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Tomato leaf curl Oman virus and associated Betasatellite causing leaf curl disease in tomato in Pakistan

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Abstract

The ongoing global spread of Tomato yellow leaf curl virus (TYLCV) poses an endemic threat to tomato production in all tropical and sub-tropical regions of the world. In Oman, TYLCV evolved into the new species Tomato leaf curl Oman virus (ToLCOMV) by recombination with Papaya leaf curl virus (PaLCuV). In March 2017, during a field survey of Sindh province of Pakistan, tomato (Solanum lycopersicum L.) plants showing typical symptoms of Tomato leaf curl disease (ToLCD); such as leaf curling, yellowing and stunted plant growth were observed. For identification and characterization of the causative agent, leaf samples were collected and tested for the presence of begomoviruses and associated DNA satellites. We have recently reported the presence of ToLCOMV-PK (previously known as TYLCV-PK strain) on Cyamopsis tetragonoloba in the same province of Pakistan. The tomato samples were analyzed for the presence of ToLCOMV-PK using specific primers. Approx. 2.8 kb and 1.4 kb PCR products were obtained which were cloned and sequenced; the results indicated the presence of ToLCOMV-PK and Tomato leaf curl betasatellite (ToLCB). We were also able to identify defective molecules of ToLCOMV-PK which were about half the size of the complete virus. Phylogenetic analysis and the sequence demarcation tool (SDT) showed that these are new isolates of ToLCOMV-PK (ToLCOMV-Pakistan strain) associated with ToLCB. Recombination analysis detected a strong recombination event in ToLCOMV-PK in which TYLCV (JQ928346) and PaLCuV (LT009400) were major and minor parents, respectively. We also corrected the classification of the previously identified distinct strain i.e. TYLCV-PK (TYLCV-Pakistan strain) into ToLCOMV-PK strain, based on our current analysis and classification. Biolistic inoculation of ToLCOMV-PK and associated ToLCB in Nicotiana benthamiana plants showed that coinfection with ToLCB resulted in enhanced symptoms and virus accumulation. This report of ToLCOMV-PK associated with ToLCB infecting tomato in Pakistan represents the widespread and vast host range of ToLCOMV and which poses serious threat to tomato production in Pakistan.

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References

  • Abhary, M., Patil, B. L., & Fauquet, C. M. (2007). Molecular biodiversity taxonomy and nomenclature of tomato yellow leaf curl -like viruses. In H. Czosnek (ed.), Tomato yellow leaf curl virus disease (pp. 85–118). Netherlands: Springer.

  • Ahmed, M. Z., De Barro, P. J., Greeff, J. M., Ren, S. X., Naveed, M., & Qiu, B. L. (2011). Genetic identity of the Bemisia tabaci species complex and association with high cotton leaf curl disease (CLCuD) incidence in Pakistan. Pest Management Science, 67(3), 307–317.

    Article  CAS  Google Scholar 

  • Al-Shihi, A. A. M., Khan, A. J., Akhtar, S., Lima, A. T. M., Zerbini, F. M., & Briddon, R. W. (2014). Occurrence of a new recombinant begomovirus species infecting tomato in the a l-B atinah region of O man. Plant Pathology, 63(5), 1177–1184.

    Article  Google Scholar 

  • Ammara, U. E., Al-Shihi, A., Amin, I., & Al-Sadi, A. M. (2015). 401601. First report of Tomato leaf curl Albatinah virus (ToLCABV) and its associated betasatellite infecting papaya in Oman. Plant Disease, 99(3), 421–421.

    Article  CAS  Google Scholar 

  • Briddon, R. W., & Markham, P. G. (1994). Universal primers for the PCR amplification of dicot-infecting geminiviruses. Molecular Biotechnology, 1(2), 202–205.

    Article  CAS  Google Scholar 

  • Briddon, R. W., Bull, S. E., Mansoor, S., Amin, I., & Markham, P. G. (2002). Universal primers for the PCR-mediated amplification of DNA β. Molecular Biotechnology, 20(3), 315–318.

    Article  CAS  Google Scholar 

  • Brown, J. K., Zerbini, F. M., Navas-Castillo, J., Moriones, E., Ramos-Sobrinho, R., Silva, J. C., et al. (2015). Revision of begomovirus taxonomy based on pairwise sequence comparisons. Archives of Virology, 160(6), 1593–1619.

    Article  CAS  Google Scholar 

  • Bull, S. E., Briddon, R. W., & Markham, P. G. (2003). Universal primers for the PCR-mediated amplification of DNA 1: A satellite-like molecule associated with begomovirus-DNA β complexes. Molecular Biotechnology, 23(1), 83–86.

    Article  CAS  Google Scholar 

  • Doyle, J. J., & Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochemical Bulletin, 19, 11–15.

    Google Scholar 

  • Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797.

    Article  CAS  Google Scholar 

  • Heydarnejad, J., Kamali, M., Hassanvand, V., Massumi, H., Shamshiri, M., & Varsani, A. (2018). Turnip leaf curl disease associated with two begomoviruses in South-Eastern Iran. Tropical Plant Pathology, 43(2), 165–169.

    Article  Google Scholar 

  • Idris, A. M., Shahid, M. S., Briddon, R. W., Khan, A. J., Zhu, J. K., & Brown, J. K. (2011). An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. Journal of General Virology, 92(3), 706–717.

    Article  CAS  Google Scholar 

  • Khan, A. J., Akhtar, S., Singh, A. K., Al-Shehi, A. A., Al-Matrushi, A. M., Ammara, U., & Briddon, R. W. (2014). Recent evolution of a novel begomovirus causing tomato leaf curl disease in the Al-Batinah region of Oman. Archives of Virology, 159(3), 445–455.

    Article  CAS  Google Scholar 

  • Khan, A. J., Idris, A. M., Al-Saady, N. A., Al-Mahruki, M. S., Al-Subhi, A. M., & Brown, J. K. (2008). A divergent isolate of tomato yellow leaf curl virus from Oman with an associated DNAβ satellite: An evolutionary link between Asian and the middle eastern virus–satellite complexes. Virus Genes, 36(1), 169–176.

    Article  CAS  Google Scholar 

  • Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870–1874.

    Article  CAS  Google Scholar 

  • Lefeuvre, P., Martin, D. P., Harkins, G., Lemey, P., Gray, A. J., Meredith, S., et al. (2010). The spread of tomato yellow leaf curl virus from the Middle East to the world. PLoS Pathogens, 6, e1001164. https://doi.org/10.1371/journal.ppat.1001164.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mabvakure, B., Martin, D. P., Kraberger, S., Cloete, L., van Brunschot, S., Geering, A. D. W., Thomas, J. E., Bananej, K., Lett, J. M., Lefeuvre, P., Varsani, A., & Harkins, G. W. (2016). Ongoing geographical spread of tomato yellow leaf curl virus. Virology, 498, 257–264. https://doi.org/10.1016/j.virol.2016.08.033.

    Article  CAS  PubMed  Google Scholar 

  • Martin, D. P., Murrell, B., Golden, M., Khoosal, A., & Muhire, B. (2015). RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evolution, 1(1).

  • Mohammed, H. S., Marmar, A., El Hussein, A. A., Navas-Castillo, J., & Fiallo-Olivé, E. (2018). Complete genome sequence of Datura leaf curl virus, a novel begomovirus infecting Datura innoxia in Sudan, related to begomoviruses causing tomato yellow leaf curl disease. Archives of Virology, 163(1), 273–275.

    Article  CAS  Google Scholar 

  • Muhire, B. M., Varsani, A., & Martin, D. P. (2014). SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One, 9(9), e108277.

    Article  Google Scholar 

  • Navot, N., Pichersky, E., Zeidan, M., Zamir, D., & Czosnek, H. (1991). Tomato yellow leaf curl virus: A whitefly-transmitted geminivirus with a single genomic component. Virology, 185(1), 151–161.

    Article  CAS  Google Scholar 

  • Tahir, M. N., Amin, I., Briddon, R. W., & 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.

    Article  CAS  Google Scholar 

  • Zaidi, S. S., Shakir, S., Farooq, M., Amin, I., & Mansoor, S. (2017). First report of a novel strain of tomato yellow leaf curl virus causing yellow leaf curl disease on cluster bean in Pakistan. Plant Disease, 101(6), 1071–1071.

    Google Scholar 

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Acknowledgments

We are highly thankful to Higher Education Commission (HEC), Pakistan for support to NA for his PhD under the “5000 PhD indigenous fellowship program” and “Pakistan-U.S. Cotton Productivity Enhancement Program” of ICARDA funded by the United States Department of Agriculture (USDA), Agricultural Research Service (ARS) for their financial support to this research. We are very thankful to Claude M. Fauquet for his critical review of our manuscript.

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Authors and Affiliations

  1. National Institute for Biotechnology and Genetic Engineering (NIBGE), Faisalabad, Pakistan

    Nasim Ahmed, Syed Shan-e-Ali Zaidi, Imran Amin & Shahid Mansoor

  2. Department of Biotechnology, Pakistan Institute of Engineering & Applied Sciences (PIEAS) Nilore, Islamabad, Pakistan

    Nasim Ahmed & Syed Shan-e-Ali Zaidi

  3. Genomics and Bioinformatics Research Unit, 141 Experiment Station Rd, Stoneville, MS, 38776, USA

    Brian E. Scheffler

Authors
  1. Nasim Ahmed
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  2. Syed Shan-e-Ali Zaidi
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  3. Imran Amin
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  4. Brian E. Scheffler
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  5. Shahid Mansoor
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Correspondence to Shahid Mansoor.

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Ahmed, N., Zaidi, S.SeA., Amin, I. et al. Tomato leaf curl Oman virus and associated Betasatellite causing leaf curl disease in tomato in Pakistan. Eur J Plant Pathol 160, 249–257 (2021). https://doi.org/10.1007/s10658-021-02242-7

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  • DOI: https://doi.org/10.1007/s10658-021-02242-7

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