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  • Review Article
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Controlled cell death, plant survival and development

Nature Reviews Molecular Cell Biology volume 5, pages 305–315 (2004)Cite this article

Key Points

  • Controlled cellular suicide in plants is important for the sculpting of organ shapes and the differentiation of specific cell types with diverse functions, as well as the removal of damaged or infected cells. These various types of programmed cell death (PCD) can have diverse morphotypes that are defined by their sequence of cytological changes, as well as the expression of various biochemical and molecular markers.

  • With the presence of a cell wall, the content of the dying cell inevitably leaks into the extracellular milieu and is then presumably recycled during the late stages of cell death in plants. This is a key differentiating feature compared with animal apoptosis where engulfment of the contents of the dead cell by neighbouring cells or macrophages prevents the activation of the inflammatory response.

  • Various phytohormones are known to function as signal molecules for cell-death pathways that are activated during pathogen defence or at a particular stage of plant development. However, their action could be dependent on the cellular context and environmental conditions.

  • Reactive oxygen species (ROS) and the mitochondrion are common mediators of PCD in plants and animals, whereas plastids provide an additional source of cell-death signalling that is specific for plant cells. Precise mechanisms and pathways through which ROS and organelle-derived signals regulate PCD in plants remain to be elucidated.

  • In spite of the lack of apparent orthologues for core regulators of cell death in animals, plants seem to use some similar molecules to serve analogous functions. These include caspase-like activities detected in different plant-cell-death model systems, the demonstration that expression of animal BAX can induce PCD in plants and fungi, and the identification of a conserved protein, BAX inhibitor-1 (BI-1), that can suppress cell death in both plants and animals.

  • The prominent vacuole and its associated process of autophagy could have important roles in plant PCD, as has been found for the animal lysosome in developmental cell death. In the future, genetic and molecular approaches with model plants such as Arabidopsis thaliana should help to delineate the possible overlaps in the autophagic and cell-death pathways in plant cells.

Abstract

For plants to develop properly and survive, programmed cell death is an important response strategy to various internal and external cues. Morphologically, a key difference between programmed cell death of plant cells and apoptosis in animals is the absence of engulfment by neighbouring cells in plants. Recent genetic, molecular and biochemical approaches have begun to reveal interesting candidate regulators in plants that show both similar and new properties compared with their animal counterparts.

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Figure 1: Examples of programmed cell death in plants.
Figure 2: Morphological comparison between programmed cell death in plants and animal apoptosis.

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References

  1. Wyllie, A. H., Kerr, J. F. & Currie, A. R. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68, 251–306 (1980).

    Article  CAS  PubMed  Google Scholar 

  2. Jacobson, M. D., Weil, M. & Raff, M. C. Programmed cell death in animal development. Cell 88, 347–354 (1997).

    Article  CAS  PubMed  Google Scholar 

  3. Pennell, R. I. & Lamb, C. Programmed cell death in plants. Plant Cell 9, 1157–1168 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Beers, E. P. & McDowell, J. M. Regulation and execution of programmed cell death in response to pathogens, stress and developmental cues. Curr. Opin. Plant Biol. 4, 561–567 (2001).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  7. Ameisen, J. C. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ. 9, 367–393 (2002).

    Article  CAS  PubMed  Google Scholar 

  8. Ito, J. & Fukuda, H. ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell 14, 3201–3211 (2002). This work shows the involvement of the Zinnia elegans nuclease ZEN1 in the nuclear DNA fragmentation process during developmental cell death that occurs during the formation of tracheary elements.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Balk, J., Chew, S. K., Leaver, C. J. & McCabe, P. F. The intermembrane space of plant mitochondria contains a DNase activity that may be involved in programmed cell death. Plant J. 34, 573–583 (2003).

    Article  CAS  PubMed  Google Scholar 

  10. Groover, A., DeWitt, N., Heidel, A. & Jones, A. M. Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma 196, 197–211 (1997).

    Article  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Jones, A. M. Programmed cell death in development and defense. Plant Physiol. 125, 94–97 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Filonova, L. H. et al. Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce. J. Cell Sci. 113, 4399–4411 (2000).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  15. Filonova, L. H., Bozhkov, P. V. & Von Arnold, S. Developmental pathway of somatic embryogenesis in Picea abies as revealed by time-lapse tracking. J. Exp. Bot. 51, 249–264 (2000).

    Article  CAS  PubMed  Google Scholar 

  16. Smertenko, A. P., Bozhkov, P. V., Filonova, L. H. & Hussey, P. J. Re-organisation of the cytoskeleton during developmental programmed cell death in Picea abies embryos. Plant J. 33, 813–824 (2003).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  19. Levine, A., Pennell, R. I., Alvarez, M. E., Palmer, R. & Lamb, C. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6, 427–437 (1996).

    Article  CAS  PubMed  Google Scholar 

  20. Skalamera, D. & Heath, M. C. Changes in the cytoskeleton accompanying infection-induced nuclear movements and the hypersensitive response in plant cells invaded by rust fungi. Plant J. 16, 191–200 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. Takemoto, D., Jones, D. A. & Hardham, A. R. GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J. 33, 775–792 (2003).

    Article  CAS  PubMed  Google Scholar 

  22. Kato, N., Pontier, D. & Lam, E. Spectral profiling for the simultaneous observation of four distinct fluorescent proteins and detection of protein-protein interaction via fluorescence resonance energy transfer in tobacco leaf nuclei. Plant Physiol. 129, 931–942 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Hoisington, D. et al. Disease lesion mimics in maize. Dev. Biol. 93, 381–388 (1982).

    Article  CAS  PubMed  Google Scholar 

  26. Lorrain, S., Vailleau, F., Balague, C. & Roby, D. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci. 8, 263–271 (2003).

    Article  CAS  PubMed  Google Scholar 

  27. Mittler, R. & Lam, E. Sacrifice in the face of foes: pathogen-induce programmed cell death in plants. Trends Microbiol. 4, 10–15 (1996).

    Article  CAS  PubMed  Google Scholar 

  28. Alvarez, M. E. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol. Biol. 44, 429–442 (2000).

    Article  CAS  PubMed  Google Scholar 

  29. Rate, D. N. & Greenberg, J. T. The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. Plant J. 27, 203–211 (2001).

    Article  CAS  PubMed  Google Scholar 

  30. Rate, D. N. et al. The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell 11, 1695–1708 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Leon, J., Lawton, M. A. & Raskin, I. Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 108, 1673–1678 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Clarke, A., Desikan, R., Hurst, R. D., Hancock, J. T. & Neil, S. J. NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J. 24, 667–677 (2000).

    Article  CAS  PubMed  Google Scholar 

  34. Delledonne, M., Zeier, J., Marocco, A. & Lamb, C. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc. Natl Acad. Sci. USA 98, 13454–13459 (2001). This paper postulates that the balance between NO and ROS concentrations is a critical factor that regulates cell-death initiation in plant cells.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Chandok, M. R., Ytterberg, J. A., van Wijk, K. J. & Klessig, D. F. 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 (2003).

    Article  CAS  PubMed  Google Scholar 

  36. Guo, F.-Q., Okamoto, M. & Crawford, N. M. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100–103 (2003).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  38. Asai, T. et al. Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 12, 1823–1836 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Orzaez, D & Granell, A. DNA fragmentation is regulated by ethylene during carpel senescence in Pisum sativum. Plant J. 11, 137–144 (1997).

    Article  CAS  Google Scholar 

  40. Drew, M. C., He, C. J. & Morgan, P. W. in Programmed Cell Death in Animals and Plants. (eds Bryant, J. A., Hughes, S. G., Garland, J. M.) 183–192 (BIOS Scientific Publishers Ltd, Oxford, 2000).

    Google Scholar 

  41. Young, T. E. & Gallie, D. R. Regulation of programmed cell death in maize endosperm by abscisic acid. Plant Mol. Biol. 42, 397–414 (2000).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Yamamoto, R. et al. Brassinosteroid levels increase drastically prior to morphogenesis of tracheary elements. Plant Physiol. 125, 556–563 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Fath, A., Bethke, P., Beligni, V. & Jones, R. Active oxygen and cell death in cereal aleurone cells. J. Exp. Bot. 53, 1273–1282 (2002).

    Article  CAS  PubMed  Google Scholar 

  45. Wang, M. et al. Apoptosis in developing anthers and the role of ABA in this process during androgenesis in Hordeum vulgare L. Plant Mol. Biol. 39, 489–501 (1999).

    Article  CAS  PubMed  Google Scholar 

  46. Mittler, R., Shulaev, V. & Lam, E. Coordinated activation of programmed cell death and defense mechanisms in transgenic tobacco plants expressing a bacterial proton pump. Plant Cell 7, 29–42 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Pontier, D., Mittler, R. & Lam, E. Mechanism of cell death and disease resistance induction by transgenic expression of bacterio-opsin. Plant J. 30, 499–509 (2002).

    Article  CAS  PubMed  Google Scholar 

  48. Wendehenne, D., Lamotte, O., Frachisse, J.-M., Barbier-Brygoo, H. & Pugin, A. Nitrate efflux is an essential component of the cryptogein signaling pathway leading to defense responses and hypersensitive cell death in tobacco. Plant Cell 14, 1937–1951 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Clough, S. J. et al. The Arabidopsis dnd1 'defense, no death' gene encodes a mutated cyclic nucleotide-gated ion channel. Proc. Natl Acad. Sci. USA 97, 9323–9328 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Balague, C. et al. HLM1, an essential signaling component in the hypersensitive response, is a member of the CNGC ion channel family. Plant Cell 12, 365–379 (2003).

    Article  CAS  Google Scholar 

  51. Jirage, D. et al. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc. Natl Acad. Sci. USA 96, 13583–13588 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Falk, A. et al. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl Acad. Sci. USA 96, 3292–3297 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Meijer, H. J. G. & Munnik, T. Phospholipid-based signaling in plants. Annu. Rev. Plant Biol. 54, 265–306 (2003).

    Article  CAS  PubMed  Google Scholar 

  54. Zhang, W. et al. The oleate-stimulated phospholipase D, PLDδ, and phosphatidic decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15, 2285–2295 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Wang, C. & Wang, X. A novel phospholipase D of Arabidopsis that is activated by oleic acid and associated with the plasma membrane. Plant Physiol. 127, 1102–1112 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Kachroo, A. et al. Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 15, 2952–2965 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Nandi, A. et al. Arabidopsis sfd mutants affect plastidic lipid composition and suppress dwarfing, cell death, and the enhanced disease resistance phenotypes resulting from the deficiency of a fatty acid desaturase. Plant Cell 15, 2383–2398 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Brodersen, P. et al. Knockout of Arabidopsis ACCELERATED-CELL-DEATH11 encoding a sphingosine transfer protein causes activation of programmed cell death and defense. Genes Dev. 16, 490–502 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Baker, C. J. & Orlandi, E. W. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33, 299–322 (1995).

    Article  CAS  PubMed  Google Scholar 

  60. Kachroo, A. et al. Induction of H2O2 in transgenic rice leads to cell death and enhanced resistance to both bacterial and fungal pathogens. Transgenic Res. 12, 577–586 (2003).

    Article  CAS  PubMed  Google Scholar 

  61. Dat, J. F. et al. Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J. 33, 621–632 (2003).

    Article  CAS  PubMed  Google Scholar 

  62. Yoda, H., Yamaguchi, Y. & Sano, H. Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol. 132, 1973–1981 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Irani, K. & Goldschmidt-Clermont, P. J. Ras, superoxide and signal transduction. Biochem. Pharmacol. 55, 1339–1346 (1998).

    Article  CAS  PubMed  Google Scholar 

  64. Torres, M. A., Dangl, J. L. & Jones, J. D. G. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl Acad. Sci. USA 99, 517–522 (2002). The isolation and characterization of A. thaliana mutants described here showed the requirement of the generation of reactive oxygen intermediates by a membrane-bound NADPH oxidase and the activation of cell death during HR.

    Article  CAS  PubMed  Google Scholar 

  65. Ono, E. et al. Essential role of the small GTPase Rac in disease resistance of rice. Proc. Natl Acad. Sci. USA 98, 759–764 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Schultheiss, H., Dechert, C., Kogel, K.-H. & Huckelhoven, R. A small GTP-binding host protein is required for entry of powdery mildew fungus into epidermal cells of barley. Plant Physiol. 128, 1447–1454 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  68. Susin, S. A. et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441–446 (1999).

    Article  CAS  PubMed  Google Scholar 

  69. Li, L. Y., Luo, X. & Wang, X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412, 95–99 (2001).

    Article  CAS  PubMed  Google Scholar 

  70. Yu, X.-H., Perdue, T. D., Heimer, Y. M. & Jones, A. M. Mitochondrial involvement in tracheary element programmed cell death. Cell Death Differ. 9, 189–198 (2002).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  72. Tiwari, B. S., Belenghi, B. & Levine, A. Oxidative stress increased respiration of reactive oxygen species, resulting in ATP depletion, opening of mitochondrial permeability transition, and programmed cell death. Plant Physiol. 128, 1271–1281 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Takahashi, A. et al. Hyperphosphorylation of a mitochondrial protein, prohibitin, is induced by calyculin A in a rice lesion-mimic mutant cdr1. Plant Physiol. 132, 1861–1869 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Hu, G., Yalpani, N., Briggs, S. P. & Johal, G. S. A porphyrin pathway impairment is responsible for the phenotype of a dominant disease lesion mimic mutant of maize. Plant Cell 10, 1095–1105 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Seo, S. et al. Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive response. Plant Cell 12, 917–932 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  77. Aviv, D. H. et al. Runaway cell death, but not basal disease resistance, in lsd1 is SA- and NIM1/NPR1-dependent. Plant J. 29, 381–391 (2002).

    Article  CAS  PubMed  Google Scholar 

  78. Epple, P., Mack, A. A., Morris, V. R. F. & Dangl, J. L. Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related, plant-specific zinc finger proteins. Proc. Natl Acad. Sci. USA 100, 6831–6836 (2003). Two related zinc-finger proteins, LSD1 and LOL1, are shown to have opposing roles in plant-cell-death signalling.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Piffanelli, P. et al. The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol. 129, 1076–1085 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kim, M. C. et al. Mlo, a modulator of plant defense and cell death, is a novel calmodulin-binding protein. J. Biol. Chem. 277, 19304–19314 (2002).

    Article  CAS  PubMed  Google Scholar 

  81. Kim, M. C. et al. Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 416, 447–450 (2002).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Solomon, M., Belenghi, B., Delledonne, M., Menachem, E. & Levine, A. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell 11, 431–444 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Lam, E. & del Pozo, O. Caspase-like proteases involvement in the control of plant cell death. Plant Mol. Biol. 44, 417–428 (2000). A comprehensive review on the evidence and characterization of caspase-like protease activities in higher plants.

    Article  CAS  PubMed  Google Scholar 

  86. Clem, R. J., Hardwick, J. M. & Miller, L. K. Anti-apoptotic genes of baculoviruses. Cell Death Differ. 3, 9–16 (1996).

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. del Pozo, O. & Lam, E. 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 (2003).

    Article  CAS  PubMed  Google Scholar 

  89. Danon, A., Rotari, V., Gordon, A., Mailhac, N. & Gallois, P. UV-C overexposure induces a programmed cell death in Arabidopsis, which is mediated by caspase-like activities and can be suppressed by caspase inhibitors, p35 and Defender against Apoptotic Death. J. Biol. Chem. 279, 779–787 (2004).

    Article  CAS  PubMed  Google Scholar 

  90. Lincoln, J. E. et al. Expression of the antiapoptotic baculovirus p35 gene in tomato blocks programmed cell death and provides broad-spectrum resistance to disease. Proc. Natl Acad. Sci. USA 99, 15217–15221 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Uren, A. G. et al. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 6, 961–967 (2000).

    CAS  PubMed  Google Scholar 

  92. Madeo, F. et al. A caspase-related protease regulates apoptosis in yeast. Mol. Cell 9, 911–917 (2002). This paper shows the involvement of the yeast metacaspase Yca1 in oxidative stress and ageing-related cell death by a combination of genetic and molecular approaches.

    Article  CAS  PubMed  Google Scholar 

  93. Szallies, A., Kubata, B. K. & Duszenko, M. A metacaspase of Trypanosoma brucei causes loss of respiration competence and clonal death in the yeast Saccharomyces cerevisiae. FEBS Lett. 517, 144–150 (2002).

    Article  CAS  PubMed  Google Scholar 

  94. Hoeberichts, F. A., ten Have, A. & Woltering, E. J. A tomato metacaspase gene is upregulated during programmed cell death in Botrytis cinerea-infected leaves. Planta 217, 517–522 (2003).

    Article  CAS  PubMed  Google Scholar 

  95. Baehrecke, E. H. How death shapes life during development. Nature Rev. Mol. Cell Biol. 3, 779–787 (2002).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  97. Pan, L. et al. The Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP) can function as a dominant suppressor of Bax-induced cell death of yeast. FEBS Lett. 508, 375–378 (2001).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  99. Kawai-Yamada, M., Jin, L., Yoshinaga, K., Hirata, A. & Uchimiya, H. Mammalian Bax-induced plant cell death can be down-regulated by overexpression of Arabidopsis Bax Inhibitor-1 (AtBI-1). Proc. Natl Acad. Sci. USA 98, 12295–12300 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Bolduc, N., Ouellet, M., Pitre, F. & Brisson, L. F. Molecular characterization of two plant BI-1 homologues which suppress Bax-induced apoptosis in human 293 cells. Planta 216, 377–386 (2003).

    Article  CAS  PubMed  Google Scholar 

  101. Bolduc, N. & Brisson, L. F. Antisense down regulation of NtBI-1 in tobacco BY-2 cells induces accelerated cell death upon carbon starvation. FEBS Lett. 532, 111–114 (2002). This work presents the first evidence that a plant BI-1 homologue is involved in regulating cell-death induction by an intrinsic plant response to nutrient limitation.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Matsumura, H. et al. Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L.) cells. Plant J. 33, 425–434 (2003).

    Article  CAS  PubMed  Google Scholar 

  104. Yu, L.-H. et al. Induction of mammalian cell death by a plant Bax inhibitor. FEBS Lett. 512, 308–312 (2002).

    Article  CAS  PubMed  Google Scholar 

  105. Lee, C.-Y. & Baehrecke, E. H. Steroid regulation of autophagic programmed cell death during development. Development 128, 1443–1455 (2001).

    Article  CAS  PubMed  Google Scholar 

  106. Liang, X. H. et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672–676 (1999).

    Article  CAS  PubMed  Google Scholar 

  107. Hanaoka, H. et al. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 129, 1181–1193 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Doelling, J. H., Walker, J. M., Friedman, E. M., Thompson, A. R. & Vierstra, R. D. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 277, 33105–33114 (2002).

    Article  CAS  PubMed  Google Scholar 

  109. Rojo, E., Gillmor, S. C., Kovaleva, V., Somerville, C. R. & Raikhel, N. V. VACUOLELESS1 is an essential gene required for vacuole formation and morphogenesis in Arabidopsis. Dev. Cell 1, 303–310 (2001).

    Article  CAS  PubMed  Google Scholar 

  110. Chautan, M. et al. Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr. Biol. 9, 967–970 (1999). This study provides an elegant illustration of the alternative cell-death pathways that might co-exist to control a developmental cell-death programme.

    Article  CAS  PubMed  Google Scholar 

  111. Wang, R., Zhou, X. & Wang, X. Chemically regulated expression systems and their applications in transgenic plants. Transgenic Res. 12, 529–540 (2003).

    Article  CAS  PubMed  Google Scholar 

  112. Innes, R. New effects of type III effectors. Mol. Microbiol. 50, 363–365 (2003).

    Article  CAS  PubMed  Google Scholar 

  113. Espinosa, A., Guo, M., Tam, V. C., Fu, Z. Q. & Alfano, J. R. The Pseudomonas syringae type III-secreted protein HopPtoD2 possesses protein tyrosine phosphatase activity and suppresses programmed cell death in plants. Mol. Microbiol. 49, 377–387 (2003).

    Article  CAS  PubMed  Google Scholar 

  114. Abramovitch, R. B., Kim, Y.-J., Chen, S., Dickman, M. B. & Martin, G. B. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 22, 60–69 (2003). This detailed study of a type-III effector clearly shows the ability of plant pathogens to take control of cell-death control in the host and show its importance in pathogenicity.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Kuriyama, H. & Fukuda, H. Developmental programmed cell death in plants. Curr. Opin. Plant Biol. 5, 568–573 (2002).

    Article  CAS  PubMed  Google Scholar 

  116. Kinoshita, T. et al. Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions. Plant J. 19, 43–53 (1999).

    Article  CAS  PubMed  Google Scholar 

  117. Hiraiwa, N., Nishimura, M. & Hara-Nishimura, I. Vacuolar processing enzyme is self-catalytically activated by sequential removal of the C-terminal and N-terminal propeptides. FEBS Lett. 447, 213–216 (1999).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Support by the United States Department of Agriculture on work related to plant cell death in my laboratory is gratefully acknowledged. I would also like to thank the New Jersey Commission on Science and Technology and the University of Hong Kong for partial support.

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Authors and Affiliations

  1. Biotechnology Center and the Department of Plant Science, Rutgers, The State University of New Jersey, New Brunswick, 08901, New Jersey, USA

    Eric Lam

  2. Department of Botany, The University of Hong Kong, Pokfulam Road, Pok Fu Lam, Hong Kong Special Administrative Region of the People's, Republic of China

    Eric Lam

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DATABASES

Saccharomyces genome database

Yca1

Apg6

Swiss-Prot

GP91 phox

TAIR

acd2

acd5

acd6

agd2

BI-1

cpr1

cpr6

DND1

eds1

hlm1

lin2

LOL1

LOL2

lsd1

pad4

ssi2

Glossary

HYPERSENSITIVE RESPONSE

A rapid plant programmed cell death that is orchestrated in and surrounding the initial site of plant pathogen entry that is typically associated with the activation of disease resistance.

TRACHEARY ELEMENTS

Specialized cells in the xylem of vascular plants that are responsible for the conductance of fluids as well as providing mechanical support.

XYLEM

A tissue that comprises a large collection of specialized cells that are involved in the transport of water and solutes in vascular plants. Mature xylem vessels contain essentially only the cell wall.

MESOPHYLL

The photosynthetic tissue of a leaf that is internal to the epidermis, and contains both palisade and spongy cell types.

AERENCHYMA

Cortical cells that have undergone programmed cell death in the roots of grasses under low-oxygen conditions.

BLEBBING

Invagination of the membrane.

GYMNOSPERM

Non-flowering plants represented by pine and spruce.

LESION MIMICS

Also known as 'disease lesion mimics', this describes a class of phenotypes in which spontaneous cell death occurs as discrete 'zones' or 'lesions' that resemble the cell death that is observed during the hypersensitive response.

SYSTEMIC ACQUIRED RESISTANCE

(SAR). General, long-lasting plant defence that is activated at a distance from the initial site of attempted invasion by an avirulent pathogen of a host plant.

ENDOSPERM

Storage tissue surrounding the embryo in the seeds of flowering plants to provide nutrients for the developing seed as well as the germinating seedling.

ALEURONE

Specialized cell layer surrounding the starchy endosperm of cereal seeds that is responsible for the secretion of hydrolytic enzymes to degrade the endosperm upon seed germination.

ELICITOR

Pathogen-derived molecules, such as fungal-cell-wall fragments and secreted proteins, that can trigger defence responses of plant cells that resemble the hypersensitive response.

CYCLIC-NUCLEOTIDE-GATED CHANNEL

(CNGC). Conserved protein family with six predicted transmembrane helices that can form cation-conducting channels and is activated by the binding of lipophilic cyclic nucleotides such as cAMP and cGMP.

CASPASES

A family of cysteine proteases with specific target-site sequences that contain an aspartate residue at the P1 position. In addition to activating programmed cell death (PCD), caspases also function in non-PCD-related roles such as the processing of cytokines.

CALMODULIN

A Ca2+ protein that is found in all eukaryotes, calmodulin has a high degree of structural conservation and can bind to target enzymes and modulate their activity as a function of the cytosolic Ca2+ concentration.

PARACASPASES

A class of cysteine protease that is found in animals and slime mould and was identified as being structurally related to caspases by iterative sequence comparison.

METACASPASES

Predicted cysteine proteases that are found in plants, fungi and protozoa and which contain homologous sequences and domains that are structurally related to metazoan caspases.

AUTOPHAGY

A pathway for the recycling of cellular contents, in which materials inside the cell are packaged into vesicles and are then targeted to the vacuole or lysosome for bulk turnover.

AUTOPHAGOSOME

A double-membraned structure containing content for turnover that fuses with the vacuole, or the animal lysosome, during autophagy.

BIOTROPHIC

A lifestyle of pathogens that is dependent on a living host.

TYPE-III EFFECTORS

Proteins that are injected by gram-negative bacterial pathogens into their host cells via a conserved type-III secretory system.

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Lam, E. Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5, 305–315 (2004). https://doi.org/10.1038/nrm1358

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