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Antimicrobial Functions of the Plant Hydrolases, Chitinase and ß-1,3-Glucanase

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Mechanisms of Plant Defense Responses

Part of the book series: Developments in Plant Pathology ((DIPP,volume 2))

Abstract

Many plant species accumulate chitinases and ß-1,3-glucanases in response to infection by plant pathogens and to treatments with the plant stress hormone, ethylene. The substrates of these two enzymes, chitin and ß-1,3-glucan, are the main components of the cell walls of most higher fungi. Taken individually, purified chitinases and ß-1,3-glucanases inhibit some fungi but do not affect most of them. However, combinations of the two enzymes inhibit many saprophytic and pathogenic fungi on agar plates or in liquid medium. Microscopic studies indicate that the enzymes attack primarily the hyphal tip. Growing hyphae are highly sensitive when suddenly brought into contact with the antifungal hydrolases. However, they have a potential to adapt and become resistant when exposed continually to the enzymes. This suggests that antifungal hydrolases may be more effective in defense when suddenly brought into contact with invading fungi, e.g. by release from an intracellular compartment, than when present constitutively in the extracellular space.

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References

  • Arlorio, M., Ludwig, A., Boiler, T., Mischiati, P. and Bonfante-Fasolo, P. (1992) Inhibition of fungal growth by plant chitinases and ß-l,3-glucanases: a morphological study. Protoplasma, in press.

    Google Scholar 

  • Abeles, F.B., Bosshart, R.P., Forrence, L.E. and Habig, W.H. (1971) Preparation and purification of glucanase and chitinase from bean leaves. Plant Physiol. 47,129–134.

    Article  PubMed  CAS  Google Scholar 

  • Benhamou, N. and Asselin, A. (1989) Attempted localization of a substrate for chitinases in plant cells reveals abundant N-acetyl-D-glucosamine residues in secondary walls. Biol. Cell 67, 341–350.

    CAS  Google Scholar 

  • Bemasconi, P., Locher, R., Pilet, P.E., Jollès, J. and Jollès, P. (1987) Purification and N-terminal amino acid sequence of a basic lysozyme from Parthenocissus quinquifolia cultured in vitro. Biochim. Biophys. Acta 915, 254–260.

    Article  Google Scholar 

  • Boiler, T. (1987) Hydrolytic enzymes in plant disease resistance, in T. Kosuge, E.W. Nester (eds.), Plant-Microbe Interactions, Vol. 2, Macmillan, New York, pp. 385–413.

    Google Scholar 

  • Boiler, T. (1988) Ethylene and the regulation of antifungal hydrolases in plants, in B.J. Miflin (ed.), Oxford Surveys of Plant Molecular and Cell Biology, Vol. 5, Oxford University Press, Oxford, pp. 145–174.

    Google Scholar 

  • Boiler, T. and Métraux, J.-P. (1988) Extracellular localization of chitinase in cucumber. Physiol. Mol. Plant Pathol. 33,11–16.

    Article  Google Scholar 

  • Boiler, T. and Vögeli, U. (1984) Vacuolar localization of ethylene-induced chitinase in bean leaves. Plant Physiol. 74, 442–444.

    Article  Google Scholar 

  • Boiler, T., Gehri, A., Mauch, F. and Vögeli, U. (1983) Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function. Planta 157, 22–31.

    Article  Google Scholar 

  • Broekaert, W.F., Van Parijs, J., Allen, A.K. and Peumans, W.J. (1988) Comparison of some molecular, enzymatic, and antifungal properties of chitinases from thorn-apple, tobacco, and wheat Physiol. Mol. Plant Pathol. 33, 319–331.

    Article  CAS  Google Scholar 

  • Broekaert, W.F., Van Parijs, J., Leyns, F., Joos, H. and Peumans, W.J. (1989) A chitin-binding lectin from stinging nettle rhizomes with antifungal properties. Science 245,1100–1102.

    Article  PubMed  CAS  Google Scholar 

  • Broekaert, W.F., Terras, F.R.G., Cammue, B.P.A. and Vanderleyden, J. (1990) An automated quantitative assay for fungal growth inhibiton. FEMS Microbiol. Lett. 69, 55–60.

    Article  CAS  Google Scholar 

  • Broglie, K., Chet, I., Holliday, M., Cressman, R., Biddle, P., Knowlton, S., Mauvis, C.J. and Broglie, R. (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254,1194–1197.

    Article  PubMed  CAS  Google Scholar 

  • Côté, F., Cutt, J.R., Asselin, A. and Klessig, D.F. (1991) Pathogenesis-related acidic ß-1,3-glucanase genes of tobacco are regulated by both stress and developmental signals. Mol. Plant-Microbe Interact. 4, 173–181.

    Article  PubMed  Google Scholar 

  • Darvill, A.G. and Albersheim, P. (1984) Phytoalexins and their elicitors - a defense against microbial infections in plants. Annu. Rev. Plant Physiol. 35,243–275.

    Article  CAS  Google Scholar 

  • De Jong, A., Cordewener, J., Lo Schiavo, F., Terzi, M., Vandekerckhove, J., Van Kammen, A. and De Vries, S.C. (1992) A carrot somatic embryo mutant is rescued by chitinase. Plant Cell 4,425–433.

    PubMed  Google Scholar 

  • Felix, G. and Meins, F., Jr. (1986) Developmental and hormonal regulation of ß-l,3-glucanase in tobacco. Planta 167, 206–211.

    Article  CAS  Google Scholar 

  • Granade, T.C., Hehmann, M.F. and Artis, W.M. (1985) Monitoring of filamentous fungal growth by in situ microspectrophotometry, fragmented mycelium absorbance density, and 14C incorporation: alternatives to mycelial dry weight. Appl. Environ. Microbiol. 49, 101–108.

    PubMed  CAS  Google Scholar 

  • Grenier, J. and Asselin, A. (1990) Some pathogenesis-related proteins are chitosanases with lytic activity against fungal spores. Mol. Plant-Microbe Interact 3, 401–407.

    Article  CAS  Google Scholar 

  • Ham, K.-S., Kaufmann, S., Albersheim, P. and Darvill, A.G. (1991) Host-Pathogen Interactions XXXIX. A soybean pathogenesis-related protein with ß-l,3-glucanase activity releases phytoalexin elicitor-active heat-stable fragments from fungal cell walls. Mol. Plant-Microbe Interact. 4,545–552.

    Article  CAS  Google Scholar 

  • Inouhe, M. and Nevins, D.J. (1991) Inhibition of auxin-induced cell elongation of maize coleoptiles by antibodies specific for cell wall glucanases. Plant Physiol. 96, 426–431.

    Article  PubMed  CAS  Google Scholar 

  • Joosten, M.H.A.J. and de Wit, P.J.G.M. (1989) Identification of several pathogenesis-related proteins in tomato leaves inoculated with Cladosporium fulvum (syn. Fulvia fulva) as 1,3-ß-glucanases and chitinases. Plant Physiol. 89, 945–951.

    Article  PubMed  CAS  Google Scholar 

  • Kaufrmann, S., Legrand, M., Geoffroy, P. and Fritig, B. (1987) Biological function of “pathogenesis-related” proteins: four PR proteins of tobacco have 1,3-ß-glucanase activity. EMBO J. 6, 3209–3212.

    Google Scholar 

  • Keefe, D., Hinz, U. and Meins, F., Jr. (1990) The effect of ethylene on the cell-type-specific and intracellular localization of ß-l,3-glucanase and chitinase in tobacco leaves. Planta 182, 43–51.

    Article  CAS  Google Scholar 

  • Koide R.T. and Schreiner R.P. (1992) Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 557–581.

    Article  CAS  Google Scholar 

  • Kombrink, E. and Hahlbrock, K. (1986) Resposes of cultured parsley cells to elicitors from phytopathogenic fungi. Timing and dose dependency of elicitor-induced reactions. Plant Physiol. 81, 216–221.

    Article  PubMed  CAS  Google Scholar 

  • Kombrink, E., Schröder, M., and Hahlbrock, K. (1988) Several “pathogenesis-related” proteins in potato are 1,3-ß-glucanases and chitinases. Proc. Natl. Acad. Sci. USA 85,782–786.

    Article  PubMed  CAS  Google Scholar 

  • Kunz, C., Ludwig, A., Bertheau, Y. and Boiler, T. (1992) Evaluation of the antifungal activity of the purified chitinase 1 from the filamentous fungus Aphanocladium album. FEMS Microbiol. Lett. 90,105–110.

    Article  CAS  Google Scholar 

  • Lawton, K., Ward, E., Payne, G., Moyer, M. and Ryals, J. (1992) Acidic and basic class III mRNA accumulation in response to TMV infection of tobacco. Plant Mol. Biol. 19, 735–743.

    Article  PubMed  CAS  Google Scholar 

  • Leah, R., Tommerup, H., Svendsen, I. and Mundy, J. (1991) Biochemical and molecular characterization of three barley seed proteins with antifungal properties. J. Biol. Chem. 266, 1564–1573.

    PubMed  CAS  Google Scholar 

  • Legrand, M., Kauffmann, S., Geoffroy, P. and Fritig, B. (1987) Biological function of pathogenesis-related proteins: four tobacco pathogenesis-related proteins are chitinases. Proc. Natl. Acad. Sci. USA 84,6750–6754.

    Article  PubMed  CAS  Google Scholar 

  • Linthorst, H.J.M. (1991) Pathogenesis-related proteins of plants. Crit. Rev. Plant Sci. 10, 123–150.

    Article  CAS  Google Scholar 

  • Lotan, T., Ori, N. and Fluhr, R. (1989) Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell 1, 881–887.

    PubMed  CAS  Google Scholar 

  • Lucas, J., Henschen, A., Lottspeich, F., Vögeli, U. and Boiler, T. (1985) Amino-terminal sequence of ethylene-induced bean leaf chitinase reveals similarities to sugar-binding domains of wheat germ agglutinin. FEBS Lett. 193, 208–210.

    Article  CAS  Google Scholar 

  • Ludwig, A. and Boiler, T. (1990) A method for the study of fimgal growth inhibition by plant proteins. FEMS Microbiol. Lett. 69, 61–66.

    Article  CAS  Google Scholar 

  • Mauch, F. and Staehelin, L.A. (1989) Functional implications of the subcellular localization of ethylene-induced chitinase and ß-l,3-glucanase in bean leaves. Plant Cell 1,447–457.

    PubMed  CAS  Google Scholar 

  • Mauch, F., Hadwiger, L.A. and Boiler, T. (1984) Ethylene: symptom, not signal for the induction of chitinase and ß-l,3-glucanase in pea pods by pathogens and elicitors. Plant Physiol. 76, 607–611.

    Article  PubMed  CAS  Google Scholar 

  • Mauch, F., Hadwiger, L.A. and Boiler, T. (1988a) Antifungal hydrolases in pea tissue I. Purification and characterization of two chitinases and two ß-l,3-glucanases differentially regulated during development and in response to fungal infectioa Plant Physiol. 87,325–333.

    Article  PubMed  CAS  Google Scholar 

  • Mauch, F., Mauch-Mani-B. and Boiler, T. (1988b) Antifungal hydrolases in pea tissue II. Inhibition of fungal growth by combinations of chitinase and ß-l,3-glucanase. Plant Physiol. 88, 936–942.

    Article  PubMed  CAS  Google Scholar 

  • Meins, F., Jr. and Ahl, P. (1989) Induction of chitinase and ß-l,3-glucanase in tobacco leaves infected with Pseudomonas tabaci and Phytophthora parasitica var. nicotianae. Plant Sci. 61, 155–161.

    Article  CAS  Google Scholar 

  • Meins, F., Jr., Neuhaus, J.-M., Sperisen, C. and Ryals, J. (1992) The primary structure of plant pathogenesis-related glucanohydrolases and their genes, in F. Meins, Jr., and T. Boiler (eds.), Genes Involved in Plant Defense, Springer Verlag, Vienna/New York, pp. 245–282.

    Chapter  Google Scholar 

  • Métraux, J.-P., Burkhart, W., Moyer, M., Dincher, S., Middlesteadt, W. Williams, S., Payne, G., Carnes, M. and Ryals, J. (1989) Isolation of a complementary DNA encoding a chitinase with structural homology to a bifunctional lysozyme/chitinase. Proc. Natl. Acad. Sci. USA 86, 896– 900.

    Article  PubMed  Google Scholar 

  • Minelman, D., Galun, E., Sharon, N. and Lotan R. (1975) Inhibition of fungal growth by wheat germ agglutinia. Nature 256, 414–416.

    Article  Google Scholar 

  • Neale, A.D., Wahleithner, J.A., Lund, M., Bonnett, H.T., Kelly, A., Meeks-Wagner, D.R., Peacock, W.J. and Dennis, E.S. (1990) Chitinase, ß-l,3-glucanase, osmotin and extensin are expressed in tobacco explants during flower formation. Plant Cell 2, 673–684.

    PubMed  CAS  Google Scholar 

  • Neuhaus, J.-M., Ahl-Goy, P., Hinz, U., Flores, S. and Meins, F., Jr. (1991a) High-level expression of a tobacco chitinase gene in Nicotiana sylvestris. Susceptibility of transgenic plants to Cercospora nicotianae infection. Plant Mol. Biol. 16,141–151.

    Article  PubMed  CAS  Google Scholar 

  • Neuhaus, J.-M., Sticher, L., Meins, F., Jr. and Boiler, T. (1991b) A short C-terminal sequence is necessary and sufficient for the targeting of chitinases to the plant vacuole. Proc. Natl. Acad. Sci. USA 88,10362–10366.

    Article  PubMed  CAS  Google Scholar 

  • Payne, G., Ahl, P., Moyer, M., Harper, A., Beck, J., Meins, F., Jr. and Ryals, J. (1990a) Isolation of complementary DNA clones encoding pathogenesis-related proteins P and Q, two acidic chitinases from tobacco. Proc. Natl. Acad. Sci. USA 87, 98–102.

    Article  PubMed  CAS  Google Scholar 

  • Payne, G., Ward, E., Gaffhey, T., Ahl-Goy, P., Moyer, M., Harper, A., Meins, F., Jr. and Ryals, J. (1990b) Evidence for a third structural class of ß-l,3-glucanase in tobacco. Plant Mol. Biol. 15, 797–808.

    Article  PubMed  CAS  Google Scholar 

  • Pegg, G.F. and Young, D.H. (1982) Purification and characterization of chitinase enzymes from healthy and Verticilliwn albo-atrwn-Mected tomato plants, and from Verticillium albo-atrum. Physiol. Plant Pathol. 21,389–409.

    Article  CAS  Google Scholar 

  • Roberts, W.K. and Selitrennikoff, C.P. (1988) Plant and bacterial chitinases differ in antifungal activity. J. Gea Microbiol. 134, 169–176.

    CAS  Google Scholar 

  • Schlumbaum, A., Mauch, F., Vögeli, U. and Boiler, T. (1986) Plant chitinases are potent inhibitors of fungal growth. Nature 324, 365–367.

    Article  CAS  Google Scholar 

  • Schröder, M., Hahlbrock, K. and Kombrink, E. (1992) Temporal and spatial patterns of 1,3-ß-glucanase and chitinase induction in potato leaves infected by Phytophthora infestans. Plant J. 2,161–172.

    Article  Google Scholar 

  • Shinshi, H., Mohnen, D. and Meins, R, Jr. (1987) Regulation of a plant pathogenesis-related enzyme: inhibition of chitinase and chitinase mRNA accumulation in cultured tobacco tissues by auxin and cytokinin. Proc. Natl. Acad. Sci. USA 84, 89–93.

    Article  PubMed  CAS  Google Scholar 

  • Shinshi, H., Wenzler, H., Neuhaus, J.-M., Felix, G., Hofsteenge, J. and Meins, F., Jr. (1988) Evidence for N- and C-terminal processing of a plant defense-related enzyme. Primary structure of tobacco prepro-ß-l,3-glucanase. Proc. Natl. Acad. Sci. USA 85, 5541–5545.

    Article  PubMed  CAS  Google Scholar 

  • Shinshi, H., Neuhaus, J.-M., Ryals, J. and Meins, F., Jr. (1990) Structure of a tobacco endochitinase gene: evidence that different chitinase genes can arise by transposition of sequences encoding a cysteine-rich domain. Plant Mol. Biol. 14, 357–368.

    Article  PubMed  CAS  Google Scholar 

  • Taiz, L. (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu. Rev. Plant Physiol. 35, 585–657.

    Article  CAS  Google Scholar 

  • Takeuchi, Y., Yoshikawa, M., Takeba, G., Tanaka, K., Shibata, D. and Horino, O. (1990) Molecular cloning and ethylene induction of mRNA encoding a phytoalexin elicitor-releasing factor, ß-l,3-endoglucanase, in soybean. Plant Physiol. 93,673–682.

    Article  PubMed  CAS  Google Scholar 

  • van den Bulcke, M., Bauw, G., Castresana, C., van Montagu, M., Vanderkerckhove, J. (1989) Characterization of vacuolar and extracellular ß-l,3-glucanases of tobacco: evidence for a strictly compartmentalized plant defense system. Proc. Natl. Acad. Sci. USA 86, 2673–2677.

    Article  PubMed  CAS  Google Scholar 

  • Van Parijs, J., Broekaert, W.F., Goldstein, I.J. and Peumans, W.J. (1991) Hevein: an antifungal protein from rubber-tree (Hevea brasiliensis) latex. Planta 183, 258–264.

    Article  Google Scholar 

  • Verburg, J.G. and Huynh, Q.K. (1991) Purification and characterization of an antifungal chitinase from Arabidopsis thaliana. Plant Physiol. 95,450–455.

    Article  PubMed  CAS  Google Scholar 

  • Vögeli, U., Meins, F., Jr. and Boiler, T. (1988) Co-ordinated regulation of chitinase and ß-1,3- glucanase in bean leaves. Planta 174, 364–372.

    Article  Google Scholar 

  • Vögeli-Lange, R., Hansen-Gehri, A., Boiler, T. and Meins, F., Jr. (1988) Induction of the defense related glucanohydrolases, ß-l,3-glucanase and chitinase, by tobacco mosaic virus infection of tobacco leaves. Plant Sci. 54, 171–176.

    Article  Google Scholar 

  • Ward, E.R., Payne, G.B., Moyer, M.B., Williams, S.C., Dincher, S.S., Sharkey, K.C., Beck, J.J., Taylor, H.T., Ahl-Goy, P., Meins, F., Jr. and Ryals, J.A. (1991) Differential regulation of ß-1,3-glucanase messenger RNAs in response to pathogen infection. Plant Physiol. 96, 390–397.

    Article  PubMed  CAS  Google Scholar 

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Boller, T. (1993). Antimicrobial Functions of the Plant Hydrolases, Chitinase and ß-1,3-Glucanase. In: Fritig, B., Legrand, M. (eds) Mechanisms of Plant Defense Responses. Developments in Plant Pathology, vol 2. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-1737-1_124

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  • DOI: https://doi.org/10.1007/978-94-011-1737-1_124

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