros, D. Quispe, S. Fuentes, I. Barker, R. Simon, Virology 388, 1–7 (2009)CrossRefPubMedGoogle Scholar
  54. 54.
    M. Aregger, B.K. Borah, J. Seguin, R. Rajeswaran, E.G. Gubaeva, A.S. Zvereva, D. Windels, F. Vazquez, T. Blevins, L. Farinelli, M.M. Pooggin, PLoS Pathog. 8, e1002941 (2012)CrossRefPubMedCentralPubMedGoogle Scholar
  55. 55.
    H.A. Ebhardt, E.P. Thi, M.B. Wang, P.J. Unrau, Proc. Natl. Acad. Sci. U.S.A. 102, 13398–13403 (2005)CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Danforth Plant Science CenterSt. LouisUSA
  2. 2.National Research Center on Plant BiotechnologyNew DelhiIndia
  3. 3.Centro Internacional de Agricultura TropicalApartado AéreoColombia

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