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Ultrastructural Observations and DNA Degradation Analysis of Pepper Leaves Undergoing a Hypersensitive Reaction to Xanthomonas campestris pv. Vesicatoria

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Abstract

Ultrastructural details of the hypersensitive reaction induced by infiltration with avirulent race 2 Xanthomonas campestris pv. vesicatoria in pepper ‘Early Calwonder-10R’ leaves (incompatible interaction) are reported. Affected cells displayed plasmalemma undulations and disruption, lysis of the chloroplast membrane, degeneration of other organelles, general cytoplasm disorganisation and, often, protoplast shrinkage. The nuclei contained large masses of electron-dense material, apparently formed by chromatin aggregation. In many cases a single chromatin-like layer was deposited on the inner side of the nuclear envelope leaving a finely granular matrix in the centre of the nucleus; the nucleolus usually disappeared. The nuclear envelope was sometimes ruptured and the internal matrix leaked into the cytoplasm. The content of many affected cells eventually coagulated and became very electron-dense. The walls often collapsed. All these alterations were especially visible in spongy mesophyll cells at sites where bacteria occurred in the intercellular spaces. Although some of the nuclear and cytoplasmic alterations recall certain aspects of apoptotic cell death, molecular determinations did not reveal any DNA degradation in hypersensitively reacting tissues. The first cell alterations in leaves infected with the virulent bacterial race 1 (compatible interaction) were observed only 27 h after inoculation, when the cytoplasm of some cells showed limited internal disorganisation and plasmolysis at sites where bacterial colonies developed.

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References

  • Al-Mousawi AH, Richardson PE, Essenberg M and Johnson WM (1982) Cotyledon and leaf ultrastructure of a bacterial blight immune cotton line inoculated with a low level of Xanthomonas campestris pv. malvacearum. Phytopathology 72: 1230–1234

    Google Scholar 

  • Ashkenazi A and Dixit VM (1998) Death receptors: signaling and modulation. Science 281: 1305–1308

    PubMed  Google Scholar 

  • Bestwick CS, Bennet MH and Mansfield JW (1995) Hrp mutants of Pseudomonas syringae pv. phaseolicola induces cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce. Plant Physiol 108: 503–516

    PubMed  Google Scholar 

  • Brown J and Mansfield J (1991) Interaction between Pseudomonas and Phaseolus vulgaris. In: Mendgen K and Lesemann DE (eds) Electron Microscopy of Plant Pathogens (pp 185–196) Springer-Verlag, Berlin

    Google Scholar 

  • Brown I, Mansfield J, Irlam I, Conradsstrauch J and Bonas U (1993) Ultrastructure of interactions between Xanthomonas campestris pv. vesicatoria and pepper, including immunocytochemical localization of extracellular polysaccharides and the Avrbs3 protein. Mol Plant Microbe Inter 6: 376–386

    Google Scholar 

  • Brown I, Mansfield J and Bonas U (1995) hrp genes in Xanthomonas campestris pv. vesicatoria determine ability to suppress papilla deposition in pepper mesophyll cells. Mol Plant Microbe Inter 8: 825–836

    Google Scholar 

  • Brown J, Trethowan J, Kerry M, Mansfield J and Bolwell GP (1998) Localization of components of the oxidative cross-linking of glycoproteins and of callose synthesis in papillae formed during the interaction between non-pathogenic strains of Xanthomonas campestris and French bean mesophyll cells. Plant J 15: 333–343

    Google Scholar 

  • D'Ovidio R, Tanzarella OA and Porceddu E (1992) Isolation of an α-type gliadin gene from Triticum durum Desf. and genetic polymorphism at the Gli-2 loci. Genet Breed 46: 41–48

    Google Scholar 

  • Dangl JL, Dietrich RA and Richberg MH (1996) Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell 8: 1793–1807

    PubMed  Google Scholar 

  • Del Pozo O and Lam E (1998) Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol 8: 1129–1132

    PubMed  Google Scholar 

  • Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA and Dangl JL (1994) Arabidopsis mutants simulating disease resistance response. Cell 77: 565–577

    Article  PubMed  Google Scholar 

  • Dixon RA, Harrison MJ and Lamb CJ (1994) Early events in the activation of plant defence responses. Annu Rev Phytopathol 32: 479–501

    Google Scholar 

  • Eleftheriou EP (1986) Ultrastructural studies on protophloem sieve elements in Triticum aestivum L. Nuclear degeneration. J Ultrastruct Mol Struct Res 98: 47–60

    Google Scholar 

  • Fett WF and Jones SB (1995) Microscopy of the interaction of hrp mutants of Pseudomonas syringae pv. phaseolicola with a nonhost plant. Plant Sci 107: 27–39

    Google Scholar 

  • Goodman RN and Novacky AJ (1994) The hypersensitive reaction in plants to pathogens: a resistance phenomenon. APS Press St. Paul, Minnesota.

    Google Scholar 

  • Greenberg JT, Guo A, Klessig DF and Ausubel FM (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defense functions. Cell 77: 551–563

    PubMed  Google Scholar 

  • Kerr JFR and Harmon BV (1991) Definition and incidence of apoptosis: and historical perspective. In: Tomei LD and Cope FO (eds) Apoptosis: The Molecular Basis of Cell Death (pp 5–31) Cold Spring Harbour Laboratory Press, New York

    Google Scholar 

  • Kosslak RM, Chamberlin MA, Palmer RG and Bowen BA (1997) Programmed cell death in the root cortex of soybean root necrosis mutants. Plant J 11: 729–745

    PubMed  Google Scholar 

  • Koulaková B, Kovarík A, Fajkus J and Široký J (1997) Chromatin fragmentation associated with apoptotic changes in tobacco cells exposed to cold stress. FEBS Lett 414: 289–292

    PubMed  Google Scholar 

  • Levine A, Pennell RI, Alvarez ME, Palmer R and Lamb C (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol 6: 427–437

    PubMed  Google Scholar 

  • Mittler R, Simon L and Lam E (1997) Pathogen-induced programmed cell death in tobacco. J Cell Sci 110: 1333–1344

    PubMed  Google Scholar 

  • Morel J-B and Dangl LD (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Differ 4: 671–683

    Google Scholar 

  • Oberhammer F, Wilson JW, Dive C, Morris ID, Hickman JA, Wakeling AE, Walker PR and Sikorska M (1993a) Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J 12: 3679–3684

    PubMed  Google Scholar 

  • Oberhammer F, Fritsch G, Schmied M, Pavelka M, Printz D, Purchio T, Lassmann H and Shulte-Hermann R (1993b) Condensation of the chromatin at the membrane of an apoptotic nucleus is not associated with the activation of an endonuclease. J Cell Sci 104: 317–326

    PubMed  Google Scholar 

  • Ryerson DE and Heath MC (1996) Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 8: 393–402

    PubMed  Google Scholar 

  • Schwartzman RA and Cidlowski JA (1993) Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr Rev 14: 133–151

    PubMed  Google Scholar 

  • Sun DY, Jiang S, Zheng LM, Ojcius DM and Young JD (1994) Separate metabolic pathways leading to DNA fragmentation and apoptotic chromatin condensation. J Exp Med 179: 559–568

    PubMed  Google Scholar 

  • Wang H, Li J, Bostock RM and Gilchrist DG (1996) Apoptosis: a functional paradigm for programmed cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell 8: 375–391

    PubMed  Google Scholar 

  • Wyllie AH (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284: 555–556

    PubMed  Google Scholar 

  • Young TE, Gallie DR and De Mason DA (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken 2 genotypes. Plant Physiol 115: 737–751

    PubMed  Google Scholar 

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Polverari, A., Buonaurio, R., Guiderdone, S. et al. Ultrastructural Observations and DNA Degradation Analysis of Pepper Leaves Undergoing a Hypersensitive Reaction to Xanthomonas campestris pv. Vesicatoria. European Journal of Plant Pathology 106, 423–431 (2000). https://doi.org/10.1023/A:1008773321809

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