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Summary

In this chapter the hypersensitive response is defined, described and analyzed. HR is described at the levels of physiology (e.g. changes in membrane potentials, ion channels etc.), biochemistry (e.g. protein phosphorylation in signal transduction, lipoxygenase and reactive oxygen intermediates in membrane damage), and genetics (e.g. studies with various classes of mutants).

An attempt has been made to put recent developments in context with the wealth of earlier data on the HR to produce a “unifying” consensus. Thus, the recently discovered role of the type III bacterial secretory pathway in delivering both virulence and avirulence gene products directly into the host cell cytoplasm has solved many incongruencies between Avr protein action, elicitor effects, and the HR induced by intact living, micro-organisms.

Emerging information on programmed cell death phenomena in the HR, analagous to some of those observed in animal systems, is discussed in the light of earlier observations and speculations, and here again the analysis of mutants is clearly of central importance.

The relationship of the HR to other defence reponses and to resistance per se against various different kinds of pathogens is also considered. The last section draws attention to some of the questions which, despite recent progress, remain to be answered.

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Abbreviations

avr:

avirulence

CAD:

caspase-induced DNase

CHS:

chalcone synthase

DAD:

defender against apoptotic death

DFF:

DNA fragmentation factor

GST:

glutathione-S-transferase

HR:

hypersensitive response

hrp:

hypersensitive response and pathogenicity

ICE:

interleukin-1B conerting enzyme

LOX:

lipoxygenase

LRR:

leucine-rich repeat

LZ:

leucine-zipper

MAP:

mitogen-activated protein

Ψm :

mitochondrial transmembrane potential

NLS:

nuclear localization signal sequence

PAL:

phenylalanine ammonia-lyase

PCD:

programmed cell death

PR:

pathogenesis-related (protein)

ROI:

reactive oxygen intermediates

SA:

salicylic acid

SAR:

systemic acquired resistance

SOD:

superoxide dismutase

TMS:

trans membrane-spanning (helix)

TMV:

tobacco mosaic virus

XR:

K+/H+ exchange response

References

  • Aikens J and Dix TA (1993) Hydrodioxyl (perhydroxyl), peroxyl, and hydroxyl radical-Initiated lipid peroxidation of large unilamellar vesicles (liposomes): comparative and mechanistic studies. Arch Biochem Biophys 305: 516–525

    Article  PubMed  CAS  Google Scholar 

  • Alfano JR, Bauer DW, Milos TM and Collmer A (1996) Analysis of the role of the Pseudomonas syringae pv. syringae HrpZ harpin in elicitation of the hypersensitive response in tobacco using functionally nonpolar deletion mutations, truncated HrpZ fragments and hrmA mutations. Mol Microbiol 19: 715–728

    CAS  Google Scholar 

  • Alvarez ME and Lamb C (1997) Oxidative burst-mediated defense responses in plant disease resistance. In: Scandelios JG (ed) Oxidative Stress and the Molecular Biology of Antioxidant Defenses, pp 815–839. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Anderson MD, Chen Z and Klessig DF (1998) Possible involvement of lipid peroxidation in salicylic acid-mediated induction of PR-1 gene expression. Phytochemistry 47: 555–566

    Article  CAS  Google Scholar 

  • Atkinson MM and Baker CJ (1987) Association of host plasma membrane K+/H+ exchange with multiplication of Pseudomonas syringae pv. syringae in Phaseolus vulgaris. Phytopathology 77: 1273–1279

    Article  CAS  Google Scholar 

  • Atkinson MM and Baker CJ (1989) Role of plasmalemma H+-ATPase in Pseudomonas syringae-induced pv. syringae in K+/H+ exchange in suspension-cultured tobacco cells. Plant Physiol 91: 298–303

    CAS  Google Scholar 

  • Atkinson MM, Keppler LD, Orlandi EW, Baker CJ and Mischke CF (1990) Involvement of plasma membrane calcium influx in bacterial induction of the K+/H+ and hypersensitive responses in tobacco. Plant Physiol 92: 215–221

    Article  PubMed  CAS  Google Scholar 

  • Atkinson M, Bina J and Sequeira L (1993) Phosphoinositide breakdown during the K+/H+ exchange response of tobacco to Pseudomonas syringae pv. syringae. Mol Plant-Microbe Interact 6: 253–260

    Article  CAS  Google Scholar 

  • Bailey JA (1982) Physiological and biochemical events associated with the expression of resistance to disease. In: Wood RKS (ed) Active Defence Mechanisms in Plants, NATO ASI Series, pp 39–65. Plenum Press, New York

    Chapter  Google Scholar 

  • Baker CJ, O’Neill N, Keppler D and Orlandi EW (1991) Early responses during plant-bacteria interactions in tobacco cell suspensions. Phytopathology 81: 1504–1507

    Article  Google Scholar 

  • Baker B, Zambryski P, Staskawicz B and Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Science 276: 726–733

    Article  PubMed  CAS  Google Scholar 

  • Bestwick CS, Bennett MH and Mansfield JW (1995) Hrp mutant 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  CAS  Google Scholar 

  • Bestwick CS, Brown IR, Bennett MH and Mansfield, JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9: 209–221

    PubMed  CAS  Google Scholar 

  • Bielski BHJ, Arudi RL and Sutherland MW (1983) A study of the reactivity of HO27O2 with unsaturated fatty acids. J Biol Chem 258: 4759–4761

    PubMed  CAS  Google Scholar 

  • Bogdanove AJ, Beer SV, Bonas U, Boucher CA, Collmer A, Coplin DL, Cornelis GR, Huang, H-C, Hutcheson, SW, Panopoulos, NJ and Van Gijsegem, F (1996) Unified nomenclature for broadly conserved hrp genes of phytopathogenic bacteria. Mol Microbiol 20: 681–683

    Article  PubMed  CAS  Google Scholar 

  • Bokoch GM (1994) Regulation of the human neutrophil NADPH oxidase by the Rac GTP-binding proteins. Curr Opin Cell Biol 6: 212–218

    Article  PubMed  CAS  Google Scholar 

  • Boller T and Kende H (1979) Hydrolytic enzymes in the central vacuole of plant cells. Plant Physiol 63: 1123–1132

    Article  PubMed  CAS  Google Scholar 

  • Bolwell GP, (1999) Role of active axygen species and NO in plant defence responses. Curr Op Plant Bio 2: 287–294

    Article  CAS  Google Scholar 

  • Bolwell GP and Wojtaszek P (1997) Mechanisms for the generation of reactive oxygen species in plant defence — a broad perspective. Physiol Mol Plant Pathol 51: 347–366

    Article  CAS  Google Scholar 

  • Bolwell GP, Butt VS, Davies DR and Zimmerlin A (1995) The origin of the oxidative burst in plants. Free Rad Res 23: 517–532

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Brown IR, 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

    Article  CAS  Google Scholar 

  • Bushneil WR (1981) Incompatibility conditioned by the Mla gene in powdery mildew of barley: the halt of cytoplasmic streaming. Phytopathology 71: 1062–1066

    Article  Google Scholar 

  • Cao H, Bowling SA, Gordon S and Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583–1592

    PubMed  CAS  Google Scholar 

  • Cao H, Glazebrook J, Clarke JD, Volko S and Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57–63

    Article  PubMed  CAS  Google Scholar 

  • Century KS, Holub EB and Staskawicz BJ (1995) NDRI, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc Natl Acad Sci USA 92: 6597–6601

    Article  PubMed  CAS  Google Scholar 

  • Chamnongpol S, Willekens H, Langebartels C, Van Montagu M, Inzé D and Van Camp W (1996) Transgenic tobacco with a reduced catalase activity develops necrotic lesions and induces pathogenesis-related expression under high light. Plant J 10: 491–503

    Article  CAS  Google Scholar 

  • Chen CY and Heath MC (1991) Cytological studies of the hypersensitive death of cowpea epidermal cells induced by basidiospores-derived infection by the cowpea rust fungus. Can J Bot 69: 1199–1206

    Article  Google Scholar 

  • Chen Z, Silva H and Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: 1883–1886

    Article  PubMed  CAS  Google Scholar 

  • Clarke JD, Liu Y, Klessig DF and Dong X (1998) Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-l mutant. Plant Cell 10: 557–569

    PubMed  CAS  Google Scholar 

  • Collinge DB and Slusarenko A (1987) Plant gene expression in response to pathogens. Plant Mol Biol 9: 389–410

    Article  CAS  Google Scholar 

  • Collmer A (1998) Determinants of pathogenicity and avirulence in plant pathogenic bacteria. Curr Opin Plant Biol 1:329–335

    Article  PubMed  CAS  Google Scholar 

  • Conklin PL, Williams EH and Last RL (1996) Environmental stress sensitivity of an ascorbate-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93: 9970–9974

    Article  PubMed  CAS  Google Scholar 

  • Cook AA and Stall RE (1968) Effect of Xanthomonas vesicatoria on loss of electrolytes from leaves of Capsicunum annuum. Phytopathology 58: 617–619

    Google Scholar 

  • Cramer CL, Bell JN, Ryder TB, Bailey JA, Schuch W, Bolwell GP, Robbins MP, Dixon RA and Lamb CJ (1985) Co-ordinated synthesis of phytoalexin biosynthetic enzymes in biologically-stressed cells of bean (Phaseolus vulgaris L.). EMBO J 4: 285–289

    PubMed  CAS  Google Scholar 

  • Croft KPC, Jüttner F and Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv. phaseolicola. Plant Physiol 101: 13–24

    CAS  Google Scholar 

  • Dangl JL, Ritter C, Gibbon MJ, Mur LAJ, Wood JR, Goss S, Mansfield J, Taylor JD and Vivian A (1992) Functional homologs of the Arabidopsis RPM1 disease resistance gene in bean and pea. Plant Cell 4: 1359–1369

    PubMed  CAS  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  CAS  Google Scholar 

  • Davis D, Merida J, Legendre L, Low PS and Heinstein P (1993) Independent elicitation of the oxidative burst and phytoalexin formation in cultured plant cells. Phytochemistry 32: 607–611

    Article  CAS  Google Scholar 

  • Deighton N, Lyon GD, Johnston D, Glidwell SM and Goodman BA (1994) Are free radical generation and phytoalexin biosynthesis coupled? Proc Roy Soc Edin 102B: 253–255

    Google Scholar 

  • Delaney TP, Friedrich L and Ryals JA (1995) Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci USA 92: 6602–6606

    Article  PubMed  CAS  Google Scholar 

  • Desikan R, Hancock JT, Coffey MJ and Neill SJ (1996) Generation of active oxygen in elicited cells of Arabidopsis thaliana is mediated by a NADPH oxidase-like enzyme. FEBS Lett 382: 213–217

    Article  PubMed  CAS  Google Scholar 

  • Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward ER and Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266: 1247–1249

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA and Lamb CJ (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394: 585–588

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Dietrich RA, Richberg MH, Schmidt R, Dean C and Dangl JL (1997) A novel zinc finger protein is encoded by the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88: 685–694

    Article  PubMed  CAS  Google Scholar 

  • Doke N and Ohashi Y (1988) Involvement of an O2—generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus. Physiol Mol Plant Pathol 32: 163–175

    Article  CAS  Google Scholar 

  • Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1: 316–323

    Article  PubMed  CAS  Google Scholar 

  • Dorey S, Kopp M, Geoffroy P, Fritig B and Kauffmann S (1999) Hydrogen peroxide from the oxidative barst is neither necessary nor sufficient for hypersensitive cell death induction, phenyl alanine ammonia lyase stimulation, salicylic acid accumulation, or scopoletin consumption in cultured tobacco cells treated with elicitin. Plant Physiol 121: 163–171

    Article  PubMed  CAS  Google Scholar 

  • Draper J (1997) Salicylate, Superoxide synthesis and cell suicide in plant defence. Trends Plant Sci 2: 162–165

    Article  Google Scholar 

  • Durner J and Klessig DF (1996) Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem 271: 28492–28501

    Article  PubMed  CAS  Google Scholar 

  • Durner J and Klessing DF (1999) Nitric oxide as a signal in plants. Curr Op Plant Biol 2: 369–374

    Article  CAS  Google Scholar 

  • Durner J, Wendehenne D and Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95: 10328–10333

    Article  PubMed  CAS  Google Scholar 

  • Dwyer SC, Legendre L, Low PS and Leto TL (1996) Plant and human neutrophil oxidative burst complexes contain immunologically related proteins. Biochim Biophys Acta 1289: 231–237

    Article  PubMed  Google Scholar 

  • Ebel J, Bhagwat AA, Cosio EG, Feger M, Kissel U, Mithfer A and Waldmüller T (1995) Elicitor-binding proteins and signal transduction in the activation of a phytoalexin defense response. Can J Bot 73: S506–S510

    Article  CAS  Google Scholar 

  • Ellis RE, Yuan J and Horwitz HR (1991) Mechanisms and functions of cell death. Annu Rev Cell Biol 7: 663–698

    Article  PubMed  CAS  Google Scholar 

  • Enari M, Sakahira H, Yokoyama H, Okawa K, Iwamatsu A and Nagata S (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391: 43–50

    Article  PubMed  CAS  Google Scholar 

  • Felix G, Regenass M, Spanu P and Boller T (1994) The protein Phosphatase inhibitor calyculin A mimics elicitor action in plant cells and induces rapid hyperphosphorylation of specific proteins as revealed by pulse labeling with [33P]phosphate. Proc Natl Acad Sci USA 91: 952–956

    Article  PubMed  CAS  Google Scholar 

  • Fett WF (1984) Accumulation of isoflavonoids and isoflavone glucosides after inoculation of soybean leaves with Xanthomonas campestris pv. glycinea and pv. campestris and a study of their role in resistance. Physiol Mol Plant Pathol 28: 67–77

    Google Scholar 

  • Freialdenhoven A, Scherag B, Hollricher K, Collinge DB, Thordal-Christensen H and Schulze-Lefert P (1994) Nar-1 and Nar-2, two loci required for Mla 12-specified race-specific resistance to powdery mildew in barley. Plant Cell 6: 983–994

    PubMed  CAS  Google Scholar 

  • Freialdenhoven A, Peterhänsel C, Kurth J, Kreuzaler F and Schulze-Lefert P (1996) Identification of genes required for the function of non-race-specific mlo resistance to powdery mildew in barley. Plant Cell 8: 5–14

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fridovich I (1988) The biology of oxygen radicals. In: Halliwell B (ed) Oxygen Radicals and Tissue Injury, Proceedings of a Brook Lodge Symposium, pp 1–5. The Upjohn Company, Bethesda, Maryland

    Google Scholar 

  • Gabriel DW (1986) Specificity and gene function in plant-pathogen interactions. American Soc Microbiol News 52: 19–25

    Google Scholar 

  • Gallois P, Makishima T, Hecht V, Despres B, Laudié M, Nishimotot T and Cooke R (1997) An Arabidopsis thaliana cDNA complementing a hamster apoptosis suppressor mutant. Plant J 11: 1325–1331

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J and Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91: 8955–8959

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J, Zook M, Mert F, Kagan I, Rogers EE, Crute IR, Holub EB, Hammerschmidt R and Ausubel FM (1997) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 146: 381–392

    PubMed  CAS  Google Scholar 

  • Glazener JA Orlandi, EW and Baker CJ (1996) The active oxygen response of cell suspensions to incompatible bacteria is not sufficient to cause hypersensitive cell death. Plant Physiol 110: 759–763

    PubMed  CAS  Google Scholar 

  • Goodman RN (1968) The hypersensitive reaction in tobacco: a reflection of changes in host cell permeability. Phytopathology 58: 872–873

    Google Scholar 

  • Gough CL, Genin S, Lopes V and Boucher CA (1993) Homology between the HrpO protein of Pseudomonas solanacearum and bacterial proteins implicated in a signal peptide-independent secretion mechanism. Mol Gen Genet 239: 378–392

    Article  PubMed  CAS  Google Scholar 

  • Gray J, Close PS, Briggs SP and Johal GS (1997) A novel suppressor of cell death in plants encoded by the Llsl gene of maize. Cell 89: 25–31

    Article  PubMed  CAS  Google Scholar 

  • Greenberg JT (1997) Programmed cell death in plant-pathogen interactions. Annu Rev Plant Physiol 48: 525–545

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Grimm C, Aufsatz W and Panopoulos NJ (1995) The hrpRS locus of Pseudomonas syringae pv. phaseolicola constitutes a complex regulatory unit. Mol Microbiol 15: 155–165

    CAS  Google Scholar 

  • Groom QJ, Torres MA, Fordham-Skelton AP, Hammond-Kosack KE, Robinson NJ and Jones JDG (1996) rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J 10: 515–522

    Article  PubMed  CAS  Google Scholar 

  • Groβkopf DG, Felix G, and Boller T (1990). K-252a inhibits the response of tomato cells to fungal elicitors in vivo and their microsomal protein kinase in vitro. FEBS Lett 275: 177–180

    Article  Google Scholar 

  • Gustine DL, Sherwood RT, Lukezic FL, Moyer BG and Devlin WS (1994) Metabolites of Pseudomonas corrugata that elicit plant defense reactions. In: Hedin PA (ed) Bioregulators for Crop Protection and Pest Control, ACS Symposium Series 557, pp 169–181. American Chemical Society, Washington

    Chapter  Google Scholar 

  • Halliwell B and Gutteridge JMC (1989) Free Radicals in Biology and Medicine. Clarendon Press, Oxford

    Google Scholar 

  • Hammond-Kosack KE and Jones JDG (1994) [atIdentification of two genes required in tomato for full C/-9-dependent resistance to Cladosporium fulvum. Plant Cell 6: 361–374

    PubMed  CAS  Google Scholar 

  • Hammond-Kosack KE and Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8: 1773–1791

    PubMed  CAS  Google Scholar 

  • Harder DE and Chong J (1991) Rust haustoria. In: Mendgen K and Leseman DE (eds) Electron Microscopy of Plant Pathogens, pp 235–250. Springer, Berlin

    Chapter  Google Scholar 

  • Harding SA and Roberts DM (1998) Incompatible pathogen infection results in enhanced reactive oxygen and cell death responses in transgenic tobacco expressing a hyperactive mutant calmodulin. Planta 206: 253–258

    Article  CAS  Google Scholar 

  • Hargreaves JA and Bailey JA (1978) Phytoalexin production by hypocotyls of Phaseolus vulgaris in response to constitutive metabolites released by damaged bean cells. Physiol Plant Pathol 13: 89–100

    Article  CAS  Google Scholar 

  • He SY, Huang H-C and Collmer A (1993) Pseudomonas syringae pv. syringae harpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell 73: 1255–1266

    CAS  Google Scholar 

  • He SY, Bauer DW, Collmer A and Beer SV (1994) Hypersensitive response elicited by Erwinia amylovora harpin requires active plant metabolism. Mol Plant-Microbe Interact 7: 289–292

    Article  CAS  Google Scholar 

  • Honée G, Buitink J, Jabs T, De Kloe J, Sijbolts F, Apotheker M, Weide R, Sijen T, Stuiver M and de Wit PJGM (1998) Induction of defense-related responses in Cf9 tomato cells by the AVR9 elicitor peptide of Cladosporium fulvum is developmentally regulated. Plant Physiol 117: 809–820

    Article  PubMed  Google Scholar 

  • Hortelano S, Dallaporta B, Zamzami N, Hirsch T, Susin SA, Marzo I, Bosca L, Kroemer G (1997) Nitric oxide induces apoptosis via triggering mitochondrial permeability transition. FEBS Lett 410: 373–377

    Article  PubMed  CAS  Google Scholar 

  • Hu G, Yalpani N, Briggs SP and Johal GS (1998) A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10: 1095–1105

    PubMed  CAS  Google Scholar 

  • Hueck CJ (1998) Type III secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379–433

    PubMed  CAS  Google Scholar 

  • Innes RW (1998) Genetic dissection of R gene signal transduction pathways. Curr Opin Plant Biol 1: 229–304

    Article  Google Scholar 

  • Jabs T (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem Pharmacol 57: 231–245

    Article  PubMed  CAS  Google Scholar 

  • Jabs T, Dietrich RA and Dangl JL (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular Superoxide. Science 273: 1853–1856

    Article  PubMed  CAS  Google Scholar 

  • Jabs T, Colling C, Tschöpe M, Hahlbrock K and Scheel D (1997) Elicitor-stimulated ion fluxes and O2 from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc Natl Acad Sci USA 94: 4800–4805

    Article  PubMed  CAS  Google Scholar 

  • Jacobson MD, Weil M and Raff MC (1997) Programmed cell death in animal development. Cell 88: 347–354

    Article  PubMed  CAS  Google Scholar 

  • Jakobek JL and Lindgren PB (1993) Generalized induction of defence responses in bean is not correlated with the induction of the hypersensitive reaction. Plant Cell 5: 49–56

    PubMed  CAS  Google Scholar 

  • Johal GS, Hulbert SH and Briggs SP (1995) Disease lesion mimics of maize: a model for cell death in plants. BioEssays 17: 685–692

    Article  Google Scholar 

  • Jones AM and Dangl JL (1996) Logjam at the Styx: programmed cell death in plants. Trends Plant Sci 1: 114–119

    Article  Google Scholar 

  • Kamoun S, van West P, Vleeshouwers VGAA, de Groot KE and Govers F (1998) Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INFI. Plant Cell 10: 1413–1425

    PubMed  CAS  Google Scholar 

  • Kang S, Sweigard JA and Valent B (1995) The PWL host-specificity gene family in the blast fungus Magnaporthe grisea. Mol Plant-Microbe Interact 8: 939–948

    Article  PubMed  CAS  Google Scholar 

  • Kauss H and Jeblick W (1995) Pretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2. Plant Physiol 108: 1171–1178

    PubMed  CAS  Google Scholar 

  • Kearney B and Staskawicz B (1990) Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346: 385–386

    Article  PubMed  CAS  Google Scholar 

  • Keen NT, Ersek T, Long M, Bruegger B and Holliday M (1981) Inhibition of the hypersensitive reaction of soybean leaves to incompatible Pseudomonas spp. by blastocidin S, streptomycin or elevated temperature. Physiol Plant Pathol 18: 325–337

    Article  CAS  Google Scholar 

  • Keller T, Damude HG, Werner D, Doerner P, Dixon RA and Lamb C (1998) A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10: 255–266

    PubMed  CAS  Google Scholar 

  • Keppler LD and Novacky A (1986) Involvement of lipid peroxidation in the development of a bacterially induced hypersensitive reaction. Phytopathology 76: 104–108

    Article  CAS  Google Scholar 

  • Keppler LD, Atkinson MM and Baker CJ (1988) Plasma membrane alteration during bacteria-induced hypersensitive reaction in tobacco suspension cells as monitored by intracellular accumulation of fluorescein. Physiol Mol Plant Pathol 32: 209–219

    Article  CAS  Google Scholar 

  • Kerr JFR, Wyllie AH and Currie AR (1972) Apoptosis: a basic biological phenomenon with wide ranging implication in tissue kinetics. Br J Cancer 26: 239–257

    Article  PubMed  CAS  Google Scholar 

  • Kieffer F, Simon-Plas F, Maume BF and Blein JP (1997) Tobacco cells contain a protein, immunologically related to the neutrophil small G protein Rac2 and involved in elicitor-induced oxidative burst. FEBS Lett 403: 149–153

    Article  PubMed  CAS  Google Scholar 

  • Kim JF and Beer SV (1998) HrpW of Erwinia amylovora, a harpin that contains a domain homologous to pectate lyases of a distinct class. J Bacteriol 180: 5203–5210

    PubMed  CAS  Google Scholar 

  • Klement Z (1971) Development of the hypersensitivity reaction induced by plant pathogenic bacteria. Proceedings of the 3rd International Conference on Plant Pathogenic Bacteria, Wageningen, pp 157–164

    Google Scholar 

  • Klement Z (1986) Hypersensitivity. In: Mount MS and Lacy GH (eds) Phytopathogenic Prokaryotes, pp 149–177. Academic Press, New York

    Google Scholar 

  • Klement Z and Goodman RN (1967) The hypersensitive reaction to infection by bacterial pathogens. Annu Rev Phytopathol 5:17–44

    Article  Google Scholar 

  • Kluck RM, Bossy-Wetzel E, Green DR and Newmeyer DD (1997a) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275 1132–1136

    Article  PubMed  CAS  Google Scholar 

  • Kluck RM, Martin SJ, Hoffman BM, Zhou JS, Green DR and Newmeyer DD (1997b) Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO J 16 4639–4649

    Article  PubMed  CAS  Google Scholar 

  • Kondo Y, Kawai Y, Hayashi T, Ohnishi M, Miyazawa T, Itoh S and Mizutani J (1993) Lipoxygenase in soybean seedlings catalyzes the oxygenation of phospholipid and such activity changes after treatment with fungal elicitor. Biochim Biophys Acta 1170: 301–306

    Article  PubMed  CAS  Google Scholar 

  • Kroemer G (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Med 3: 614–620

    Article  PubMed  CAS  Google Scholar 

  • Kroemer G, Petit P, Zamzami N, Vayssiere JL and Mignotte B (1995) The biochemistry of programmed cell death. Faseb J 9: 1277–1287

    PubMed  CAS  Google Scholar 

  • Kroemer G, Zamzani N and Susin SA (1997) Mitochondrial control of apoptosis. Immunol Today 18: 44–51

    Article  PubMed  CAS  Google Scholar 

  • Kuwana T, Smith JJ, Muzio M, Dixit V, Newmeyer DD and Kornbluth S (1998) Apoptosis induction by caspase-8 is amplified through the mitochondrial release of cytochrome c. J Biol Chem 273: 16589–16594

    Article  PubMed  CAS  Google Scholar 

  • Lamb CJ and Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 76: 419–422

    Google Scholar 

  • Lamb CJ, Corbin DR, Lawton M, Sauer N and Wingate VPM (1986) Recognition and response in plantpathogen interactions. In: Lugtenberg B (ed) Recognition in Microbe-Plant Symbiotic and Pathogenic Interactions, NATO ASI Series, pp 333–344. Springer, Berlin

    Chapter  Google Scholar 

  • Legendre L, Heinstein PF and Low PS (1992) Evidence for participation of GTP-binding proteins in elicitation of the rapid oxidative burst in cultured soybean cells. J Biol Chem 267: 20140–20147

    PubMed  CAS  Google Scholar 

  • Leist M and Nicotera P (1997) The shape of cell death. Biochem Biophys Res Commun 236: 1–9

    Article  PubMed  CAS  Google Scholar 

  • Leist M, Fava E, Montecucco C and Nicotera P (1997a) Peroxynitrite and nitric oxide donors induce neuronal apoptosis by eliciting autocrine excitotoxicity. Eur J Neurosci 9 1488–1498

    Article  PubMed  CAS  Google Scholar 

  • Leist M, Single B, Castoldi AF, Kuhnle S and Nicotera P (1997b) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185 1481–1486

    Article  PubMed  CAS  Google Scholar 

  • Levine A, Tenhaken R, Dixon RA and Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583–593

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES and Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-l/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479–489

    Article  PubMed  CAS  Google Scholar 

  • Ligterink W, Kroj T, zur Nieden U, Hirt H and Scheel D (1997) Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science 276: 2054–2057

    Article  PubMed  CAS  Google Scholar 

  • Lin KT, Xue JY, Sun FF and Wong PYK (1997) Reactive oxygen species participate in peroxynitrite-induced apoptosis in HL-60 cells. Biochem Biophys Res Commun 230: 115–119

    Article  PubMed  CAS  Google Scholar 

  • Lindgren, PB, Peet RC and Panopoulos NJ (1986) Gene cluster of Pseudomonas syringae pv. phaseolicola controls pathogenicity of bean plants and hypersensitivity on nonhost plants. J. Bacteriol 168: 512–22

    PubMed  CAS  Google Scholar 

  • Lindgren PB, Panopoulos NJ, Staskawicz BJ and Dahlbeck D (1988) Genes required for pathogenicity and hypersensitivity are conserved and interchangeable among pathovars of Pseudomonas syringae. Mol Gen Genet 211: 499–506

    Article  CAS  Google Scholar 

  • Lindgren PB, Frederick R, Govindarajan AG, Panopoulos NJ, Staskawicz BJ and Lindow SW (1989). An ice nucleation reporter gene system: Identification of inducible pathogenicity genes in Pseudomonas syringae pv. phaseolicola. EMBO J 8: 1291–1301

    PubMed  CAS  Google Scholar 

  • Liu X, Kim CN, Yang J, Jemmerson R and Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147–157

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Zou H, Slaughter C and Wang X (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89: 175–184

    Article  PubMed  CAS  Google Scholar 

  • Loh Y-T and Martin GB (1995) The Pto bacterial resistance gene and the Fen insecticide sensitivity gene encode functional protein kinases with serine/threonine specificity. Plant Physiol 108: 1735–1739

    Article  PubMed  CAS  Google Scholar 

  • Lyon F and Wood RKS (1976) The hypersensitive reaction and other responses of bean leaves to bacteria. Ann Bot 40: 479–491

    Google Scholar 

  • Lyon F and Wood RKS (1977) Alterations of response of bean leaves to compatible and incompatible bacteria. Ann Bot 41: 359–367

    Google Scholar 

  • Maccarrone M, van Arle PGM, Veldink GA and Vliegenthart JFG (1994) In vitro oxygenation of soybean biomembranes by lipoxygenase-2. Biochim Biophys Acta 1190: 164–169

    Article  PubMed  CAS  Google Scholar 

  • Macré F, Braidot E, Petrussa E and Vianello A (1994) Lipoxygenase activity associated to isolated soybean plasma membranes. Biochim Biophys Acta 1215: 109–114

    Article  Google Scholar 

  • Malamy J, Carr JP, Klessig DF and Raskin I (1990) Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002–1004

    Article  PubMed  CAS  Google Scholar 

  • Manon S, Chaudhuri B and Guerin M (1997) Release of cytochrome c and decrease of cytochrome c oxidase in Bax-expressing yeast cells, and prevention of these effects by coexpression of Bcl-xL. FEBS Lett 415: 29–32

    Article  PubMed  CAS  Google Scholar 

  • Matile P (1975) The Lytic Compartment of Plant Cells. Springer, Wien and New York

    Book  Google Scholar 

  • Matile P (1987) The sap of plant cells. New Phytol 105: 1–26

    Article  CAS  Google Scholar 

  • Mauch-Mani B and Slusarenko AJ (1996) Production of salicylic acid precursors is a major function of Phenylalanine ammonia lyase in the resistance of Arabidopsis to Peronospora parasitica. Plant Cell 8: 203–212

    PubMed  CAS  Google Scholar 

  • May MJ, Hammond-Kosack KE and Jones JDG (1996a) Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol 110 1367–1379

    PubMed  CAS  Google Scholar 

  • May MJ, Parker JE, Daniels MJ, Leaver CJ and Cobbett CS (1996b) An Arabidopsis mutant depleted in glutathione shows unaltered responses to fungal and bacterial pathogens. Mol Plant-Microbe Interact 9 349–356

    Article  CAS  Google Scholar 

  • Meier BM, Shaw N and Slusarenko AJ (1993) Spatial and temporal accumulation of defense gene transcripts in bean (Phaseolus vulgaris) leaves in relation to bacteria-induced hypersensitive cell death. Mol Plant-Microbe Interact 6: 453–466

    Article  PubMed  CAS  Google Scholar 

  • Métraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W and Inverardi B (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250: 1004–1006

    Article  PubMed  Google Scholar 

  • Mishra OP, Delivoria-Papadopoulos M, Cahillane G and Wagerle LC (1989) Lipid peroxidation as the mechanism of modification of the affinity of the Na+,K+-ATPase active sites for ATP, K+, Na+, and strophanthidin in vitro. Neurochem Res 14: 845–851

    Article  PubMed  CAS  Google Scholar 

  • Mittler R and Lam E (1996) Sacrifice in the face of foes: pathogen-induced programmed cell death in plants. Trends Microbiol 4: 10–15

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Shulaev V, Seskar M and Lam E (1996) Inhibition of programmed cell death in tobacco plants during a pathogen-induced hypersensitive response at low oxygen pressure. Plant Cell 8: 1991–2001

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mock H-P, Keetman U, Kruse E, Rank B and Grimm B (1997) Defense responses to tetrapyrrole-induced oxidative stress in transgenic plants with reduced uroporphyrinogen decarboxylase or coporphyrinogen oxidase activity. Plant Physiol 116: 107–116

    Article  Google Scholar 

  • Mock H-P, Keetman U and Grimm B (1998) Photosensitizing tetrapyrroles induce anti-oxidative and pathogen defence responses in plants, Proceedings of the 7th International Congress of Plant Pathology, Abstract 1.2.16. International Society for Plant Pathology, Edinburgh

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Naton B, Hahlbrock K and Schmelzer E (1996) Correlation of rapid cell death with metabolic changes in fungus-infected, cultured parsley cells. Plant Physiol 112: 433–444

    PubMed  CAS  Google Scholar 

  • Newmeyer DD, Farschon DM and Reed JC (1994) Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79: 353–364

    Article  PubMed  CAS  Google Scholar 

  • Nguyen M, Branton PE, Walton PA, Oltvai ZN, Korsmeyer SJ and Shore GC (1994) Role of membrane anchor domain of Bcl-2 in suppression of apoptosis caused by ElB-defective adenovirus. J Biol Chem 269: 16521–16524

    PubMed  CAS  Google Scholar 

  • Nicotera P and Leist M (1997) Energy supply and the shape of death in neurons and lymphoid cells. Cell Death Differ 4: 435–442

    Article  PubMed  CAS  Google Scholar 

  • Ninnemann H and Maier J (1996) Indications for the occurrence of nitric oxide synthases in fungi and plants and the involvement in photoconidiation of Neurospora crassa. Photochem Photobiol 64: 393–398

    Article  PubMed  CAS  Google Scholar 

  • Novacky A and Ullrich-Eberius CI (1982) Relationship between membrane potential and ATP level in Xanthomonas campestris pv. malvacearum infected cotton cotyledons. Physiol Plant Pathol 21:237–249

    Article  CAS  Google Scholar 

  • Nürnberger T, Colling C, Hahlbrock K, Jabs T, Renelt A, Sacks WR and Scheel D (1994a) Perception and transduction of an elicitor signal in cultured parsley cells. Biochem Soc Symp 60 173–182

    PubMed  Google Scholar 

  • Nürnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K and Scheel D (1994b) High-affinity binding of a fungal Oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78 449–460

    Article  PubMed  Google Scholar 

  • Parker JE, Holub EB, Frost LM, Falk A, Gunn N and Daniels MJ (1996) Characterization of edsl, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different Rpp genes. Plant Cell 8: 2033–2046

    PubMed  CAS  Google Scholar 

  • Pavlovkin J, Novacky A and Ullrich-Eberius CI (1986) Membrane potential changes during bacteria-induced hypersensitive reaction. Physiol Mol Plant Pathol 28: 125–135

    Article  CAS  Google Scholar 

  • Peng M and Kuc J (1992) Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks. Phytopathology 82: 696–699

    Article  CAS  Google Scholar 

  • Pennell RI and Lamb C (1997) Programmed cell death in plants. Plant Cell 9: 1157–1168

    Article  PubMed  CAS  Google Scholar 

  • Peterhänsel C, Freialdenhoven A, Kurth J, Kölsch R and Schulze-Lefert P (1997) Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. Plant Cell 9: 1397–1409

    PubMed  Google Scholar 

  • Petit PX, Susin SA, Zamzami N, Mignotte B and Kroemer G (1996) Mitochondria and programmed cell death: back to the future. FEBS Lett 396: 7–13

    Article  PubMed  CAS  Google Scholar 

  • Popham PL and Novacky A (1991) Use of dimethyl sulphoxide to detect hydroxyl radical during bacteriainduced hypersensitive reaction. Plant Physiol 96: 1157–1160

    Article  PubMed  CAS  Google Scholar 

  • Rahme L, Frederick RT, Grim C, Minderinos M and Panopoulos NJ (1988) Transcriptional organization of pathogenicity/hypersensitivity controlling genes (hrp) in Pseudomonas syringae pv. phaseolicola (Abstract). Fifth International Congress of Plant Pathology, Japan

    Google Scholar 

  • Rancé I, Fournier J, Esquerré-Tugayé M-T (1998) The incompatible interaction between Phytophthora parasitica var. nicotianae race 0 and tobacco is suppressed in transgenic plants expressing antisense lipoxygenase sequences. Proc Natl Acad Sci USA 95: 6554–6559

    Google Scholar 

  • Rasmussen JB, Hammerschmidt R and Zook MN (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv. syringae. Plant Physiol 97: 1342–1347

    Article  CAS  Google Scholar 

  • Reed JC (1997) Cytochrome c: can’t live with it — can’t live without it. Cell 91: 559–562

    Article  PubMed  CAS  Google Scholar 

  • Renelt A, Colling C, Hahlbrock K, Nürnberger T, Parker JE, Sacks WR and Scheel D (1993) Studies on elicitor recognition and signal transduction in plant defence. J Exp Bot 44S: 257–268

    Google Scholar 

  • Ribnicky DM, Shulaev V and Raskin I (1998) Intermediates of salicylic acid biosynthesis in tobacco. Plant Physiol 118:565–572

    Article  PubMed  CAS  Google Scholar 

  • Riely CA, Cohen G and Liebermann M (1974) Ethane evolution: a new index of lipid peroxidation. Science 183: 208–210

    Article  PubMed  CAS  Google Scholar 

  • Riparbelli MG, Callaini G, Tripodi SA, Cintorino M, Tosi P and Dallai R (1995) Localization of the Bcl-2 protein to the outer mitochondrial membrane by electron microscopy. Exp Cell Res 221: 363–369

    Article  PubMed  CAS  Google Scholar 

  • Ritter C and Dangl JL (1995) The avrRpml gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol Plant-Microbe Interact 8: 444–453

    Article  CAS  Google Scholar 

  • Roebuck P, Sexton R and Mansfield JW (1978) Ultrastructural observations on the development of the hypersensitive reaction in leaves of Phaseolus vulgaris cv. red Mexican inoculated with Pseudomonas phaseolicola Race 1). Physiol Plant Path 12: 151–1

    Google Scholar 

  • Rosqvist R, Magnusson K-E and Wolf-Watz H (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J 13: 964–972

    PubMed  CAS  Google Scholar 

  • Ryals J, Weymann K, Lawton K, Friedrich L, Ellis D, Steiner HY, Johnson J, Delaney TP, Jesse T, Vos P and Uknes S (1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell 9: 425–439

    PubMed  CAS  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  CAS  Google Scholar 

  • Schlesinger PH, Gross A, Yin XM, Yamamoto K, Saito M, Waksman G and Korsmeyer SJ (1997) Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc Natl Acad Sci USA 94: 11357–11362

    Article  PubMed  CAS  Google Scholar 

  • Schmidt HHHW and Walter U (1994) NO at work. Cell 78: 919–925

    Article  PubMed  CAS  Google Scholar 

  • Shirasu K, Nakajima H, Rajasekhar VK, Dixon RA and Lamb C (1997) Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9: 261–270

    PubMed  CAS  Google Scholar 

  • Solomon M, Belenghi B, Delledonne M, Menachem E and Levine A (1999) The involvemnet of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11: 431–434

    PubMed  CAS  Google Scholar 

  • Slusarenko AJ (1996) The role of lipoxygenase in resistance to infection. In: Piazza GJ (ed) Lipoxygenase and Lipoxygenase Pathway Enzymes, pp 176–197. American Oil Chemists Society Press, Champaign, Illinois

    Chapter  Google Scholar 

  • Slusarenko AJ and Longland A (1986) Changes in gene activity during expression of the hypersensitive response in Phaseolus vulgaris cv. Red Mexican to an avirulent race 1 isolate of Pseudomonas syringae pv. phaseolicola. Physiol Mol Plant Pathol 29: 79–84

    Article  CAS  Google Scholar 

  • Slusarenko AJ, Croft KPC and Voisey CR (1991) Biochemical and molecular events in the hypersensitive response of bean to Pseudomonas syringae pv. phaseolicola. In: Smith C (ed) Biochemistry and Molecular Biology of Plant:Pathogen Interactions, pp 126–143. Oxford University Press, Oxford

    Google Scholar 

  • Stäb MR and Ebel J (1987) Effects of Ca2+ on phytoalexin induction by fungal elicitor in soybean cells. Arch Biochem Biophys 257: 416–423

    Article  PubMed  Google Scholar 

  • Stakmann EC (1915) Relation between Puccinia graminis and plants highly resistant to its attack. J Agric Res 4: 193–199

    Google Scholar 

  • Staskawicz BJ, Dahlbeck D and Keen NT (1984) Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L). Merr. Proc Natl Acad Sci USA 81: 6024–6028

    Article  CAS  Google Scholar 

  • Sutherland MW (1991) The generation of oxygen radicals during host plant responses to infection. Physiol Mol Plant Pathol 39: 79–93

    Article  CAS  Google Scholar 

  • Takahashi H, Chen ZX, Du H, Liu YD and Klessig DF (1997) Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. Plant J 11: 993–1005

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Makishima T, Sasabe M, Ichinose Y, Shiraishi T, Nishimoto T and Yamada T (1997) dad-1, a putative programmed cell death suppressor gene in rice. Plant Cell Physiol 38: 379–383

    Article  PubMed  CAS  Google Scholar 

  • Tavernier E, Wendehenne D, Blein J-P and Pugin A (1995) Involvement of free calcium in action of cryptogein, a proteinaceous elicitor of hypersensitive reaction in tobacco cells. Plant Physiol 109: 1025–1031

    PubMed  CAS  Google Scholar 

  • Templeton MD and Lamb CJ (1988) Elicitors and defence gene activation. Plant Cell Environ 11: 395–401

    Article  CAS  Google Scholar 

  • Tenhaken R, Levine A, Brisson LF, Dixon RA and Lamb C (1995) Function of the oxidative burst in hypersensitive disease resistance. Proc Natl Acad Sci USA 92: 4158–4163

    Article  PubMed  CAS  Google Scholar 

  • Tenhaken R, Rübel C (1998) Cloning of putative subunits of the soybean plasma membrane NADPH-oxidase involved in the oxidative burst by antibody expression screening. Protoplasma, in press

    Google Scholar 

  • Thompson JE, Legge RL and Barber RF (1987) The role of free radicals in senescence and wounding. New Phytol 105: 317–344

    Article  CAS  Google Scholar 

  • Turner JG and Novacky A (1974) The quantitative relation between plant and bacterial cells involved in the hypersensitive reaction. Phytopathology 64: 885–890

    Article  Google Scholar 

  • Van den Ackerveken, G, Marois, E and Bonas, U (1996) Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87: 1307–1316

    Article  PubMed  Google Scholar 

  • Van Gijsegem F, Genin S and Boucher C (1993) Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol 1: 175–180

    Article  PubMed  Google Scholar 

  • Van Camp W, Van Montagu M and Inzé D (1998) H2O2 and NO: redox signals in disease resistance. Trends Plant Sci 3: 330–334

    Article  Google Scholar 

  • Vianello A, Braidot E, Bassi G and Macré F (1995) Lipoxygenase activity on the plasmalemma of sunflower protoplasts and its modulation. Biochim Biophys Acta 1255: 57–62

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ward HM (1902) On the relations between host and parasite in the bromes and their brown rust, Puccinia dispersa (Erikss). Ann Bot 16: 233–315

    Google Scholar 

  • Wei Z-M, Laby RJ, Zumoff CH, Bauer DW, He SY, Collmer A and Beer SV (1992) Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257: 85–88

    Article  PubMed  CAS  Google Scholar 

  • Weymann K, Hunt M, Uknes S, Neuenschwander U, Lawton K, Steiner H-Y and Ryals J (1995) Suppression and restoration of lesion formation in Arabidopsis Isd mutants. Plant Cell 7: 2013–2022

    PubMed  CAS  Google Scholar 

  • White E (1996) Life, death, and the pursuit of apoptosis. Genes Dev 10: 1–15

    Article  PubMed  CAS  Google Scholar 

  • Wisman E, Cardon GH, Fransz P and Saedler H (1998) The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant Mol Biol 37: 989–999

    Article  PubMed  CAS  Google Scholar 

  • Wolff SP, Garner A and Dean RT (1986) Free radicals, lipids and protein degradation. Trends Biochem Sci 11: 27–31

    Article  CAS  Google Scholar 

  • Woods AM, Fagg J and Mansfield J (1988) Fungal development and irreversible membrane damage in cells of Lactuca sativa undergoing the hypersensitive reaction to the downy mildew fungus Bremia lactucae. Physiol Mol Plant Pathol 32: 483–497

    Article  Google Scholar 

  • Wyllie AH, Morris RG, Smith AL and Dunlop D (1984) Chromatin cleavage in apoptosis: association with Condensed chromatin morphology and dependence on macromolecular synthesis. J Pathol 142: 67–77

    Article  PubMed  CAS  Google Scholar 

  • Wyman JG and Van Etten HD (1982) Isoflavonoid phytoalexins and nonhypersensitive resistance of beans to Xanthomonas campest ris pv. phaseoli. Phytopathology 72: 1419–1424

    Article  CAS  Google Scholar 

  • Xing T, Higgins VJ and Blumwald E (1997) Race-specific elicitors of Cladosporium fulvum promote transiocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells. Plant Cell 9: 249–259

    PubMed  CAS  Google Scholar 

  • Xu H and Heath MC (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell 10: 585–597

    PubMed  CAS  Google Scholar 

  • Yalpani N, Leon J, Lawton MA and Raskin I (1993) Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco. Plant Physiol 103: 315–321

    PubMed  CAS  Google Scholar 

  • Yu IC, Parker J and Bent AF (1998) Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd 1 mutant. Proc Natl Acad Sci USA 95: 7819–7824

    Article  PubMed  CAS  Google Scholar 

  • Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B and Kroemer G (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182: 367–377

    Article  PubMed  CAS  Google Scholar 

  • Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M and Kroemer G (1996) Mitochondrial control of nuclear apoptosis. J Exp Med 183: 1533–1544

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann S, Nürnberger T, Frachisse J-M, Wirtz W, Guern J, Hedrich R and Scheel D (1997) Receptormediated activation of a plant Ca2+-permeable ion channel involved in pathogen defense. Proc Natl Acad Sci USA 94: 2751–2755

    Article  PubMed  CAS  Google Scholar 

  • Zhou J, Loh Y-T, Bressan RA and Martin GB (1995) The tomato gene Ptil encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83: 925–935

    Article  PubMed  CAS  Google Scholar 

  • Zhou JM, Tang XY and Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J 16: 3207–3218

    Article  PubMed  CAS  Google Scholar 

  • Zou H, Henzel WJ, Liu X, Lutschg A and Wang X (1997) Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405–413

    CAS  Google Scholar 

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Jabs, T., Slusarenko, A.J. (2000). The Hypersensitive Response. In: Slusarenko, A.J., Fraser, R.S.S., van Loon, L.C. (eds) Mechanisms of Resistance to Plant Diseases. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-3937-3_9

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