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Cell wall synthesis in cotton roots after infection with Fusarium oxysporum

The deposition of callose, arabinogalactans, xyloglucans, and pectic components into walls, wall appositions, cell plates and plasmodesmata

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Abstract

Fusarium oxysporum f. sp. vasinfectum penetration hyphae infect living cells in the meristematic zone of cotton (Gossypium barbadense L.) roots. We characterized wall modifications induced by the fungus during infection of the protodermis using antibodies against callose, arabinogalactan-proteins, xyloglucan, pectin, polygalacturonic acid and rhamnogalacturonan I in high-pressure frozen, freeze-substituted root tissue. Using quantitative immunogold labelling we compared the cell walls before and after hyphal contact, cell plates with plasmodesmata during cytokinesis, and wall appositions induced by fungal contact. In the already-existing wall, fungal contact induced only minor modifications such as an increase of xyloglucan epitopes. Wall appositions mostly exhibited epitopes similar to the cell plate except that wall appositions had a much higher callose content. This study shows that wall appositions induced by Fusarium oxysporum hyphae are the result of normal cell wall synthesis and the addition of large amounts of callose. The appositions do not stop fungal growth.

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Abbreviations

AG:

arabinogalactan

AGP:

arabinogalactan glycoprotein

HRGP:

hydroxyproline-rich glycoprotein

RGI:

rhamnogalacturonan I

XG:

xyloglucan

References

  • Aist JR, Bushnell WR (1991) Invasion of plants by powdery mildew fungi, and cellular mechanisms of resistance. In: Cole TG, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York, pp 321–345

    Google Scholar 

  • Balestrini R, Romera C, Puigdomenech P, Bonfante P (1994) Location of a cell-wall hydroxyproline-rich glycoprotein, cellulose and β-1,3-glucans in apical and differentiated regions of maize mycorrhizal roots. Planta 195: 201–209

    Google Scholar 

  • Bohlmann H, Apel K (1991) Thionins. Annu Rev Plant Physiol Plant Mol Biol 42: 227–240

    Google Scholar 

  • Bonfante-Fasolo P, Vian B, Perotto S, Faccio A, Knox JP (1990) Cellulose and pectin localization in roots of mycorrhizal Allium porrum: labeling continuity between host cell wall and interfacial material. Planta 180: 537–547

    Google Scholar 

  • Bonfante-Fasolo P, Peretto R, Perotto S (1992) Cell surface interactions in endomycorrhizal symbiosis. In: Callow JA, Green JR, (eeds) Perspectives in plant cell recognition. Cambridge University Press, Cambridge, pp 239–255

    Google Scholar 

  • Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6: 1703–1712

    Google Scholar 

  • Bushnell WR (1984) Structural and physiological alterations in susceptible host tissue. In: Bushnell WP, Roelfs AP (eds) The cereal rusts. Academic Press, Inc., Orlando, Florida, pp 477–507

    Google Scholar 

  • Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in the flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3: 1–30

    Article  CAS  PubMed  Google Scholar 

  • Driouich A, Levy S, Staehelin A, Faye L (1994) Structural and functional organization of the Golgi apparatus in plant cells. Plant Physiol Biochem 32: 731–749

    Google Scholar 

  • Esquerré-Tugayé MT, Lafitte C, Mazau D, Toppan AT (1979) Cell surfaces in plant-microorganism interactions. II Evidence for the accumulation of hydroxyproline-rich glycoproteins in the cell wall of diseased plants as a defense mechanism. Plant Physiol 64: 320–326

    Google Scholar 

  • Freytag S, Arabatzis N, Hahlbrock K, Schmelzer E (1994) Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell death and defence-related gene activation in potato/ Phytophthora infestans interactions. Planta 194: 123–135

    Google Scholar 

  • Gibeaut DM, Carpita NC (1994) Biosynthesis of plant cell wall polysaccharides. FASEB J 8: 904–915

    Google Scholar 

  • Gollote A, Gianinazzi-Pearson V, Giovannetti M, Sbrana C, Alvio L, Gianinazzi S (1993) Cellular localization and cytochemical probing of resistance reactions to arbuscular mycorrhizal fungi in a ‘locus a’ myc− mutant of Pisum sativum L. Planta 191: 122–122

    Google Scholar 

  • Hächler H, Hohl HR (1984) Temporal and spatial distribution patterns of collar and papillae wall appositions in resistant and susceptible tuber tissue of Solanum tuberosum infected by Phytophthora infestans. Physiol Plant Pathol 24: 107–118

    Google Scholar 

  • Hayat MA (1975) Positive staining for electron microscopy. Van Nostrand Rheinhold Company, New York

    Google Scholar 

  • Heath MC (1972) Ultrastructure of host and nonhost reactions to cowpea rust. Phytopathology 62: 27–38

    Google Scholar 

  • Herman EM, Lamb CJ (1992) Arabinogalactan-rich glycoproteins are localized on the cell surface and in intravacuolar multivesicular bodies. Plant Physiol 98: 264–272

    Google Scholar 

  • Hohl HR, Suter E (1976) Host parasite interfaces in a resistant and susceptible cultivar of Solanum tuberosum inoculated with Phytophthora infestans: leaf tissue. Can J Bot 54: 1956–1970

    Google Scholar 

  • Homblé F, Foissner I (1993) Electron microscopy and electrophysiology of local cell wall formation in Chara corallina. Plant Cell Physiol 34: 1283–1289

    Google Scholar 

  • Hoson T (1991) Structure and function of plant cell walls: immunological approaches. Int Rev Cytol 130: 233–268

    Google Scholar 

  • Hussey RS, Mims CW, Wescott SW (1992) Immunocytochemical localization of callose in root cortical cells parasitized by the ring nematode Criconemella xenoplax. Protoplasma 171: 1–6

    Google Scholar 

  • Iiyama K, Lam TB, Stone BA (1994) Covalent cross-links in the cell wall. Plant Physiol 104: 315–320

    Google Scholar 

  • Kauss H (1995) Callose synthesis. In: Smallwood M, Knox P, Bowles DJ (eds) Membranes: Specialized functions in plant cells. JAI Press, In press

  • Knox JP (1992) Molecular probes for the plant cell surface. Protoplasma 167: 1–9

    Google Scholar 

  • Knox JP, Day S, Roberts K (1989) A set of cell surface glycoproteins forms an early marker of cell position, but not cell type, in the root apical meristem of Daucus carota. Development 106: 47–56

    Google Scholar 

  • Knox JP, Linstead PJ, King J, Cooper C, Roberts K (1990) Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181: 512–521

    Google Scholar 

  • Kunoh H (1982) Primary germ tubes of Erysiphe graminis conidia. In: Asada Y (ed) Plant infection: the physiological and biochemical basis. Japan Sci Soc Press, Tokyo/Berlin, pp 45–59

    Google Scholar 

  • Levy S, Staehelin A (1992) Synthesis, assembly and function of plant cell wall macromolecules. Curr Opin Cell Biol 1992: 856–862

    Google Scholar 

  • Lucas WJ, Ding B, Van der Schoot C (1993) Plasmodesmata and the supracellular nature of plants. New Phytol 125: 435–476

    Google Scholar 

  • Mendgen K, Welter K, Scheffold F, Knauf-Beiter G (1991) High pressure freezing of rust infected plant leaves. In: Mendgen K, Leseman DE (eds) Electron microscopy of plant pathogens. Springer Verlag, Berlin Heidelberg, pp 31–41

    Google Scholar 

  • Moore PJ, Staehelin LA (1988) Immunogold localization of the cell-wall-matrix polysaccharides rhamnogalacturonan I and xyloglucan during cell expansion and cytokinesis in Trifolium pratense L.; implication for secretory pathways. Planta 174: 433–445

    Google Scholar 

  • Moore PJ, Swords KMM, Lynch MA, Staehelin LA (1991) Spatial organization of the assembly pathways of glycoproteins and complex polysaccharides in the Golgi apparatus of plants. J Cell Biol 112:589–602

    Google Scholar 

  • Mueller WC, Morgham AT, Roberts EM (1994) Immunocytochemical localization of callose in the vascular tissue of tomato and cotton plants infected with Fusarium oxysporum. Can J Bot 72: 505–509

    Google Scholar 

  • Northcote DH, Davey R, Lay J (1989) Use of antisera to localize callose, xylan and arabinogalactan in the cell-plate, primary and secondary walls of plant cells. Planta 178: 353–366

    Google Scholar 

  • Pennell RI (1992) Cell surface arabinogalactan proteins, arabinogalactans and plant development. In: Callow JA, Green JR (eds) Perspectives in plant recognition. Cambridge University Press, Cambridge, pp 105–121

    Google Scholar 

  • Pennell RI, Knox JP, Scofield GN, Selvendran RR, Roberts K (1989) A family of abundant plasma membrane-associated glycoproteins related to the arabinogalactan proteins is unique to flowering plants. J Cell Biol 108: 1967–1977

    Google Scholar 

  • Puhlmann J, Bucheli E, Swain MJ, Dunning N, Albersheim P, Darvill AG, Hahn MG (1994) Generation of monoclonal antibodies against plant cell-wall polysaacharides. Plant Physiol 104: 699–710

    Google Scholar 

  • Rae A, Bonfante-Fasolo P, Brewin N (1992) Structure and growth of infection threads in the legume symbiosis with Rhizobium leguminosarum. Plant J 2(3): 385–395

    Google Scholar 

  • Ride JP, Pearce RB (1979) Lignification and papilla formation at sites of attempted penetration of wheat leaves by non-pathogenic fungi. Physiol Plant Path 15: 79–92

    Google Scholar 

  • Roberts K (1994) The plant extracellular matrix: in a new expansive mood. Curr Op Cell Biol 6: 688–694

    Google Scholar 

  • Rodriguez-Gálvez E, Mendgen K (1995) The Infection process of Fusarium oxysporum in cotton root tips. Protoplasma, In press

  • Russo VM, Bushnell WR (1989) Responses of barley cells to puncture by microneedles and to attempted penetration by Erysiphe graminis f. sp. hordei system. Can J Bot 67: 2912–2921

    Google Scholar 

  • Sargent C, Gay JL (1977) Barley epidermal apoplast structure and modification by powdery mildew contact. Physiol Plant Pathol 11: 195–205

    Google Scholar 

  • Sherrier DJ, VandenBosch KA (1994) Localization of repetitive proline-rich proteins in the extracellular matrix of pea root nodules. Protoplasma 183: 148–161

    Google Scholar 

  • Sherwood RT, Vance CP (1982) Initial events in the epidermal layer during penetration. In: Asada Y (ed) Plant infection: The physiological and biochemical basis. Japan Sci Soc Press/Springer Verlag, Tokyo/Berlin, pp 27–44

    Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5: 9–25

    Article  CAS  PubMed  Google Scholar 

  • Smart MG (1991) The plant cell wall as a barrier to fungal invasion. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum Press, New York and London, pp 47–66

    Google Scholar 

  • Stark-Urnau M, Mendgen K (1995) Sequential deposition of plant gycoproteins and polysaccharides into the host-parasite interface of Uromyces vignae and Vigna sinencis. Evidence for endocytosis and secretion. Protoplasma 186: 1–11

    Google Scholar 

  • Steffan W, Kovác P, Albersheim P, Darvill AG, Hahn MG (1995) Characterization of a monoclonal antibody that recognizes an arabinosylated (1-6)-β-d-galactan epitope in plant complex carbohydrates. Carbohydr Res, In press

  • Turner A, Wells B, Roberts K (1994) Plasmodesmata of maize root tips: structure and composition. J Cell Sci 107: 3351–3361

    Google Scholar 

  • Xu H, Mendgen K (1994) Endocytosis of 1,3-β-glucans by broad bean cells at the penetration site of the cowpea rust fungus (haploid stage). Planta 195: 282–290

    Google Scholar 

  • Zhang GF, Driouich A, Staehelin A (1993) Effect of monensin on plant Golgi: re-examination of the changes in cisternal architecture and function activities of the Golgi apparatus of sycamore suspension-cultured cells. J Cell Sci 104: 819–831

    Google Scholar 

  • Zhang GF, Staehelin LA (1992) Functional compartmentation of the Golgi apparatus of plant cells. Plant Physiol 99: 1070–1083

    Google Scholar 

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Authors and Affiliations

  1. Lehrstuhl für Phytopathologie, Fakultät für Biologie der Universität Konstanz, D-78434, Konstanz, Germany

    E. Rodríguez-Gálvez & K. Mendgen

Authors
  1. E. Rodríguez-Gálvez
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  2. K. Mendgen
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Additional information

We thank Dr. Holger Deising and Dr. Matthias Hahn (Lehrstuhl für Phytopathologie, Universität Konstanz, Konstanz, Germany) for reading the manuscript. We thank Dr. Michael Hahn (Complex Carbohydrate Research Center, University of Georgia, Athens, USA) for providing the antibodies CCRC-M1, CCRC-M2 and CCRC-M8 and Dr. Paul Knox (Centre for Plant Biochemistry and Biotechnology, University of Leeds, UK) for providing the antibodies JIM 5 and JIM 7. The first author is grateful to the Deutsche Akademische Austauschdienst for a scholarship.

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Rodríguez-Gálvez, E., Mendgen, K. Cell wall synthesis in cotton roots after infection with Fusarium oxysporum . Planta 197, 535–545 (1995). https://doi.org/10.1007/BF00196676

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  • DOI: https://doi.org/10.1007/BF00196676

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