Abstract
Tomato mosaic virus (ToMV) is a consistent problem threatening tomato production worldwide, including Pakistan. In this paper, we report characterization of a ToMV strain from naturally infected tomato in Pakistan and response of 128 diverse tomato genotypes to identify potential resistance sources in Solanum and its related wild species that can be incorporated into breeding programs. Upon ToMV inoculation, local necrotic lesion developed within 1 wk on plants of Nicotiana tabacum var. xanthi, N. tabacum var. glutinosa, Chenopodium album and Datura alba except N. tabacum var. K-399 which showed systemic mosaic symptoms. Coat protein (CP) sequence of ToMV strain (GenBank accession No. MG975645) in present study showed a high level of similarity with the sequence of different ToMV strains submitted in GenBank NCBI. Of 128 tomato genotypes inoculated with ToMV-Pak in controlled conditions, 13 were highly resistant, three resistant, 24 tolerant, 62 susceptible and 26 highly susceptible against ToMV. Among highly resistant germplasm, one genotype (LO6170 with unknown ToMV-resistant gene) and 11 genotypes with ToMV-resistant gene (Tm-22) belonged to cultivated Solanum lycopersicum whereas one genotype (LA0111) belonged to the wild species, S. arcanum. Presence of Tm-22 in the 11 highly resistant genotypes was confirmed using CAPS marker in PCR. Of resistant genetic resources, LB2 belonged to S. lycopersicum, LO6122 to S. arcanum and LO4166 belonged to S. pimpinellifolium. Presence or absence of ToMV in all the tested genotypes plants was confirmed using ELISA and its absence in symptomless highly resistant genotypes with negative ELISA results were further confirmed using RT-PCR. Resistant genotypes of S. lycopersicum identified in the present study can be easily used for heterosis and recombination breeding aiming to develop high yielding and ToMV tolerant cultivars. However, wild genotypes resistant to ToMV can be used in a wide hybridization breeding programme with cultivated S. lycopersicum keeping in view the genetic barriers and appropriate pattern of crossing.
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References
Adams, M. J., Heinze, C., Jackson, A. O., Kreuze, J. F., Macfarlane, S. A., & Torrance, L. (2012). Virgaviridae. In A. M. O. King, E. Lefkowitz, M. J. Adams, & E. B. Carstens (Eds.), Virus taxonomy: Ninth report of the international committee on taxonomy of viruses (pp. 1139–1162). London: Elsevier/Academic Press.
Akhtar, K. P., Saleem, M. Y., Asghar, M., Ahmad, M., & Sarwar, N. (2010). Resistance of Solanum species to cucumber mosaic virus subgroup IA and its vector Myzus persicae. Eurpean Journal of Plant Pathology, 128, 435–450.
Akhtar, K. P., Saleem, M. Y., Iqbal, Q., Asghar, M., Hameed, A., & Sarwar, N. (2016). Evaluation of tomato genotypes for late blight resistance using low tunnel assay. Journal of Plant Pathology, 98, 421–428.
Alexander, L. J. (1971). Host pathogen dynamics of Tobacco mosaic virus on tomato. Phytopathology, 61(61), 1–617.
Aramburu, J., & Galipienso, L. (2005). First report in Spain of a variant of tomato mosaic virus (ToMV) overcoming the tm-22 resistance gene in tomato (Lycopersicon esculentum). Plant Pathology, 54, 566–566.
Aslam, M. Q., Akhtar, K. P., Saleem, M. Y., Sarwar, N., & Yousaf, S. (2017). Association of chili leaf curl betasatellite with tomato leaf curl disease. Journal of General Plant Pathology, 83(6), 402–405.
Azizi, A., Mozafari, J., & Shams-bakhsh, M. (2008). Phenotypic and molecular screening of tomato germplasm for resistance to tomato yellow leaf curl virus. Iranian Journal of Biotechnology, 6(4), 199–206.
Buchen-Osmond, C. (2006). ICTVdB—The universal virus database, version 4. New York: Columbia University.
Chitra, T. R., Prakash, H. S., Albrechtsen, S. E., Shetty, H. S., & Mathur, S. B. (1999). Infection of tomato and bell pepper by ToMV and TMV at different growth stages and establishment of virus in seeds. Journal of Plant Pathology, 81, 123–126.
Chitra, T. R., Prakash, H. S., Albrechtsen, S. E., Shetty, H. S., & Mathur, S. B. (2002). Indexing of leaf and seed samples of tomato and bell pepper for tobamoviruses. Indian Phytopathology, 55, 84–86.
Clark, M. F., & Adams, A. N. (1977). Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology, 34, 475–483.
Dax, E., Livneh, O., Aliskevicius, E., Edelbaum, O., Kedar, N., Gavish, N., Milo, J., Geffen, F., Blumenthal, A., Rabinowich, H. D., & Sela, I. (1998). A SCAR marker linked to the ToMV resistance gene, Tm2(2), in tomato. Euphytica., 101, 73–77.
Di Candilo, M., Faccioli, G., Grassi, G., Faeti, V. (1992). Effect of tomato mosaic virus (ToMV) on yield of machine-harvested processing tomatoes. Phytopathologia Mediterranea, 32–36.
Doyle, J. J. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical bulletin, 19, 11–15.
Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
Goyal, A., Maheshwari, P. (2012). Accurate diagnosis of a plant disease and its pathogen is the first crucial step for its management. 1:116–136.
Hall, T. J. (1980). Resistance at the tm-2 locus in the tomato to tomato mosaic virus. Euphytica, 29, 189–197.
Hameed, A., Saleem, M. Y., Akhtar, K. P., Shoaib, M., Iqbal, Q., & Asghar, M. (2017). Molecular confirmation of intraspecific tomato (Solanum lycopersicum) hybrids and their evaluation against late blight and cucumber mosaic virus. Molecular Biotechnology, 59, 234–240.
Hanssen, I. M., Lapidot, M., & Thomma, B. P. (2010). Emerging viral diseases of tomato crops. Molecular Plan-Microbe Interaction, 23(5), 539–548.
Hoon, P. K., & Jin, C. B. (2002). Detection of TMV, ToMV and CMV from tomato seeds and plants. Research in Plant Disease, 8, 101–106.
Ishibashi, K., Mawatari, N., Miyashita, S., Kishino, H., Meshi, T., & Ishikawa, M. (2012). Coevolution and hierarchical interactions of tomato mosaic virus and the resistance gene tm-1. PLoS Pathogen, 8(10), e1002975.
Khan, I. A. (1997). Occurrence, distribution, host range, symptomatology and purification of ToMV on tomato. Pakistan Journal of Zoology, 29, 385–389.
King, A.M., Adams, M.J., Lefkowitz, E.J., Carstens, E.B. (2011). Virus taxonomy: IXth report of the international committee on taxonomy of viruses.
Kumar, S., Udaya, Shankar, A. C., Nayaka, S. C., Lund, O. S., & Prakash, H. S. (2011). Detection of tobacco mosaic virus and tomato mosaic virus in pepper and tomato by multiplex RT–PCR. Letters in Applied Microbiology, 53(3), 359–363.
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.
Kuria, P., Ilyas, M., Ateka, E., Miano, D., Onguso, J., Carrington, J. C., & Taylor, N. J. (2017). Differential response of cassava genotypes to infection by cassava mosaic geminiviruses. Virus Research, 227, 69–81.
Lacroix, C., Renner, K., Cole, E., Seabloom, E. W., Borer, E. T., & Malmstrom, C. M. (2016). Methodological guidelines for accurate detection of viruses in wild plant species. Applied and Environmental Microbiology, 82, 1966–1975.
Lanfermeijer, F. C., Dijkhuis, J., Sturre, M. J., de Haan, P., & Hille, J. (2003). Cloning and characterization of the durable tomato mosaic virus resistance gene tm-2 2 from Lycopersicon esculentum. Plant Molecular Biology, 52(5), 1039–1051.
Lapidot, M., Friedmann, M., Lachman, O., Yehezkel, A., Nahon, S., Cohen, S., & Pilowsky, M. (1997). Comparison of resistance level to tomato yellow leaf curl virus among commercial cultivars and breeding lines. Plant Disease., 81, 1425–1428.
Luria, N., Smith, E., Reingold, V., Bekelman, I., Lapidot, M., Levin, I., Elad, N., Tam, Y., Sela, N., Abu-Ras, A., & Ezra, N. (2017). A new Israeli Tobamovirus isolate infects tomato plants harboring tm-22 resistance genes. PLoS One, 12(1), e0170429.
Mansoor, S., Amin, I., Iram, S., Hussain, M., Zafar, Y., Malik, K. A., & Briddon, R. W. (2003). Breakdown of resistance in cotton to cotton leaf curl disease in Pakistan. Plant Pathology, 52, 784.
Motoyoshi, F., & Oshima, N. (1977). Expression of genetically controlled resistance to tobacco mosaic virus infection in isolated tomato leaf mesophyll protoplasts. Journal of General Virology, 34, 499–506.
Nono-Womdim, R., Swai, I. S., Green, S. K., Gebre-Selassie, K., Laterrot, H., Marchoux, G., & Opena, R. T. (1996). Tomato viruses in Tanzania: Identification, distribution and disease incidence. J. S. Afr. Soc. Hort. Scie., 61, 41–44.
Ohmori, T., Murata, M., & Motoyoshi, F. (1996). Molecular characterization of RAPD and SCAR markers linked to the tm-1 locus in tomato. Theoretical and Applied Genetics, 92, 151–156
Otieno, E. A. (1985). Identification of tomato mosaic strain of Tobacco mosaic virus (TMV) and its effects on yield of tomato (Lycopersicon esculentum) varieties moneymaker and Roma-vf in kenya. Journal of Agriculture and Environment, 3, 56–58.
Panthee, D. R., Brown, A. F., Yousef, G. G., Ibrahem, R., & Anderson, C. (2013). Novel molecular marker associated with T m2a gene conferring resistance to tomato mosaic virus in tomato. Plant Breeding, 132(4), 413–416.
Pelham, J. (1966). Resistance in tomato to tobacco mosaic virus. Euphytica, 15, 258–267.
Pelham, J. (1972). Strain-genotype interaction of tobacco mosaic virus in tomato. Annals of Applied Biology, 71, 219–228.
Pfitzner, A.J. (2006). Resistance to tobacco mosaic virus and tomato mosaic virus in tomato. In Natural Resistance Mechanisms of Plants to Viruses. 399–413.
Pico, B., Díez, M. J., & Nuez, F. (1999). Improved diagnostic techniques for tomato yellow leaf curl virus in tomato breeding programs. Plant diseas, 83(11), 1006–1012.
Shi, A., Vierling, R., Grazzini, R., Chen, P., Caton, H., & Panthee, D. (2011). Molecular markers for tm-2 alleles of tomato mosaic virus resistance in tomato. American Journal of Plant Sciences, 2(2), 180–189.
Smith, S., & Murakishi, H. H. (1993). Restricted virus multiplication and movement of tomato mosaic virus in resistant tomato somaclones. Plant Science, 89, 113–122.
Strange, R. N., & Scott, P. R. (2005). Plant disease: A threat to global food security. Phytopathology, 43, 83–116.
Strasser, M., & Pfitzner, A. J. P. (2007). The double-resistance-breaking tomato mosaic virus strain ToMV1-2 contains two independent single resistance-breaking domains. Archives of Virology, 152, 903–914.
Tanwir, F. (2012). Analysis of the structure of Tomato mosaic virus movement protein based on virus host interactions. PhD Thesis.
Tariq, R.M.S., Akhtar, K.P., Hameed, A., Ullah, N., Saleem, M.Y. Haq, I. (2018). Determination of the role of salicylic acid and Benzothiadiazole on physico-chemical alterations caused by cucumber mosaic virus in tomato. Eurpean Journal of Plant Pathology, 1–12.
Ullah, N., Ali, A., Ahmad, M., Fahim, M., Din, N., & Ahmad, F. (2017). Evaluation of tomato germplasm for the source of resistance against tomato mosaic virus (ToMV) and effect of the virus on yield contributing parameters. Pakistan Journal of Botany, 49(4), 1585–1592.
Varshney, R. K., Graner, A., & Sorrells, M. E. (2005). Genomics-assisted breeding for crop improvement. Trends in Plant Science, 10(12), 621–630.
Weber, H., & Pfitzner, A. J. (1998). Tm-22 resistance in tomato requires recognition of the carboxy terminus of the movement protein of tomato mosaic virus. Molecular Plant-Microbe Interactions, 11(6), 498–503.
Weber, H., Ohnesorge, S., Silber, M. V., & Pfitzner, A. J. (2004). The tomato mosaic virus 30 kDa movement protein interacts differentially with the resistance genes tm-2 and tm-2(2). Archives of Virology, 149, 1499–1514.
Yamaji, Y., Maejima, K., Komatsu, K., Shiraishi, T., Okano, Y., Himeno, M., Sugawara, K., Neriya, Y., Minato, N., Miura, C., & Hashimoto, M. (2012). Lectin-mediated resistance impairs plant virus infection at the cellular level. Plant Cell, 24, 778–793.
Yazdani-Khameneh, S., Hamedi, A., Farahani, A. A., Hashemi, S., Golnaraghi, A. R., & Rakhshandehroo, F. (2013). Tomato mosaic virus on cucumber and potato in Iran. Journal of Plant Pathology, 95(3), 659–668.
Yu, C., Hu, D., Dong, J., Cui, X., Wu, J., Yu, J., & Zhou, X. (2004). The symptom difference induced by tobacco mosaic virus and tomato mosaic virus in tobacco plants containing the N gene is determined by movement protein gene. Science in China Series C: Life Sciences, 47(6), 503–509.
Zhang, H., Zhao, J., Liu, S., Zhang, D. P., & Liu, L. (2013). Tm-22 confers different resistance responses against tobacco mosaic virus dependent on its expression level. Molecular Plant, 6, 971–974.
Zhao, J., Liu, Q., Zhang, H., Jia, Q., & Hong, L. Y. (2013). The Rubisco small subunit is involved in Tobamovirus movement and tm-22-mediated extreme resistance. Plant Physiology, 161, 374–383.
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Ullah, N., Akhtar, K.P., Saleem, M.Y. et al. Characterization of tomato mosaic virus and search for its resistance in Solanum species. Eur J Plant Pathol 155, 1195–1209 (2019). https://doi.org/10.1007/s10658-019-01848-2
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DOI: https://doi.org/10.1007/s10658-019-01848-2