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Effect of Nikkomycin Z, a chitin-synthase inhibitor, on hyphal growth and cell wall structure of two arbuscular-mycorrhizal fungi

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Summary

Different concentrations of Nikkomycin Z, a competitive inhibitor of chitin-synthase, were applied to the arbuscular-mycorrhizal fungi (AMF)Gigaspora margarita andGlomus intraradices under in vitro conditions. These two fungi are known to differ in the structure and composition of their cell wall. The two AMF were able to grow in the presence of a higher concentration of this antibiotic than so far reported for other fungi. Fluorescence, electron microscopic and cytochemical studies showed that the blocking of the fungal chitin-synthase activity induces alterations in hyphal morphology, a reduction in fungal wall thickness, and several other changes in the hyphal wall structure and organization. The possible role of chitin-synthase in the hyphal growth and morphogenesis of these symbiotic fungi and its putative regulation by the host plant during the symbiosis are discussed.

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Abbreviations

AM:

arbuscular mycorrhiza

AMF:

arbuscular-mycorrhizal fungus

DAPI:

4′-6-diamidino-2-phenylindole

MIC:

minimal inhibitory concentration

NAG:

N-acetylglucosamine

TEM:

transmission electron microscopy

T50, T5, T0.5:

treatments with different Nikkomycin Z concentrations (50 μg/ml, 5 μg/ml, 0.5 μg/ml)

UDP-NAG:

uridine-diphosphate-N-acetylglucosamine

WGA:

wheat germ agglutinin

References

  • Allen AK, Neuberger A, Sharon N (1973) The purification, composition and specificity of wheat germ agglutinin. Biochem J 131: 155–162

    Google Scholar 

  • Arlorio M, Ludwig A, Boller T, Mischiati P, Bonfante P (1991) Effects of chitinase and β-1,3-glucanase from pea on the growth of saprophitic, pathogenic and mycorrhizal fungi. G Bot Ital 125: 956–958

    Google Scholar 

  • Åström H, Giovannetti M, Raudaskoski M (1994) Cytoskeletal components in the arbuscular mycorrhizal fungusGlomus mosseae. Mol Plant Microbe Interact 7: 309–312

    Google Scholar 

  • Bartnicki-Garcia S (1987) The cell wall: a crucial structure in fungal evolution. In: Rayner DM, Brasier CM, Moore D (eds) Evolutionary biology of the fungi. Cambridge University Press, Cambridge, pp 389–403

    Google Scholar 

  • Bécard G, Piché Y (1989) Fungal growth stimulation by CO2 and root exudates in vesicular-arbuscular mycorrhizal symbiosis. Appl Environ Microbiol 55: 2320–2325

    Google Scholar 

  • Benhamou N (1989) Preparation and application of lectin-gold complexes. In: Hayat MA (ed) Colloidal gold, Principles, methods and applications. Academic Press, San Diego, pp 96–145

    Google Scholar 

  • Bonfante P, Perotto S (1995) Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol 130: 3–21

    Google Scholar 

  • Bonfante-Fasolo P (1984) Anatomy and morphology of VA mycorrhizae. In: Powell CL. Bajyaraj DJ (eds) VA mycorrhiza. CRC Press, Boca Raton, pp 5–33

    Google Scholar 

  • — (1987) Vesicular-arbuscular mycorrhizae: fugus-plant interactions at the cellular level. Symbiosis 3: 249–268

    Google Scholar 

  • — (1988) The role of the cell wall as a signal in mycorrhizal associations. In: Scannerini S, Smith D, Bonfante-Fasolo P, Gianinazzi-Pearson V (eds) Cell to cell signals in plant, animal and microbial symbiosis. Springer, Berlin Heidelberg New York Tokyo, pp 219–236 (NATO ASI series, series H, vol 17)

    Google Scholar 

  • —, Grippiolo R (1982) Ultrastructural and cytochemical changes in the wall of a vesicular-arbuscular mycorrhizal fungus during symbiosis. Can J Bot 60: 2303–2312

    Google Scholar 

  • — — (1984) Cytochemical and biochemical observations on the cell wall of the spore ofGlomus epigaeum. Protoplasma 123: 140–151

    Google Scholar 

  • —, Faccio A, Perotto S, Schubert A (1990) Correlation between chitin distribution and cell wall morphology in the mycorrhizal fungusGlomus versiforme. Mycol Res 94: 157–165

    Google Scholar 

  • Cassone A (1986) Cell walls of pathogenic yeasts and implications for antimycotic therapy. Drugs Exp Clin Res 12: 635–643

    Google Scholar 

  • Cabib E (1991) Differential inhibition of chitin synthases 1 and 2 fromSaccharomyces cerevisiae by Polioxin D and nikkomycins. Antimicrob Agents Chem 35: 170–173

    Google Scholar 

  • Chabot S, Bécard G, Piché Y (1992) Life cycle ofGlomus intraradix in root organ culture. Mycologia 84: 315–321

    Google Scholar 

  • Chapman T, Kinsman O, Houston J (1992) Chitin biosynthesis inCandida albicans grown in vitro and in vivo and its inhibition by Nikkomycin Z. Antimicrob Agents Chem 36: 1909–1914

    Google Scholar 

  • Cohen E (1987) Chitin biochemistry: synthesis and inhibition. Annu Rev Entomol 32: 71–93

    Google Scholar 

  • Cubero B, Ruiz-Herrera J, Cerdà-Olmedo E (1993) Chitin synthetase mutants ofPhycomyces blakesleeanus. Mol Gen Genet 240: 9–16

    Google Scholar 

  • Dähn U, Hagenmaier H, Höhne H, König WA, Wolf G, Zähner H (1976) Stoffwechselprodukte von Mikroorganismen. 154. Mitteilung. Nikkomycin, ein neuer Hemmstoff der Chitinsynthese bei Pilzen. Arch Microbiol 107: 143–160

    Google Scholar 

  • Decker H, Zähner H, Heitsch H, König WA, Fiedler H-P (1991) Structure-activity relationships of the nikkomycins. J Gen Microbiol 137: 1805–1813

    Google Scholar 

  • Dumas-Gaudot E, Grenier J, Furlan V, Asselin A (1992) Chitinase, chitosanase and β-1,3-glucanase activities inAllium andPisum roots colonized byGlomus species. Plant Sci 84: 17–24

    Google Scholar 

  • Ebel J, Cosio EG (1994) Elicitors of plant defense responses. Int Rev Cytol 148: 1–36

    Google Scholar 

  • Elorza MV, Murgui A, Rico H, Miragall F, Sentandreu R (1987) Formation of new cell wall by protoplasts ofCandida albicans: effect of Papulacandin B, Tunicamycin and Nikkomycin. J Gen Microbiol 133: 2315–2325

    Google Scholar 

  • Franke M, Morton J (1994) Ontogenic comparison of the arbuscular mycorrhizal fungiScutellospora heterogama andScutellospora pellucida: revision of taxonomical character concepts, species description and phylogenetic hypotheses. Can J Bot 72: 122–134

    Google Scholar 

  • Gerdemann JW, Nicolson JH (1963) Spores of mycorrhizalEndogone species extracted from soil by wet-sieving and decanting. Trans Br Mycol Soc 46: 235–244

    Google Scholar 

  • Gianinazzi-Pearson V, Lemoine M-C, Gollotte A, Morton JB (1994) Localization of β (1 → 3) glucans in spore and hyphal walls of fungi in the Glomales. Mycologia 86: 478–485

    Google Scholar 

  • Giovannetti M, Gianinazzi-Pearson V (1994) Biodiversity in arbuscular mycorrhizal fungi. Mycol Res 98: 705–715

    Google Scholar 

  • Grandmaison J, Benhamou N, Furlan V, Visser SA (1988) Ultrastructural localization of N-acetylglucosamine residues in the cell wall ofGigaspora margarita throughout its life-cycle. Biol Cell 63: 89–100

    Google Scholar 

  • Hadwiger LA, Kendra DF, Fristensky GW, Wagoner W (1986) Chitosan both activates genes in plants and inhibits RNA synthesis in fungi. In: Muzzarelli R, Jeuniaux C, Gooday GW (eds) Chitin in nature and technology. Plenum, New York, pp 209–214

    Google Scholar 

  • Halbrock B, Cuypers B, Douglas C, Fritzmeier KH, Hoffman H, Rohwer F, Scheel D, Schulz W (1986) Biochemical interactions of plants with potentially pathegenic fungi. In: Lugtenberg B (ed) Recognition in microbe-plant symbiotic and pathogenic interactions. Springer, Berlin Heidelberg New York Tokyo, pp 311–323

    Google Scholar 

  • Harley JL, Smith SE (1983) Mycorrhizal symbiosis. Academic Press, London

    Google Scholar 

  • Heath B (1987) Fluorescent staining of fungal nuclei. In: Fuller MS, Jaworski A (eds) Zoosporic fungi in teaching and research. Southeastern Publishing, Greenville, NC, pp 169–171

    Google Scholar 

  • Jacquelinet-Jeanmougin J, Gianinazzi-Pearson V, Gianinazzi S (1987) Endomycorrhizas in the Gentianaceae. II. Ultrastructural aspects of symbionts relationships inGentiana lutea L. Symbiosis 3: 269–286

    Google Scholar 

  • Koide RT, Schreiner RP (1992) Regulation of the vesicular-arbuscular mycorrhizal symbiosis. Annu Rev Plant Mol Biol 43: 557–581

    Google Scholar 

  • Lambais MR, Mehdy C (1993) Suppression of endochitinase, β-1,3-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhizal roots under different soil phosphate conditions. Mol Plant Microbe Interact 6: 75–83

    Google Scholar 

  • Lewis DH (1991) Fungi and sugars — a suite of interactions. Mycol Res 95: 897–904

    Google Scholar 

  • Marsh BAB (1971) Measurement of length in random arrangement of lines. J Appl Ecol 8: 265–267

    Google Scholar 

  • Mosse B (1962) The stablishment of vesicular-arbuscular mycorrhiza under aseptic conditions. J Gen Microbiol 27: 509–520

    Google Scholar 

  • Müller H, Furter R, Zähner H, Rast DM (1981) Metabolie products of microorganisms. 203. Inhibition of chitosomal chitin synthetase and growth ofMucor rouxiii by Nikkomycin Z, Nikkomycin X, and Polyoxin A: a comparison. Arch Microbiol 130: 195–197

    Google Scholar 

  • Nicholas RO, Williams DW, Hunter PA (1994) Investigation of the value of β-glucan-specific fluorochromes for predicting the β-glucan content of the cell walls of zoopathogenic fungi. Mycol Res 98: 694–698

    Google Scholar 

  • Peberdy JF (1979) Fungal protoplasts: isolation, reversion and fusion. Annu Rev Microbiol 33: 21–39

    Google Scholar 

  • Pozo MJ, Dumas-Gaudot E, Slezack S, Cordier C, Asselin A, Gianinazzi S, Gianinazzi-Pearson V, Azcon-Aguilar C, Barea JM (1996) Detection of new chitinase isoforms in arbuscular mycorrhizal tomato roots: implications in protection againstPhytophthora nicotianae var. parasitica. Plant Soil (in press)

  • Reinhardt MO (1892) Das Wachstum der Pilzhyphen. Jahrb Wiss Bot 23: 479–565

    Google Scholar 

  • Roth J (1983) Application of lectin-gold complexes for electron microscopic localization of glycoconjugates on thin sections. J Histochem Cytochem 31: 987–999

    Google Scholar 

  • Sentandreu R, Mormeneo S, Ruiz-Herrera J (1994) Biogenesis of the fungal cell wall. In: Esser K, Lemke PA (eds) The Mycota. I. Growth, differentiation and sexuality. Springer, Berlin Heidelberg New York Tokyo, pp 111–124

    Google Scholar 

  • Simon L, Bousquet J, Lévesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular lands plants. Nature 363: 67–69

    Google Scholar 

  • Spanu P, Boller T, Ludwig A, Wiemken A, Faccio A, Bonfante-Fasolo P (1989) Chitinase in roots of mycorrhizalAllium porrum: regulation and localization. Planta 177: 447–455

    Google Scholar 

  • Vierheilig H, Alt M, Neuhaus J-M, Boller T, Wiemken A (1993) Colonization of transgenicNicotiana plants, expressing different forms ofNicotiana tabacum chitinase, by the root pathogenRhizoctonia solani and the mycorrhizal symbiontGlomus mosseae. Mol Plant Microbe Interact 6: 261–264

    Google Scholar 

  • — —, Mohr U, Boiler T, Wiemken A (1994) Ethylene biosynthesis and activities of chitinase and β-1,3-glucanase in the roots of host and non-host plants of vesicular-arbuscular mycorrhizal fungi after inoculation withGlomus mosseae. J Plant Physiol 143: 337–343

    Google Scholar 

  • — —, Lange J, Gut-Rella M, Wiemken A, Boller T (1995) Colonization of transgenic tobacco constitutively expressing pathogenesis-related proteins by the vesicular-arbuscular mycorrhizal fungusGlomus mosseae. Appl Environ Microbiol 61: 3031–3034

    Google Scholar 

  • Volpin H, Elkind Y, Okon Y, Kapulnik Y (1994) A vesicular arbuscular mycorrhizal fungus (Glomus intraradix) induces a defence response in alfalfa roots. Plant Physiol 104: 683–689

    Google Scholar 

  • Wessels JGH (1994) Developmental regulation of fungal cell wall formation. Annu Rev Phytopathol 32: 413–437

    Google Scholar 

  • Wood PJ, Fulcher RG (1983) Dye interactions. A basis for specific detection and histochemistry of polysaccharides. J Histochem Cytochem 31: 823–826

    Google Scholar 

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Bago, B., Chamberland, H., Goulet, A. et al. Effect of Nikkomycin Z, a chitin-synthase inhibitor, on hyphal growth and cell wall structure of two arbuscular-mycorrhizal fungi. Protoplasma 192, 80–92 (1996). https://doi.org/10.1007/BF01273247

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