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Determination of the role of salicylic acid and Benzothiadiazole on physico-chemical alterations caused by Cucumber mosaic virus in tomato

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Abstract

Shoe-string disease caused by Cucumber mosaic virus (CMV) is one of the major threats to tomato production worldwide. The alteration in some biochemical parameters in leaves of the susceptible tomato genotype (Nagina) associated with CMV infection and the effect of exogenous application of salicylic acid (SA) and benzothiadiazole (BTH) were studied in this paper. Results showed that exogenous treatment with SA and BTH not only led to plants which gave significantly more yield than diseased controls (DC), but also delayed symptom expression and reduced disease severity. Analysis of biochemical parameters indicated that exogenous application of elicitors and viral infection, significantly affected the activity of peroxidase (POD), superoxide dismutase (SOD), catalase (CAT) and ascorbate peroxidase (APX). Compared to the DC plants, minimum disease severity and maximum number of fruit were recorded after a single dose of SA + BTH. Maximum plant height was recorded after weekly application of SA and maximum fruit yield per plant was gained with single dose of SA. Moreover, the activity of POD was significantly elicited many-fold after weekly application of SA + BTH, while higher amount of SOD was recorded with single dose of SA. The activity of CAT was also significantly accelerated after weekly application of SA + BTH while increased level of APX was noticed with single dose of BTH. In conclusion, the combined application of SA and BTH played an important role in induction of defense mechanism against CMV infection and can be useful in tomato disease management programs.

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References

  • Akhtar, K. P., Saleem, M. Y., Asghar, M., Ahmad, M., & Sarwar, N. (2010). Resistance of solanum species to cucumber mosaic virus sub group IA and its vector Myzus persicae. European Journal of Plant Pathology, 128, 435–450.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • An, C., & Mou, Z. (2011). Salicylic acid and its function in plant immunity. Journal of Integrative Plant Biology, 53, 412–428.

    Article  CAS  PubMed  Google Scholar 

  • Anfoka, G. H. (2000). Benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester induces systemic resistance in tomato (Lycopersicum esculentum mill cv. Vollendung) to cucumber mosaic virus. Crop Protection, 19, 401–405.

    Article  CAS  Google Scholar 

  • Bailly, C., Leymarie, J., Lehner, A., Rousseau, S., Côme, D., & Corbineau, F. (2004). Catalase activity and expression in developing sunflower seeds as related to drying. Journal of Experimental Botany, 55, 475–483.

    Article  CAS  PubMed  Google Scholar 

  • Baysal, O., Soylu, E. M., & Soylu, S. (2003). Induction of defense-related enzymes and resistance by the plant activator acibenzolar-S-methyl in tomato seedlings against bacterial canker caused by Clavibacter michiganensis. Plant Pathology, 52, 747–753.

    Article  CAS  Google Scholar 

  • Caverzan, A., Passaia, G., Rosa, S. B., Ribeiro, C. W., Lazzarotto, F., & Margis-Pinheiro, M. (2012). Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. Genetics and Molecular Biology, 35, 1011–1019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chance, M., & Maehly, A. C. (1955). Assay of catalases and peroxidases. Methods in Enzymology, 2, 764–817.

    Article  Google Scholar 

  • Dallagnol, L. J., Rodrigues, F. A., Martins, S. C. V., Cavatte, P. C., & DaMatta, F. M. (2011). Alterations on rice leaf physiology during infection by Bipolaris oryzae. Australasian Plant Pathology, 40, 360–365.

    Article  CAS  Google Scholar 

  • Debona, D., Rodrigues, F. Á., Rios, J. A., & Nascimento, K. J. T. (2012). Biochemical changes in the leaves of wheat plants infected by Pyricularia oryzae. Phytopathology, 102, 1121–1129.

    Article  CAS  PubMed  Google Scholar 

  • Dieng, H., Satho, T., Hassan, A. A., Aziz, A. T., Morales, R. E., Hamid, S. A., Miake, F., & Abubakar, S. (2011). Peroxidase activity after viral infection and whitefly infestation in juvenile and mature leaves of Solanum lycopersicum. Journal of Phytopathology, 159, 707–712.

    Article  CAS  Google Scholar 

  • Durrant, W. E., & Dong, X. (2004). Systemic acquired resistance. Annual Review of Phytopathology, 42, 185–209.

    Article  CAS  PubMed  Google Scholar 

  • El-Zahabi, H. M., Gullner, G., & Királi, Z. (1995). Effects of powdery mildew infection of barley on the ascorbate-glutathione cycle and other antioxidants in different host–pathogen interactions. Phytopathology, 85, 1225–1230.

    Article  Google Scholar 

  • Garcia-Arenal, F., & Palukaitis, P. (2008). Cucumber mosaic virus. In B. W. J. Mahy & M. H. V. van Regenmortel (Eds.), Encyclopedia of virology (3rd ed., pp. 614–619). San Diego: Elsevier- Academic Press.

    Chapter  Google Scholar 

  • Giovannucci, E. (1999). Tomatoes, tomato-based products, lycopene and cancer, review of the epidemiologic literature. Journal of the National Cancer Institute, 91, 317–331.

    Article  CAS  PubMed  Google Scholar 

  • Godard, J. F., Ziadi, S., Monot, C., Le Corre, D., & Silué, D. (1999). Benzothiadiazole (BTH) induces resistance in cauliflower (Brassica oleraceavarbotrytis) to downy mildew of crucifers caused by Peronosporaparasitica. Crop Protection, 18, 397–405.

    Article  CAS  Google Scholar 

  • Gondim, D. M. F., Terao, D., Martins-Miranda, A. S., Vasconcelos, I. M., & Oliveira, J. T. A. (2008). Benzo-thiadiazole-7-carbothioic acid S-methyl ester does not protect melon fruits against Fusarium pallidoroseum infection but induces defence responses in melon seedlings. Journal of Phytopathology, 156, 607–614.

    Article  CAS  Google Scholar 

  • Govrin, E. M., & Levine, A. (2000). The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology, 10, 751–757.

    Article  CAS  PubMed  Google Scholar 

  • Grudkowska, M., & Zagdańska, B. (2004). Multifunctional role of plant cysteine proteinases. Acta Biochimica Polonica, 51, 609–624.

    CAS  PubMed  Google Scholar 

  • Hameed, A., & Iqbal, N. (2014). Chemo-priming with mannose, mannitol and H2O2 mitigate drought stress in wheat. Cereal Research Communications, 42, 450–462.

    Article  CAS  Google Scholar 

  • Hameed, A., Bibi, N., Akhter, J., & Iqbal, N. (2011). Differential changes in antioxidants, proteases, and lipid peroxidation in flag leaves of wheat genotypes under different levels of water deficit conditions. Review of Plant Physiology and Biochemistry, 49, 178–185.

    Article  CAS  Google Scholar 

  • Hameed, S., Akhtar, K. P., Hameed, A., Gulzar, T., Kiran, S., Yousaf, S., Abbas, G., Asghar, M. J., & Sarwar, N. (2017). Biochemical changes in the leaves of mungbean (Vigna radiata) plants infected by phytoplasma. Turkish Journal of Biochemistry. https://doi.org/10.1515/tjb-2016-0304.

  • Heil, M., Hilpert, A., Kaiser, W., & Linsenmair, K. E. (2000). Reduced growth and seed set following chemical induction of pathogen defence: does systemic acquired resistance (SAR) incur allocation costs? Journal of Ecology, 88, 645–654.

    Article  CAS  Google Scholar 

  • Junqueira, A., Bedendo, I., & Pascholati, S. (2004). Biochemical changes in corn plants infected by the maize bushy stunt phytoplasma. Physiological and Molecular Plant Pathology, 65, 181–185.

    Article  CAS  Google Scholar 

  • Kalogirou, M. (2012). Antiviral and quality effects of chemical elicitors and Cucumber mosaic virus (CMV) infection on tomato plants and fruits. PhD thesis. Cranfield University, UK.

  • Kazmi, M. (2014). Effect of foliar application with salicylic acid and methyl jasmonate on growth, flowering, yield and fruit quality of tomato. Bulletin of Environment, Pharmacology and Life Sciences, 3, 154–158.

    Google Scholar 

  • Khan, N. A. (2010). Application of salicylic acid increase contents of nutrients and antioxidative metabolism in mungbean and alleviated adverse effects of salinity stress. International Journal of Plant Biology, 1, 1–8.

    Article  CAS  Google Scholar 

  • Kim, C. H., & Palukaitis, P. (1997). The plant defense response to cucumber mosaic virus in cowpea is elicited by the viral polymerase gene and affects virus accumulation in single cells. European Molecular Biology Organization Journal, 16, 4060–4068.

    Article  CAS  Google Scholar 

  • Kiraly, Z., Barna, B., Kecskes, A., & Fodor, J. (2002). Down regulation of antioxidative capacity in a transgenic tobacco, which fails to develop acquired resistance to necrotization caused by tobacco mosaic virus. Free Radical Research, 36, 981–991.

    Article  CAS  PubMed  Google Scholar 

  • Kundu, S., Chakraborty, D., & Pal, A. (2011). Proteomic analysis of salicylic acid induced resistance to Mungbean yellow mosaic India virus in Vigna mungo. Journal of Proteomics, 74, 337–349.

    Article  CAS  PubMed  Google Scholar 

  • Kyriakopoulou, P. E., Perdikis, D. C. H., Sclavounos, A. P., Girgis, S. M., Lykouressis, D. P., Tsitsipis, J. A., & Christakis, P. A. (2000). Cucumber mosaic cucumovirus incidence in open-field tomato in the Olympia area and trap captures of alate aphids. Bulletin OEPP/EPPO, 30, 305–315.

    Article  Google Scholar 

  • Lawton, K., Friedrich, L., Hunt, M., Weymann, K., Delaney, T., Kessmann, H., Staub, T., & Ryals, J. (1996). Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant Journal, 10, 71–82.

    Article  CAS  PubMed  Google Scholar 

  • Leonardi, C., Ambrosino, P., Esposito, F., & Fogliano, V. (2000). Antioxidant activity and carotenoid and tomatine contents in different typologies of fresh 'consumption tomatoes. Journal of Agricultural and Food Chemistry, 48, 4723–4727.

    Article  CAS  PubMed  Google Scholar 

  • Magbanua, Z. V., De Moraes, C. M., Brooks, T. D., Williams, W. P., & Luthe, D. S. (2007). Is catalase activity one of the factors associated with maize resistance to Aspergillus flavus? Molecular Plant-Microbe Interactions, 20, 697–706.

    Article  CAS  PubMed  Google Scholar 

  • Maksimov, I., Troshina, N., Surina, O., & Cherepanova, E. (2014). Salicylic acid increases the defense reaction against bunt and smut pathogens in wheat calli. Journal of Plant Interactions, 9, 306–314.

    Article  CAS  Google Scholar 

  • Malamy, J., Carr, J. P., Klessig, D. F., & Raskin, I. (1990). Salicylic acid-a likely endogenous signal in the resistance response of tobacco to viral infection. Science, 250, 1002–1004.

    Article  CAS  PubMed  Google Scholar 

  • Mayers, C. N., Lee, K., Moore, C. A., Wong, S., & Carr, J. P. (2005). Salicylic acid-induced resistance to cucumber mosaic virus in squash and arabidopsis thaliana: contrasting mechanisms of induction and antiviral action. Molecular Plant-Microbe Interactions, 18, 428–434.

    Article  CAS  PubMed  Google Scholar 

  • Mydlarz, L. D., & Harvell, C. D. (2006). Peroxidase activity and inducibility in the see fan coral exposed to a fungal pathogen. Comparative Biochemistry and Physiology, 10, 1016.

    Google Scholar 

  • Nasir, F., Akhtar, K. P., Hameed, A., Yousaf, S., Gulzar, T., Sarwar, N., Shah, T. M., & Kiran, S. (2017). Biochemical alterations in the leaves of different desi and Kabuli type chickpea genotypes infected by phytoplasma. Turkish Journal of Biochemistry. https://doi.org/10.1515/tjb-2016-0177.

  • Nischwitz, C., Csinos, A. S., Mullis, S. W., Hickman, L. L., Stevenson, K. L., & Gitaitis, R. D. (2008). Effect of transplant age, tobacco cultivar Acibenzolar S-methyl, and imidacloprid on tomato spotted wilt infection in flue-cured tobacco. Plant Disease, 92, 1524–1528.

    Article  CAS  Google Scholar 

  • Palma, J. M., Sandalio, L. M., Corpas, F. J., Romero-Puertas, M. C., McCarthy, I., & del Río, L. A. (2002). Plant proteases, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiology and Biochemistry, 40, 521–530.

    Article  CAS  Google Scholar 

  • Palukaitis, P., & García-Arenal, F. (2003). Cucumoviruses. Advances in Virus Research, 62, 241–323.

    Article  CAS  PubMed  Google Scholar 

  • Palukaitis, P., Roossinck, M. J., Dietzgen, R. G., & Francki, R. I. B. (1992). Cucumber mosaic virus. Advances in Virus Research, 41, 281–348.

    Article  CAS  PubMed  Google Scholar 

  • Pignocchi, C., Fletcher, J. M., Wilkinson, J. E., Barnes, J. D., & Foyer, C. H. (2003). The function of ascorbate oxidase in tobacco. Plant Physiology, 132, 1631–1641.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riedle-Bauer, M. (2000). Role of reactive oxygen species and antioxidant enzymes in systemic virus infections of plants. Journal of Phytopathology, 148, 297–302.

    Article  CAS  Google Scholar 

  • Roossinck, M. J. (2002). Evolutionary history of cucumber mosaic virus deduced by phylogenetic analyses. Journal of Virology, 76, 3382–3387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saleem, M. Y., Akhtar, K. P., Iqbal, Q., Asghar, M., Hameed, A., & Shoaib, M. (2016). Development of tomato hybrids with multiple disease tolerance. Pakistan Journal of Botany, 48, 771–778.

    CAS  Google Scholar 

  • Sekine, K. T., Nandi, A., Ishihara, T., Hase, S., Ikegami, M., Shah, J., & Takahashi, H. (2004). Enhanced resistance to cucumber mosaic virus in the Arabidopsis Thaliana ssi2 mutant is mediated via an SA-independent mechanism. Molecular Plant-Microbe Interactions, 17, 623–632.

    Article  CAS  PubMed  Google Scholar 

  • Shahzadi, H., Sheikh, M. A., Hameed, A., Jamil, A., & Rehman, S. U. (2015). Comparative antioxidant potential and bioactivity of maize (Zea mays) ear tissues from different genotypes. International Journal of Agriculture and Biology, 17, 539–546.

    Article  CAS  Google Scholar 

  • Siddique, Z., Akhtar, K. P., Hameed, A., Sarwar, N., Ul-Haq, I., & Khan, S. A. (2014). Biochemical alterations in leaves of resistant and susceptible cotton genotypes infected systemically by cotton leaf curl Burewala virus. Journal of Plant Interactions, 9, 702–711.

    Article  Google Scholar 

  • Siddique, Z., Akhtar, K. P., Hameed, A., Ul-Haq, I., Ashraf, M. Y., Sarwar, N., & Khan, M. K. R. (2015). Physiological response of cotton leaf curl Burewala virus-infected plants of tolerant and susceptible genotypes of different gossypium species. Journal of Plant Pathology, 97, 1–8.

    Google Scholar 

  • Smith-Becker, J., Keena, N. T., & Becker, J. O. (2003). Acibenzolar-S-methyl induces resistance to Colletotrichum lagenarium and Cucumber mosaic virus in cantaloupe. Crop Protection, 22, 769–774.

    Article  CAS  Google Scholar 

  • Song, X., Wang, Y., Mao, W., Shi, K., Zhou, Y., Nogue, S., & Yu, J. (2009). Effects of cucumber mosaic virus infection on electron transport and antioxidant system in chloroplasts and mitochondria of cucumber and tomato leaves. Physiologia Plantarum, 135, 246–257.

    Article  CAS  PubMed  Google Scholar 

  • Sticher, L., Mauch-Mani, B., & Metraux, J. P. (1997). Systemic acquired resistance. Annual Review of Phytopathology, 35, 235–270.

    Article  CAS  PubMed  Google Scholar 

  • Sulman, M., Fox, G., Osman, A., Inkerman, A., Williams, P., & Michalowitz, M. (2001). Relationship between total peroxidase activity and susceptibility to black point in mature grain of some barley cultivars. Proceeding of the 10th Australian barley technical symposium. Canberra, ACT, Australia, 16–20 Sep. 2001. http://www.regional.org.au/au/abts/2001/t4/sulman.htm.

  • Trejo-Saavedra, D. L., Garcia-Neria, M. A., & Rivera-Bustamante, R. F. (2013). Benzothiadiazole (BTH) induces resistance to pepper golden mosaic virus (PepGMV) in pepper (Capsicum annuum L.) Biological Research, 46, 333–340.

    Article  CAS  PubMed  Google Scholar 

  • Vallad, G. E., & Goodman, R. M. (2004). Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Science, 44, 1920–1934.

    Article  Google Scholar 

  • Vlot, A. C., Dempsey, D. A., & Klessig, D. F. (2009). Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology, 47, 177–206.

    Article  CAS  PubMed  Google Scholar 

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Sabir Tariq, R.M., Akhtar, K.P., Hameed, A. et al. Determination of the role of salicylic acid and Benzothiadiazole on physico-chemical alterations caused by Cucumber mosaic virus in tomato. Eur J Plant Pathol 150, 911–922 (2018). https://doi.org/10.1007/s10658-017-1332-4

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