Skip to main content
SpringerLink
Log in

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

  • Applied genetics and molecular biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Tomato leaf curl New Delhi virus (ToLCNDV) (Geminiviridae) is an important pathogen that severely affects tomato production. An extensive survey was carried out during 2003–2010 to study the diversity of begomoviruses found in tomato, potato, and cucurbits that showed symptoms of leaf puckering, distortion, curling, vein clearing, and yellow mosaic in various fields in different regions of India. Ten begomovirus isolates were cloned from infected samples and identified as belonging to the species ToLCNDV. A total of 44 % of the samples showed association of betasatellites, with CLCuMuB and LuLDB being the most frequent. The ToLCNDV cloned component DNA A and DNA B were agroinoculated on Nicotiana benthamiana and tomato (Solanum lycopersicum) plants with or without betasatellites, CLCuMuB or LuLDB. The viral genome levels were then monitored by real-time polymerase chain reaction at different time points of disease development. Plants co-inoculated with betasatellites showed enhanced symptom severity in both N. benthamiana and tomato, as well as increases in helper viral DNA A and DNA B levels. The DNA B and betasatellites acted antagonistically to each other, so that the level of DNA B was 16-fold greater in the presence of betasatellites, while accumulation of betasatellites, CLCuMuB and LuLDB, were reduced by 60 % in the presence of DNA B. DNA B-mediated symptoms predominated in CLCuMuB-inoculated plants, whereas betasatellite-mediated leaf abnormalities were prominent in LuLDB-co-inoculated plants. Inoculation with the cloned components will be a good biotechnological tool in resistance breeding program.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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 begomovirus–betasatellite complex. Mol Plant Microbe Interact 24:973–983

    Article  CAS  Google Scholar 

  • Bevan MW (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res 12:8711–8721

    Article  CAS  Google Scholar 

  • Briddon RW, Stanley J (2006) Subviral agents associated with plant single-stranded DNA viruses. Virology 344:198–210

    Article  CAS  Google Scholar 

  • Briddon RW, Mansoor S, Bedford ID, Pinner MS, Saunders K, Stanley J, Zafar Y, Malik K, Markham PG (2001) Identification of DNA components required for induction of cotton leaf curl disease. Virology 285:234–243

    Article  CAS  Google Scholar 

  • Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG (2002) Universal primers for the PCR-mediated amplification of DNA β: a molecule associated with some monopartite begomoviruses. Mol Biol Technol 20:315–318

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bull SE, Tsai WS, Briddon RW, Markham PG, Stanley J, Green SK (2004) Diversity of begomovirus DNA β satellites of non-malvaceous plants in east and south east Asia. Arch Virol 149:1193–1200

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cui X, Li G, Wang D, Hu D, Zhou XP (2005) A begomovirus DNA β-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 79:10764–10775

    Article  CAS  Google Scholar 

  • Duan YP, Powell CA, Purcifull DE, Broglio P, Hiebert E (1997) Phenotypic variation in transgenic tobacco expressing mutated geminivirus movement/pathogenicity (BC1) proteins. Mol Plant Microbe Interact 10:1065–1074

    Article  CAS  Google Scholar 

  • Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gopal P, Kumar PP, Sinilal B, Jose J, Yadunandam KA, Usha R (2007) Differential roles of C4 and βC1 in mediating suppression of post-transcriptional gene silencing: evidence for transactivation by the C2 of Bhendi yellow vein mosaic virus, a monopartite begomovirus. Virus Res 123:9–18

    Article  CAS  Google Scholar 

  • Guo W, Jiang T, Zhang X, Li G, Zhou X (2008) Molecular variation of satellite DNA β molecules associated with Malvastrum yellow vein virus and their role in pathogenicity. Appl Environ Microbiol 74:1909–1913

    Article  CAS  Google Scholar 

  • Guo W, Yang X, Xie Y, Cui X, Zhou X (2009) Tomato yellow leaf curl Thailand virus-[Y72] from Yunnan is a monopartite begomovirus associated with DNAβ. Virus Genes 38:328–333

    Article  CAS  Google Scholar 

  • Haible D, Kober S, Jeske H (2006) Rolling circle amplification revolutionizes diagnosis and genomics of geminiviruses. J Virol Meth 135:9–16

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp 41:95–98

    CAS  Google Scholar 

  • Hanley-Bowdoin L, Settlage SB, Orozco BM, Nagar S, Robertson D (1999) Geminiviruses: models for plant DNA replication, transcription and cell cycle regulation. Crit Rev Plant Sci 18:71–106

    Article  CAS  Google Scholar 

  • Hood EE, Gelvin SB, Melchers S, Hoekema A (1993) New Agrobacterium helper plasmid for gene transfer to plants (EHA 105). Transgenic Res 2:208–218

    Article  CAS  Google Scholar 

  • Hou YM, Saunders R, Ursin VM, Gilbertson RL (2000) Transgenic plants expressing geminivirus movement proteins: abnormal phenotypes and delayed infection by tomato mottle virus in transgenic tomatoes expressing the bean dwarf mosaic virus BV1 or BC1 proteins. Mol Plant Microbe Interact 13:297–308

    Article  CAS  Google Scholar 

  • Hussain M, Mansoor S, Iram S, Fatima AN, Zafar Y (2005) The nuclear shuttle protein of tomato leaf curl New Delhi virus is a pathogenicity determinant. J Virol 79:4434–4439

    Article  CAS  Google Scholar 

  • Ilyas M, Qazi J, Mansoor S, Briddon RW (2010) Genetic diversity and phylogeography of begomoviruses infecting legumes in Pakistan. J Gen Virol 91:2091–2101

    Article  CAS  Google Scholar 

  • Ingham DJ, Pascal E, Lazarowitz SG (1995) Both bipartite geminivirus movement proteins define viral host range, but only BL1 determines viral pathogenicity. Virology 207:191–204

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kings AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (2011) Virus taxonomy. Ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, San Diego

    Google Scholar 

  • Kon T, Sharma P, Ikegami M (2007) Suppressor of RNA silencing encoded by the monopartite tomato leaf curl Java begomovirus. Arch Virol 152:1273–1282

    Article  CAS  Google Scholar 

  • Kumari P, Singh AK, Sharma VK, Chattopadhyay B, Chakraborty S (2011) A novel recombinant tomato-infecting begomovirus capable of trans-complementing heterologous DNA-B components. Arch Virol 156:769–783

    Article  CAS  Google Scholar 

  • Li ZH, Xie Y, Zhou XP (2005) Tobacco curly shoot virus DNA-β is not necessary for infection but intensifies symptoms in a host-dependent manner. Phytopathol 95:902–908

    Article  CAS  Google Scholar 

  • Lin B, Behjatnia SAA, Dry IB, Randles JW, Rezaian MA (2003) High-affinity Rep-binding is not required for the replication of a geminivirus DNA and its satellite. Virology 305:353–363

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔC T Method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Mansoor S, Briddon RW, Bull SE, Bedford ID, Bashir A, Hussain M, Saeed M, Zafar MY, Malik KA, Fauquet CM, Markham PG (2003) Cotton leaf curl disease is associated with multiple monopartite begomoviruses supported by single DNA β. Arch Virol 148:1969–1986

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Padidam M, Beachy RN, Fauquet CM (1995) Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol 76:25–35

    Article  CAS  Google Scholar 

  • Pascal E, Goodlove PE, Wu LC, Lazarowitz SG (1993) Transgenic tobacco plants expressing the geminivirus BL1 protein exhibit symptoms of viral disease. Plant Cell 5:795–807

    CAS  Google Scholar 

  • Pratap D, Kashikar AR, Mukherjee SK (2011) Molecular characterization and infectivity of a tomato leaf curl New Delhi virus variant associated with newly emerging yellow mosaic disease of eggplant in India. Virology J 8:305

    Article  Google Scholar 

  • Qazi J, Ilyas M, Mansoor S, Briddon RW (2007) Legume yellow mosaic viruses: genetically isolated begomoviruses. Mol Plant Pathol 8:343–348

    Article  Google Scholar 

  • Rojas MR, Jiang H, Salati R, Xoconostle-Cázares B, Sudarshana MR, Lucas WJ, Gilbertson RL (2001) Functional analysis of proteins involved in movement of the monopartite begomovirus, tomato yellow leaf curl virus. Virology 5:110–125

    Article  Google Scholar 

  • Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Ann Rev Phytopathol 43:361–394

    Article  CAS  Google Scholar 

  • 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 DNA β. Plant Pathol 54:259

    Article  Google Scholar 

  • Rouhibakhsh A, Priya J, Periasamy M, Haq QMI, Malathi VG (2008) An improved DNA isolation method and PCR protocol for efficient detection of multicomponents of begomovirus in legumes. J Virol Meth 147:37–42

    Article  CAS  Google Scholar 

  • Saeed M, Behjatnia SAA, Mansoor S, Zafar Y, Hasnain S, Rezaian MA (2005) A single complementary-sense transcript of a geminiviral DNA-β satellite is determinant of pathogenicity. Mol Plant Microbe Interact 18:7–14

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sahu PP, Rai NK, Chakraborty S, Singh M, Chandrappa PH, Ramesh B, Chattopadhyay D, Prasad M (2010) Tomato cultivar tolerant to tomato leaf curl New Delhi virus infection induces virus-specific short interfering RNA accumulation and defence-associated host gene expression. Mol Plant Pathol 11:531–544

    Article  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning a laboratory manual, vol I, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Saunders K, Salim N, Mali VR, Malathi VG, Briddon RW, Markham PG, Stanley J (2002) Characterisation of Sri Lankan cassava mosaic virus and Indian cassava mosaic virus: evidence for acquisition of a DNA B component by a monopartite begomovirus. Virology 293:63–74

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Saunders K, Briddon RW, Stanley J (2008) Replication promiscuity of DNA-β satellites associated with monopartite begomoviruses; deletion mutagenesis of the Ageratum yellow vein virus DNA-β satellite localizes sequences involved in replication. J Gen Virol 89:3165–3172

    Article  CAS  Google Scholar 

  • Sharma P, Ikegami M, Kon T (2010) Identification of the virulence factors and suppressors of posttranscriptional gene silencing encoded by Ageratum yellow vein virus, a monopartite begomovirus. Virus Res 149:19–27

    Article  CAS  Google Scholar 

  • Shimura H, Pantaleo V (2011) Viral induction and suppression of RNA silencing in plants. Biochim Biophys Acta 1809:601–612

    Article  CAS  Google Scholar 

  • Sivalingam PN, Malathi VG, Varma A (2010) Molecular diversity of the DNA-β satellites associated with tomato leaf curl disease in India. Arch Virol 155:757–764

    Article  CAS  Google Scholar 

  • Srivastava KM, Hallan V, Raizada RK, Chandra G, Singh BP, Sane PV (1995) Molecular cloning of Indian tomato leaf curl virus genome following a simple method of concentrating the supercoiled replicative form of viral DNA. J Virol Meth 51:297–304

    Article  CAS  Google Scholar 

  • Stanley J (1985) The molecular biology of geminiviruses. Adv Virus Res 30:139–177

    Article  CAS  Google Scholar 

  • Stanley J, Townsend R (1985) Characterization of DNA forms associated with cassava latent virus infection. Nucleic Acids Res 13:2189–2206

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tiwari N, Padmalatha KV, Singh VB, Haq QMI, Malathi VG (2010) Tomato leaf curl Bangalore virus (ToLCBV): infectivity and enhanced pathogenicity with diverse betasatellites. Arch Virol 155:1343–1347

    Article  CAS  Google Scholar 

  • von Arnim A, Stanley J (1992) Determinants of tomato golden mosaic virus symptom development located on DNA B. Virology 186:286–293

    Article  Google Scholar 

  • Yang JY, Iwasaki M, Machida C, Machida Y, Zhou X, Chua NH (2008) βC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 15:2564–2577

    Article  Google Scholar 

  • Yang X, Wang Y, Guo W, Xie Y, Xie Q, Fan L, Zhou X (2011) Characterization of small interfering RNAs derived from the geminivirus/betasatellite complex using deep sequencing. PLoS One 6:e16928

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful for the facilities provided by Dr. H.S. Gupta, The Director, Indian Agricultural Research Institute and Dr. R.K. Jain, Head, Division of Plant Pathology in conducting this study. The authors are also thankful to Darren P. Martin and Brejnev Muhire, Institute of Infectious Disease and Molecular Medicine, Computational Biology Group, University of Cape Town, South Africa for their guidance in the SDT analysis. The financial assistance by the Department of Biotechnology, Government of India, Project BT/PR/5351/AGR/16/482/2004-II is duly acknowledged. The support of the National Phytotron Facility is highly appreciated.

Author information

Authors and Affiliations

  1. Advanced Centre for Plant Virology, Division of Plant Pathology, Indian Agricultural Research Institute, New Delhi, India, 110012

    P. Jyothsna, Q. M. I. Haq, Priyanka Singh, K. V. Sumiya, Shelly Praveen & V. G. Malathi

  2. MM (PG) College, Modinagar, Uttar Pradesh, India, 201204

    Ramaveer Rawat

  3. National Institute for Biotechnology and Genetic Engineering, Jhang Road, P.O. Box 577, Faisalabad, Pakistan

    Rob W. Briddon

Authors
  1. P. Jyothsna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Q. M. I. Haq
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Priyanka Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. V. Sumiya
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shelly Praveen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ramaveer Rawat
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rob W. Briddon
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. V. G. Malathi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to V. G. Malathi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 378 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jyothsna, P., Haq, Q.M.I., Singh, P. et al. 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 (2013). https://doi.org/10.1007/s00253-012-4685-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-012-4685-9

Keywords

Search

Navigation