European Journal of Plant Pathology

, Volume 149, Issue 1, pp 145–156 | Cite as

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

  • Edit LudmerszkiEmail author
  • Sengnirane Chounramany
  • Csilla Oláh
  • György Kátay
  • Ilona Rácz
  • Asztéria Almási
  • Ádám Solti
  • Iván Bélai
  • Szabolcs Rudnóy


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.


S-methylmethionine-salicylate Maize dwarf mosaic virus Ascorbate peroxidase Guaiacol peroxidase qRT-PCR Chlorophyll a fluorescence induction 



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).


  1. 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.Google Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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
  4. Baker, N. R. (2008). Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology, 59, 89–113.CrossRefPubMedGoogle Scholar
  5. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. Beddard, G. S., & Porter, G. (1976). Concentration quenching in chlorophyll. Nature, 260, 366–367.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.Google Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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.Google Scholar
  21. Gell, G., Balázs, E., & Petrik, K. (2010). Genetic diversity of Hungarian maize dwarf mosaic virus isolates. Virus Genes, 40, 277–281.CrossRefPubMedGoogle Scholar
  22. Hammond, J. (1998). Serological relationship between the cylindrical inclusion proteins of potyviruses. Phytopathology, 88, 965–971.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefPubMedCentralGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar
  26. 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.CrossRefPubMedGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. 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.CrossRefPubMedGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.CrossRefPubMedGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22, 867–880.Google Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefPubMedGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  46. Raskin, I. (1992). Role of salicylic acid in plants. Annual Review of Plant Physiology, 43, 439–463.CrossRefGoogle Scholar
  47. Reneiro, A., & Beachy, R. N. (1986). Association of TMV coat protein with chloroplast membranes in virus-infected leaves. Plant Molecular Biology, 6, 291–301.CrossRefGoogle Scholar
  48. 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.CrossRefPubMedGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefPubMedGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. Tóbiás, I., Bakardjieva, N., & Palkovics, L. (2007). Comparison of Hungarian and Bulgarian isolates of maize dwarf mosaic virus. Cereal Research Communications, 35, 1643–1651.CrossRefGoogle Scholar
  53. 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
  54. Urcuqui-Inchima, S., Haenni, A. L., & Bernardi, F. (2001). Potyvirus proteins: A wealth of functions. Virus Research, 74, 157–175.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 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
  57. 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.CrossRefPubMedGoogle Scholar
  58. White, R. F. (1979). Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology, 99, 410–412.CrossRefPubMedGoogle Scholar
  59. Williams, M. M., & Pataky, J. K. (2012). Interactions between maize dwarf mosaic and weed interference on sweet corn. Field Crops Research, 128, 48–54.CrossRefGoogle Scholar
  60. 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.Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2017

Authors and Affiliations

  • Edit Ludmerszki
    • 1
    Email author
  • Sengnirane Chounramany
    • 1
  • Csilla Oláh
    • 1
  • György Kátay
    • 2
  • Ilona Rácz
    • 1
  • Asztéria Almási
    • 2
  • Ádám Solti
    • 1
  • Iván Bélai
    • 2
  • Szabolcs Rudnóy
    • 1
  1. 1.Department of Plant Physiology and Molecular Plant BiologyEötvös Loránd UniversityBudapestHungary
  2. 2.Plant Protection Institute, Centre for Agricultural ResearchHungarian Academy of SciencesBudapestHungary

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