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Ultrastructural and cytochemical characterization of elicitor-induced structural responses in tomato root tissues infected by Fusarium oxysporum f.sp. radicis-lycopersici

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Abstract

Commercial chitosan and laminarin, as well as β-glucans, isolated from either Phytophthora megasperma f.sp. glycinea or Saccharomyces cerevisiae, were applied to decapitated tomato (Lycopersicon esculentum Mill.) plants and evaluated for their potential to induce defense mechanisms in root tissues infected by Fusarium oxysporum f.sp. radicis-lycopersici. A significant decrease in disease incidence was monitored in elicitor-treated plants as compared to water-treated plants. No difference was detected in the capacity of the elicitors under study to confer enhanced protection against pathogen attack. Ultrastructural investigations of the infected root tissues from watertreated (control) plants showed a rapid colonization of all tissues including the vascular stele. Fungal ingress was lways associated with marked host cell disorganization and cell wall alteration. In root tissues from elicitortreated plants, restriction of fungal growth to the epidermis and the outer cortex, decrease in pathogen viability, and formation of numerous wall appositions at sites of attempted penetration were the main features of the hostpathogen interaction. The wall appositions were found to vary greatly in their appearance from multi-textured to multi-layered structures, from elongated deposits to hemispherical protuberances. Application of various goldcomplexed probes to root tissue sections revealed that callose, pectin and phenolic-like compounds (likely lignin) were the main components of the newly-formed barriers. By contrast, cellulose appeared confined to outer or intermediate layers resembling the host cell wall in terms of structure and architecture. In the absence of fungal challenge, the cytologically visible consequences of elicitation were restricted to a discrete deposition of electron-opaque substances in the vacuoles of some cells, and wall appositions were not detected. The key importance of fungal challenge in the elaboration of defense mechanisms is discussed in relation to the possibility that an alarm ignal provided by the pathogen itself is required for the expression of resistance in plants previously sensitized by an exogenous elicitor.

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Abbreviations

AGL:

Aplysia gonad lectin

FORL:

Fusariumoxysporum f.sp. radicis-lycopersici

References

  • Albersheim, P., Mühlethaler, K., Frey-Wyssling, A. (1960) Stained pectin as seen in the electron microscope. J. Biophys. Biochem. Cytol. 8, 501–506

    Google Scholar 

  • Benhamou, N. (1992) Ultrastructural detection of β-1,3-glucans in tobacco root tissues infected by Phytophthora parasitica var. nicotianae using a gold-complexed tobacco β-1,3-glucanase. Physiol. Mol. Plant Pathol. 41, 351–370

    Google Scholar 

  • Benhamou, N., Theriault, G. (1992) Treatment with chitosan enhances resistance of tomato plants to the crown and root rot pathogen, Fusarium oxysporum f.sp. radicis-lycopersici. Physiol. Mol. Plant Pathol. 41, 33–52

    Google Scholar 

  • Benhamou, N., Chamberland, H., Ouellette, G.B., Pauze, F.J. (1987) Ultrastructural localization of β-1,4-d-glucans in two pathogenic fungi and in their host tissues by means of an exoglucanase-gold complex. Can. J. Microbiol. 33, 405–417

    Google Scholar 

  • Benhamou, N., Gilboa-Garber, N., Trudel, J., Asselin, A. (1988) Introduction of a new lectin-gold complex for the ultrastructural localization of galacturonic acids. J. Histochem. Cytochem. 36, 1403–1411

    Google Scholar 

  • Benhamou, N., Mazau, D., Grenier, J., Esquerré-Tugayé, M.T. (1991) Time-course study of the accumulation of hydroxyprolinerich glycoproteins in root cells of susceptible and resistant tomato plants infected by Fusarium oxysporum f.sp. radicis-lycopersici. Planta 184, 196–208

    Google Scholar 

  • Benhamou, N., Fortin, J.A., Hamel, C., St Arnaud, M., Shatilla, A. (1994) Resistance responses of mycorrhizal Ri T-DNA transformed carrot roots to infection by Fusarium oxysporum f.sp. chrysanthemi. Phytopathology 84, 958–968

    Google Scholar 

  • Berstein, M.H. (1956) Iron as a stain for nucleic acids in electron microscopy. J. Biophys. Biochem. Cytol. 2, 633–634

    Google Scholar 

  • Blanchette, R.A. (1991) Delignification by wood-decay fungi. Annu. Rev. Phytopathol. 29, 381–398

    Google Scholar 

  • Bonhoff, A., Reith, B., Golecki, J., Grisebach, H. (1987) Race cultivar-specific differences in callose deposition in soybean roots following infection with Phytophthora megasperma f.sp. glycinea. Planta 172, 101–105

    Google Scholar 

  • Brammall, R.A., Higgins, V.J. (1988) A histological comparison of fungal colonization in tomato seedlings susceptible and resistant toFusarium crown and root rot disease. Can. J. Bot. 66, 915–925

    Google Scholar 

  • Bruce, R.J., West, C.A. (1989) Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean. Plant Physiol. 91, 889–897

    Google Scholar 

  • Cabib, E., Bowers, B. (1971) Chitin and yeast budding: Localization of chitin in bud scars. J. Biol. Chem. 246, 152–159

    Google Scholar 

  • Charest, P.M., Ouellette, G.B., Pauze, F.J. (1984) Cytological observations of early infection process of Fusarium oxysporum f.sp. radicis-lycopersici. Can. J. Bot. 62, 1232–1244

    Google Scholar 

  • Chérif, M., Benhamou, N., Menzies, J.G., Bélanger, R.R. (1992) Silicon induced resistance in cucumber plants against Pythium ultimums. Physiol. Mol. Plant Pathol. 41, 411–425

    Google Scholar 

  • Chet, I., Hens, Y., Mitchell, R. (1967) Chemical composition of hyphal and sclerotial walls of Sclerotium rolfsii Sacc. Can. J. Microbiol. 13, 137–141

    Google Scholar 

  • Collmer, A., Keen, N.T. (1986) The role of pectic enzymes in plant pathogenesis. Annu. Rev. Phytopathol. 24, 383–409

    Google Scholar 

  • Dixon, R.A., Lamb, C.J. (1990) Molecular communication in interactions between plants and microbial pathogens. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 339–367

    Google Scholar 

  • Frens, G., (1973) Controlled nucleation for the regulation of the particle size in monodisperse gold solutions. Nature Phys. Sci. 241, 20–22

    Google Scholar 

  • Fry, S.C. (1986) Polymer-bound phenols as natural substrates of peroxidases. In: Molecular and physiological aspects of plant peroxidase, pp. 169–182, Greppin, H., Penel, C., Gaspar, Th., eds., Université de Genève, Switzerland

    Google Scholar 

  • Geiger, J.P., Rio, B., Nandris, D., Nicole, M. (1986) Laccases of Rigidoporus lignosus and Phellinus noxius; 1. Purification and some physicochemical properties. Appl. Biochem. Biotechnol. 12, 121–133

    Google Scholar 

  • Hahlbrock, K., Scheel, D. (1989) Physiology and molecular biology of phenylpropanoid metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 347–364

    Google Scholar 

  • Hahn, M.G., Bucheli, P., Cervone, F., Doares, S.H., O'Neill, R.A., Darvill, A., Albersheim, P. (1989) The roles of cell wall constituents in plant-pathogen interactions. In: Plant-microbe interactions, vol. 3, pp. 131–181, Nester, E., Kosuge, T. eds. Mc Graw-Hill, New York

    Google Scholar 

  • Jarvis, W.R. (1988) Fusarium crown and root rot of tomatoes. Phytoprotection 69, 49–64

    Google Scholar 

  • Kúc, J., (1987) Plant immunization and its applicability for disease control. In: Innovative approaches to plant disease control, pp. 255–274, Chet, L., ed. John Wiley & Sons, New York

    Google Scholar 

  • Mayer, A.M. (1987) Polyphenol oxidases in plants: recent progress. Phytochemistry 26, 11–20

    Google Scholar 

  • Minor, J.L. (1991) Location of lignin-bonded polysaccharides. J. Wood Chem. Technol. 11, 159–169

    Google Scholar 

  • Ricci, P., Bonnet, P., Huet, J.C., Sallantin, M., Beauvais-Cante, F., Bruneteau, M., Billard, V., Michel, G., Pernollet, J.C. (1989) Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco. Eur. J. Biochem. 183, 555–563

    Google Scholar 

  • Ride, J.P. (1983) Cell wall and other structural barriers in defense. In: Biochemical plant pathology, pp. 215–235, Callow, J.A. ed. John Wiley & Sons, New York

    Google Scholar 

  • Ride, J.P., Barber, M.S. (1987) The effects of various treatments on induced lignification and resistance of wheat to fungi. Physiol. Mol. Plant Pathol. 31, 349–360

    Google Scholar 

  • Robb, J., Brisson, J.D., Busch, L., Lu, B.C. (1978) Ultrastructure of wilt syndrome caused by Verticillium dahliae. Attempted localization of phenolic compounds in the vascular region. Can. J. Bot. 56, 2594–2612

    Google Scholar 

  • Ryerson, D.E., Heath, M.C. (1992) Fungal elicitation of wall modification in leaves of Phaseolus vulgaris L. cv. Pinto. II. Effect of fungal wall components. Physiol. Mol. Plant Pathol. 40, 283–298

    Google Scholar 

  • Sharp, J.K., Valent, B., Albersheim, P. (1984) Purification and partial characterization of a β-glucan fragment that elicits phytoalexin accumulation in soybean. J. Bio. Chem. 259, 11312–11320

    Google Scholar 

  • Sherwood, R.T., Vance, C.P. (1976) Histochemistry of papillae formed in reed canarygrass leaves in response to noninfecting pathogenic fungi. Phytopathology 66, 503–510

    Google Scholar 

  • Southerton, S.G., Deverall, B.J. (1990). Changes in phenolic acid level in wheat leaves expressing resistance to Puccinia recondita f.sp. tritici. Physiol.Mol.Plant Pathol. 37, 437–450

    Google Scholar 

  • Walton, J.D. (1994) Deconstructing the cell wall. Plant Physiol. 104, 1113–1118

    Google Scholar 

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Authors and Affiliations

  1. Recherches en Sciences de la Vie et de la Santé, Pavillon Charles-Eugène Marchand, Université Lavai, G1K 7P4, Sainte-Foy, Québec, Canada

    Nicole Benhamou & Pierre J. Lafontaine

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  1. Nicole Benhamou
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  2. Pierre J. Lafontaine
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The authors wish to thank Sylvain Noël for excellent technical assistance and Drs. J.P. Geiger and Michel Nicole (ORSTOM, Montpellier, France) for providing the purified laccase. This work was supported by a grant from the FCAR-CQVB (Fonds Québécois pour la Formation de Chercheurs et l'Aide à la Recherche and Centre Québécois de Valorisation de la Biomasse) and by a contract from the Company Tourbières Premier Ltée, Rivière-du-Loup, Québec.

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Benhamou, N., Lafontaine, P.J. Ultrastructural and cytochemical characterization of elicitor-induced structural responses in tomato root tissues infected by Fusarium oxysporum f.sp. radicis-lycopersici . Planta 197, 89–102 (1995). https://doi.org/10.1007/BF00239944

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