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Protective role of S-methylmethionine-salicylate in maize plants infected with Maize dwarf mosaic virus

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Abstract

This study aimed to detect the harmful effects of Maize dwarf mosaic virus (MDMV) infection, and to demonstrate the potential benefits of S-methylmethionine-salicylate (MMS) pretreatment in infected maize (Zea mays L.) plants. The results of chlorophyll a fluorescence measurements showed that in MDMV-infected plants additional quenchers of fluorescence appear, probably as the result of associations between the virus coat protein and thylakoid membranes. It is important to note that when infected plants were pretreated with MMS, such associations were not formed. MDMV infection and MMS pretreatment resulted in a decrease in ascorbate peroxidase (APX) activity in maize leaves, while infection contributed to an increase in activity in the roots. Infection raised the guaiacol peroxidase (GPX) enzyme activity level, which was reduced by MMS pretreatment. MMS contributed to a decrease in both the RNA and coat protein content of MDMV, to an equal extent in maize leaves and roots. The results showed that MMS pretreatment enhanced the stress response reactions against MDMV infection in maize plants and retarded the spreading of infection.

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References

  • Amako, K., Chen, G.-X., & Asada, K. (1994). Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isoenzymes of ascorbate peroxidase in plants. Plant and Cell Physiology, 35, 497–504.

    CAS  Google Scholar 

  • Antoniw, J. F., & White, R. F. (1980). The effects of aspirin and polyacrylic acid on soluble leaf proteins and resistance to virus infection in five cultivars of tobacco. Journal of Phytopathology, 98, 331–341.

    Article  CAS  Google Scholar 

  • Asada, K. (1996). Radical production and scavenging in the chloroplasts. In N. R. Baker (Ed.), Photosynthesis and the environment (pp. 123–150). Dordrecht: Kluwer Academic Publishers.

    Google Scholar 

  • Baker, N. R. (2008). Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology, 59, 89–113.

    Article  CAS  PubMed  Google Scholar 

  • Balachandran, S., Osmond, C. B., & Daley, P. F. (1994). Diagnosis of the earliest strain-specific interactions between tobacco mosaic virus and chloroplasts of tobacco leaves in vivo by means of chlorophyll fluorescence imaging. Plant Physiology, 104, 1059–1065.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balaji, B., Bucholtz, D. B., & Anderson, J. M. (2003). Barley yellow dwarf virus and Cereal yellow dwarf virus quantification by real-time polymerase chain reaction in resistant and susceptible plants. Phytopathology, 93, 1386–1392.

    Article  CAS  PubMed  Google Scholar 

  • Beddard, G. S., & Porter, G. (1976). Concentration quenching in chlorophyll. Nature, 260, 366–367.

    Article  CAS  Google Scholar 

  • Belkhodja, R., Morales, F., Sanz, M., Abadía, A., & Abadía, J. (1998). Iron deficiency in peach trees: Effects on leaf chlorophyll and nutrient concentrations in flowers and leaves. Plant and Soil, 203, 257–268.

    Article  CAS  Google Scholar 

  • Bi, Y.-M., Kenton, P., Mur, L., Darby, R., & Draper, J. (1995). Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. The Plant Journal, 8, 235–245.

    Article  CAS  PubMed  Google Scholar 

  • Cassone, B. J., Chen, Z., Chiera, J., Stewart, L. R., & Redinbaugh, M. G. (2014). Responses of highly resistant and susceptible maize to vascular puncture inoculation with Maize dwarf mosaic virus. Physiological and Molecular Plant Pathology, 86, 19–27.

    Article  CAS  Google Scholar 

  • Chen, S., Das, P., & Hari, V. (1994). In situ localization of ATPase activity in cells of plants infected by maize dwarf mosaic potyvirus. Archives of Virology, 134, 433–439.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Conrath, U., Chen, Z., Ricigliano, J. R., & Klessig, D. F. (1995). Two inducers of plant defence responses, 2,6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proceedings of the National Academy of Sciences USA, 92, 7143–7147.

    Article  CAS  Google Scholar 

  • D’Ambrosio, N., Guadagno, C.R., & Virzo De Santo, A. (2008). Is qE always the major component of non-photochemical quenching? In J. F. Allen, E. Gantt, J. H. Golbeck, B. Osmond (eds). Photosynthesis energy from the sun: 14th International Congress on Photosynthesis. (pp. 1001–1004). Netherlands: Springer.

  • Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Ward, E., & Ryals, J. (1994). A central role of salicylic acid in plant disease resistance. Science, 266, 1247–1250.

    Article  CAS  PubMed  Google Scholar 

  • Dodd, I. C., Critchley, C., Woodall, G. S., & Stewart, G. R. (1998). Photoinhibition in differently coloured juvenile leaves of Syzygium species. Journal of Experimental Botany, 49, 1437–1445.

    Article  CAS  Google Scholar 

  • Durner, J., & Klessig, D. F. (1995). Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proceedings of the National Academy of Sciences USA, 92, 11312–11316.

    Article  CAS  Google Scholar 

  • Fodor, J., Gullner, G., Adam, A. L., Barna, B., Komives, T., & Kiraly, Z. (1997). Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco (role in systemic acquired resistance). Plant Physiology, 114, 1443–1451.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fryer, M. J., Andrews, J. R., Oxborough, K., Blowers, D. A., & Baker, N. R. (1998). Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves in maize in the field during periods of low temperature. Plant Physiology, 116, 571–580.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gates, D. W., & Gudauskas, R. T. (1969). Photosynthesis, respiration and evidence of a metabolic inhibitor in corn infected with maize dwarf mosaic virus. Phytopathology, 59, 575–580.

    CAS  Google Scholar 

  • Gell, G., Balázs, E., & Petrik, K. (2010). Genetic diversity of Hungarian maize dwarf mosaic virus isolates. Virus Genes, 40, 277–281.

    Article  CAS  PubMed  Google Scholar 

  • Hammond, J. (1998). Serological relationship between the cylindrical inclusion proteins of potyviruses. Phytopathology, 88, 965–971.

    Article  CAS  PubMed  Google Scholar 

  • Hodgson, R. A. J., Beachy, R. N., & Pakrasi, H. B. (1989). Selective inhibition of photosystem II in spinach by tobacco mosaic virus: An effect of the viral coat protein. The Federation of European Biochemical Societies, 245, 267–270.

    Article  CAS  Google Scholar 

  • Horton, P. (2012). Optimization of light harvesting and photoprotection: Molecular mechanisms and physiological consequences. Philosophical Transactions of the Royal Society, B: Biological Sciences, 367, 3455–3465.

    Article  CAS  PubMed Central  Google Scholar 

  • Kang, H.-M., & Saltveit, M. E. (2002). Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiologia Plantarum, 115, 571–576.

    Article  CAS  PubMed  Google Scholar 

  • Kingston-Smith, A. H., & Foyer, C. H. (2000). Bundle sheath proteins are more sensitive to oxidative damage than those of the mesophyll in maize leaves exposed to paraquat or low temperatures. Journal of Experimental Botany, 51, 123–130.

    Article  CAS  PubMed  Google Scholar 

  • Kiss, A. Z., Ruban, A. V., & Horton, P. (2008). The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. Journal of Biological Chemistry, 283, 3972–3978.

    Article  CAS  PubMed  Google Scholar 

  • Ko, S., Eliot, A. C., & Kirsch, I. F. (2004). S-methylmethionine is both a substrate and an inactivator of 1-aminocyclopropane-1-carboxylate synthase. Archives of Biochemistry and Biophysics, 421, 85–90.

    Article  CAS  PubMed  Google Scholar 

  • López-Fabuel, I., Wetzel, T., Bertolini, E., Bassler, A., Vidal, E., Torres, L. B., Yuste, A., & Olmos, A. (2013). Real-time multiplex RT-PCR for the simultaneous detection of the five main grapevine viruses. Journal of Virological Methods, 188, 21–24.

    Article  PubMed  Google Scholar 

  • Ludmerszki, E., Almási, A., Rácz, I., Szigeti, Z., Solti, Á., Oláh, C., & Rudnóy, S. (2015). S-methylmethionine contributes to enhanced defense against Maize dwarf mosaic virus infection in maize. Brazilian Journal of Botany, 38, 771–782.

    Article  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 

  • Mateo, A., Funck, D., Mühlenbock, P., Kular, B., Mullineaux, P. M., & Karpinski, S. (2006). Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. Journal of Experimental Botany, 57, 1795–1807.

    Article  CAS  PubMed  Google Scholar 

  • Mayhew, D. E., & Ford, R. E. (1974). Detection of ribonuclease-resistant RNA in chloroplasts of corn leaf tissue infected with maize dwarf mosaic virus. Virology, 57, 503–509.

    Article  PubMed  Google Scholar 

  • Métraux, J. P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W., & Inverardi, B. (1990). Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science, 250, 1004–1006.

    Article  PubMed  Google Scholar 

  • Mittler, R., Feng, X., & Cohen, M. (1998). Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell, 10, 461–473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moharekar, S. T., Lokhande, S. D., Hara, T., Tanaka, R., Tanaka, A., & Chavan, P. D. (2003). Effect of salicylic acid on chlorophyll and carotenoid contents of wheat and moong seedlings. Photosynthetica, 41, 315–317.

    Article  CAS  Google Scholar 

  • Murry, L. E., Elliott, L. G., Capitant, S. A., West, J. A., Hanson, K. K., Scarafia, L., Johnston, S., DeLuca-Flaherty, C., Nichols, S., Cunanan, D., Dietrich, P. S., Mettler, I. J., Dewald, S., Warnick, D. A., Rhodes, C., Sinibaldi, R. M., & Brunke, K. J. (1993). Transgenic corn plants expressing MDMV strain B coat protein are resistant to mixed infections of maize dwarf mosaic virus and maize chlorotic mottle virus. Nature Biotechnology, 11, 1559–1564.

    Article  CAS  Google Scholar 

  • Musetti, R., Bruni, L., & Favali, M. A. (2002). Cytological modifications in maize plants infected by barley yellow dwarf virus and maize dwarf mosaic virus. Micron, 33, 681–686.

    Article  CAS  PubMed  Google Scholar 

  • Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22, 867–880.

    CAS  Google Scholar 

  • Oertel, U., Schubert, J., & Fuchs, E. (1997). Sequence comparison of the 3′-terminal parts of the RNA of four German isolates of sugarcane mosaic potyvirus (SCMV). Archives of Virology, 142, 675–687.

    Article  CAS  PubMed  Google Scholar 

  • Osbourn, J. K., Sarkar, S., & Wilson, T. M. A. (1990). Complementation of coat protein-defective TMV mutants in transgenic tobacco plants expressing TMV coat protein. Virology, 179, 921–925.

    Article  CAS  PubMed  Google Scholar 

  • Páldi, K., Rácz, I., Szigeti, Z., & Rudnóy, S. (2014). S-methylmethionine alleviates the cold stress by protection of the photosynthetic apparatus and stimulation of the phenylpropanoid pathway. Biologia Plantarum, 58, 189–194.

    Article  Google Scholar 

  • Rácz, I., Páldi, E., Szalai, G., Janda, T., Pál, M., & Lásztity, D. (2008). S-methylmethionine reduces cell membrane damage in higher plants exposed to low-temperature stress. Journal of Plant Physiology, 165, 1483–1490.

    Article  PubMed  Google Scholar 

  • Ranocha, P., McNeil, S. D., Ziemak, M. J., Li, C., Tarczynski, M. C., & Hanson, A. D. (2001). The S-methylmethionine cycle in angiosperms: Ubiquity, antiquity and activity. The Plant Journal, 25, 575–584.

    Article  CAS  PubMed  Google Scholar 

  • Rao, M. V., Paliyath, G., Ormrod, D. P., Murr, D. P., & Watkins, C. B. (1997). Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes (salicylic acid-mediated oxidative damage requires H2O2). Plant Physiology, 115, 137–149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raskin, I. (1992). Role of salicylic acid in plants. Annual Review of Plant Physiology, 43, 439–463.

    Article  CAS  Google Scholar 

  • Reneiro, A., & Beachy, R. N. (1986). Association of TMV coat protein with chloroplast membranes in virus-infected leaves. Plant Molecular Biology, 6, 291–301.

    Article  Google Scholar 

  • Shaw, J. G., Plaskitt, K. A., & Wilson, T. M. A. (1986). Evidence that tobacco mosaic virus particles disassemble contranslationally in vivo. Virology, 148, 326–336.

    Article  CAS  PubMed  Google Scholar 

  • Smith, T. N., Wylie, S. J., Coutts, B. A., & Jones, R. A. C. (2006). Localized distribution of iris yellow spot virus within leeks and its reliable large-scale detection. Plant Disease, 90, 729–733.

    Article  Google Scholar 

  • Stewart, L. R., Bouchard, R., Redinbaugh, M. G., & Meulia, T. (2012). Complete sequence and development of a full-length infectious clone of an Ohio isolate of maize dwarf mosaic virus (MDMV). Virus Research, 165, 219–224.

    Article  CAS  PubMed  Google Scholar 

  • Tan, R., Wang, L., Hong, N., & Wang, G. (2010). Enhanced efficiency of virus eradication following thermotherapy of shoot-tip cultures of pear. Plant Cell, Tissue and Organ Culture, 101, 229–235.

    Article  Google Scholar 

  • Tóbiás, I., Bakardjieva, N., & Palkovics, L. (2007). Comparison of Hungarian and Bulgarian isolates of maize dwarf mosaic virus. Cereal Research Communications, 35, 1643–1651.

    Article  Google Scholar 

  • Tu, J. C., Ford, R. E., & Krass, C. J. (1968). Comparisons of chloroplasts and photosynthesis rates of plants infected and not infected by maize dwarf mosaic virus. Phytopathology, 58, 285–288.

    Google Scholar 

  • Urcuqui-Inchima, S., Haenni, A. L., & Bernardi, F. (2001). Potyvirus proteins: A wealth of functions. Virus Research, 74, 157–175.

    Article  CAS  PubMed  Google Scholar 

  • Vernooij, B., Friedrich, L., Morse, A., Reist, R., Kolditz-Jawhar, R., Ward, E., Uknes, S., Kessmann, H., & Ryals, J. (1994). Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. The Plant Cell, 6, 959–985.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, M. B., Abbott, D. C., Upadhyaya, N. M., Jacobsen, J. V., & Waterhouse, P. M. (2001). Agrobacterium tumefaciens – Mediated transformation of an elite Australian barley cultivar with virus resistance and reporter genes. Australian Journal of Plant Physiology, 28, 149–156.

    Google Scholar 

  • Wei, T., Huang, T.-S., McNeil, J., Laliberté, J.-F., Hong, J., Nelson, R. S., & Wang, A. (2010). Sequential recruitment of the endoplasmic reticulum and chloroplasts for plant potyvirus replication. Journal of Virology, 84, 799–809.

    Article  CAS  PubMed  Google Scholar 

  • White, R. F. (1979). Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology, 99, 410–412.

    Article  CAS  PubMed  Google Scholar 

  • Williams, M. M., & Pataky, J. K. (2012). Interactions between maize dwarf mosaic and weed interference on sweet corn. Field Crops Research, 128, 48–54.

    Article  Google Scholar 

  • Ye, X. S., Pan, S. Q., & Kuć, J. (1990). Activity, isozyme pattern, and cellular localization of peroxidase as related to systemic resistance of tobacco to blue mold (Peronospora tabacina) and to tobacco mosaic virus. Plant Physiology and Biochemistry, 80, 1295–1299.

    CAS  Google Scholar 

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Acknowledgements

The authors thank Dr. Demeter Lásztity for all his help and advice, Györgyi Balogh for her technical assistance and Barbara Harasztos for revising the manuscript linguistically. This research was funded by a grant from the Hungarian Scientific Research Fund (OTKA 108834).

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Correspondence to Edit Ludmerszki.

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Ludmerszki, E., Chounramany, S., Oláh, C. et al. Protective role of S-methylmethionine-salicylate in maize plants infected with Maize dwarf mosaic virus . Eur J Plant Pathol 149, 145–156 (2017). https://doi.org/10.1007/s10658-017-1174-0

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