Abstract
βC1 proteins, encoded by betasatellites, are known to be pathogenicity determinants, and they are responsible for symptom expression in many devastating diseases caused by begomoviruses. We report the involvement of βC1 in pathogenicity determination of a mastrevirus. Analysis of field samples of wheat plants containing wheat dwarf India virus (WDIV) revealed the presence of a full-length and several defective betasatellite molecules. The detected betasatellite was identified as ageratum yellow leaf curl betasatellite (AYLCB). No begomovirus was detected in any of the samples. The full-length AYLCB contained an intact βC1 gene, whereas the defective molecules contained complete or partial deletions of βC1. Agroinoculation of wheat with the full-length AYLCB and WDIV or of tobacco with ageratum enation virus enhanced the pathogenicity and accumulation of the respective viruses, whereas the defective molecules could not. This study indicates that βC1 is a pathogenicity determinant for WDIV and can interact functionally not only with begomoviruses but also with a mastrevirus.
References
Briddon RW, Bull SE, Amin I, Idris AM, Mansoor S, Bedford ID, Dhawan P, Rishi N, Siwatch SS, Abdel-Salam AM, Brown JK, Zafar Y, Markham PG (2003) Diversity of DNAβ a satellite molecule associated with some monopartite begomoviruses. Virology 312:106–121
Briddon RW, Stanley J (2006) Subviral agents associated with plant single stranded DNA viruses. Virology 344:198–210
Nawaz-ul-Rehman MS, Fauquet CM (2009) Evolution of geminiviruses and their satellites. FEBS Lett 583:1825–1832
Saeed M, Behjatnia SAA, Mansoor S, Zafar Y, Hasnain S, Rezaian MA (2005) A single complementary-sense transcript of a geminiviral DNA b satellite is determinant of pathogenicity. Mol Plant Microbe Interact 18:7–14
Tahir MN, Mansoor S (2011) βC1 of chili leaf curl betasatellite is a pathogenicity determinant. Virol J 8:509
Saunders K, Norman A, Gucciardo S, Stanley J (2004) The DNA β satellite component associated with ageratum yellow vein disease encodes an essential pathogenicity protein (βC1). Virology 324:37–47
Cui X, Tao X, Xie Y, Fauquet CM, Zhou X (2004) A DNAβ associated with Tomato yellow leaf curl China virus is required for symptom induction. J Virol 78:13966–13974
Li Z, Xie Y, Zhou X (2005) Tobacco curly shoot virus DNA β is not necessary for infection but intensifies symptoms in a host-dependent manner. Phytopathology 95:902–908
Cui X, Li G, Wang D, Hu D, Zhou X (2005) A begomovirus DNAβ-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 79:10764–10775
Eini O, Dogra SC, Dry IB, Randles JW (2010) Silencing suppressor activity of a begomovirus DNAβ encoded protein and its effect on heterologous helper virus replication. Virus Res 167:97–101
Saeed M, Zafar Y, Randles JW, Rezaian MA (2007) A monopartite begomovirus-associated DNA β satellite substitutes for the DNA B of a bipartite begomovirus to permit systemic infection. J Gen Virol 88:2881–2889
Nawaz-ul-Rehman MS, Mansoor S, Briddon RW, Fauquet CM (2009) Maintenance of an old world betasatellite by a new world helper begomovirus and possible rapid adaptation of the betasatellite. J Virol 83:9347–9355
Patil BL, Fauquet CM (2010) Differential interaction between cassava mosaic geminiviruses and geminivirus satellites. J Gen Virol 91:1871–1882
Briddon RW, Mansoor S, Bedford ID, Pinner MS, Saunders K, Stanley J, Zafar Y, Malik KA, Markham PG (2001) Identification of DNA components required for induction of cotton leaf curl disease. Virology 285:234–243
Jose J, Usha R (2003) Bhendi yellow vein mosaic disease in India is caused by association of a DNA β satellite with a begomovirus. Virology 305:310–317
Rouhibakhsh A, Malathi VG (2005) Severe leaf curl disease of cowpea—a new disease of cowpea in northern India caused by Mungbean yellow mosaic India virus and a satellite DNAβ. Plant Pathol 54:259
Jyothsna P, Haq QM, Singh P, Sumiya KV, Praveen S, Rawat R, Briddon RW, Malathi VG (2013) Infection of Tomato leaf curl New Delhi virus (ToLCNDV), a bipartite begomovirus with betasatellites, results in enhanced level of helper virus components and antagonistic interaction between DNA B and betasatellites. Appl Microbiol Biotechnol 97:5457–5471
Sivalingam PN, Varma A (2012) Role of betasatellite in the pathogenesis of a bipartite begomovirus affecting tomato in India. Arch Virol 157:1081–1092
Kumar J, Kumar J, Singh SP, Tuli R (2014) Association of satellites with a mastrevirus in natural infection: complexity of Wheat dwarf India virus disease. J Virol 88:7093–7104. doi:10.1128/JVI.02911-13
Saunders K, Briddon RW, Stanley J (2008) Replication promiscuity of DNA-beta satellites associated with monopartite begomoviruses; deletion mutagenesis of the Ageratum yellow vein virus DNA-beta satellite localizes sequences involved in replication. J Gen Virol 89:3165–3172
Stenger DC, Stevenson MC, Hormuzdi SG, Bisaro DM (1992) A number of subgenomic DNAs are produced following agroinoculation of plants with beet curly top virus. J Gen Virol 73:237–242
Stanley J, Frischmuth T, Ellwood S (1990) Defective viral DNA ameliorates symptoms of geminivirus infection in transgenic plants. Proc Nat Acad Sci USA 87:6291–6295
Stanley J, Saunders K, Pinner MS, Wong SM (1997) Novel defective interfering DNAs associated with ageratum yellow vein geminivirus infection of Ageratum conyzoides. Virology 239:87–96
Frischmuth T, Stanley J (1994) Beet curly top virus symptom amelioration in Nicotiana benthamiana transformed with a naturally occurring viral subgenomic DNA. Virology 200:826–830
Acknowledgements
The authors are grateful to the Department of Biotechnology, Government of India for supporting the present work at National Agri-Food Biotechnology Institute, Mohali, India; to the Council of Scientific and Industrial Research for Senior Research Fellowship to JK and JK; and to the Department of Science and Technology, Government of India, for the JC Bose Fellowship to RT.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kumar, J., Kumar, J., Singh, S.P. et al. βC1 is a pathogenicity determinant: not only for begomoviruses but also for a mastrevirus. Arch Virol 159, 3071–3076 (2014). https://doi.org/10.1007/s00705-014-2149-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-014-2149-5