Controlled cell death, plant survival and development (original) (raw)

• 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
• Jacobson, M. D., Weil, M. & Raff, M. C. Programmed cell death in animal development. Cell 88, 347–354 (1997).
  Article CAS PubMed Google Scholar
• Pennell, R. I. & Lamb, C. Programmed cell death in plants. Plant Cell 9, 1157–1168 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Jones, A. M. Programmed cell death in development and defense. Plant Physiol. 125, 94–97 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Raff, M. C. Social controls on cell survival and cell death. Nature 356, 397–400 (1992).
  Article CAS PubMed Google Scholar
• 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
• Hoisington, D. et al. Disease lesion mimics in maize. Dev. Biol. 93, 381–388 (1982).
  Article CAS PubMed Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Rao, M. V. & Davis, K. R. The physiology of ozone induced cell death. Planta 213, 682–690 (2001).
  Article CAS PubMed Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Meijer, H. J. G. & Munnik, T. Phospholipid-based signaling in plants. Annu. Rev. Plant Biol. 54, 265–306 (2003).
  Article CAS PubMed Google Scholar
• 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
• 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
• 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
• 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
• 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
• Baker, C. J. & Orlandi, E. W. Active oxygen in plant pathogenesis. Annu. Rev. Phytopathol. 33, 299–322 (1995).
  Article CAS PubMed Google Scholar
• 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
• 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
• 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
• Irani, K. & Goldschmidt-Clermont, P. J. Ras, superoxide and signal transduction. Biochem. Pharmacol. 55, 1339–1346 (1998).
  Article CAS PubMed Google Scholar
• Torres, M. A., Dangl, J. L. & Jones, J. D. G. Arabidopsis gp91 phox 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
• 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
• 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
• 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
• Susin, S. A. et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397, 441–446 (1999).
  Article CAS PubMed Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Baehrecke, E. H. How death shapes life during development. Nature Rev. Mol. Cell Biol. 3, 779–787 (2002).
  Article CAS Google Scholar
• Jin, C. & Reed, J. C. Yeast and apoptosis. Nature Rev. Mol. Cell Biol. 3, 453–459 (2002).
  Article CAS Google Scholar
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• 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
• Innes, R. New effects of type III effectors. Mol. Microbiol. 50, 363–365 (2003).
  Article CAS PubMed Google Scholar
• 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
• 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
• Kuriyama, H. & Fukuda, H. Developmental programmed cell death in plants. Curr. Opin. Plant Biol. 5, 568–573 (2002).
  Article CAS PubMed Google Scholar
• 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
• 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