Skip to main content
SpringerLink
Log in

Programmed Cell Death in Plants During Development and Stress Responses

  • Chapter
Cell Engineering

Part of the book series: Cell Engineering ((CEEN,volume 4))

  • 792 Accesses

Conclusions

Compelling evidence indicates that plants possess an intrinsic program for cell suicide. Though enormous progress has been made in understanding the genetic and biochemical basis of programmed cell death in animal cells, very little is known about similar processes in plants. However, there seems to be a continuum between different forms of cell death in plants, with apoptotic-like death at one extreme, necrosis at the other extreme and autolysis in between. Elucidation of the relevant cell death mechanisms is important to understanding plant development, environmental stress responses, as well as plant-pathogen interactions. Knowledge about cell life/death pathways in plants might be exploited for engineering crop resistance against common plant pathogens, extending post-harvest shelf-life of vegetables, fruits, and flowers, and for engineering hardier strains of plants that survive adverse climates. The key now is to identify plant counterparts that function similarly to animal regulators of cell life and death.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abramovitch, R. B., Kim, Y. J., Chen, S., Dickman, M. B., and Martin, G. B. (2003) Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J 22, 60–69.

    Article  CAS  PubMed  Google Scholar 

  • Adams, J. M., and Cory, S. (2002). Apoptosomes: engines for caspase activation. Curr Opin Cell Biol. 14, 715–720.

    Article  CAS  PubMed  Google Scholar 

  • Adrain, C. and Martin, S. J. (2001) The mitochondrial apoptosome: a killer unleashed by the cytochrome seas. Trends. Biochem. Sci. 26, 390–397.

    Article  CAS  PubMed  Google Scholar 

  • Alvarez, M. E., Pennell, R. I., Meijer, P. J., Ishikawa, A., Dixon, R. A., Lamb, C. (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784.

    Article  CAS  PubMed  Google Scholar 

  • Apse, M. P., Aharon, G. S., Snedden, W. A., and Blumwald, E. (1999). Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256–1258.

    Article  CAS  PubMed  Google Scholar 

  • Armstrong, W. (1979) Aeration in higher plants. Adv. Bot. Res. 7, 225–332.

    CAS  Google Scholar 

  • Asai, T., Stone, J. M., Heard, J. E., Kovtun, Y., Yorgey, P., Sheen, J., and Ausubel, F. M. (2000) Fumonisin B1-induced cell death in arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12, 1823–1836.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Austin, M. J., Muskett, P., Kahn, K., Feys, B. J., Jones, J. D. G., and Parker, J. E. (2002) Regulatory role of SGT1 in early R gene-mediated plant defences. Science 295, 2077–2080.

    Article  CAS  PubMed  Google Scholar 

  • Azevedo, C., Santos-Rosa, M. J., and Shirasu, K. (2001) The U-box protein family in plants. Trends Plant Sci. 6, 354–358.

    Article  CAS  PubMed  Google Scholar 

  • Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K., and Schulze-Lefert, P. (2002) The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science 295, 2073–2076.

    Article  CAS  PubMed  Google Scholar 

  • Bachmair, A., Becker, F., Masterton, R. V., and Schell, J. (1990) Perturbation of the ubiquitin system causes leaf curling, vascular tissue alterations and necrotic lesions in a higher plant. EMBO J. 9, 4543–4549.

    CAS  PubMed  Google Scholar 

  • Balk, J., Leaver, C. J., and McCabe, P. F. (1999). Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett. 463, 151–154.

    Article  CAS  PubMed  Google Scholar 

  • Beers, E. P., and Freeman, T. B. (1997) Protease activity during tracheary element differentiation in Zinnia mesophyll cells. Plant Physiol. 113, 873–880.

    CAS  PubMed  Google Scholar 

  • Bertin, J., Nir, W. J., Fisher, C. M., Tayber, O. V., Errada, P. R., Grant, J. R., Keilty, J. J., Gosselin, M. L., Robinson, K. E., Wong, G. H., Glucksmann, M. A., and DiStefano, P. S. (1999). Human CARD4 protein is a novel CED-4/Apaf-1 cell death family member that activates NF-kappaB. J. Biol. Chem. 274, 12955–12958.

    Article  CAS  PubMed  Google Scholar 

  • Bethke, P. C., Lonsdale, J. E., Fath, A., and Jones, R. L. (1999) Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell 11, 1033–1045.

    Article  CAS  PubMed  Google Scholar 

  • Bolduc, N., Ouellet, M., Pitre, F., and Brisson, L. F. (2002) Molecular characterization of two plant BI-1 homologues which suppress Bax-induced apoptosis in human 293 cells. Planta 216, 377–386.

    PubMed  Google Scholar 

  • Bowling, S. A., Clarke, J. D., Liu, Y., Klessig, D. F., and Dong, X. (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9, 1573–1584.

    Article  CAS  PubMed  Google Scholar 

  • Boyer, J. S. (1982) Plant productivity and environment. Science 218, 443–448.

    Google Scholar 

  • Boyes, D. C., Nam, J., and Dangl, J. L. (1998) The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc. Natl. Acad. Sci. USA 95, 15849–15854.

    Article  CAS  PubMed  Google Scholar 

  • Brandwagt, B. F., Mesbah, L. A., Takken, F. L., Laurent, P. L., Kneppers, T. J., Hille, J., and Nijkamp, H. J. (2000) A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1. Proc. Natl. Acad. Sci. U. S. A. 97, 4961–4966.

    Article  CAS  PubMed  Google Scholar 

  • Brodersen, P., Petersen, M., Pike, H. M., Olszak, B., Skov, S., N. Odum, Jorgensen, L. B., Brown, R. E., and Mundy, J. (2002) Knockout of arabidopsis accelerated-cell-death11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev. 16, 490–502.

    Article  CAS  PubMed  Google Scholar 

  • Buschges, R., Hollricher, K., Panstruga, R., Simons, G., Wolter, M., Frijters, A., Van Daelen, R., Van Der Lee, T., Diergaarde, P., Groenendijk, J., Topsch, S., Vos, P., Salamini, F., and Schulze-Lefert, P. (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88, 695–705.

    Article  CAS  PubMed  Google Scholar 

  • Cessna, S. G., Sears, V. E., Dickman, M. B., and Low, P. S. (2000) Oxalic acid, a pathogenicity factor for Sclerotinia sclerotiorum, suppresses the oxidative burst of the host plant. Plant Cell 12, 2191–2200.

    Article  CAS  PubMed  Google Scholar 

  • Chandok, M. R., Ytterberg, A. J., Van Wijk, K. J., Klessig, D. F. (2003) The Pathogen-Inducible Nitric Oxide Synthase (iNOS) in Plants Is a Variant of the P Protein of the Glycine Decarboxylase Complex. Cell 113, 469–482.

    Article  CAS  PubMed  Google Scholar 

  • Chang, J. H., Rathjen, J. P., Bernal, A. J., Staskawicz, B. J., and Michelmore, R. W. (2000) avrPto enhances growth and necrosis caused by Pseudomonas syringae pv.tomato in tomato lines lacking either Pto or Prf. Mol. Plant Microbe Interact. 13, 568–571.

    CAS  PubMed  Google Scholar 

  • Chen, F., and Foolad, M. R. (1997) Molecular organization of a gene in barley which encodes a protein similar to aspartic protease and its specific expression in nucellar cells during degeneration. Plant Mol. Biol. 35, 821–831.

    Article  CAS  PubMed  Google Scholar 

  • Chen, H.-M., Zhou, J., and Dai, Y.-R. (2000) Cleavage of lamin-like proteins in vivo and in vitro apoptosis of tobacco protoplasts induced by heat shock. FEBS Lett. 480, 165–168.

    Article  CAS  PubMed  Google Scholar 

  • Chen, S., Dunigan, D. D., and Dickman, M. B. (2003). Bcl-2 family members inhibit oxidative stress-induced programmed cell death in Saccharomyces cerevisiae. Free Radical Biol. Med. 34, 1315–1325.

    CAS  Google Scholar 

  • Clouse, S. D., and Gilchrist, D. G. (1986) Interaction of the as locus in F8 paired lines of tomato with Alternaria alternata f. sp. lycopersici and AAL toxin. Phytopathol. 77, 80–82.

    Google Scholar 

  • Crosti, P., Malerba, M., and Bianchetti, R. (2001) Tunicamycin and Brefeldin A induce in plant cells a programmed cell death showing apoptotic features. Protoplasma 216, 31–38.

    CAS  PubMed  Google Scholar 

  • Curtis, M. J., and Wolpert, T. J. (2002) The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death. Plant J. 29, 295–312.

    Article  PubMed  Google Scholar 

  • Dangl, J. L., and Jones, J. D. (2001). Plant pathogens and integrated defence responses to infection. Nature 411, 826–833.

    Article  CAS  PubMed  Google Scholar 

  • Danon, A., and Gallois, P. (1998) UV-C radiation induces apoptotic-like changes in Arabidopsis thaliana. FEBS Lett. 437, 131–136.

    Article  CAS  PubMed  Google Scholar 

  • Daugas, E., Nochy, D., Ravagnan, L., Loeffler, M., Susin, S. A., Zamzami, N., and Kroemer, G. (2000). Apoptosis-inducing factor (AIF): a ubiquitous mitochondrial oxidoreductase involved in apoptosis. FEBS Lett. 476, 118–123.

    Article  CAS  PubMed  Google Scholar 

  • De Jong, A. J., Hoeberichts, F. A., Yakimova, E. T., Maximova, E., and Woltering, E. J. (2000) Chemical-induced apoptotic cell death in tomato cells: involvement of caspase-like proteases. Planta 211, 656–662.

    PubMed  Google Scholar 

  • Dellaporta, S. L., and Calderon-Urrea, A. (1993). Sex determination in flowering plants. Plant Cell 5, 1241–1251.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Delledonne, M., Zeier, J., Marocco, A., and Lamb, C. (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl. Acad. Sci. U. S. A. 98, 13454–13459.

    Article  CAS  PubMed  Google Scholar 

  • Delorme, V. G. R., McCabe, P. F., Kim, D.-J., and Leaver, C. J. (2000) A matrix metalloproteinase gene is expressed at the boundary of senescence and programmed cell death in cucumber. Plant Physiol. 123, 917–927.

    Article  CAS  PubMed  Google Scholar 

  • Del Pozo, E., and Lam, E. (1998) Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol. 8, 1129–1131.

    PubMed  Google Scholar 

  • Del Pozo, O., and Lam, E. (2003) Expression of the baculovirus p35 protein in tobacco affects cell death progression and compromises N gene—mediated disease resistance response to tobacco mosaic virus. Mol. Plant-Microbe Interact. 16, 485–494.

    PubMed  Google Scholar 

  • Demura, T., Tashiro, G., Horiguchi, G., Kishimoto, N., Kubo, M., Matsuoka, N., Minami, A., Nagata-Hiwatashi, M., Nakamura, K., Okamura, Y., Sassa, N., Suzuki, S., Yazaki, J., Kikuchi, S., and Fukuda, H. (2002) Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells. Proc. Natl. Acad. Sci. U. S. A. 99, 15794–15799.

    Article  PubMed  Google Scholar 

  • DeSalle, L. M., and Pagano, M. (2001) Regulation of the G1 to S transition by the ubiquitin pathway. FEBS Lett. 490, 179–189.

    Google Scholar 

  • Desikan, R., Reynolds, A., Hancock, J. T., and Neill, S. J. (1998) Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures. Biochem. J. 330, 115–120.

    CAS  PubMed  Google Scholar 

  • Devadas, S. K., Enyedi, A., and Raina, R. (2002) The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signalling in cell death and defence against pathogens. Plant J. 30, 467–480.

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri, S., and Estelle, M. (2002) The role of regulated protein degradation in auxin response. Plant Mol. Biol. 49, 401–409.

    Article  CAS  PubMed  Google Scholar 

  • Dickman, M. B., Park, Y. K., Oltersdorf, T., Li, W., Clemente, T., and French, R. (2001). Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc. Natl. Acad. Sci. USA 98, 6957–6962.

    Article  CAS  PubMed  Google Scholar 

  • Dietrich, R. A., Delaney, T. P., Uknes, S. J., Ward, E. R., Ryals, J. A., and Dangl, J. L. (1994) Arabidopsis mutants simulating disease resistance response. Cell 77, 565–577.

    Article  CAS  PubMed  Google Scholar 

  • Dietrich, R. A., Richberg, M. H., Schmidt, R., Dean, C., and Dangl, J. L. (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  CAS  PubMed  Google Scholar 

  • Dixon, M. S., Golstein, C., Thomas, C. M., Van der Biezen, E. A., and Jones, J. D. (2000) Genetic complexity of pathogen perception by plants: the example of Rcr3, a tomato gene required specifically by Cf-2. Proc. Natl. Acad. Sci. USA 97, 8807–8814.

    Article  CAS  PubMed  Google Scholar 

  • Dominguez, F., Moreno, J., and Cejudo, F. J. (2001) The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development. Planta 213, 352–360.

    CAS  PubMed  Google Scholar 

  • Drew, M. C., Jackson, M. B., and Giffard, S. (1979) Ethylene promoted adventitious rooting and development of cortical air spaces in Zea mays L. Planta 147, 83–88.

    Article  CAS  Google Scholar 

  • Du, C., Fang, M., Li, Y., Li, C. and Wang, X. (2000) Smac, a mitochondrial protein that promotes cytochrome C-dependent caspase activation by eliminating IAP inhibition. Cell 102, 33–42.

    Article  CAS  PubMed  Google Scholar 

  • El-Antably, H. M. M., Wareing, P. F., and Hillman, J. (1967) Some physiological responses to D,L abscisin (dormin). Planta 73, 74–90.

    Article  CAS  Google Scholar 

  • Elbaz, M., Avni, A., and Weil, M. (2002) Constitutive caspase-like machinery executes programmed cell death in plant cells. Cell Death Differ. 9, 726–733.

    Article  CAS  PubMed  Google Scholar 

  • Fath, A., Bethke, P., Lonsdale, J., Mez-Romero, R., and Jones, R. (2000) Programmed cell death in barley aleurone. Plant Mol. Biol. 44, 255–266.

    Article  CAS  PubMed  Google Scholar 

  • Ferri, K. F., and Kroemer, G. (2001) Organelle-specific initiation of cell death pathways. Nature Cell Biol. 3, E255–E263

    Article  CAS  PubMed  Google Scholar 

  • Feys, B., Benedetti, C. E., Penfold, C. N., and Turner, J. G. (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine Are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6, 751–759.

    Article  CAS  PubMed  Google Scholar 

  • Filonova, L. H., Von Arnold, S., Daniel, G., and Bozhkov, P. V. (2002). Programmed cell death eliminates all but one embryo in a polyembryonic plant seed. Cell Death Differ. 9, 1057–1062.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fukuda, H. (1997) Programmed cell death during vascular system formation. Cell Death. Differ. 4, 684–688.

    Article  CAS  Google Scholar 

  • Fukuda, H. (2000) Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol. Biol. 44, 245–253.

    CAS  PubMed  Google Scholar 

  • Fukuda, H., and Komamine, A. (1980a) Direct evidence for cytodifferentiation to tracheary elements without intervening mitosis in a culture of single cells isolated from the mesophyll cells of Zinnia elegans. Plant Physiol. 65, 61–64.

    CAS  Google Scholar 

  • Fukuda, H., and Komamine, A. (1980b) Establishment of an experimental system for the tracheary element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol. 65, 57–60.

    CAS  Google Scholar 

  • Funk, V., Kositsup, B., Zhao, C., and Beers, E. P. (2002) The arabidopsis xylem peptidase XCP1 is a tracheary element vacuolar protein that may be a papain ortholog. Plant Physiol. 128, 85–94.

    Article  Google Scholar 

  • Gazitt, Y., Fey, V., Thomas, C., and Alvarez, R. (1998). Bcl-2 overexpression is associated with resistance to dexamethasone, but not melphalan, in multiple myeloma cells. Int. J. Oncol. 13, 397–405.

    CAS  PubMed  Google Scholar 

  • Godoy, G., Steadman, J. R., Dickman, M. B., and Dam, R. (1989) Use of mutants to demonstrate the role of oxalic acid in pathogenicity of Sclerotinia sclerotiorum on Phaseolus vulgaris. Physiol. Mol. Plant Pathol. 37, 179–191.

    Google Scholar 

  • Gray, J., Close, P. S., Briggs, S. P., and Johal, G. S. (1997) A novel suppressor of cell death in plants encoded by the Lls gene of maize. Cell 89, 25–31.

    Article  CAS  PubMed  Google Scholar 

  • Gray, J., Janick-Buckner, D., Buckner, B., Close, P. S., and Johal, G. S. (2002) Light-dependent death of Maize lls1 cells is mediated by mature chloroplasts. Plant Physiol. 130, 1894–1907.

    Article  CAS  PubMed  Google Scholar 

  • Gray, W. M., Muskett, P. R., Chuang, H.-W., Parker, J. E. (2003). Arabidopsis SGT1b is required for SCFTIR1-mediated auxin response. In Plant biology: functions and control of cell death. J. Dangl, P. Schulze-Lefert and J. Glazebrook, eds., Keystone Symposia, Snowbird, Utah, 61.

    Google Scholar 

  • Greenberg, J. T. (1997) Programmed cell death in plant-pathogen interactions. Annu. Rev. Plant Pathol. Plant Mol. Biol. 48, 525–545.

    CAS  Google Scholar 

  • Greenberg, J. T., Guo, A., Klessig, D. F., and Ausubel, F. M. (1994) Programmed cell death in plants: a pathogen-triggered response activated coordinately with multiple defence functions. Cell 77, 551–563.

    Article  CAS  PubMed  Google Scholar 

  • Greenberg, J. T., Silverman, F. P., and Liang, H. (2000). Uncoupling salicylic acid-dependent cell death and defence-related responses from disease resistance in the Arabidopsis mutant acd5. Genetics 156, 341–350.

    CAS  PubMed  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.

    Article  Google Scholar 

  • Groover, A., and Jones, A. M. (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol. 119, 375–384.

    Article  CAS  PubMed  Google Scholar 

  • Gunawardena, A. H. L. A. N., Pearce, D. M., Jackson, M. B., Hawes, C. R., and Evans, D. E. (2001). Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212, 205–214.

    Article  CAS  PubMed  Google Scholar 

  • Guttman, D. S., Vinatzer, B. A., Sarkar, S. F., Ranall, M. V., Kettler, G., and Greenberg, J. T. (2002). A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295, 1722–1726.

    Article  CAS  PubMed  Google Scholar 

  • He, C. J., Morgan, P. W., and Drew, M. C. (1996) Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiol. 112, 463–472.

    CAS  PubMed  Google Scholar 

  • Heath, M. (1998) Apoptosis, programmed cell death and the hypersensitive response. Eur. J. Plant Pathol. 104, 117–124.

    Article  CAS  Google Scholar 

  • Hengartner, M. O. (2000). The biochemistry of apoptosis. Nature 407, 770–776.

    Article  CAS  PubMed  Google Scholar 

  • Hoeberichts, F. A., and Woltering, E. J. (2002) Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. Bio Essays 25, 47–57.

    CAS  Google Scholar 

  • Howe G. A., Lightner, J., Browse, J., and Ryan, C. A. (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell. 8, 2067–2077.

    Article  CAS  PubMed  Google Scholar 

  • Hu, G., Richter, T. E., Hulbert, S. H., and Pryor, T. (1996) Disease lesion mimicry caused by mutations in the rust resistance gene rp1. Plant Cell 8, 1367–1376.

    Article  CAS  PubMed  Google Scholar 

  • Huang, F. Y., Philosoph-Hadas, S., Meir, S., Callaham, D. A., Sabato, R., Zelcer, A., and Hepler, P. K. (1997). Increases in cytosolic Ca2+ in parsley mesophyll cells correlate with leaf senescence. Plant Physiol. 115, 51–60.

    CAS  PubMed  Google Scholar 

  • Huckelhoven, R., Dechert, C., Trujillo, M., and Kogel, K. H. (2001) Differential expression of putative cell death regulator genes in near-isogenic, resistant and susceptible barley lines during interaction with the powdery mildew fungus. Plant Mol. Biol. 47, 739–748.

    CAS  PubMed  Google Scholar 

  • Huckelhoven, R., Dechert, C., and Kogel, K. H. (2003). Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis. Proc. Natl. Acad. Sci. U.S.A. 100, 5555–5560.

    Article  CAS  PubMed  Google Scholar 

  • Huguet, E (2000) Bacterial pathogenicity. In: Annual Plant Reviews Volume 4: Molecular Plant Pathology. M Dickinson and J Beynon eds., Sheffield Academic Press, 26–64

    Google Scholar 

  • Huh, G.-H., Damsz, B., Matsumoto, T. K., Reddy, M. P., Rus, A. M., Ibeas, J. I., Narasimhan, M. L., Bressan, R. A., and Hasegawa, P. M. (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29, 649–659.

    Article  CAS  PubMed  Google Scholar 

  • Hunt, M. D., Neuenschwander, U. H., Delaney, T. P., Weymann, K. B., Friedrich, L. B., Lawton, K. A., Steiner, H. Y. and Ryals, J. A. (1996) Recent advances in systemic acquired resistance research—a review. Gene 179, 89–95.

    Article  CAS  PubMed  Google Scholar 

  • Hunt, M. D., Neuenschwander, U. H., Delaney, T. P., Weymann, K. B., Friedrich, L. B., Lawton, K. A., Steiner, H. Y. and Ryals, J. A. (1996) Recent advances in systemic acquired resistance research—a review. Gene 179, 89–95.

    Article  CAS  PubMed  Google Scholar 

  • Innes, R. W., Bent, A. F., Kunkel, B. N., Bisgrove, S. R., and Staskawicz, B. J. (1993) Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J. Bacteriol. 175, 4859–4869.

    CAS  PubMed  Google Scholar 

  • Inukai, T., Inoue, A., Kurosawa, H., Goi, K., Shinjyo, T., Ozawa, K., Mao, M., Inaba, T., and Look, A. T. (1999). SLUG, a ces-1-related zinc finger transcription factor gene with antiapoptotic activity, is a downstream target of the E2A-HLF oncoprotein. Mol. Cell. 4, 343–352.

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa, A., Okamoto, H., Iwasaki, Y., and Asahi, T. (2001) A deficiency of coproporphyrinogen III oxidase causes lesion formation in Arabidopsis. Plant J. 27, 89–99.

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa, A., Tanaka, H., Nakai, M., and Asahi, T. (2003) Deletion of a chaperonin 60beta gene leads to cell death in the arabidopsis lesion initiation 1 mutant. Plant Cell Physiol. 44, 255–261.

    Article  CAS  PubMed  Google Scholar 

  • Itai, C. (1999) Role of phytohormones in plant responses to stresses. In Plant responses to environmental stresses: from phytohormones to genome reorganization. H. R. Lerner, ed., Marcel Dekker Inc., New York, 287–301

    Google Scholar 

  • Ito, J., and Fukuda, H. (2002) ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell 12, 3201–3211

    Google Scholar 

  • Iwasaki, T., and Shibaoka, H. (1991) Brassinosteroids act as regulators of tracheary-element differentiation in isolated Zinnia mesophyll cells. Plant Cell Physiol. 32, 1007–1014.

    CAS  Google Scholar 

  • Jabs, T., Dietrich, R. A., and Dangl, J. L. (1996) Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science 273, 1853–1856.

    CAS  PubMed  Google Scholar 

  • Jackson, R. W., Mansfield, J. W., Ammouneh, H., Dutton, L. C., Wharton, B., Ortiz-Barredo, A., Arnold, D. L., Tsiamis, G., Sesma, A., Butcher, D., Boch, J., Kim, Y. J., Martin, G. B., Tegli, S., Murillo, J., and Vivian, A. (2002). Location and activity of members of a family of virPphA homologues in pathovars of Pseudomonas syringae and P. savastanoi. Mol. Plant Pathol. 3, 205–216.

    Article  CAS  Google Scholar 

  • Ji, C., Boyd, C., Slaymaker, D., Okinawa, T., Takeuchi, Y., Midland, S. L., Sims, J. J., Herman, E., and Keen, N. (1998) Characterisation of a 34-kDa soybean binding protein for the syringolide elicitors. Proc. Natl. Acad. Sci. USA 95, 3306–3311.

    CAS  PubMed  Google Scholar 

  • Jin, C., and Reed, J. C. (2002). Yeast and apoptosis. Nat. Rev. Mol. Cell Biol. 3, 453–459.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • John, I., Drake, R., Farrell, A., Cooper, W., Lee, P., Horton, P., and Grierson, D. (1995) Delayed leaf senescence in ethylene-deficient ACC oxidase antisense tomato plants: molecular and physiological analysis. Plant J 7, 483–490.

    Article  CAS  Google Scholar 

  • Jonak, C., Okresz, L., Bogre, L., and Hirt, H. (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol. 5, 415–424.

    Article  CAS  PubMed  Google Scholar 

  • Jones, C., Ciacci-Zanella, J.R., Zhang, Y., Henderson, G., and Dickman, M.B. 2001. Analysis of fumonisin induced apoptosis. Environmental Health Perspectives 109:1–7.

    Google Scholar 

  • Katsuhara M (1997) Apoptosis-like cell death in barley roots under salt stress. Plant Cell Physiol. 38, 1091–1093.

    CAS  Google Scholar 

  • Katsuhara, M., and Shibasaka, M. (2000) Cell death and growth recovery of barley after transient salt stress. J. Plant Res. 113, 239–243.

    CAS  Google Scholar 

  • Kawai, M., Pan, L., Reed, J. C., and Uchimiya, H. (1999) Evolutionally conserved plant homologue of the Bax inhibitor-1 (BI-1) gene capable of suppressing Bax-induced cell death in yeast. FEBS Lett. 464, 143–147.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kidd, D., Liu, Y., and Cravatt, B. F. (2001) Profiling serine hydrolase activities in complex proteomes. Biochemistry 40, 4005–4015.

    CAS  PubMed  Google Scholar 

  • Kim, P. K., Kwon, Y. G., Chung, H. T., and Kim, Y. M. (2002a) Regulation of caspases by nitric oxide. Ann. N. Y. Acad. Sci. 962, 42–52.

    CAS  PubMed  Google Scholar 

  • Kim, M. C., Panstruga, R., Elliott, C., Muller, J., Devoto, A., Yoon, H. W., Park, H. C., Cho, M. J., and Schulze-Lefert, P. (2002b) Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 416, 447–450.

    Article  CAS  PubMed  Google Scholar 

  • Kim, M. C., Lee, S. H., Kim, J. K., Chun, H. J., Choi, M. S., Chung, W. S., Moon, B. C., Kang, C. H., Park, C. Y., Yoo, J. H., Kang, Y. H., Koo, S. C., Koo, Y. D., Kung, J. C., Kim, S. T., Schulze-Lefert, P., Lee, S. Y., and Cho, M. J. (2002c) Mlo, a modulator of plant defense and cell death, is a novel calmodulin-binding protein. Isolation and characterization of a rice Mlo homologue. J. Biol. Chem. 277, 19304–19314.

    CAS  PubMed  Google Scholar 

  • Kim, Y. J., Lin, N. C., and Martin, G. B. (2002d). Two distinct Pseudomonas effector proteins interact with the Pto kinase and activate plant immunity. Cell 109, 589–598.

    CAS  PubMed  Google Scholar 

  • Kim, M., Ahn, J. W., Jin, U. H., Choi, D., Paek, K. H., and Pai, H. S. (2003) Activation of the programmed cell death pathway by inhibition of proteasome function in plants. J. Biol. Chem. 278, 19406–19415.

    CAS  PubMed  Google Scholar 

  • Kitagawa, K., Skowyra, D., Elledge, S. J., Harper, J. W., and Hieter, P. (1999) SGT1 encodes an essential component of the yeast kinetochore assembly pathway and a novel subunit of the SCF ubiquitin ligase complex. Mol. Cell 4, 21–33.

    Article  CAS  PubMed  Google Scholar 

  • Kliebenstein, D. J., Dietrich, R. A., Martin, A. C., Last, R. L., and Dangl, J. L. (1999) LSD1 regulates salicylic acid induction of copper zinc superoxide dismutase in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 12, 1022–1026.

    CAS  PubMed  Google Scholar 

  • Kloek, A. P., Verbsky, M. L., Sharma, S. B., Schoelz, J. E., Vogel, J., Klessig, D. F., and Kunkel, B. N. (2001). Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J. 26, 509–522.

    Article  CAS  PubMed  Google Scholar 

  • Koch, J. R., Creelman, R. A., Eshita, S. M., Seskar, M., Mullet, J. E., and Davis, K. R. (2000) Ozone sensitivity in hybrid poplar correlates with insensitivity to both salicylic acid and jasmonic acid. The role of programmed cell death in lesion formation. Plant Physiol. 123, 487–496.

    Article  CAS  PubMed  Google Scholar 

  • Kooman-Gersmann, M., Honee, G., Bonnema, G., and De Wit, P. G. J. M. (1996). A high-affinity binding site for the AVR9 peptide elicitor of Cladosporium fulvum is present on plasma membranes of tomato and other Solanaceous plants. Plant Cell 8, 929–938.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kruft, V., Eubel, H., Jansch, L., Werhahn, W., and Braun, H. P. (2001) Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiol. 127, 1694–1710.

    Article  CAS  PubMed  Google Scholar 

  • Kuo, A., Cappelluti, S., Cervantes-Cervantes, M., Rodriguez, M., and Bush, D. S. (1996) Okadaic acid, a protein phosphatase inhibitor, blocks calcium changes, gene expression, and cell death induced by gibberellin in wheat aleurone cells. Plant Cell 8, 259–269.

    Article  CAS  PubMed  Google Scholar 

  • Lacomme, C., and Santa-Cruz, S. (1999) Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc. Natl. Acad. Sci. U.S.A. 96, 7956–7961.

    Article  CAS  PubMed  Google Scholar 

  • Lam, E., Kato, N. and Lawton, M. (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411, 848–853

    Article  CAS  PubMed  Google Scholar 

  • Lane, B. G. (2002) Oxalate, germins, and higher-plant pathogens. IUBMB Life 53, 67–75.

    CAS  PubMed  Google Scholar 

  • Larkindale, J., and Knight, M. R. (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol. 128, 682–695.

    Article  CAS  PubMed  Google Scholar 

  • Lecourieux, D., Mazars, C., Pauly, N., Ranjeva, R., and Pugin, A. (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14, 2627–2641.

    Article  CAS  PubMed  Google Scholar 

  • Lee, J. C., and Peter, M. E. (2002). Regulation of apoptosis by ubiquitinylation. Immunol. Reviews 193, 39–47.

    Google Scholar 

  • Leister, R. T., and Katagiri, F. (2000) A resistance gene product of the nucleotide binding site-leucine-rich repeat class can form a complex with bacterial avirulence proteins in vivo. Plant J. 22, 345–354.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li, F., Srinivasan, A., Wang, Y., Armstrong, R. C., Tomaselli, K. J., and Fritz, L. C. (1997) Cell-specific induction of apoptosis by microinjection of cytochrome c. Bcl-xL has activity independent of cytochrome c release. J. Biol. Chem. 272, 30299–30305.

    CAS  PubMed  Google Scholar 

  • Li, X., Marani, M., Mannucci, R., Kinsey, B., Andriani, F., Nicoletti, I., Denner, L., and Marcelli, M. (2001). Overexpression of BCL-X(L) underlies the molecular basis for resistance to staurosporine-induced apoptosis in PC-3 cells. Cancer Res. 61, 1699–1706.

    CAS  PubMed  Google Scholar 

  • Ligterink, W. (2000) MAP kinases in plant signal transduction: how many, and what for? Results Probl. Cell Differ. 27, 11–27.

    CAS  PubMed  Google Scholar 

  • Lin, A. (2002). Activation of the JNK signaling pathway: breaking the brake on apoptosis. BioEssays 25, 17–24.

    CAS  Google Scholar 

  • Lincoln, J. E., Richael, B., Overduin, B., Smith, K., Bostock, R., and Gilchrist, D. G. (2002) Expression of the antiapoptotic baculovirus p35 gene in tomato blocks programmed cell death and provides broad-spectrum resistance to disease. Proc. Natl. Acad. Sci. U.S.A. 99, 15217–15521.

    CAS  PubMed  Google Scholar 

  • Lord, S. J., Rajotte, R. V., Korbutt, G. S., and Bleackley, R. C. (2003) Granzyme B: a natural born killer. Immunol. Reviews 193, 31–38.

    CAS  Google Scholar 

  • Luderer, R., Rivas, S., Nurnberger, T., Mattei, B., Hooven, H. W. V. d., Hoorn, R. A. V. d., Romeis, T., Wehrfritz, J. M., Blume, B., Nennstiel, D., Zuidema, D., Vervoort, J., Lorenzo, G. D., Jones, J. D., Wit, P. J. D., and Joosten, M. H. (2001) No evidence for binding between resistance gene product Cf-9 of tomato and avirulence gene product AVR9 of Cladosporium fulvum. Mol. Plant Microbe Interact. 14, 867–876.

    CAS  PubMed  Google Scholar 

  • Lui, H. M., Chen, J., Wang, L., and Naumovski, L. (2003) ARMER, apoptotic regulator in the membrane of the endoplasmic reticulum, a novel inhibitor of apoptosis. Mol. Cancer Res. 1, 508–518.

    CAS  PubMed  Google Scholar 

  • Lund, S. T., Stall, R. E., and Klee, H. J. (1998) Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell 10, 371–382.

    Article  CAS  PubMed  Google Scholar 

  • Mach, J. M., Castillo, A. R., Hoogstraten, R., and Greenberg, J. T. (2001) The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA 98, 771–776.

    Article  CAS  PubMed  Google Scholar 

  • Mackey, D., Holt, B. F., Wiig, A., and Dangl, J. L. (2002). RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108, 743–754.

    Article  CAS  PubMed  Google Scholar 

  • Mackey, D., Belkhadir, Y., Alonso, J. M., Ecker, J. R., and Dangl, J. L. (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389.

    Article  CAS  PubMed  Google Scholar 

  • Madeo, F., Frohlich, E., Ligr, M., Grey, M., Sigrist, S. J., Wolf, D. H., and Frohlich, K. U. (1999). Oxygen stress: a regulator of apoptosis in yeast. J. Cell. Biol. 145, 757–767.

    Article  CAS  PubMed  Google Scholar 

  • Marcelli, M., Marani, M., Li, X., Sturgis, L., Haidacher, S. J., Trial, J. A., Mannuci, R., Nicoletti, I., and Denner, L. (2000). Heterogeneous apoptotic responses of prostate cancer cell lines identify an association between sensitivity to staurosporine-induced apoptosis, expression of Bcl-2 family members, and caspase activation. Prostate 42, 260–273.

    Article  CAS  PubMed  Google Scholar 

  • Martins, L. M. (2002). The serine protease Omi/HtrA2: a second mammalian protein with a Reaper-like function. Cell Death Differ. 9, 699–701.

    Article  CAS  PubMed  Google Scholar 

  • Matsumara, H., Nirasawa, S., Kiba, A., Urasaki, N., Saitoh, H., Ito, M., Kawai-Yamada, M., Uchimiya, H., and Terauchi, R. (2003) Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L) cells. Plant J. 33, 425–434.

    Google Scholar 

  • Mayama, S., Tani, T., Ueno, T., Midland, S. L., Simms, J. J., and Keen, N. T. (1985) Association of avenalumin accumulation with co-segregation of victorin sensitivity and crown rust resistance in oat lines carrying the Pc-2 gene. Physiol. Mol. Plant Pathol. 46, 263–274.

    Google Scholar 

  • McCabe, P. F., Levine, A., Meijer, P.-J., Tapon, N. A., and Pennell, R. I. (1997) A programmed cell death pathway activated in carrot cells cultured at low cell density. Plant J. 12, 267–280.

    Article  CAS  Google Scholar 

  • Millar, A. H., Sweetlove, L. J., Giege, P., and Leaver, C. J. (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol. 127, 1711–1727.

    Article  CAS  PubMed  Google Scholar 

  • Minami, A., and Fukuda, H. (1995) Transient and specific expression of a cysteine endopeptidase associated with autolysis during differentiation of Zinnia mesophyll cells into tracheary elements. Plant Cell. Physiol. 36, 1599–1606.

    CAS  PubMed  Google Scholar 

  • Mitsuhara, I., Malic, A. M., Miura, M., and Ohashi, Y. (1999) Animal cell death suppressors Bcl-xl and Ced-9 inhibit cell death in tobacco plants. Curr. Biol. 9, 775–778.

    Article  CAS  PubMed  Google Scholar 

  • Mittler, R., and Lam, E. (1995) In situ detection of nDNA fragmentation during the differentiation of tracheary elements in higher plants. Plant Physiol. 108, 489–493.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Mlejnek, P. and Prochazka, S. (2002) Activation of caspase-like proteases and induction of apoptosis by isopentenyladenosine in tobacco BY-2 cells. Planta. 215, 158–66

    Article  CAS  PubMed  Google Scholar 

  • Moeder, W., Barry, C. S., Tauiainen, A. A., Betz, C., Tuomainen, J., Utriainen, M., Grierson, D., Sandermann, H., Langebartels, C., and Kangasjarvi, J. (2002) Ethylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiol. 130, 1918–1926.

    Article  CAS  PubMed  Google Scholar 

  • Molina, A., Volrath, S., Guyer, D., Maleck, K., Ryals, J., and Ward, E. (1999) Inhibition of protoporphyrinogen oxidase expression in Arabidopsis causes a lesion-mimic phenotype that induces systemic acquired resistance. Plant J. 17, 667–678.

    Article  CAS  PubMed  Google Scholar 

  • Moore, T., Martineau, B., Bostock, R. M., Lincoln, J. E., and Gilchrist, D. G. (1999) Molecular and genetic characterisation of ethylene involvement in mycotoxin-induced plant cell death. Physiol. Molec. Plant Pathol 42, 359–371.

    Google Scholar 

  • Mothes, K., and Engelbrecht, L. (1961) Kinetin-induced directed transport of substances in excised leaves in the dark. Phytochem. 1, 58–62.

    Article  CAS  Google Scholar 

  • Mou, Z., He, Y., Dai, Y., Liu, X., and Li, J. (2000). Deficiency in fatty acid synthase leads to premature cell death and dramatic alterations in plant morphology. Plant Cell 12, 405–417.

    Article  CAS  PubMed  Google Scholar 

  • Navarre, D. A., and Wolpert, T. J. (1999) Victorin induction of an apoptotic/senescence-like response in oats. Plant Cell 11, 237–249.

    Article  CAS  PubMed  Google Scholar 

  • Newmeyer, D. D., Farschon, D. M., and Reed, J. C. (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  CAS  PubMed  Google Scholar 

  • Nooden, L. D. (1988) The phenomena of senescence and aging. In Senescence and aging in plants. L. D. Nooden and A. C. Leopold, eds. Academic Press. 1–50.

    Google Scholar 

  • Obara, K., Kuriyama, H., and Fukuda, H. (2001) Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol. 125, 615–626.

    Article  CAS  PubMed  Google Scholar 

  • O’Brien, I. E. W., Baguley, B. C., Murray, B. G., Morris, B. A. M., Ferguson, I. B. (1998) Early stages of the apoptotic pathway in plant cells are reversible. Plant J. 13, 803–814.

    Google Scholar 

  • O’Donnell, P. J., Jones, J. B., Antoine, F. R., Ciardi, J. and Klee H. J. (2001) Ethylene-dependent salicylic acid regulates an expanded cell death response to a plant pathogen. Plant J. 25, 315–23.

    Google Scholar 

  • O’Donnell, P. J., Schmelz, E. A., Moussatche, P., Lund, S. T., Jones, J. B. and Klee, H. J. (2003) Susceptible to intolerance—a range of hormonal actions in a susceptible Arabidopsis pathogen response. Plant J. 33, 245–57

    Google Scholar 

  • Olson, M. R., Holley, C. L., Yoo, S. J., Huh, J. R., Hay, B. A., Kornbluth, S. (2003) Reaper is regulated by IAP-mediated ubiquitinylation. J. Biol. Chem. 278, 4028–4034

    CAS  PubMed  Google Scholar 

  • Orvar, B. L., McPherson, J., and Ellis, B. E. (1997) Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. Plant J 11, 203–212.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Orzaez, D., Blay, R., and Granell, A. (1999) Programme of senescence in petals and carpels of Pisum sativum L. flowers and its control by ethylene. Planta 208, 220–226.

    CAS  PubMed  Google Scholar 

  • Otsuki, Y., Li, Z. and Shibata, M. A. (2003) Apoptotic detection methods—from morphology to gene. Prog Histochem Cytochem. 38, 275–339.

    PubMed  Google Scholar 

  • Overmyer, K., Tuominen, H., Kettunen, R., Betz, C., Langebartels, C., Sandermann, H., and Kangasjarvi, J. (2000) Ozone-sensitive arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12, 1849–1862.

    Article  CAS  PubMed  Google Scholar 

  • Pan, J.-W., Zhu, M.-Y., and Chen, H. (2001) Aluminium-induced cell death in root-tip cells of barley. Envir. Exper. Bot. 46, 71–79.

    CAS  Google Scholar 

  • Peart, J. R., Lu, R., Sadanandom, A., Malcuit, I., Moffett, P., Brice, D. C., Schauser, L., Jaggard, D. A., Xiao, S., Coleman, M. J., Dow, M., Jones, J. D., Shirasu, K., and Baulcombe, D. C. (2002) Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. U. S. A. 99, 10865–10869.

    Article  CAS  PubMed  Google Scholar 

  • Peltier, J. B., Friso, G., Kalume, D. E., Roepstorff, P., Nilsson, F., Adamska, I., and Van Wijk, K. J. (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12, 319–341.

    Article  CAS  PubMed  Google Scholar 

  • Picton, S., Barton, S. L., Bouzayen, M., Hamilton, A. J., and Grierson, D. (1993) Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. Plant J 3, 469–481.

    CAS  Google Scholar 

  • Pilloff, R. K., Devadas, S. K., Enyedi, A., and Raina, R. (2002) The Arabidopsis gain-of-function mutant dll1 spontaneously develops lesions mimicking cell death associated with disease. Plant J. 30, 61–70.

    Article  CAS  PubMed  Google Scholar 

  • Prime, T. A., Sherrier, D. J., Mahon, P., Packman, L. C., and Dupree, P. (2001) A proteomic analysis of organelles from Arabidopsis thaliana. Electrophoresis 21, 3488–3499.

    Google Scholar 

  • Qiao, J., Mitsuhara, I., Yazaki, Y., Sakano, K., Gotoh, Y., Miura, M., and Ohashi, Y. (2002) Enhanced resistance to salt, cold and wound stresses by overproduction of animal cell death suppressors Bcl-xL and Ced-9 in tobacco cells — their possible contribution through improved function of organella. Plant Cell Physiol. 43, 992–1005.

    Article  CAS  PubMed  Google Scholar 

  • Quirino, B. F., Noh, Y.-S., Himelblau, E., and Amasino, R. M. (2000) Molecular aspects of leaf senescence. Tr. Plant Sci. 5, 278–282.

    CAS  Google Scholar 

  • Raff, M. C. (1992) Social controls on cell survival and cell death. Nature 356, 397–400

    Article  CAS  PubMed  Google Scholar 

  • Rao, M. V., and Davis, K. R. (2001) The physiology of ozone-induced cell death. Planta 213, 682–690.

    Article  CAS  PubMed  Google Scholar 

  • Rao, M. V., and Davis, K. R. (1999) Ozone-induced cell death occurs via two distinct mechanisms. The role of salicylic acid. Plant J 16, 603–614.

    Google Scholar 

  • Rao, M. V., Lee, H., Creelman, R. A., Mullet, J. E., and Davis, K. R. (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12, 1633–1646.

    Article  CAS  PubMed  Google Scholar 

  • Rao, M. V., Lee, H. I., and Davis, K. R. (2002) Ozone-induced ethylene production is dependent on salicylic acid, and both salicylic acid and ethylene act in concert to regulate ozone-induced cell death. Plant J 32, 447–456.

    Article  CAS  PubMed  Google Scholar 

  • Rathjen, J. P., Chang, J. H., Staskawicz, B. J., and Michelmore, R. W. (1999). Constitutively active Pto induces a Prf-dependent hypersensitive response in the absence of avrPto. EMBO J 18, 3232–3240.

    Article  CAS  PubMed  Google Scholar 

  • Raven, P. R., Evert, R. F., H. Curtis (1976) Biology of plants, second edition. Worth Publishers Inc. 391–497.

    Google Scholar 

  • Reed, J.R. 1997. Cytochrome c: Can’t live with it — can’t live without it. Cell 91, 559–562

    Article  CAS  PubMed  Google Scholar 

  • Ren, D., Yang, H., and Zhang, S. (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem. 277, 559–565.

    CAS  PubMed  Google Scholar 

  • Richael, C., Lincoln, J. E., Bostock, R. M., and Gilchrist, D. G. (2001) Caspase inhibitors reduce symptom development and limit bacterial proliferation in susceptible plant tissues. Physiol. Molec. Plant Pathol. 59, 213–221.

    CAS  Google Scholar 

  • Rubenstein, B. (2000) Regulation of cell death in flower petals. Plant Mol. Biol. 44, 303–318.

    Google Scholar 

  • Rines, H. W., and Luke, H. H. (1985) Selection and regeneration of toxin-sensitive plants from tissue cultures of oats (Avena sativa) susceptible to Helminthosporum victoriae. Theor. Appl. Genet. 71, 16–21.

    Article  Google Scholar 

  • Ritter, C., and Dangl, J. L. (1995) The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis. Mol. Plant Microbe Interact. 8, 444–453.

    CAS  PubMed  Google Scholar 

  • Rivas, S., Romeis, T., and Jones, J. D. (2002a) The Cf-9 disease resistance protein is present in an approximately 420-kilodalton heteromultimeric membrane-associated complex at one molecule per complex. Plant Cell 14, 689–702.

    Article  CAS  PubMed  Google Scholar 

  • Rivas, S., Mucyn, T., Van Den Burg, H. A., Vervoort, J., and Jones, J. D. (2002b) An approximately 400 kDa membrane-associated complex that contains one molecule of the resistance protein Cf-4. Plant J. 29, 783–796.

    Article  CAS  PubMed  Google Scholar 

  • Ronald, P. C., Salmeron, J. M., Carland, F. M., and Staskawicz, B. J. (1992). The cloned avirulence gene avrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. J. Bacteriol. 174, 1604–1611.

    CAS  PubMed  Google Scholar 

  • Roulston, A., Marcellus, R. C., and Branton, P. E. (1999). Viruses and apoptosis. Annu. Rev. Microbiol. 53, 577–628.

    Article  CAS  PubMed  Google Scholar 

  • Runeberg-Roos, P., and Saarma, M. (1998) Phytepsin, a barley vacuolar aspartic proteinase, is highly expressed during autolysis of developing tracheary elements and sieve cells. Plant J. 15, 139–145.

    Article  CAS  PubMed  Google Scholar 

  • Ryerson, D. E., and Heath, M. C. (1996). Cleavage of nuclear DNA into oligonucleosomal fragments during cell death induced by fungal infection or by abiotic treatments. Plant Cell 8, 393–402.

    Article  CAS  PubMed  Google Scholar 

  • Salchert, K., Bhalerao, R., Koncz-Kalman, Z., and Koncz, C. (1998). Control of cell elongation and stress responses by steroid hormones and carbon catabolic repression in plants. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353.

    Google Scholar 

  • Samuel, M. A., and Ellis, B. E. (2002) Double jeopardy: both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive. Plant Cell 14, 2059–2069.

    Article  CAS  PubMed  Google Scholar 

  • Samuilov, V. D., Lagunova, E. M., Dzyubinskaya, E. V., Izyumov, D. S., Kiselevsky, D. B., and Makarova, Y. V. (2002) Involvement of chloroplasts in the programmed death of plant cells. Biochemistry (Mosc.) 67, 627–634.

    CAS  Google Scholar 

  • Sanchez, P., de Torres Zabala, M., and Grant, M. (2000) AtBI-1, a plant homologue of Bax inhibitor-1, suppresses Bax-induced cell death in yeast and is rapidly upregulated during wounding and pathogen challenge. Plant J. 21, 393–399.

    Article  CAS  PubMed  Google Scholar 

  • Saviani, E. E., Orsi, C. H., Oliveira, J. F., Pinto-Maglio, C. A., and Salgado, I. (2002). Participation of the mitochondrial permeability transition pore in nitric oxide-induced plant cell death. FEBS Lett. 510, 136–140.

    Article  CAS  PubMed  Google Scholar 

  • Schmid, M., Simpson, D., and Gletl, C. (1999) Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes. Proc. Natl. Acad. Sci. U.S.A. 96, 14159–14164.

    Article  CAS  PubMed  Google Scholar 

  • Schraudner, M., Langebartles, C., and Sandermann, H. (1997). Changes in the biochemical status of plant cells induced by the environmental pollutant ozone. Physiol. Plant. 100, 274–280.

    Article  CAS  Google Scholar 

  • Shah, J., Kachroo, P., and Klessig, D. F. (1999) The arabidopsis ssi1 mutation restores pathogenesis-related gene expression in npr1 plants and renders defensin gene expression salicylic acid dependent. Plant Cell 11, 191–206.

    Article  CAS  PubMed  Google Scholar 

  • Shirasu, K., Lahaye, T., Tan, M.-W., Zhou, F., Azevedo, C., and Schulze-Lefert, P. (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell 99, 355–366.

    Article  CAS  PubMed  Google Scholar 

  • Simons, B. H., and Lambers, H. (1999). The alternative oxidase: is it a respiratory pathway allowing a plant to cope with stress? In: Plant responses to environmental stresses: from phytohormones to genome reorganization. H. R. Lerner, ed., Marcel Dekker Inc., New York. 265–286.

    Google Scholar 

  • Solomon, M., Belenghi, B., Delledonne, M., Menachem, D., and Levine, A. (1999) The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11, 431–443.

    Article  CAS  PubMed  Google Scholar 

  • Somerville, C., and Somerville, S. (1999). Plant functional genomics. Science 285, 380–383.

    Article  CAS  PubMed  Google Scholar 

  • Spassieva, S. D., Markham, J. E., and Hille, J. (2002) The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J. 32, 561–572.

    Article  CAS  PubMed  Google Scholar 

  • Staskawicz, B. J., Ausubel, F. M., Baker, B. J., Ellis, J. G., and Jones, J. D. (1995) Molecular genetics of plant disease resistance. Science 268, 661–667.

    CAS  PubMed  Google Scholar 

  • Stein, J. C., and Hansen, G. (1999) Mannose induces an endonuclease responsible for DNA laddering in plant cells. Plant Physiol. 121, 71–79.

    Article  CAS  PubMed  Google Scholar 

  • Stein, M., and Somerville, S. C. (2002) MLO, a novel modulator of plant defenses and cell death, binds calmodulin. Trends Plant Sci. 7, 379–380.

    Article  CAS  PubMed  Google Scholar 

  • Stone, J. M., Heard, J. E., Asai, T., and Ausubel, F. M. (2000). Simulation of fungal-mediated cell death by fumonisin B1 and selection of fumonisin B1-resistant (fbr) Arabidopsis mutants. Plant Cell 12, 1811–1822.

    Article  CAS  PubMed  Google Scholar 

  • Strasser, A., O’Conner, L. and Dixit, V.M. (2000) Apoptosis signaling. Ann. Rev. Biochem. 69, 217–245

    CAS  PubMed  Google Scholar 

  • Subbaiah, C., Kollipara, K. P., and Sachs, M. M. (1999) A Ca2+-dependent cysteine protease is associated with anoxia-induced root tip death in maize. J. Exp. Bot. 51, 721–731.

    Google Scholar 

  • Swidzinski, J. A., Sweetlove, L. J., and Leaver, C. J. (2002) A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J. 30, 431–446.

    Article  CAS  PubMed  Google Scholar 

  • Tameling, W. I., Elzinga, S. D., Darmin, P. S., Vossen, J. H., Takken, F. L., Haring, M. A., and Cornelissen, B. J. (2002) The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14, 2929–2939.

    Article  CAS  PubMed  Google Scholar 

  • Tian, R.-H., Zhang, G.-Y., Yan, C.-H., and Dai, Y.-R. (2000) Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells. FEBS Lett. 474, 1–15.

    Article  Google Scholar 

  • Tor, M., Gordon, P., Cuzick, A., Eulgem, T., Sinapidou, E., Mert-Turk, F., Can, C., Dangl, J. L., and Holub, E. B. (2002) Arabidopsis SGT1b is required for defense signaling conferred by several powdery mildew resistance genes. Plant Cell 14, 993–1003.

    Article  CAS  PubMed  Google Scholar 

  • Tornero, P., Merritt, P., Sadanandom, A., Shirasu, K., Innes, R. W., and Dangl, J. L. (2002) RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis and their relative contributions are dependent on the R gene assayed. Plant Cell 14, 105–1015.

    Google Scholar 

  • Townsend, P. A., Cutress, R. I., Sharp, A., Brimmell, M., and Packham, G. (2003). BAG-1: a multifunctional regulator of cell growth and survival. Biochim. Biophys. Acta. 1603, 83–98.

    CAS  PubMed  Google Scholar 

  • Trotochaud, A. E., Hao, T., Wu, G., Yang, Z., and Clark, S. E. (1999) The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11, 393–406.

    Article  CAS  PubMed  Google Scholar 

  • Turner, J. G., Ellis, C., and Devoto, A. (2002) The jasmonate signal pathway. Plant Cell 14, S153–S164.

    CAS  PubMed  Google Scholar 

  • Ueda, J., and Kato, J. (1980). Isolation and identification of a senescence-promoting substance from wormwood (Artemisia absintuim L.). Plant Physiol. 66, 246–249.

    CAS  Google Scholar 

  • Van der Biezen, E. A., and Jones, J. D. (1998). The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8, R226–R227.

    PubMed  Google Scholar 

  • Van Loo, G., Saelens, X., Van Gurp, M., MacFarlane, M., Martin, S. J. and Vandenabeele, P. (2002) The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 9, 1031–1042

    PubMed  Google Scholar 

  • Van Wees, S. C. M., Luijendijk, M., Smoorenburg, I., Van Loon, L. C. and Pieterse, C. M. J. (1999). Rhizobacteria-mediated induced systemic resistance (ISR) in Arabidopsis is not associated with a direct effect on expression of known defense-related genes but stimulates the expression of the jasmonate-inducible gene Atvsp upon challenge. Plant Mol. Biol. 41, 537–549.

    PubMed  Google Scholar 

  • Van Wees, S. C., and Glazebrook, J. (2003) Loss of non-host resistance of Arabidopsis NahG to Pseudomonas syringae pv. phaseolicola is due to degradation products of salicylic acid. Plant J. 33, 733–742.

    PubMed  Google Scholar 

  • Vercammen, D., Van de Cotte, B., Vandepoele, K., Declercq, W., Dejaeger, G., Edkhout, D., Inze, D., and Van Breusegem, F. (2003) Cloning and characterisation of the family of Arabidopsis thaliana metacaspases. In Plant biology: functions and control of cell death. J. Dangl, P. Schulze-Lefert and J. Glazebrook, eds., Keystone Symposia, Snowbird, Utah, 60.

    Google Scholar 

  • Vernooij, B., Uknes, S., Ward, E., and Ryals, J. (1994) Salicylic acid as a signal molecule in plant-pathogen interactions. Curr. Opin. Cell Biol. 6, 275–279.

    Article  CAS  PubMed  Google Scholar 

  • Wan, L., Xia, Q., Qiu, X., and Sevaraj, G. (2002) Early stages of seed development in Brassica napus: a seed coat-specific cysteine proteinase associated with programmed cell death of the inner integument. Plant J. 30, 1–10.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wang, H., Jones, C., Ciacci-Zanella, J., Holt, T., Gilchrist, D. G., Dickman, M. B. (1996b) Fumonisins and Alternaria alternata lycopersici toxins: sphinganine analog mycotoxins induce apoptosis in monkey kidney cells. Proc. Natl. Acad. Sci. U. S. A. 93, 3461–3465.

    CAS  PubMed  Google Scholar 

  • Wang, M., Oppedijk, B. J., Lu, X., Van Duijn, B., and Schilperoort, R. A. (1996c). Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol. Biol. 32, 1125–1134.

    Article  CAS  PubMed  Google Scholar 

  • Wang, M., Hoekstra, S., Van Bergen, S., Lamers, G. E., Oppendijk, B. J., Van der Heijden, M. W., De Priester, W. and Schilperoort, R. A. (1999) Apoptosis in developing anthers and the role of ABA in this process during androgenesis in Hordeum vulgare L. Plant Mol. Biol., 39, 489–501.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Yang, C., Chai, J., Shi, Y., and Xue, D. (2002). Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science 298, 1587–1592.

    CAS  PubMed  Google Scholar 

  • Woffenden, B. J., Freeman, T. B., and Beers, E. P. (1998) Proteasome inhibitors prevent tracheary element differentiation in Zinnia mesophyll cell cultures. Plant Physiol. 118, 419–430.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wolpert, T. J., and Macko, V. (1989) Specific binding of victorin to a 100-kD protein from oats. Proc. Natl. Acad. Sci. U. S. A. 86, 4092–4096.

    CAS  Google Scholar 

  • Wolpert, T. J., Macko, V., Acklin, W., Jaun, B., Seibl, J., Meili, J., and Arigoni, D. (1994) Identification of the 100-kD victorin-binding protein from oats. Plant Cell 6, 1145–1155.

    Article  CAS  PubMed  Google Scholar 

  • Wolpert, T. J., Dunkle, L. D., and Ciuffetti, L. M. (2002). Host-selective toxins and avirulence determinants: what’s in a name. Annu. Rev. Phytopathol. 40, 251–285.

    Article  CAS  PubMed  Google Scholar 

  • Woo, H. R., Chung, K. M., Park, J. H., Oh, S. A., Ahn, T., Hong, S. H., Jang, S. K., and Nam, H. G. (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13, 1779–1790.

    CAS  PubMed  Google Scholar 

  • Wu, H.-M., and Cheung, A. Y. (2000) Programmed cell death in plant reproduction. Plant Mol. Biol. 44, 267–281.

    PubMed  Google Scholar 

  • Xu, H., and Heath, M. C. (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell 10, 585–598.

    CAS  PubMed  Google Scholar 

  • Xu, Q., and Reed, J. C. (1998) Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol. Cell 1, 337–346.

    CAS  PubMed  Google Scholar 

  • Xu, F.-X., and Chye, M.-L. (1999) Expression of cysteine proteinase during developmental events associated with programmed cell death in brinjal. Plant J. 17, 321–327.

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto, R., Demura, T., and Fukuda, H. (1997) Brassinosteroids induce entry into the final stage of tracheary element differentiation in cultured Zinnia cells. Plant Cell Physiol. 38, 980–983.

    CAS  PubMed  Google Scholar 

  • Ye, Z.-H., and Varner, J. E. (1996). Induction of cysteine and serine proteases during xylogenesis in Zinnia elegans. Plant Mol. Biol. 30, 1233–1246.

    CAS  PubMed  Google Scholar 

  • Young, T. E., Gallie, D. R., and DeMason, D. A. (1997) Ethylene-mediated programmed cell death during maize endosperm development of Su and sh2 genotypes. Plant Physiol. 115, 737–751.

    CAS  PubMed  Google Scholar 

  • Young, T. E., and Gallie, D. R. (1999) Analysis of programmed cell death in wheat endosperm reveals differenes in endosperm development between cereals. Plant Mol. Biol. 39, 915–926.

    Article  CAS  PubMed  Google Scholar 

  • Yu, I. C., Parker, J. and Bent, A. F. (1998) Gene-for-gene resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc. Natl. Acad. Sci. U. S. A. 95, 7819–7824.

    CAS  PubMed  Google Scholar 

  • Yu, L.-H., Kawai-Yamada, M., Naito, M., Watanabe, K., Reed, J. C., and Uchimiya, H. (2002) Induction of mammalian cell death by a plant Bax inhibitor. FEBS Lett. 512, 308–312.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, S., and Klessig, D. F. (2001) MAPK cascades in plant defense signaling. Trends Plant Sci. 6, 520–527.

    Article  CAS  PubMed  Google Scholar 

  • Zhivotovsky, B., Orrenius, S., Brustugun, O. T., and Doskeland, S. O. (1998). Injected cytochrome C induces apoptosis. Nature 391, 449–450.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, Q., Snipas, S., Orth, K., Muzio, M., Dixit, V. M., and Salvesen, G. S. (1997). Target protease specificity of the viral serpin CrmA. Analysis of five caspases. J. Biol. Chem. 272, 7797–7800.

    CAS  PubMed  Google Scholar 

  • Zimmermann, K. C., Ricci, J. E., Droin, N. M., and Green, D. R. (2002). The role of ARK in stress-induced apoptosis in Drosophila cells. J. Cell. Biol. 156, 1077–1087

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Plant Pathology, University of Nebraska-Lincoln, 406G Plant Sciences, Lincoln, NE, 68583-0722, USA

    S. Panter & M. Dickman

Authors
  1. S. Panter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Dickman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Dickman .

Editor information

Editors and Affiliations

  1. School of Chemical Engineering, The University of Birmingham, Edgbaston, Birmingham, UK

    Mohamed Al-Rubeai

  2. Swiss Federal Institute of Technology, Zurich, Switzerland

    Martin Fussenegger

Rights and permissions

Reprints and permissions

Copyright information

© 2004 Kluwer Academic Publishers

About this chapter

Cite this chapter

Panter, S., Dickman, M. (2004). Programmed Cell Death in Plants During Development and Stress Responses. In: Al-Rubeai, M., Fussenegger, M. (eds) Cell Engineering. Cell Engineering, vol 4. Springer, Dordrecht. https://doi.org/10.1007/1-4020-2217-4_5

Download citation

Publish with us

Policies and ethics

Search

Navigation