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Apoptosis, programmed cell death and the hypersensitive response

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Abstract

Apoptosis is typically a morphologically identifiable form of programmed cell death in mammals that is regulated by genes with homologues in other animal Phyla. Although both plants and fungal plant pathogens exhibit forms of developmental programmed cell death, demonstrated morphological or genetic homologies with mammalian apoptosis are still generally lacking. Because of its ubiquity and the involvement of signal transduction pathways in its induction, a strong case is developing that the hypersensitive response is a specific form of plant programmed cell death evolved as a defense against microbial parasites. Data suggest that separate signalling pathways may lead to the cell death and the defense gene activation that characterize this response and that parasite-specific resistance genes represent only one of many types of genes involved in response regulation. However, despite some biochemical similarities between the hypersensitive response, forms of developmental programmed cell death in plants, and animal apoptosis, no unique and consistent markers for the hypersensitive response (or plant programmed cell death in general) have yet been found. Whether any of these forms of plant cell death should be called apoptosis depends on how the term is defined. Assuming the hypersensitive response is a form of programmed cell death and is the ‘default state’ upon pathogen entry into a cell, it seems likely that intracellular biotrophic plant pathogens resemble some animal viruses in being able to suppress this response in susceptible hosts.

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References

  • Ameisen JC (1996) The origin of programmed cell death. Science 272: 1278-1279

    Google Scholar 

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

    Google Scholar 

  • Baker CJ and Orlandi EW (1995) Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33: 299-321

    Google Scholar 

  • Bell PR (1996) Megaspore abortion: a consequence of selective apoptosis? Int J Plant Sci 157: 1-7

    Google Scholar 

  • Bennett M, Gallagher M, Fagg J, Bestwick C, Paul T, Beale M and Mansfield J (1996) The hypersensitive reaction, membrane damage and accumulation of autofluorescent phenolics in lettuce cells challenged by Bremia lactucae. Plant J 9: 851-865

    Google Scholar 

  • Bestwick CS, Bennett MH and Mansfield JW (1995) Hrp mutant of Pseudomonas syringaepv phaseolicolainduced cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce. Plant Physiol 108: 503-516

    Google Scholar 

  • Bohland C, Balkenhohl T, Loers G, Feussner I and Grambow HJ (1997) Differential induction of lipoxygenase isoforms in wheat upon treatment with rust fungus elicitor, chitin oligosaccharides, chitosan, and methyl jasmonate. Plant Physiol 114: 679-685

    Google Scholar 

  • Bowen ID (1984) Laboratory techniques for demonstrating cell death. In: Davies I and Sigee DC (eds) Cell Ageing and Cell Death (pp. 5-40) Cambridge University Press

  • Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Ex Bot 48: 181-199

    Google Scholar 

  • Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F and Schulze-Lefert P (1997) the barley Mlogene: a novel control element of plant pathogen resistance. Cell 88: 695-705

    Google Scholar 

  • Chandra S, Martin GB and Low PS (1996) The Pto kinase mediates a signalling pathway leading to the oxidative burst in tomato. Proc Natl Acad Sci USA 93: 13393-13397

    Google Scholar 

  • Chen CY and Heath MC (1994) Features of the rapid cell death induced in cowpea by the monokaryon of the cowpea rust fungus or the monokaryon-derived cultivar-specific elicitor of necrosis. Physiol Mol Plant Pathol 44: 157-170

    Google Scholar 

  • Chinnaiyan AM and Dixit VM (1996) The cell-death machine. Curr Biol 6: 555-562

    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

    Google Scholar 

  • Feuillet C, Schachermayr G and Keller B (1997) Molecular cloning of a new receptor-like kinase gene encoded at the Lr10disease resistance locus of wheat. Plant J 11: 45-52

    Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9: 275-296

    Google Scholar 

  • Fukuda H (1997) Tracheary element differentiation. Plant Cell 9: 1147-1156

    Google Scholar 

  • Gilchrist DG (1997) Mycotoxins reveal connections between plants and animals in apoptosis and ceramide signalling. Cell Death & Differentiation 4: 689-698

    Google Scholar 

  • Goodman RN and Novacky AJ (1994) The Hypersensitive Reaction in Plants to Pathogens. APS Press, St. Paul, MN

    Google Scholar 

  • Grafi G, Burnett RJ, Helentjaris T, Larkins BA, DeCaprio JA, Sellers WR, and Kaelin Jr WG (1996) A maize cDNA encoding a member of the retinoblastoma protein family: involvement in endoreduplication. Proc Natl Acad Sci USA 93: 8962-8967

    Google Scholar 

  • Gray J, Close PS, Briggs SP and Johal GS (1997) A novel suppressor of cell death in plants encoded by the lls1gene of maize. Cell 98: 25-31

    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

    Google Scholar 

  • Groover A, DeWitt N, Heidel A and Jones A (1997) Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma 196: 197-211

    Google Scholar 

  • Hale AJ, Smith CA, Sutherland LC, Stoneman VEA, Longthorne VL, Culhane AC and Williams GT (1996) Apoptosis: molecular regulation of cell death. Eur J Biochem 236: 1-26

    Google Scholar 

  • Hammond-Kosack KE and Jones JDG (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48: 575-607

    Google Scholar 

  • Hampton MB, Vanags DM, Pornares MI and Orrenius S (1996) Involvement of extracellular calcium in phosphatidylserine exposure during apoptosis. Febs Lett 399: 277-282

    Google Scholar 

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

    Google Scholar 

  • Havel L and Durzan DJ (1996a) Apoptosis during diploid parthenogenesis and early somatic embryogenesis of Norway spruce. Int J Plant Sci 157: 8-16

    Google Scholar 

  • Havel L and Durzan DJ (1996b) Apoptosis in plants. Bot. Acta 109: 268-277

    Google Scholar 

  • Heath MC (1976) Hypersensitivity, the cause or consequence of rust resistance? Phytopath 66: 935-936

    Google Scholar 

  • Heath MC (1997) Evolution of plant resistance and susceptibility to fungal parasites. In: Carroll GC and Tudzynski P (eds) TheMycota, Vol. V Part B (pp. 257-276) Springer, Berling Heidelberg New York

    Google Scholar 

  • Heath MC and Stumpf (1986) Ultrastructural observation of penetration sites of the cowpea rust fungus in untreated and silicon-depleted French bean cells. Physiol Mol Plant Pathol 29: 27-39

    Google Scholar 

  • Heath MC and Perumalla (1988) Haustorial mother cell development by Uromyces vignaeon collodion membranes. Can J Bot 66: 736- 741

    Google Scholar 

  • Heath MC and Skalamera D (1997) Cellular interactions between plants and biotrophic fungal parasites. Adv Bot Res 24: 195-225

    Google Scholar 

  • Heath MC, Nimchuk ZL and Xu H (1997) Plant nuclear migrations as indicators of critical interactions between resistant or susceptible cowpea epidermal cells and invasion hyphae of the cowpea rust fungus. New Phytol 135: 689-700

    Google Scholar 

  • Hunt MD, Delaney TP, Dietrich RA, Weymann KB, Dangl JL and Ryals JA (1997) Salicylate-independentlesion formation in Arabidopsis lsdmutants. Mol Plant-MicrobeInt 10: 531-536

    Google Scholar 

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

    Google Scholar 

  • Katsuhara M and Kawasaki T (1996) Salt stress induced nuclear and DNA degradation in meristematic cells of barley roots. Plant Cell Physiol 37: 169-173

    Google Scholar 

  • Kelleher DJ and Gilmore R (1997) Dad1, the defender against apoptotic cell death, is a subunit of the mammalian oligosaccharyl-transferase. Proc Natl Acad Sci USA 94: 4994-4999

    Google Scholar 

  • King KL and Cidlowski JA(1995) Cell cycle and apoptosis: common pathways to life and death. J. Cellul Biochem 58: 175-180

    Google Scholar 

  • Kombrink E and Somssich IE (1995) Defense responses of plants to pathogens. Advances in Botanical Research Vol 21: 2-33

    Google Scholar 

  • Leslie JF and Zeller KA (1996) Heterokaryon incompatibility in fungi: more than just another way to die. J Genet 75:415-424

    Google Scholar 

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

    Google Scholar 

  • Littlefield LJ and Heath MC (1979) Ultrastructure of Rust Fungi. Academic Press, London

    Google Scholar 

  • Lockshin RA and Zakeri Z (1994) Programmed cell death: early changes in metamorphosing cells. Biochem Cell Biol 72: 589- 596

    Google Scholar 

  • Lummerzhein M, Sandroni M, Castresana C, De Oliveira D, Van Montagu M, Roby D and Timmerman B (1995) Comparative microscopic and enzymatic characterization of the leaf necrosis induced in Arabidopsis thalianaby lead nitrate and by Xanthomonas campestrispv. campestrisafter foliar spray. Plant Cell and Env 18: 499-509

    Google Scholar 

  • Meikrantz W Schlegel R 1995 Apoptosis and the cell cycle. J. Cellul Biochem 58: 160-174

    Google Scholar 

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

    Google Scholar 

  • Motizuki M, Yokota S and Tsurugi K (1995) Autophagic death after cell cycle arrest at the restrictive temperature in temperature-sensitive cell division cycle and secretory mutants of the yeast Saccharomyces cerevisiae. Eur J Cell Biol 68: 275-287

    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

    Google Scholar 

  • Nicholson RL and Hammerschmidt R (1992) Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol 30:369-389

    Google Scholar 

  • Orzaez D and Granell A (1997a) DNA fragmentation is regulated by ethylene during carpel senescence in Pisum sativum. Plant J 11: 137-144

    Google Scholar 

  • Orzaez D and Granell A(1997b) The plant homologue of the defender against apoptotic deathgene is down-regulated during senescence of flower petals. FEBS Lett 404: 275-278

    Google Scholar 

  • Pandey A, Walker PR and Sikorska M (1994) Separate pools of endonuclease activity are responsible for internucleosomal and high molecular mass DNA fragmentation during apoptosis. Biochem Cell Biol. 72: 625-629

    Google Scholar 

  • Perez V, Huet J-C, Nespoulous C and Pernollet J-C (1997) Mapping the elicitor and necrotic sites of Phytophthoraelicitins with synthetic peptides and reporter genes controlled by tobacco defense gene promoters. Mol Plant-Microbe Int 10: 750-760

    Google Scholar 

  • Raff MC (1992) Social controls on cell survival and cell death. Nature 356: 397-400

    Google Scholar 

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

    Google Scholar 

  • Stakman EC (1915) Relation between Puccinia graminisand plants highly resistant to its attack. J Agric Res 4: 193-299

    Google Scholar 

  • Strittmatter G, Janssens J, Opsomer C and Botterman J (1995) Inhibition of fungal disease development in plants by engineering controlled cell death. Bio/Techn 13: 1085-1089

    Google Scholar 

  • Tao WK, Kurschner C, Morgan JI (1997) Modulation of cell death in yeast by the bcl-2 family of proteins. J Biol Chem 272: 15547- 15552

    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

    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

    Google Scholar 

  • Wojtaszek P (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322: 681-692

    Google Scholar 

  • Xie Q, Sanz-Burgos P, Hannon GJ and Gutiérrez C (1996). Plant cells contain a novel member of the retinoblastoma family of growth regulatory proteins. Embo J 15: 4900-4908

    Google Scholar 

  • Zhou J, Loh Y-T, Bressan RA and Martin GB(1995) The tomato gene Pti1encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83: 925- 935

    Google Scholar 

  • Zhou J, Tang X and Martin GB (1997) The Pto kinase conferring resistance to tomato bacterial speck disease interactswith proteins that bind a cis-element of pathogenesis-related genes. Embo J 11: 3207-3218

    Google Scholar 

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Heath, M.C. Apoptosis, programmed cell death and the hypersensitive response. European Journal of Plant Pathology 104, 117–124 (1998). https://doi.org/10.1023/A:1008645520976

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