Acta Biologica Hungarica

, Volume 68, Issue 4, pp 376–387 | Cite as

How Arbuscular Mycorrhizal Fungi Influence the Defense System of Sunflower During Different Abiotic Stresses

  • Zoltán MayerEmail author
  • Nguyen Hong Duc
  • Zita Sasvári
  • Katalin Posta


The association between terrestrial plants and arbuscular mycorrhizal (AM) fungi is one of the most common and widespread mutualistic plant-fungi interaction. AM fungi are of beneficial effects on the water and nutrient uptake of plants and increase plant defense mechanisms to alleviate different stresses. The aim of this study was to determine the level of polyphenol oxidase (PPO), guaiacol peroxidase (POX) and glutathione S-transferase (GST) enzyme activities and to track the expression of glutathione S-transferase (GST) gene in plant-arbuscular mycorrhizal system under temperature- and mechanical stress conditions. Our results suggest that induced tolerance of mycorrhizal sunflower to high temperature may be attributed to the induction of GST, POX and PPO enzyme activities as well as to the elevated expression of GST. However, the degree of tolerance of the plant is significantly influenced by the age which is probably justified by the energy considerations.


Enzyme activity GST gene-expression arbuscular mycorrhizal fungi stress plantdefense system 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Azcón-Aguilar, C., Barea, J. M. (1997) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens - an overview of the mechanisms involved. Mycorrhiz. 6, 457–464.Google Scholar
  2. 2.
    Baslam, M., Goicoechea, N. (2012) Water deficit improved the capacity of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of antioxidant compounds in lettuce leaves. Mycorrhiz. 22, 347–359.Google Scholar
  3. 3.
    Bonfante-Fasolo, P. (1988) The role of the cell wall as a signal in mycorrhizal associations. In: Scannerini, S., Smith, D., Bonfante-Fasolo, P., Gianinnazzi, V. (eds) Cell to cell signals in plant, animal and microbial symbiosis. Springer Berlin Heidelberg, pp. 219–235.Google Scholar
  4. 4.
    Bowles, T. M., Barrios-Masias, F. H., Carlisle, E. A., Cavagnaro, T. R., Jackson, L. E. (2016) Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions. Sci. Total Environ. 566–567, 1223–1234.Google Scholar
  5. 5.
    Bradford M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.Google Scholar
  6. 6.
    Bunn, R., Lekberg, Y., Zabinski, C. (2009) Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants. Ecolog. 90, 1378–1388.Google Scholar
  7. 7.
    Cameron, D. D., Neal, A. L., van Wees, S. C. M., Ton, J. (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci. 18, 539–545.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Cetinkaya, H., Tasci, E., Dinler, B. S. (2014) Regulation of glutathione S-transferase enzyme activity with salt pre-treatment under heat stress in maize leaves. Res. Plant Biol. 4, 5.Google Scholar
  9. 9.
    Chen, S., Jin, W., Liu, A., Zhang, S., Liu, D., Wang, F., Lin, X., He, C. (2013) Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Sci. Horticult. 160, 222–229.Google Scholar
  10. 10.
    Cordier, C., Pozo, M. J., Barea, J. M., Gianinazzi, S., Gianinazzi, Pearson V. (1998) Cell defence responses associated with localized and systemic resistance to Phytophthora induced in tomato by an arbuscular mycorrhizal fungus. Mol. Plant Microbe Interact. 11, 1017–1028.Google Scholar
  11. 11.
    Dehghan, G., Amjad, L., Nosrati, H. (2013) Enzymatic and non-enzymatic antioxidant responses of alfalfa leaves and roots under different salinity levels. Acta Biol. Hung. 64, 207–217.PubMedGoogle Scholar
  12. 12.
    Edwards, E., Dixon, P. D., Walbot V. (2000) Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. Trends Plant Sci. 5, 193–198.PubMedGoogle Scholar
  13. 13.
    Elstner, E. F. (1982) Oxygen activation and oxygen-toxicity. Ann. Rev. Plant Physiol. Plant Mol. Biol. 33, 73–96.Google Scholar
  14. 14.
    El-Tohamy, W., Schnitzler, W. H., El-Behairy, U., El-Beltagy, M. S. (1999) Effect of VA mycorrhiza on improving drought and chilling tolerance of bean plants (Phaseolus vulgaris L.). Angewandte Botani. 73, 178–183.Google Scholar
  15. 15.
    Ergün, N., Özçubukçu, S., Kolukirik, M., Temizkan, Ö. (2014) Effects of temperature-heavy metal interactions, antioxidant enzyme activity and gene expression in wheat (Triticum aestivum L.) seedlings. Acta Biol. Hung. 65, 439–450.PubMedGoogle Scholar
  16. 16.
    Fehrmann, H., Dimond, A. E. (1967) Peroxidase activity and phytophthora resistance in different organs of the potato plant. Phytopatholog. 57, 69–72.Google Scholar
  17. 17.
    Giovannetti, M., Mosse, B. (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologis. 84, 489–500.Google Scholar
  18. 18.
    Habig, W., Pabst, M. J., Jakoby, W. B. (1974) The first enzymatic step in mercapturic acid formation. Glutathione-S-transferase. J. Biol. Chem. 249, 7130–7139.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Jung, S. C., Martinez-Medina, A., Lopez-Raez, J. A., Pozo, M. J. (2012) Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol. 38, 651–664.PubMedGoogle Scholar
  20. 20.
    Kohler, J., Hernández, J. A., Caravaca, F., Roldán, A. (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ. Exp. Bot. 65, 245–252.Google Scholar
  21. 21.
    Lambais, M. R., Ríos-Ruiz, W. F., Andrade, R. M. (2003) Antioxidant responses in bean (Phaseolus vulgaris) roots colonized by arbuscular mycorrhizal fungi. New Phytologis. 160, 421–428.Google Scholar
  22. 22.
    Latef, A. A. H. A., Chaoxing, H. (2011) Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. Acta Physiol. Plant. 33, 1217–1225.Google Scholar
  23. 23.
    Lendzemo, V. W., Kuyper, T. W., Matusova, R., Bouwmeester, H. J., Ast, A. V. (2007) Colonization by arbuscular mycorrhizal fungi of sorghum leads to reduced germination and subsequent attachment and emergence of Striga hermonthica. Plant Signal. Behavio. 2, 58–62.Google Scholar
  24. 24.
    Liu, X., Mao, K., Angela, Y. H., Omairi-Nasser, A., Austin, J., Glick, B. S., Klionsky, D. J. (2016) The Atg17-Atg31-Atg29 complex coordinates with Atg11 to recruit the Vam7 SNARE and mediate autophagosome-vacuole fusion. Current Biol. 26, 150–160.Google Scholar
  25. 25.
    López-Ráez, J. A., Charnikhova, T., Fernández, I., Bouwmeester, H., Pozo, M. J. (2011) Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J. Plant physiol. 168, 294–297.PubMedGoogle Scholar
  26. 26.
    Matsumura, A., Horii, S., Ishii, T. (2007) Effects of arbuscular mycorrhizal fungi and intercropping with bahiagrass on growth and anti-oxidative enzyme activity of radish. J. Jap. Soc. Horticult. Sci. 76, 224–229.Google Scholar
  27. 27.
    Mayer, A. M. (2006) Polyphenol oxidases in plants and fungi: Going places? A review. Phytochem. 67, 2318–2331.Google Scholar
  28. 28.
    Mittler R. (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405–410.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Ordoñez, N. M., Marondedze, C., Thomas, L., Pasqualini, S., Shabala, L., Shabala, S., Gehring, C. (2014) Cyclic mononucleotides modulate potassium and calcium flux responses to H2O2 in Arabidopsis roots. FEBS letters. 588, 1008–1015.PubMedGoogle Scholar
  30. 30.
    Passardi, F., Penel, C., Dunand, C. (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci. 9, 534–540.PubMedGoogle Scholar
  31. 31.
    Paszkowski U. (2006) Mutualism and parasitism: the yin and yang of plant symbioses. Curr. Op. Plant Biol. 9, 364–370.Google Scholar
  32. 32.
    Pérez, E., Rodríguez, Y., Hernández, M. A., de la Novaly B. M. (2004) Dinámica de inducción de algunos sistemas de defensa en la interacción HMA-tomate (Lycopersicon esculentum Mill.) var. Amalia. II. Inducción y expresión de peroxidasas y polifenoloxidasas en raíces de tomate. Cultivos Tropicale. 25, 45–52.Google Scholar
  33. 33.
    Pfeiffer, T., Štolfa, I., Žanić, M., Pavičić, N., Cesar, V., Lepeduš, H. (2013) Oxidative stress in leaves of two olive cultivars under freezing conditions. Acta Biol. Hung. 64, 341–351.PubMedGoogle Scholar
  34. 34.
    Pozo, M. J., López-Ráez, J. A., Azcón-Aguilar, C., García-Garrido, J. M. (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol. 205, 1431–1436.PubMedGoogle Scholar
  35. 35.
    Pozo, M. J., Azcón-Aguilar, C. (2007) Unravelling mycorrhiza-induced resistance. Curr. Op. Plant Biol. 10, 393–398.Google Scholar
  36. 36.
    Pozo, M. J., Cordier, C., Dumas-Gaudot, E. (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J. Exp. Bot. 53, 525–534.PubMedGoogle Scholar
  37. 37.
    Radwan, O., Mouzeyar, S., Venisse, J. S., Nicolas, P., Bouzidi, M. F. (2005) Resistance of sunflower to the biotrophic oomycete Plasmopara halstedii is associated with a delayed hypersensitive response within the hypocotyls. J. Exp. Bot. 56, 1683–2693.Google Scholar
  38. 38.
    Rahmaty, R., Khara, J. (2011) Effects of vesicular arbuscular mycorrhiza Glomus intraradices on photosynthetic pigments, antioxidant enzymes, lipid peroxidation, and chromium accumulation in maize plants treated with chromium. Turkish J. Biol. 35, 51–58.Google Scholar
  39. 39.
    Rathmell, W. G., Sequeira, L. (1974) Soluble peroxidase in fluid from the intercellular spaces of tobacco leaves. Plant Physiol. 53, 317–318.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Rodríguez, Y., Vierheilig, H., Mazorra, L. M. (2012) Alterations of the Antioxidant Enzyme Activities are not General Characteristics of the Colonization Process by Arbuscular Mycorrhizal Fungi. Chilean J. Agric. Res. 72, 411–418.Google Scholar
  41. 41.
    Scervino, J. M., Gottlieb, A., Silvani, V. A., Pérgola, M., Fernández, L., Godeas, A. M. (2009) Exudates of dark septate endophyte (DSE) modulate the development of the arbuscular mycorrhizal fungus (AMF) Gigaspora rosea. Soil Biol. Biochem. 41, 1753–1756.Google Scholar
  42. 42.
    Scervino, J. M., Ponce, M. A., Erra-Bassells, R., Vierheilig, H., Ocampo, J. A., Godeas, A. (2005) Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycol. Res. 109, 789–794.PubMedGoogle Scholar
  43. 43.
    Scervino, J. M., Ponce, M. A., Erra-Bassells, R., Bornpadre, J., Vierheilig, H., Ocampo, J. A., Godeas, A. (2007) The effect of flavones and flavonols on colonization of tomato plants by arbuscular mycorrhizal fungi of the genera Gigaspora and Glomus. Can. J. Microbiol. 53, 702–709.PubMedGoogle Scholar
  44. 44.
    Sharma, R., Yang, Y., Sharma, A., Awasthi, S., Awasthi, Y. C. (2004) Antioxidant role of glutathione S-transferases: protection against oxidant toxicity and regulation of stress-mediated apoptosis. Antioxid. Redox Signal. 6, 289–300.PubMedGoogle Scholar
  45. 45.
    Smith, S. E., Jakobsen, I., Grønlund, M., Smith, F. A. (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 156, 1050–1057.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Smith, S. E., Read, D. J. (1997) Mycorrhizal Symbiosis, 2nd ed. Academic Press, London.Google Scholar
  47. 47.
    Smith, S. E., Read, D. J. (2008) Mycorrhizal Symbiosis, 3rd ed. Academic Press, London.Google Scholar
  48. 48.
    Smith, S. E., Smith, F. A. (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystems scales. Annu. Rev. Plant Biol. 63, 227–250.Google Scholar
  49. 49.
    Steinkellner, S., Lendzemo, V., Langer, I., Schweiger, P., Khaosaad, T., Toussaint, J. P., Vierheilig, H. (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plantfungus interactions. Molecule. 12, 1290–1306.Google Scholar
  50. 50.
    Taylor, T. N., Remy, W., Hass, H., Kerp, H. (1995) Fossil arbuscular mycorrhizae from the Early Devonian. Mycologi. 87, 560–573.Google Scholar
  51. 51.
    Vierheilig, H., Coughlan, A. P., Wyss, U., Piché, Y. (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl. Environ. Microbiol. 64, 5004–5007.PubMedPubMedCentralGoogle Scholar
  52. 52.
    Wagner, U., Edwards, R., Dixon, D. P., Mauch, F. (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49, 515–532.Google Scholar
  53. 53.
    Wu, Q. S., Zou, Y. N. (2009) Mycorrhiza has a direct effect on reactive oxygen metabolism of drought-stressed citrus. Plant Soil Environ. 55, 436–442.Google Scholar
  54. 54.
    Xin, Z., Browse, J. (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant, Cell & Environ. 23, 893–902.Google Scholar
  55. 55.
    Zhu, J., Ha Lee B., Dellinger M., Cui X., Zhang C., Wu S., Nothnagel E.A., Zhu J.K. (2010) A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J. 63, 128–140.PubMedPubMedCentralGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2017

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Zoltán Mayer
    • 1
    Email author
  • Nguyen Hong Duc
    • 1
  • Zita Sasvári
    • 1
  • Katalin Posta
    • 1
  1. 1.Szent István UniversityInstitute of Genetics, Microbiology and BiotechnologyGödöllőHungary

Personalised recommendations