Abstract
Cotton leaf curl disease (CLCuD) is a major limitation to cotton production on the Indian subcontinent. A survey for viruses causing CLCuD was conducted during the 2009 and 2010 cropping seasons in the northwestern Indian cotton-growing belt in the states of Punjab, Haryana and Rajasthan. Partial sequences of 258 and full-length sequences of 22 virus genomes were determined. This study shows that the resistance-breaking cotton leaf curl Burewala virus (CLCuBuV) is now the dominant virus in many fields. The spread and establishment of the mutant CLCuBuV in northwestern India, the variation in its genomic sequence, its virulence and infectivity, and the implications for cotton breeding are discussed.
Similar content being viewed by others
References
Ahuja SL, Monga D, Dhayal LS (2007) Genetics of resistance to cotton leaf curl disease in Gossypium hirsutum L. under field conditions. J Hered 98:79–83
Akhtar KP, Haidar S, Khan MKR, Ahmad M, Sarwar N, Murtaza MA, Aslam M (2010) Evaluation of Gossypium species for resistance to Cotton leaf curl Burewala virus. Ann Appl Biol 157:135–147
Amin I, Hussain K, Akbergenov R, Yadav JS, Qazi J, Mansoor S, Hohn T, Fauquet CM, Briddon RW (2011) Suppressors of RNA silencing encoded by the components of the Cotton leaf curl begomoviurus-betasatellite complex. Mol Plant Microb Interact 8:973–983
Amrao L, Amin I, Shahid MS, Briddon RW, Mansoor S (2010) Cotton leaf curl disease in resistant cotton is associated with a single begomovirus that lacks an intact transcriptional activator protein. Virus Res 152:153–163
Amrao L, Akter A, Tahir MN, Amin I, Briddon RW, Mansoor S (2010) Cotton leaf curl disease in Sindh Province of Pakistan is associated with recombinant begomovirus components. Virus Res 153:161–165
Aslam M, Gilani A (2000) Resistance of different cotton varieties to Cotton leaf curl virus under field conditions. J Res Sci 11:42–45
Balaji S, Sunter J, Sunter G (2007) Transcriptional analysis of complementary sense genes in Spinach curly top virus and functional role of C2 in pathogenesis. Mol Plant Microb Interact 20:194–206. doi:10.1094/MPMI-20-2-0194
Bonas U, Lahaye T (2002) Plant disease resistance triggered by pathogen-derived molecules: refined models of specific recognition. Curr Opin Microbiol 5:44–50
Briddon RW (2003) Cotton leaf curl disease, a multi component begomovirus complex. Mol Plant Pathol 4:427–434
Briddon RW, Bull SE, Amin I, Mansoor S, Bedford ID, Rishi N, Siwatch S, Zafar MY, Abdel-Salam AM, Markham PG (2004) Diversity of DNA1; a satellite-like molecule associated with monopartite begomovirus–DNA complexes. Virology 324:462–474
Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG (2002) Universal primers for the PCR-mediated amplification of DNA; a molecule associated with some monopartite begomoviruses. Mol Biotechnol 20:315–318
Briddon RW, Markham PG (2000) Cotton leaf curl virus disease. Virus Res 71:151–159
Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X, Fauquet CM (2008) Recommendations for the classification and nomenclature of the DNA-β satellites of begomoviruses. Arch Virol 153:763–781
Bull SE, Briddon RW, Markham PG (2003) Universal primers for the PCR- mediated amplification of DNA1: a satellite-like molecule associated with begomovirus-DNA complexes. Mol Biotechnol 23:83–86
Cai JH, Xie K, Lin L, Qin BX, Chen BS, Meng JR, Liu YL (2010) Cotton leaf curl Multan virus newly reported to be associated with cotton leaf curl disease in China. New Dis Rep 20:29
Davino S, Napoli S, Davino M, Accotto GP (2006) Spread of Tomato yellow leaf curl virus in Sicily: partial displacement of another geminivirus originally present. Eur J Plant Pathol 114:293–299
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
Fauquet CM, Briddon RW, Brown JK, Moriones E, Stanley J, Zerbini M, Zhou X (2008) Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821
Fernandes JJ, Carvalho MG, Brommonschenkel SH, Fontes EPB, Zerbini FM (2006) Biological and molecular properties of Tomato rugose mosaic virus (ToRMV), a new tomato-infecting begomovirus from Brazil. Plant Pathol 55:513–522
Galvão RM, Mariano AC, Luz DF, Alfenas PF, Andrade EC, Zerbini FM, Almeida MR, Fontes EPB (2003) A naturally occurring recombinant DNA-A of a typical bipartite begomovirus does not require the cognate DNA-B to infect Nicotiana benthamiana systemically. J Gen Virol 84:715–726
Haible D, Kober S, Jeske H (2006) Rolling circle amplification revolutionizes diagnosis and genomics of geminiviruses. J Virol Methods 135:9–16
Haley A, Zhan X, Richardson K, Head K, Morris B (1992) Regulation of the activities of African cassava mosaic virus promoters by the AC1, AC2, and AC3 gene products. Virology 188:905–909
Hussain T, Ali M (1975) A review of cotton diseases of Pakistan. Pakistan Cotton 19:77–78
Hussain M, Mansoor S, Iram S, Zafar Y, Briddon RW (2007) The hypersensitive response to Tomato leaf curl New Delhi virus nuclear shuttle protein is inhibited by transcriptional activator protein. Mol Plant Microbe Interact 20:1581–1588
Hong YG, Robinson DJ, Harrison BD (1993) Nucleotide sequence evidence for the occurrence of three distinct whitefly-transmitted geminiviruses in cassava. J Gen Virol 74:2437–2443
Jin M, Li C, Shi Y, Ryabov E, Huang J, Wu Z, Fan Z, Hong Y (2008) A single amino acid change in a geminiviral Rep protein differentiates between triggering a plant defence response and initiating viral DNA replication. J Gen Virol 89:2636–2641
Khan JA, Ahmad J (2005) Diagnosis, monitoring and transmission characteristics of Cotton leaf curl virus. Curr Sci 88:1803–1809
Kheyr PA, Bananej K, Dafalla GA, Caciagli P, Noris E, Ahoonmanesh A, Lecoq H, Gronenborn B (2000) Watermelon chlorotic stunt virus from the Sudan and Iran: Sequence comparisons and identification of a whitefly-transmission determinant. Phytopathology 90:629–635
Kirthi N, Priyadarshini CGP, Sharma P, Maiya SP, Hemalatha V, Sivaraman P, Dhawan P, Rishi N, Savithri HS (2004) Genetic variability of begomoviruses associated with cotton leaf curl disease originating from India. Arch Virol 149:2047–2057
Kumar B (2002) Genetic studies on cotton leaf curl virus disease and characters of economic importance in cotton (Gossypium hirsutum L.). PhD thesis, CCS Haryana Agricultural University, Hisar, India
Kumar A, Kumar J, Khan JA (2010) Sequence characterization of cotton leaf curl virus from Rajasthan: phylogenetic relationship with other members of geminiviruses and detection of recombination. Virus Genes 40:282–289
Malathi VG, Padamalatha KV, Sivalingam P, Gandhakrishnan N, Mandal B, Monga D, Ajmera BD, Varma A (2004) Begomoviruses causing cotton leaf curl disease in India. In: National seminar on cotton leaf curl virus disease: present status and future strategies for its management at central institute for cotton research regional station, Sirsa, Haryana
Mansoor S, Amin I, Iram S, Hussain M, Zafar Y, Malik KA, Briddon RW (2003) Breakdown of resistance in cotton to cotton leaf curl disease in Pakistan. Plant Pathol 52:784
Mansoor S, Briddon RW, Bull SE, Bedford ID, Bashir A, Hussain M, Saeed M, Zafar MY, Malik KA, Fauquet C, Markham PG (2003) Cotton leaf curl disease is associated with multiple monopartite begomoviruses supported by single DNA. Arch Virol 148:1969–1986
Mansoor S, Zafar Y, Briddon RW (2006) Geminivirus disease complexes: the threat is spreading. Trends Plant Sci 11:209–212
Mansoor S, Briddon RW (2007) Cotton leaf curl disease. In: Proceedings of the world cotton research conferences-4, Texas, 10–14 Sep 2007. http://www.icac.org/meetings/wcrc/wcrc4/presentations/start.htm
Martin DP, Rybicki EP (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563
Monga D, Raj S, Mayee CD (2004) Strategies for cotton leaf curl virus disease management. In: National symposium on changing world order-cotton research development and policy in context, ANGRAU, Hyderabad, 10–12 Aug 2004, pp 205–213
Monga D, Chakrabarty PK, Kranthi KR (2011a) Cotton leaf curl virus disease in India- Recent status and management strategies. In: Fifth meeting of Asian cotton research and development network, Lahore, 23–25 Feb 2011
Monga D, Kranthi KR, Gopalakrishnan N, Mayee CD (2011b) Changing scenario of cotton disease in India-The challenge ahead. In: Kranthi KR (ed) Book of Papers, World cotton Research Conference-5, Mumbai, 7–11 Nov, pp 272–280
Monga D, Manocha, Veena, Kumar, Kishor C, Soni R, Singh NP (2011) Occurrence and prediction of cotton leaf curl virus disease in northern zone. J Cot Res Dev 25:273–277
Nateshan HM, Muniyappa V, Swanson MM, Harrison BD (1996) Host range, vector relations and serological relationships of cotton leaf curl virus in South India. Ann Appl Biol 126:233–244
Nawaz-ul-Rehman MS, Nahid N, Mansoor S, Briddon RW, Fauquet CM (2010) Post-transcriptional gene silencing suppressor activity of the alpha-Rep of non-pathogenic alphasatellites associated with begomoviruses. Virology 405:300–308
Nischwitz C, Pappu HR, Mullis SW, Sparks AN, Langston DR, Csinos AS, Gitaitis RD (2007) Phylogenetic analysis of Iris yellow spot virus isolates from onion (Allium cepa) in Georgia and Peru. J Phytopathol 155:531–535
Qazi J, Amin I, Mansoor S, Iqbal MJ, Briddon RW (2007) Contribution of the satellite encoded gene βC1 to cotton leaf curl disease symptoms. Virus Res 128:135–139
Rahman M, Hussain D, Malik TA, Zafar Y (2005) Genetics of resistance to cotton leaf curl disease in Gossypium hirsutum. Plant Pathol 54:764–772
Raghavan V, Malik PS, Choudhury NR, Mukherjee SK (2004) The DNA-A component of a plant geminivirus (Indian mung bean yellow mosaic virus) replicates in budding yeast cells. J Virol 78:2405–2413
Rajeswaran R, Sunitha S, Padubidri V, Shivaprasad PV, Pooggin MM, Hohn T, Veluthambi (2007) The mungbean yellow mosaic begomovirus transcriptional activator protein transactivates the viral promoter-driven transgene and causes toxicity in transgenic tobacco plants. Mol Plant Microbe Interact 20:1545–1554. doi:10.1094/MPMI-20-12-1545
Rashida AP, Sultan MK, Sultan MK, Khan (2005) Screening of Cotton Germplasm Against Cotton Leaf Curl Begomovirus (CLCuV). J Agric Soc Sci 1:235–238
Rishi N, Chauhan MS (1994) Appearance of leaf curl diseases of cotton in North India. J Cotton Res Dev 8:179–180
Sánchez-Campos S, Navas-Castillo J, Camero R, Soria C, Díaz JA, Moriones E (1999) Displacement of Tomato yellow leaf curl virus (TYLCV)-Sr by TYLCV-Is in tomato epidemics in Spain. Phytopathology 89:1038–1043
Sánchez-Campos S, Díaz JA, Monci F, Bejarano ER, Reina J, Navas-Castillo J, Aranda MA, Moriones E (2002) High genetic stability of the begomovirus Tomato yellow leaf curl Sardinia virus in southern Spain over an 8-year period. Phytopathology 92:842–849
Seo J-K, Lee S-H, Kim K-H (2009) Strain-specific cylindrical inclusion protein of Soybean mosaic virus elicits extreme resistance and a lethal systemic hypersensitive response in two resistant soybean cultivars. Mol Plant Microbe Interact 22:1151–1159
Seo J-K, Shon SH (2011) Kim K-H (2009) A single amino acid change in HC-Pro of soybean mosaic virus alters symptom expression in a soybean cultivar carrying Rsv1 and Rsv3. Arch Virol 156:135–141. doi:10.1007/s00705-010-0829-3
Shivaprasad PV, Akbergenov R, Trinks D, Rajeswaran R, Veluthambi K, Hohn T, Pooggin MM (2005) Promoters, transcripts, and regulatory proteins of mungbean yellow mosaic geminivirus. J Virology 79:8149–8163. doi:10.1128/JVI.79.13.81498163.2005
Singh D, Singh P, Gill JS, Brar JS (2010) Weather based prediction model for forecasting cotton leaf curl disease in American cotton. Indian Phytopathol 63:87–90
Sunter G, Bisaro DM (1992) Transactivation of geminivirus AR1 and BR1 gene expression by the viral AL2 gene product occurs at the level of transcription. Plant Cell 4:1321–1331
Tahir MN, Amin I, Briddon RW, Mansoor S (2011) The merging of two dynasties—identification of an african cotton leaf curl disease-associated begomovirus with cotton in Pakistan. PLoS ONE 6(5):e20366. doi:10.1371/journal.pone.0020366
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface; flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Torres Pacheco I, Garzon Tiznado JA, Herrera Estrella L, Rivera Bustamante RF (1993) Complete nucleotide sequence of pepper huasteco virus: Analysis and comparison with bipartite geminiviruses. J Gen Virol 74:2225–2231
Vanitharani R, Chellappan P, Fauquet CM (2005) Geminiviruses and RNA silencing. Trends Plant Sci 10:144–151
Varma A, Malathi VG (2003) Emerging geminivirus problems: a serious threat to crop production. Ann Appl Biol 142:145–164
Acknowledgments
This research was partially funded by an ‘SBIRI’ grant (No.BT/04(SBIRI)/05/2006) from the Biotech Consortium India Limited, Department of Biotechnology, India, to Maharashtra Hybrid Seeds Company Limited (MHSCL), Maharashtra, India. We thank the cotton farmers for giving access to their fields and for providing information on prevalence of diseases during our field visits. We are thankful to Dr. A. K. Agarwal and his team for their assistance during the 2010 survey. We are very grateful to Dr. R.W. Briddon for discussions, valuable suggestions, and critical review of the manuscript. We would also like to thank Dr. H. S. Savithri and Dr. Bharat Char for their input.
Author information
Authors and Affiliations
Corresponding author
Additional information
The full-length nucleotide sequences of DNA A and DNA beta of 29 cotton leaf curl–associated begomoviruses (CBVs) were characterized in this study. The sequences were submitted to NCBI GenBank, and accession numbers are presented in Table 2.
Rights and permissions
About this article
Cite this article
Rajagopalan, P.A., Naik, A., Katturi, P. et al. Dominance of resistance-breaking cotton leaf curl Burewala virus (CLCuBuV) in northwestern India. Arch Virol 157, 855–868 (2012). https://doi.org/10.1007/s00705-012-1225-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-012-1225-y