Interaction of a tomato leaf curl New Delhi virus with a betasatellite enhances symptom severity in field-infected tomato plants

Abstract

Two field-collected tomato plants, with severe and mild tomato leaf curl disease symptoms, were shown to be infected with tomato leaf curl New Delhi virus. The plant with severe symptoms was shown to additionally contain tobacco leaf curl betasatellite (TobLCuB). Inoculation of Nicotiana benthamiana plants with the cloned components showed the severe symptoms to be due to the presence of TobLCuB. A shorter latent period was associated with the presence of TobLCuB except in the presence of the DNA-A and DNA-B components of the severe type. The DNA-B component from the mild type also reduced the latent period, more so than the DNA-B from the severe type, except in the interaction with the DNA-A from the mild type. These differences in the effects of the virus components from the two isolates may possibly be due to mutations in the DNA-B from the severe type. The results show that betasatellites can enhance the virulence of bipartite begomoviruses, even for isolates that induce quite mild symptoms.

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References

  1. Adams MJ, Lefkowitz EJ, King AMQ, Harrach B, Harrison RL, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Mushegian AR, Nibert M, Sabanadzovic S, Sanfaçon H, Siddell SG, Simmonds P, Varsani A, Zerbini FM, Gorbalenya AE, Davison AJ (2017) Changes to taxonomy and the international code of virus classification and nomenclature ratified by the international committee on taxonomy of viruses (2017). Archives of Virology 162:2505–2538

    CAS  Article  Google Scholar 

  2. Anwar S (2017) Distinct association of an alphasatellite and a betasatellite with Tomato leaf curl New Delhi virus in field-infected cucurbit. Journal of General Plant Pathology 83:185–188

    CAS  Article  Google Scholar 

  3. Anwar I, Bukhari HA, Nahid N, Rashid K, Amin I, Shaheen S, Hussain K, Mansoor S (2020) Association of cotton leaf curl Multan betasatellite and Ageratum conyzoides symptomless alphasatellite with tomato leaf curl New Delhi virus in Luffa cylindrica in Pakistan. Australasian Plant Pathology 49:25–29

    CAS  Article  Google Scholar 

  4. Argüello-Astorga GR, Guevara-González LR, Herrera-Estrella LR, Rivera-Bustamante RF (1994) Geminivirus replication origins have a group-specific organization of iterative elements: a model for replication. Virology 203:90–100

    Article  Google Scholar 

  5. Briddon RW, Mansoor S, Bedford ID, Pinner MS, Markham PG (2000) Clones of cotton leaf curl geminivirus induce symptoms atypical of cotton leaf curl disease. Virus Genes 20:19–26

    CAS  Article  Google Scholar 

  6. 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

    CAS  Article  Google Scholar 

  7. 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. Molecular Biotechnology 20:315–318

    CAS  Article  Google Scholar 

  8. 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 DNA β: a satellite molecule associated with some monopartite begomoviruses. Virology 312:106–121

    CAS  Article  Google Scholar 

  9. Briddon RW, Ghabrial S, Lin N-S, Palukaitis P, Scholthof K-BG, Vetten H-J (2012) Satellites and other virus-dependent nucleic acids. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy - ninth report of the international committee on taxonomy of viruses. Associated Press, Elsevier Inc., London, Waltham, San Diego, pp 1209–1219

    Google Scholar 

  10. Brown JK, Zerbini FM, Navas-Castillo J, Moriones E, Ramos-Sobrinho R, Silva JF, Fiallo-Olivé E, Briddon RW, Hernández-Zepeda C, Idris A, Malathi VG, Martin DP, Rivera-Bustamante R, Ueda S, Varsani A (2015) Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Archives of Virology 160:1593–1619

    CAS  Article  Google Scholar 

  11. Bull SE, Tsai W-S, 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. Archives of Virology 149:1193–1200

    CAS  Article  Google Scholar 

  12. Chang H-H, Ku H-M, Tsai W-S, Chien R-C, Jan F-J (2010) Identification and characterization of a mechanical transmissible begomovirus causing leaf curl on oriental melon. European Journal of Plant Pathology 127:219–228

    Article  Google Scholar 

  13. Chatterji A, Padidam M, Beachy RN, Fauquet CM (1999) Identification of replication specificty determinants in two strains of tomato leaf curl virus from New Delhi. Journal of Virology 73:5481–5489

    CAS  Article  Google Scholar 

  14. Chatterji A, Chatterji U, Beachy RN, Fauquet CM (2000) Sequence parameters that determine specificity of binding of the replication-associated protein to its cognate site in two strains of Tomato leaf curl virus-New Delhi. Virology 273:341–350

    CAS  Article  Google Scholar 

  15. Czosnek H, Laterrot H (1997) A worldwide survey of tomato yellow leaf curl viruses. Archives of Virology 142:1391–1406

    CAS  Article  Google Scholar 

  16. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15

    Google Scholar 

  17. Fondong VN (2013) Geminivirus protein structure and function. Molecular Plant Pathology 14:635–649

    CAS  Article  Google Scholar 

  18. Hameed A, Tahir MN, Amin I, Mansoor S (2017) First report of Tomato leaf curl New Delhi virus and a tomato yellow leaf curl Thailand betasatellite causing severe leaf curl disease of potato in Pakistan. Plant Disease 101:1065–1065

    Article  Google Scholar 

  19. Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S (2013) Geminiviruses: masters at redirecting and reprogramming plant processes. Nature Reviews. Microbiology 11:777–788

    CAS  Article  Google Scholar 

  20. Idris AM, Shahid MS, Briddon RW, Khan AJ, Zhu JK, Brown JK (2011) An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. The Journal of General Virology 92:706–717

    CAS  Article  Google Scholar 

  21. Iqbal Z, Shafiq M, Ali I, Mansoor S, Briddon RW (2017) Maintenance of cotton leaf curl Multan betasatellite by Tomato leaf curl New Delhi virus - analysis by mutation. Frontiers in Plant Science 8:2208

    Article  Google Scholar 

  22. Jyothsna P, Haq QMI, Singh P, Sumiya KV, Praveen S, Rawat R, Briddon R, 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. Applied Microbiology and Biotechnology 97:5457–5471

    CAS  Article  Google Scholar 

  23. Kanakala S, Ghanim M (2019) Global genetic diversity and geographical distribution of Bemisia tabaci and its bacterial endosymbionts. PLoS One 14:e0213946

    CAS  Article  Google Scholar 

  24. Kumar A, Gupta T, Singh S, Sarin NB (2017) Complete nucleotide sequence of a monopartite tomato leaf curl New Delhi virus and betasatellite DNA associated with leaf curl disease of tomato in India. International Journal of Advanced Research 5:1683–1686

    Article  Google Scholar 

  25. Moriones E, Praveen S, Chakraborty S (2017) Tomato leaf curl New Delhi virus: an emerging virus complex threatening vegetable and fiber crops. Viruses 9:264

    Article  Google Scholar 

  26. Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277

    Article  Google Scholar 

  27. 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. The Journal of General Virology 76:25–35

    CAS  Article  Google Scholar 

  28. Raemakers CJJM, Sofiari E, Taylor N, Henshaw G, Jacobsen E, Visser RGF (1996) Production of transgenic cassava (Manihot esculenta Crantz) plants by particle bombardment using luciferase activity as selection marker. Molecular Breeding 2:339–349

    CAS  Article  Google Scholar 

  29. Saunders K, Bedford ID, Briddon RW, Markham PG, Wong SM, Stanley J (2000) A unique virus complex causes Ageratum yellow vein disease. Proceedings of the National Academy of Sciences of the United States of America 97:6890–6895

    CAS  Article  Google Scholar 

  30. Shahid MS, Mansoor S, Briddon RW (2007) Complete nucleotide sequences of cotton leaf curl Rajasthan virus and its associated DNA β molecule infecting tomato. Archives of Virology 152:2131–2134

    CAS  Article  Google Scholar 

  31. Sivalingam P, Varma A (2012) Role of betasatellite in the pathogenesis of a bipartite begomovirus affecting tomato in India. Archives of Virology 157:1081–1092

    CAS  Article  Google Scholar 

  32. Stanley J, Gay MG (1983) Nucleotide sequence of cassava latent virus DNA. Nature 301:260–262

    CAS  Article  Google Scholar 

  33. Venkataravanappa V, Lakshminarayana Reddy CN, Shankarappa KS, Jayappa J, Pandey S, Krishna Reddy M (2019) Characterization of tomato leaf curl New Delhi virus and DNA-satellites association with mosaic disease of cucumber. International Journal of Biotechnology and Bioengineering 5:93–109

    Google Scholar 

  34. Wilisiani F, Neriya Y, Tagami M, Kaneko M, Hartono S, Nishigawa H, Natsuaki T (2019) Complete genome sequence of tomato leaf curl New Delhi virus from Luffa in Indonesia. Microbiology Resource Announcements 8:e01605–e01618

    Article  Google Scholar 

  35. Zaidi SS-e-A, Martin DP, Amin I, Farooq M, Mansoor S (2017) Tomato leaf curl New Delhi virus; a widespread bipartite begomovirus in the territory of monopartite begomoviruses. Molecular Plant Pathology 18:901–911

    CAS  Article  Google Scholar 

  36. Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, Rivera-Bustamante R, Varsani A, ICTV Report Consortium (2017) ICTV virus taxonomy profile: Geminiviridae. The Journal of General Virology 98:131–133

    CAS  Article  Google Scholar 

  37. Zhou X (2013) Advances in understanding begomovirus satellites. Annual Review of Phytopathology 51:357–381

    CAS  Article  Google Scholar 

Download references

Acknowledgments

MSS was supported by a Ph.D. fellowship and International Research Support Initiative Program (IRSIP) fellowship from the Higher Education Commission (HEC), Government of Pakistan. RWB was supported by the HEC under the ‘Foreign Faculty Hiring Program’.

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MS, SM, and RWB conceived and designed the study. MS conducted the study and analyzed the results with the assistance of RWB and JB. The first draft of the manuscript was written by MS and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to M. S. Shahid.

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Shahid, M.S., Mansoor, S., Brown, J.K. et al. Interaction of a tomato leaf curl New Delhi virus with a betasatellite enhances symptom severity in field-infected tomato plants. Trop. plant pathol. (2021). https://doi.org/10.1007/s40858-020-00414-0

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Keywords

  • Geminivirus
  • Begomovirus
  • Betasatellite
  • Tomato leaf curl New Delhi virus
  • Tobacco leaf curl betasatellite