Plant Protect. Sci., 2013, 49(3):105-119 | DOI: 10.17221/51/2012-PPS

Reactive oxygen and nitrogen species and hormone signalling in systemic infection of pea by Pea enation mosaic virusOriginal Paper

Helena KYSELÁKOVÁ1, Michaela SEDLÁŘOVÁ2, Martin KUBALA3, Vladimíra NO®KOVÁ1, Jana PITERKOVÁ4, Lenka LUHOVÁ4, Ondřej NOVÁK5, Petr ILÍK1
1 Centre of the Region Haná for Biotechnological and Agricultural Research
2 Department of Botany, Faculty of Science, Palacky University in Olomouc, Olomouc, Czech Republic
3 Department of Biophysics, Faculty of Science, Palacky University in Olomouc, Olomouc, Czech Republic
4 Department of Biochemistry, Faculty of Science, Palacky University in Olomouc, Olomouc, Czech Republic
5 Laboratory of Growth Regulators, Palacky University and Institute of Experimental Botany AS CR, Olomouc, Czech Republic

The physiological responses of pea plants during 40 days of compatible interaction with Pea enation mosaic virus (PEMV) were evaluated. PEMV induces systemic changes in the concentration of phytohormones. At 5 days post inoculation (dpi), a simultaneous increase in abscisic acid (ABA) level and a decrease in salicylic acid (SA) level was observed, which is known to be involved in the suppression of hypersensitive reaction. In our pathosystem it preceded the virus presence in the systemic leaves. PEMV induces the accumulation of ABA, SA and Hsp70 and enhances peroxidase (POX) activity at 15 dpi, when it is already transmitted throughout the plant. The formation of enations was preceded by a local accumulation of nitric oxide, which was followed by the appearance of reactive oxygen species, mostly in the vicinity of leaf veins. Such heterogeneity suggests involvement of these molecules in the control of hyperplasia and tissue differentiation.

Keywords: PEMV; Pisum sativum; heat shock proteins; hydrogen peroxide; nitric oxide; phytohormones

Published: September 30, 2013  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
KYSELÁKOVÁ H, SEDLÁŘOVÁ M, KUBALA M, NO®KOVÁ V, PITERKOVÁ J, LUHOVÁ L, et al.. Reactive oxygen and nitrogen species and hormone signalling in systemic infection of pea by Pea enation mosaic virus. Plant Protect. Sci. 2013;49(3):105-119. doi: 10.17221/51/2012-PPS.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Adie B.A., Pérez-Pérez J., Pérez-Pérez M.M., Godoy M., Sánchez-Serrano J.J., Schmelz E.A., Solano R. (2007): ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. The Plant Cell, 19: 1665-1681. Go to original source... Go to PubMed...
    2. Anderson J.P., Badruzsaufari E., Schenk P.M., Manners J.M., Desmond O.J., Ehlert Ch., Maclean D.J., Ebert P.R., Kazana K. (2004): Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defence gene expression and disease resistance in Arabidopsis. Plant Cell, 16: 3460-3479. Go to original source... Go to PubMed...
    3. Angeliny R., Manes F., Federico R. (1990): Spatial and functional correlation between diamine-oxidase and peroxidase activities and their dependence upon deetiolation and wounding in chick-pea stems. Planta, 182: 89-96. Go to original source... Go to PubMed...
    4. Arias M. C., Luna C., Rodríguez M., Lenardon S., Taleisnik E. (2005): Sunflower chlorotic mottle virus in compatible interactions with sunflower: ROS generation and antioxidant response. European Journal of Plant Pathology, 113: 223-232. Go to original source...
    5. Baebler ©., Stare K., Kovač M., Blejec A., Prezelj N., Stare T., Kogovąek P., Pompe-Novak M., Rosah S., Ravnikar M., Gruden K. (2011): Dynamics of responses in compatible potato - Potato virus Y interaction are modulated by salicylic acid. PLoS ONE 6(12): e29009. doi:10.1371/journal.pone.0029009 Go to original source... Go to PubMed...
    6. Bari R., Jones J.D.G. (2009): Role of plant hormones in plant defence responses. Plant Molecular Biology, 69: 473-488. Go to original source... Go to PubMed...
    7. Bell E., Creelman R.A., Mullet J.E. (1995): A chloroplast lipoxygenase is required for wound induced accumulation of jasmonic acid in Arabidopsis. Proceedings of National Academy of Science USA, 92: 8675-8679. Go to original source... Go to PubMed...
    8. Bendahmane A., Kanyuka K., Baulcombe D.C. (1999): The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell, 11: 781-791. Go to original source... Go to PubMed...
    9. Bergougnoux V., Hlaváčková V., Plotzová R., Novák O., Fellner M. (2009): The 7B-1 mutation in tomato (Solanum lycopersicum L.) confers a blue light-specific lower sensitivity to coronatine, a toxin produced by Pseudomonas syringae pv. tomato. Journal of Experimental Botany, 60: 1219-1230. Go to original source... Go to PubMed...
    10. Byth H.-A., Kuun K.G., Bornman L. (2001): Virulencedependent induction of Hsp70/Hsc70 in tomato by Ralstonia solanacearum. Plant Physiology and Biochemistry, 39: 697-705. Go to original source...
    11. Cao F.Y., Yoshioka K., Desveaux D. (2011): The role of ABA in plant-pathogen interactions. Journal of Plant Research 124: 489-499. Go to original source... Go to PubMed...
    12. Chen Z., Zhou T., Wu X., Hong Y., Fan Z., Li H. (2008): Influence of cytoplasmic heat shock protein 70 on viral infection of Nicotiana benthamiana. Molecular Plant Pathology, 9: 809-817. Go to original source... Go to PubMed...
    13. Choi J., Choi D., Lee S., Ryu C.-M., Hwang I. (2011): Cytokinins and plant immunity: Old foes or new friends? Trends in Plant Science, 16: 388-394. Go to original source... Go to PubMed...
    14. Clarke S.F., Burritt D.J., Jameson P.E., Guy P.L. (1998): Influence of plant hormones on virus replication and pathogenesis-related proteins in Phaseolus vulgaris L. infected with white clover mosaic potexvirus. Physiology and Molecular Plant Pathology, 53: 195-207. Go to original source...
    15. Clarke S.F., Guy P.L, Jameson P.E., Schmierer D., Burritt D.J. (2000): Influence of white clover mosaic potexvirus infection on the endogenous levels of jasmonic acid and related compounds in Phaseolus vulgaris L. seedlings. Journal of Plant Physiology, 156: 433-437. Go to original source...
    16. Clarke S.F., Guy P.L, Burritt D.J., Jameson P.E. (2002): Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment. Physiologia Plantarum, 114: 157-164. Go to original source... Go to PubMed...
    17. Cole A.B., Király L., Ross K., Schoelz J.E. (2001): Uncoupling resistance from cell death in the hypersensitive response of Nicotiana species to Cauliflower mosaic virus infection. Molecular Plant-Microbe Interactions, 14: 31-41. Go to original source... Go to PubMed...
    18. Cooley M.B., Pathirana S., Wu H.-J., Kachroo P., Klessig D.F. (2000): Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. Plant Cell, 12: 663-676. Go to original source...
    19. Demler S.A., de Zoeten G.A., Adam G., Harris K.F. (1996): Polyhedral Virions and Bipartite RNA Genomes. In: Harrison B.D., Murant A.F. (eds): The Plant Viruses. Vol. 5. Plenum Press, New York: 303-304.
    20. Díaz-Vivancos P., Rubio M., Mesonero V., Periago P.M., Ros Barceló A., Martínez-Gómez P., Hernández J.A. (2006): The apoplastic antioxidant system in Prunus: Response to plum pox virus. Journal of Experimental Botany, 57: 3813-3824. Go to original source...
    21. El-Fahaam Y.M., Fegla G.I., Wagih E.E., El-Karyoni H.A. (1990): Biochemical changes in lettuce plants infected with lettuce mosaic virus. Journal of King Saud University, 2: 271-277.
    22. El Rahman T.A., El Oirdi M., Gonzalez-Lamothe R., Bouarab K. (2012): Necrotrophic pathogens use the salicylic acid signaling pathway to promote disease development in tomato. Molecular Plant-Microbe Interactions, 25: 1584-1593. Go to original source... Go to PubMed...
    23. Fujita M., Fujita Y., Noutoshi Y., Takahashi F., Narusaka Y., Yamaguchi-Shinozaki K., Shinozaki K.. (2006): Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Current Opinion in Plant Biology, 9: 436-442. Go to original source... Go to PubMed...
    24. Glazebrook J. (2005): Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathogy, 43: 205-227. Go to original source... Go to PubMed...
    25. Grünwald N.J., Chen W., Larsen R.C. (2004): Pea diseases and their management. In: Naqvi S.A.M.H. (ed.): Diseases of Fruits and Vegetables. Volume II. Kluwer Academic Publishers, Dordrecht: 301-331. Go to original source...
    26. Gundlach H., Muller M.J., Kutchan T.M., Zenk M.H. (1992): Jasmonic acid is a signal transducer in elicitorinduced plant cell cultures. Proceedings of the National Academy of Science USA, 89: 2389-2393. Go to original source... Go to PubMed...
    27. Hernández J.A., Rubio M., Olmos E., Ros-Barceló A., Martínez-Gómez P. (2004): Oxidative stress induced by long-term plum pox virus infection in peach (Prunus persica). Physiologia Plantarum, 122: 486-495. Go to original source...
    28. Hinrichs-Berger J., Harfold M., Berger S., Buchenauer H. (1999): Cytological responses of susceptible and extremely resistant potato plants to inoculation with potato virus Y. Physiological and Molecular Plant Pathology, 55: 143-150. Go to original source...
    29. Hlaváčková V., Krchňák P., Nauą J., Novák O., ©pundová M., Strnad M. (2006): Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning. Planta, 225: 235-244. Go to original source... Go to PubMed...
    30. Jameson P.E., Clarke S.F. (2002): Hormone-virus interactions in plants. Critical Reviews in Plant Sciences, 21: 205-228. Go to original source...
    31. Jiang M., Zhang J. (2001): Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant and Cell Physiology 42: 1265-1273. Go to original source... Go to PubMed...
    32. Koornneef A., Pieterse C.M.J. (2008): Cross talk in defense signaling. Plant Physiology, 146: 839-844. Go to original source... Go to PubMed...
    33. Kyseláková H., Prokopová J., Nauą J., Novák O., Navrátil M., ©afářová D., ©pundová M., Ilík P. (2011): Photosynthetic alterations of pea leaves infected systemically by pea enation mosaic virus: A coordinated decrease in efficiencies of CO2 assimilation and photosystem II photochemistry. Plant Physiology and Biochemistry, 49: 1279-1289. Go to original source... Go to PubMed...
    34. Lamotte L., Courtois C., Barnavon L., Pugin A., Wendehenne D. (2005): Nitric oxide in plants: the biosynthesis and cell signalling properties of a fascinating molecule. Planta, 221: 1-4. Go to original source... Go to PubMed...
    35. Li L., Li C., Howe G.A. (2001): Genetic analysis of wound signaling in tomato. Evidence for a dual role of jasmonic acid in defense and female fertility. Plant Physiology, 127: 1414-1417. Go to original source...
    36. Love A.J., Yun B.W., Laval V., Loake G.J., Milner J.J. (2005): Cauliflower mosaic virus, a compatible pathogen of Arabidopsis, engages three distinct defense-signaling pathways and activates rapid systemic generation of reactive oxygen species. Plant Physiology, 139: 935-948. Go to original source... Go to PubMed...
    37. Madhusudhan K.N., Srikanta B.M., Shylaja M.D., Prakash H.S., Shetty H.S. (2009): Changes in antioxidant enzymes, hydrogen peroxide, salicylic acid and oxidative stress in compatible and incompatible host-tobamovirus interaction. Journal of Plant Interactions, 4: 157-166. Go to original source...
    38. Mauch-Mani B., Mauch F. (2005): The role of abscisic acid in plant-pathogen interactions. Current Opinion in Plant Biology, 8: 409-414. Go to original source... Go to PubMed...
    39. Maule A., Leh V., Lederer C. (2002): The dialogue between viruses and hosts in compatible interactions. Current Opinion in Plant Biology, 5: 279-284. Go to original source... Go to PubMed...
    40. Mayer M.P., Bakau B. (2005): Hsp70 chaperones: Cellular functions and molecular mechanism. Cell and Molecular Life Sciences, 62: 670-684. Go to original source... Go to PubMed...
    41. Milavec M., Ravnikar M., Kovač M. (2001): Peroxidases and photosynthetic pigments in susceptible potato infected with potato virus YNTN. Plant Physiology and Biochemistry, 39: 891-898. Go to original source...
    42. Mur L.A.J., Kenton P., Atzorn R., Miersch O., Wasternack C. (2006): The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiology, 140: 249-262. Go to original source... Go to PubMed...
    43. Niki T., Mitsuhara I., Seo S., Ohtsubo N., Ohashi Y. (1998): Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiology 39: 500-507. Go to original source...
    44. Panavas T., Walker E.L., Rubinstein B. (1998): Possible involvement of abscisic acid in senescence of daylily petals. Journal of Experimental Botany, 49: 1987-1997. Go to original source...
    45. Pei Z.-M., Murata Y., Benning G., Thomine S., Klusener B., Allen G.J., Grill E., Schroeder J.I. (2000): Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature, 406: 731-734. Go to original source... Go to PubMed...
    46. Piterková J., Petřivalský M., Luhová L., Mieslerová B., Sedlářová M., Lebeda A. (2009): Local and systemic production of nitric oxide in tomato responses to powdery mildew infection. Molecular Plant Pathology, 10: 501-513. Go to original source... Go to PubMed...
    47. Preston C.A., Lewandowski C., Enyedi A.J., Baldwin I.T. (1999): Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants. Planta, 209: 87-95. Go to original source... Go to PubMed...
    48. Prins M., Laimer M., Noris E., Schubert J., Wassenegger M., Tepfer M. (2008): Strategies for antiviral resistance in transgenic plants. Molecular Plant Pathology, 9: 73-83. Go to original source...
    49. Quiroga M., Guerrero C., Botella M.A., Ros Barceló A., Amaya I., Medina M.I., Alonso F.J., de Forchetti S.M., Tigier H., Valpuesta V. (2000): A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiology, 122: 1119-1127. Go to original source... Go to PubMed...
    50. Radwan D.E.M., Fayez K.A., Mahmoud S.Y., Hamad A., Lu G. (2007): Physiological and metabolic changes of Cucurbita pepo leaves in response to zucchini yellow mosaic virus (ZYMV) infection and salicylic acid treatments. Plant Physiology and Biochemistry, 45: 480-489. Go to original source... Go to PubMed...
    51. Radwan D.E., Lu G., Fayez K.A., Mahmoud S.Y. (2008): Protective action of salicylic acid against Bean yellow mosaic virus infection in Vicia faba leaves. Journal of Plant Physiology, 165: 845-857. Go to original source... Go to PubMed...
    52. Riedle-Bauer M. (2000): Role of reactive oxygen species and antioxidant enzymes in systemic virus infections of plants. Journal of Phytopathology, 148: 297-302. Go to original source...
    53. Reymond P., Weber H., Damond M., Farmer E.E. (2000): Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. The Plant Cell, 12: 707-719. Go to original source... Go to PubMed...
    54. Robert-Seilaniantz A., Grant M., Jones J.D.G. (2011): Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology, 49: 317-343. Go to original source... Go to PubMed...
    55. Salgueiro S., Hull R. (1999): Comparison of pea enation mosaic virus (PEMV) isolates: Sequence of coat protein and aphid transmission protein genes of a European isolate. Journal of Phytopathology, 147: 391-396. Go to original source...
    56. Sedlářová M., Luhová L., Petřivalský M., Lebeda A. (2007): Localization and metabolism of reactive oxygen species during Bremia lactucae pathogenesis in Lactuca sativa and wild Lactuca spp. Plant Physiology and Biochemistry, 45: 607-616. Go to original source... Go to PubMed...
    57. Smith C.M., Rodriquez-Buey M., Karlsson J., Campbell M.M. (2004): The response of the poplar transcriptome to wounding and subsequent infection by a viral pathogen. The New Physiologist, 164: 123-136. Go to original source... Go to PubMed...
    58. Smith J.L., De Morales C.M., Mescher M.C. (2009): Jasmonate- and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Management Science, 65: 497-503. Go to original source... Go to PubMed...
    59. Spoel S.H., Dong X. (2008): Making sense of hormone crosstalk during plant immune responses. Cell Host and Microbe, 3: 348-351. Go to original source... Go to PubMed...
    60. Thordal-Christensen H., Zhang Z., Wei Y., Collinge D.B. (1997): Subcellular localization of H2O 2 in plants in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal, 11: 1187-1194. Go to original source...
    61. von Bargen S., Salchert K., Paape M., Piechulla B., Kellmann J.W. (2001): Interactions between the tomato spotted wilt virus movement protein and plant proteins showing homologies to myosin, kinesin and DnaJ-like chaperones. Plant Physiology and Biochemistry, 39: 1083-1093. Go to original source...
    62. Whitham S.A., Wang Y.Z. (2004): Roles for host factors in plant viral pathogenicity. Current Opinion in Plant Biology, 7: 365-371. Go to original source... Go to PubMed...

    This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content