Biologia plantarum 64: 710-716, 2020 | DOI: 10.32615/bp.2020.088

Rapid increases in β-1,3-glucanase and chitinase activities are markers of resistance to Microdochium nivale in grasses of the Lolium‑Festuca complex

K. MARZEC-SCHMIDT*, K. HURA, A. PŁAŻEK
Department of Plant Physiology, Faculty of Agriculture and Economics, University of Agriculture in Kraków, PL-30239 Kraków, Poland

Microdochium nivale causes pink snow mould - a destructive disease of seedlings, stem bases, and ears of winter grasses and cereals. Glucanase and chitinase belong to pathogenesis-related proteins and exhibit a specific activity in response to pathogens. The aim of this study was to investigate changes in the activity of these enzymes in the leaves of chosen forage grasses during Microdochium nivale infection. Different cultivars of Festuca arudinacea, F. pratensis, Festulolium brauni, Lolium multiflorum, and L. perenne were prehardened at 12 °C and hardened at 2 °C and then inoculated with M. nivale mycelium. Leaf samples were collected before infection, as well as two, four, and eight days after inoculation. Each cultivar showed a specific pattern of changes in the enzymatic activities in response to M. nivale infection. We conclude that a rapid increase in glucanase and chitinase activities after M. nivale attack enhanced resistance to this pathogen and may be recognized as a physiological marker of grass resistance to this snow mould.

Keywords: forage grasses; pathogenesis-related proteins; snow mould.

Received: February 7, 2020; Revised: May 25, 2020; Accepted: June 8, 2020; Published online: October 9, 2020Show citation

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MARZEC-SCHMIDT, K., HURA, K., & PŁAŻEK, A. (2020). Rapid increases in β-1,3-glucanase and chitinase activities are markers of resistance to Microdochium nivale in grasses of the Lolium‑Festuca complex. Biologia plantarum, 64, 710-716. doi: 10.32615/bp.2020.088.
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    References

    1. Anuratha, C.S., Zen, K.C., Cole, K.C., Mew, T., Muthukrishnan, S.: Induction of chitinases and beta-glucanases in Rhizoctonia solani-infected rice plants: Isolation of an infection-related chitinase cDNA clone. - Physiol. Plant. 97: 39-46, 1996. Go to original source...
    2. Bradford, M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Ann. Biochem. 72: 248-254, 1976. Go to original source...
    3. Collinge, D.B., Kragh, K.M., Mikkelsen, J.D., Nielsen, K.K., Rasmussen, U., Vad, K.: Plant chitinase. - Plant J. 3: 31-40, 1993. Go to original source...
    4. Dahl, A.S.: Snowmold of turf grasses caused by Fusarium nivale. - Phytopathology 34: 197-214, 1934.
    5. Ergon, A., Klemsdal, S.S., Tronsmo, A.M.: Interactions between cold hardening and Microdochium nivale infection on expression of pathogenesis-related genes in winter wheat. - Physiol. mol. Plant Pathol. 53: 301-310, 1998. Go to original source...
    6. Fink, W., Liefland, M., Mendgen, K.: Chitinase and β-1,3-glucanases in the apoplastic compartment of oat leaves (Avena sativa L.). - Plant Physiol. 88: 270‑275, 1988. Go to original source...
    7. Garcia-Olmedo, F., Molina, A., Alamillo, J.M., Rodriguez-Palenzuela, P.: Plant defense peptides. - Biopolymers 47: 479-491, 1998. Go to original source...
    8. Gaudet, D.A., Laroche, A., Frick, M., Davoren, J., Puchalski, B., Ergon, A.: Expression of plant defence-related (PR-proteins) transcripts during hardening and dehardening of winter wheat. - Physiol. mol. Plant Pathol. 57: 15-24, 2000. Go to original source...
    9. Gaudet, D.A., Laroche, A., Yoshida, M.: Low temperature-wheat-fungal interactions: a carbohydrate connection. - Physiol. Plant. 106: 437- 444, 1999. Go to original source...
    10. Ghesquière, M., Baert, J., Barth, S., Černoch, V., Grogan, D., Humphreys, M., Murray, P., Østrem, L., Sokolović, D., Paszkowski, E., Zwierzykowski, Z.: Enhancing the productivity in forage grasses on the European scale using interspecific hybridization. - In: Roldán-Ruiz, I., Baert, J., Reheul, D. (ed.): Breeding in a World of Scarcity (Proceedings of the Meeting of the Section "Forage Crops and Amenity Grasses" of Eucarpia 2015). Pp. 199-204, Springer, Cham 2016. Go to original source...
    11. Hammond-Kosack, K.E., Jones, J.: Resistance gene-dependent plant defence response. - Plant Cell 8: 1773-1791, 1996.
    12. Hartman, C.L., McCoy, T.J., Knous, T.R.: Selection of alfalfa (Medicago sativa) cell lines and regenerations of plant resistant to the toxin(s) produced by Fusarium oxysporum f.sp. medicaginis. - Plant Sci. Lett. 34: 183-194, 1984. Go to original source...
    13. Hiilovaara-Teijo, M., Hannukkala, A., Griffith, M., Yu, X.M., Pihakaski‑Maunsbach, K.: Snow-mould-induced apoplastic proteins in winter rye leaves lack antifreeze activity. - Plant Physiol. 121: 665-673, 1999. Go to original source...
    14. Hon, W.C., Griffith, M., Chong, P., Yang, D.S.C.: Extraction and isolation of antifreeze proteins from winter rye (Secale cereale L.) leaves. - Plant Physiol. 109: 879-889, 1994. Go to original source...
    15. Hon, W.C., Griffith, M., Młynarz, A., Kwok, Y.C., Yang, D.S.C.: Antifreeze proteins in winter rye are similar to pathogenesis-related proteins. - Plant Physiol. 109: 879-889, 1995. Go to original source...
    16. Jamalainen, E.A.: Resistance in winter cereals and grasses to low-temperature parasitic fungi. - Annu. Rev. Phytopathol. 12: 281-302, 1974. Go to original source...
    17. Jongedijk, E., Tigelaar, H., Van Roekel, S.C., Bres-Vloemans, S.A., Dekker, I., Van den Elzen, P.J.M., Cornelissen, B.J.C., Melchers, L.S.: Synergistic activity of chitinases and β-1,3-glucanases enhances fungal resistance in transgenic tomato plants. - Euphytica 85: 173-180, 1995. Go to original source...
    18. Jutidamrongphan, W., Anderson, J.B., Mackinnon, G., Manners, J.M., Simpson, R.S., Scott, K.J.: Induction of β-1,3-glucanase in barley in response to infection by fungal pathogens. - Mol. Plant-Microbe Interact. 4: 234-238, 1991. Go to original source...
    19. Jutidamrongphan, W., Mackinnon, G., Manners, J.M., Scott, K.J.: Sequence of a near-full length cDNA clone for a mRNA of barley induced by fungal infection. - Nucl. Acids Res. 17: 9478, 1989. Go to original source...
    20. Kuwabara, C., Takezawa, D., Shimada, T., Hamada, T., Fujikawa, S., Arakawa, K.: Abscisic acid- and cold-induced thaumatin-like protein in winter wheat has an antifungal activity against snow mould, Microdochium nivale. - Physiol. Plant. 115: 101-110, 2002. Go to original source...
    21. Kuźniak, E., Urbanek, H.: Induction of hydrolytic enzymes in bean cell and protoplast cultures treated with Botrytis cinerea mycelium extract. - Acta Physiol. Plant. 15: 227-236, 1997.
    22. Legrand, M., Kauffmann, S., Geoffroy, P., Fritig, B.: Biological function of pathogenesis-related proteins: four tobacco pathogenesis-related proteins are chitinases. - Proc. nat. Acad. Sci. USA 84: 6750-6754, 1987. Go to original source...
    23. Margis-Pinheiro, M., Martin, C., Didierjean, L., Burkard, G.: Differentiation expression of bean chitinase genes by virus infection, chemical treatment or UV radiation. - Plant mol. Biol. 22: 659-668, 1993. Go to original source...
    24. Marzec-Schmidt, K., Hura, K., Płażek, A.: Changes in antioxidants activity in grasses from complex Lolium-Festuca as response to Microdochium nivale infection. - Physiol. mol. Plant Pathol. 104: 40-47, 2018. Go to original source...
    25. Masajada, K. Augustyniak, A., Perlikowski, D., Ratajczak, D., Zwierzykowski, W., Pawłowicz, I., Kosmala, A.: Physiological indicators of tolerance to soil water deficit in Lolium multiflorum/Festuca arundinacea introgression forms. - In: Brazauskas, G., Statkevičiūtė, G., Jonavičienė, K. (ed.): Breeding Grasses and Protein Crops in the Era of Genomics. Pp. 176-180. Springer-Verlag, Berlin - Heidelberg 2018. Go to original source...
    26. Mauch, F., Mauch-Moni, B., Boller, T.: Antifungal hydrolases in pea tissue II. Inhibition of fungal growth by combinations of chitinase and β‑1,3‑glucanase. - Plant Physiol. 88: 936-942, 1988. Go to original source...
    27. Mohase, L., Van der Westhuizen, A.J.: Glycoproteins from Russian wheat aphid infested wheat induce defence responses. - J. Biosci. 57: 867-873, 2002.
    28. Münch-Garthoff, S., Neuhaus, J.M., Boller, T., Kemmerling, B., Kogel, K.H.: Expression of β-1,3-glucanase and chitinase in healthy, stem-rust-affected and elicitor-treated near-isogenic wheat lines showing Sr5- or Sr24-specified race-specific rust resistance. - Planta 201: 235-244, 1997. Go to original source...
    29. Nakajima, T., Abe, J.: Environmental factors affecting the expression of resistance in winter wheat to pink snow mould caused by Microdochium nivale. - Can. J. Bot. 73: 1783-1788, 1996. Go to original source...
    30. Nelson, N.: A photometric adaptation of the Somogyi method for the determination of glucose. - J. biol. Chem. 153: 375-380, 1944.
    31. Okushima, Y., Koizumi, N., Kusano, T., Sano, T.: Secreted proteins of tobacco cultured BY2 cells: identification of new member of pathogenesis-related proteins. - Plant mol. Biol. 42: 479-488, 2000. Go to original source...
    32. Perlikowski, D., Kosmala, A., Rapacz, M., Kościelniak, J., Pawłowicz, I., Zwierzykowski, Z.: Influence of short-term drought conditions and subsequent re-watering on the physiology and proteome of Lolium multiflorum/Festuca arundinacea introgression forms, with contrasting levels of tolerance to long-term drought. - Plant Biol. 16: 385-394, 2013.
    33. Płażek, A., Pociecha, E., Augustyniak, A., Masajada, K., Dziurka, M., Majka, J., Perlikowski, D., Pawłowicz, I., Kosmala, A.: Dissection of resistance to Microdochium nivale in Lolium multiflorum/Festuca arudinacea introgression forms. - Plant Physiol. Biochem. 123: 43-53, 2018. Go to original source...
    34. Płażek, A., Żur, I.: Cold-induced plant resistance to necrotrophic pathogens and antioxidant enzyme activities and cell membrane permeability. - Plant Sci. 164: 1019-1028, 2003. Go to original source...
    35. Prończuk, M., Prończuk, S., Żebrowski, J.: Response of Lolium perenne cultivars and ecotypes to artificial and natural shade conditions. - Czech J. Genet. Plant Breed. 39: 363-366, 2003.
    36. Prończuk, M., Zagdańska, B.: Effect of Microdochium nivale and low-temperature on winter survival of perennial ryegrass. - J. Phytopatol. 138: 1-8, 1993. Go to original source...
    37. Ryan, C.: Oligosaccharides as recognition signals for the expression of defensive genes in plants. - Biochemistry 27: 879-882, 1988. Go to original source...
    38. Somogyi, M.: Notes on sugar determination. - J. biol. Chem. 195: 19-23, 1952.
    39. Stintzi, A., Heitz, T., Prasad, V., Wiedemann-Merdinoglu, S., Kauffmann, S., Geoffroy, P., Legrand, M., Friting, B.: Plant "pathogenesis-related" proteins and their role in defence against pathogens. - Biochimie 75: 687-706, 1993. Go to original source...
    40. Strömqvist, J., Jarvis, N.: Sorption, degradation and leaching of the fungicide iprodine in a golf green under Scandinavian conditions: measurements, modelling and risk assessment. - Pest. Manage. Sci. 61: 1168-1178, 2005.
    41. Watschke, T.L., Dernoeden, P.H., Shetlar, D.J.: Managing Turfgrass Pests. 2nd Edition. CRC Press, Boca Raton - London - New York 2013. Go to original source...
    42. Wiśniewski, K., Zagdańska, B., Prończuk, M.: Interrelationship between frost tolerance, drought and resistance to snow mould (Microdochium nivale). - In: Bedö, Z., Sutka, J., Tischner, T., Veisz, O. (ed.): Proceedings from International Symposium "Cereal Adaptation to Low Temperature Stress in Controlled Environments". Pp. 221-226. Agricultural Research Institute of the Hungarian Academy of Sciences, Martonvásár 1997.
    43. Yu, X., Griffith, M.: Antifreeze proteins in winter rye leaves form oligomeric complexes. - Plant Physiol. 119: 1361-1369, 1999. Go to original source...
    44. Yu, X., Griffith, M.: Winter rye antifreeze activity increases in response to cold and drought, but not abscisic acid. - Physiol. Plant. 112: 78-86, 2001. Go to original source...
    45. Yun, D.-J., Bressan, R.A., Hasegawa, P.M.: Plant antifungal proteins. - Plant Breed. Rev. 14: 39-88, 1997.
    46. Żur, I.A., Dubas, E., Pociecha, E., Dubert, F., Kolasińska, I., Płażek, A.: Cytological analysis of infection process and the first defence responses induced in winter rye (Secale cereale L.) seedling inoculated with Microdochium nivale. - Physiol. mol. Plant Phytopatol. 76: 189-196, 2011.
    47. Żur, I., Gołębiowska, G., Dubas, E., Golemiec, E., Matušíková, I., Libantová, J., Moravčíková, J.: β-1,3-glucanase and chitinase activities in winter triticales during cold hardening and subsequent infection by Microdochium nivale. - Biologia 68: 241-248, 2013.

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