Abstract
Five genes encoded by Banana bunchy top virus (BBTV) originating from Pakistan were expressed in Nicotiana benthamiana using a Potato virus X (PVX) vector. Expression of the master replication-associated protein (mRep) and movement protein (MP) resulted in necrotic cell death of inoculated tissues, as well as leaf curling and necrosis along the veins in newly emerging leaves. The systemic necrosis induced by the expression of MP was discolored (dark) in comparison to that induced by mRep. Expression of the cell-cycle link protein (Clink), the coat protein (CP), and the nuclear shuttle protein from the PVX vector induced somewhat milder symptoms, consisting of mild leaf curling and mosaic, although expression of the CP caused a necrotic response in inoculated leaf. The accumulation of viral RNA was enhanced by MP, Clink, and CP. Of the five BBTV-encoded gene products two, the MP and Clink, stabilized GFP-specific mRNA and reduced GFP-specific small interfering RNA in N. benthamiana line 16c when expressed under the control of the 35S promoter and co-inoculated with a construct for the expression of GFP hairpin RNA construct. These results identified MP and Clink as suppressors of RNA silencing. Taken together the ability of MP to induce severe symptoms in plants and suppress RNA silencing implicates this product as a major pathogenicity determinant of BBTV.
Similar content being viewed by others
References
T. Fahmy, Minerals and Agriculture in Egypt Bulletin, p. 30 (1927)
C.W. Wardlaw, Banana Diseases (Longmans, Green and Co Ltd, London, 1961), p. 648
M. Sharman, J.E. Thomas, S. Skabo, T.A. Holton, Arch. Virol. 153, 135–147 (2008)
B. Mandal, S. Mandal, K.B. Pun, A. Varma, Plant Dis. 88, 428 (2004)
I. Grigoras, T. Timchenko, B. Gronenborn, J. Gen. Virol. 89, 583–593 (2008)
W. Rohde, J.W. Randles, P. Langridge, D. Hanold, Virology 176, 648–651 (1990)
I. Grigoras, T. Timchenko, L. Katul, A. Grande-Perez, H.J. Vetten, B. Gronenborn, J. Virol. 83, 10778–10787 (2009)
I. Grigoras, B. Gronenborn, J. Vetten, Plant Dis. 94, 642 (2010)
H.J. Vetten, P.W.G. Chu, J.L. Dale, R. Harding, J. Hu, L. Katul, M. Kojima, J.W. Randles, Y. Sano, J.E. Thomas, in Virus Taxonomy, VIIIth Report of the ICTV, ed. by C.M. Fauquet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball (Academic Press/Elsevier, London, 2005), pp. 343–352
T. Timchenko, L. Katul, M. Aronson, J.C. Vega-Arreguín, B.C. Ramirez, H.J. Vetten, B. Gronenborn, J. Gen. Virol. 87, 1735–1743 (2006)
C.L. Horser, M. Karan, R.M. Harding, J.L. Dale, Arch. Virol. 146, 71–86 (2001)
T. Timchenko, L. Katul, Y. Sano, F. de Kouchkovsky, H.J. Vetten, B. Gronenborn, Virology 274, 189–195 (2000)
M.N. Aronson, A.D. Meyer, J. Györgyey, L. Katul, H.J. Vetten, B. Gronenborn, T. Timchenko, J. Virol. 74, 2967–2972 (2000)
E. Bernstein, A.A. Caudy, S.M. Hammond, G.J. Hannon, Nature 409, 363–366 (2001)
S.M. Hammond, E. Bernstein, D. Beach, G.J. Hannon, Nature 404, 293–296 (2000)
A. Verdel, S. Jia, S. Gerber, T. Sugiyama, S. Gygi, S.I.S. Grewal, D. Moazed, Science 303, 672–676 (2004)
D.P. Bartel, Cell 116, 281–297 (2004)
G.J. Hannon, Nature 418, 244–251 (2002)
D.C. Baulcombe, Science 290, 1108 (2000)
O. Voinnet, Nat. Genet. 6, 206–221 (2005)
D.M. Bisaro, Virology 344, 158–168 (2006)
C. Llave, K. Kasschau, J.C. Carrington, Proc. Natl. Acad. Sci. USA 97, 13401–13406 (2000)
K.D. Kasschau, J.C. Carrington, Cell 95, 461–470 (1998)
L. Lakatos, G. Szittya, D. Silhavy, J. Burgyan, EMBO J. 23, 876–884 (2004)
D. Silhavy, J. Burgyan, Trends Plant Sci. 9, 76–83 (2004)
J.M. Vargason, G. Szittya, J. Burgyan, T.M. Hall, Cell 115, 799–811 (2003)
Z. Xie, L.K. Johansen, A.M. Gustafson, K.D. Kasschau, A.D. Lellis, D. Zilberman, S.E. Jacobsen, J.C. Carrington, PLoS Biol. 2, E104 (2004)
B. Brigneti, O. Voinnet, W.-X. Li, L.-H. Ji, S.-W. Ding, D.C. Baulcombe, EMBO J. 17, 6739–6746 (1998)
H.S. Guo, S.W. Ding, EMBO J. 21, 398–407 (2002)
R. Vanitharani, P. Chellappan, J.S. Pita, C.M. Fauquet, J. Virol. 78, 9487–9498 (2004)
I. Amin, J. Qazi, S. Mansoor, M. Ilyas, R.W. Briddon, Virus Genes 36, 191–198 (2008)
T.M. Ruiz, O. Voinnet, D.C. Baulcombe, Plant Cell 10, 937–946 (1998)
R. Lu, I. Malcuit, P. Moffett, M.T. Ruiz, J. Peart, A.-J. Wu, J.P. Rathjen, A. Bendahmane, L. Day, D.C. Baulcombe, EMBO J. 22, 5690–5699 (2003)
K.R. Siemering, R. Golbik, R. Sever, J. Haseloff, Curr. Biol. 6, 1653–1663 (1996)
F. Guerineau, A. Lucy, P. Mullineaux, Plant Mol. Biol. 18, 815–818 (1992)
R.P. Hellens, E.A. Edwards, N.R. Leyland, S. Bean, P.M. Mullineaux, Plant Mol. Biol. 42, 819–832 (2000)
C.L. Thomas, V. Leh, C. Lederer, A.J. Maule, Virology 306, 33–41 (2003)
J. Haseloff, K.R. Siemering, D.C. Prasher, S. Hodge, Proc. Natl. Acad. Sci. USA 94, 2122–2127 (1997)
A. Kerschen, C.A. Napoli, R.A. Jorgensen, A.E. Muller, FEBS Lett. 566, 223–228 (2004)
S. Chapman, T. Kavanagh, D. Baulcombe, Plant J. 2, 549–557 (1992)
E.J. Chapman, A.I. Prokhnevsky, K. Gopinath, V.V. Dolja, J.C. Carrington, Genes Dev. 18, 1179–1186 (2004)
P. Dunoyer, C.-H. Lecellier, E.A. Parizotto, C. Himber, O. Voinnet, Plant Cell 16, 1235–1250 (2004)
C.R.R. Hooks, M.G. Wright, D.S. Kabasawa, R. Manandhar, R.P.P. Almeida, Ann. Appl. Biol. 153, 1–9 (2008)
M. Hussain, S. Mansoor, S. Iram, Y. Zafar, R.W. Briddon, Mol. Plant Microbe Interact. 20, 1581–1588 (2007)
M. Mubin, I. Amin, L. Amrao, R.W. Briddon, S. Mansoor, Mol. Plant Pathol. 11, 245–254 (2010)
V.A. Herrera-Valencia, B. Dugdale, R.M. Hardingand, J.L. Dale, J. Gen. Virol. 87, 3409–3412 (2006)
C.L. Horser, R.M. Harding, J.L. Dale, J. Gen. Virol. 82, 459–464 (2001)
G. Hafner, R. Harding, J. Dale, J. Gen. Virol. 78, 479–486 (1997)
L.A. Selth, J.W. Randles, M.A. Rezaian, Mol. Plant Microbe Interact. 17, 27–33 (2004)
R. van Wezel, X. Dong, P. Blake, J. Stanley, Y. Hong, Mol. Plant Pathol. 3, 461–471 (2002)
C.V. Jordan, W. Shen, L.K. Hanley-Bowdoin, D.N. Robertson, Plant Mol. Biol. 65, 163–175 (2007)
S. Lageix, O. Catrice, J.-M. Deragon, B. Gronenborn, T. Pelissier, B.C. Ramirez, J. Virol. 81, 4177–4185 (2007)
R. Wanitchakorn, G.J. Hafner, R.M. Harding, J.L. Dale, J. Gen. Virol. 81, 299–306 (2000)
M.R. Rojas, H. Jiang, R. Salati, B. Xoconostle-Cazares, M.R. Sudarshana, W.J. Lucas, R.L. Gilbertson, Virology 291, 110–125 (2001)
J. Qazi, I. Amin, S. Mansoor, M.J. Iqbal, R.W. Briddon, Virus Res. 128, 135–139 (2007)
R. Lu, A. Folimonov, M. Shintaku, W.-X. Li, B.W. Falk, W.O. Dawson, S.-W. Ding, Proc. Natl. Acad. Sci. USA 101, 15742–15747 (2004)
S. Niu, B. Wang, X. Guo, J. Yu, X. Wang, K. Xu, Y. Zhai, J. Wang, Z. Liu, Arch. Virol. 154, 1775–1783 (2009)
M. Karan, R.M. Harding, J.L. Dale, J. Gen. Virol. 75, 3541–3546 (1994)
Acknowledgments
M.I. was supported by a PhD fellowship from the Higher Education Commission (HEC), Government of Pakistan. R.W.B. is supported by the HEC under the “Foreign Faculty Hiring Program.” The authors are grateful to Dr. Peter Moffett (Boyce Thompson Institute for Plant Research) for providing the TCV-CP and HC-Pro constructs used in the study. The funds for this study were provided by a Pak-US linkage project.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Amin, I., Ilyas, M., Qazi, J. et al. Identification of a major pathogenicity determinant and suppressors of RNA silencing encoded by a South Pacific isolate of Banana bunchy top virus originating from Pakistan. Virus Genes 42, 272–281 (2011). https://doi.org/10.1007/s11262-010-0559-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11262-010-0559-3