Skip to main content

A cellular suicide strategy of plants: vacuole-mediated cell death

Apoptosis volume 11, pages 905–911 (2006)Cite this article

Abstract

Programmed cell death (PCD) occurs in animals and plants under various stresses and during development. Recently, vacuolar processing enzyme (VPE) was identified as an executioner of plant PCD. VPE is a cysteine protease that cleaves a peptide bond at the C-terminal side of asparagine and aspartic acid. VPE exhibited enzymatic properties similar to that of a caspase, which is a cysteine protease that mediates the PCD pathway in animals, although there is limited sequence identity between the two enzymes. VPE and caspase-1 share several structural properties: the catalytic dyads and three amino acids forming the substrate pockets (Asp pocket) are conserved between VPE and caspase-1. In contrast to such similarities, subcellular localizations of these proteases are completely different from each other. VPE is localized in the vacuoles, while caspases are localized in the cytosol. VPE functions as a key molecule of plant PCD through disrupting the vacuole in pathogenesis and development. Cell death triggered by vacuolar collapse is unique to plants and has not been seen in animals. Plants might have evolved a VPE-mediated vacuolar system as a cellular suicide strategy.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  1. Pennell RI, Lamb C. Programmed cell death in plants. Plant Cell 1997; 9: 1157–1168.

    PubMed  CAS  Article  Google Scholar 

  2. Greenberg JT, Yao N. The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol. 2004; 6: 201–211.

    PubMed  CAS  Article  Google Scholar 

  3. Lam E. Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 2004; 5: 305–315.

    PubMed  CAS  Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Article  Google Scholar 

  6. Ferri K, Kroemer G. Mitochondria–the suicide organelles. Bioessays 2001; 23: 111–115.

    PubMed  CAS  Article  Google Scholar 

  7. Lam E, Kato N, Lawton M. Programmed cell death, mitochondria and the plant hypersensitive response. Nature 2001; 411: 848–853.

    PubMed  CAS  Article  Google Scholar 

  8. Yao N, Eisfelder BJ, Marvin J, Greenberg JT. The mitochondrion–an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J 2004; 40: 596–610.

    PubMed  CAS  Article  Google Scholar 

  9. Yu XH, Perdue TD, Heimer YM, Jones AM. Mitochondrial involvement in tracheary element programmed cell death. Cell Death Differ 2002; 9: 189–198.

    PubMed  CAS  Article  Google Scholar 

  10. Cohen GM. Caspase: The executioners of apoptosis. Biochem J 1997; 326: 1–16.

    PubMed  CAS  Google Scholar 

  11. Woltering EJ, van der Bent A, Hoeberichts FA. Do plant caspases exist? Plant Physiol 2002; 130: 1764–1769.

    PubMed  CAS  Article  Google Scholar 

  12. del Pozo O, Lam E. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr Biol 1998; 8: 1129–1132.

    PubMed  Article  Google Scholar 

  13. Rojo E, Martin R, Carter C, et al. VPEgamma exhibits a caspase-like activity that contributes to defense against pathogens. Curr Biol 2004; 14: 1897–1906.

    PubMed  CAS  Article  Google Scholar 

  14. De Jong AJ, Hoeberichts FA, Yakimova ET,  Maximova E, Woltering EJ. Chemical-induced apoptotic cell death in tomato cells: involvement of caspase-like proteases. Planta 2000; 211: 656–662.

    PubMed  Article  Google Scholar 

  15. Clarke A, Desikan R, Hurst RD, Hancock JT, Neill SJ. NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J 2000; 24: 667–677.

    PubMed  CAS  Article  Google Scholar 

  16. Korthout H, Berecki G, Bruin W, van Duijin B, Wang M. The presence and subcellular localization of caspase 3-like proteinases in plant cells. FEBS Lett 2000; 475: 139–144.

    PubMed  CAS  Article  Google Scholar 

  17. Coffeen WC, Wolpert TJ. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 2004; 16: 857–873.

    PubMed  CAS  Article  Google Scholar 

  18. Uren AG, Orourke K, Aravind L, 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 2000; 6: 961–967.

    PubMed  CAS  Google Scholar 

  19. Suarez MF, Filonova LH, Smertenko A, et al. Metacaspase-dependent programmed cell death is essential for plant embryogenesis. Curr Biol 2004; 14: R339–340.

    PubMed  CAS  Article  Google Scholar 

  20. Vercammen D, van de Cotte B, De Jaeger G, et al. Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J Biol Chem 2004; 279: 45329–45336.

    PubMed  CAS  Article  Google Scholar 

  21. Watanabe N, Lam E. Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J Biol Chem 2005; 280: 14691–14699.

    PubMed  CAS  Article  Google Scholar 

  22. Hatsugai N, Kuroyanagi M, Yamada K, et al. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 2004; 305: 855–858.

    PubMed  CAS  Article  Google Scholar 

  23. Kuroyanagi M, Yamada K, Hatsugai N, et al. Vacuolar Processin enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. J Biol Chem 2005; 280: 32914–32920.

    PubMed  CAS  Article  Google Scholar 

  24. van Doorn WG, Woltering EJ. Many ways to exist? Cell death categories in plants. Trends Plant Sci 2005; 10: 117–122.

    PubMed  Google Scholar 

  25. Woltering EJ. Death proteases come alive. Trends Plant Sci 2004; 9 : 469–472.

    PubMed  CAS  Article  Google Scholar 

  26. Lam E. Vacuolar proteases livening up programmed cell death. Trend. Cell Biol 2005; 15: 124–127.

    CAS  Article  Google Scholar 

  27. Hara-Nishimura I, Nishimura M, Akazawa T. Biosynthesis and intracellular transport of 11S globulin in developing pumpkin cotyledons. Plant Physiol 1985; 77: 747–752.

    PubMed  CAS  Google Scholar 

  28. Hara-Nishimura I, Nishimura M. Proglobulin processing enzyme in vacuoles isolated from developing pumpkin cotyledons. Plant Physiol 1987; 85: 440–445.

    PubMed  CAS  Article  Google Scholar 

  29. Yamada K, Shimada T, Kondo M, Nishimura M, Hara-Nishimura I. Multiple functional proteins are produced by cleaving Asn-Gln bonds of a single precursor by vacuolar processing enzyme. J Biol Chem 1999; 274: 2563–2570.

    PubMed  CAS  Article  Google Scholar 

  30. Hara-Nishimura I, Inoue K, Nishimura M. A unique vacuolar processing enzyme responsible for conversion of several proprotein precursors into the mature forms. FEBS Lett 1991; 294: 89–93.

    PubMed  CAS  Article  Google Scholar 

  31. Hara-Nishimura I, Takeuchi Y, Nishimura M. Molecular characterization of a vacuolar processing enzyme related to a putative cysteine proteinase of Schistosoma mansoni. Plant Cell 1993; 5: 1651–1659.

    PubMed  CAS  Article  Google Scholar 

  32. 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 1999; 447: 213–216.

    PubMed  CAS  Article  Google Scholar 

  33. Kuroyanagi M, Nishimura M, Hara-Nishimura I. Activation of Arabidopsis vacuolar processing enzyme by self-catalytic removal of an auto-inhibitory domain of the C-terminal propeptide. Plant Cell Physiol 2002; 43: 143–151.

    PubMed  CAS  Article  Google Scholar 

  34. Yamada K, Shimada T, Nishimura M, Hara-Nishimura I. A VPE family supporting various vacuolar functions in plants. Physiol Plant, Special Issue 2005; 123: 369–375.

    CAS  Article  Google Scholar 

  35. Nakaune S, Yamada K, Kondo M, et al. A novel-type VPE, δVPE, is involved in seed coat formation at the early stage of seed development. Plant Cell 2005; 17: 876–887.

    PubMed  CAS  Article  Google Scholar 

  36. Kinoshita T, Nishimura M, Hara-Nishimura I. The sequence and expression of theγ-VPE gene, one member of a family of three genes for vacuolar processing enzymes in Arabidopsis thaliana. Plant Cell Physiol 1995; 36: 1555–1562.

    PubMed  CAS  Google Scholar 

  37. Kinoshita T, Nishimura M, Hara-Nishimura I. Homologues of a vacuolar processing enzyme that are expressed in different organs in Arabidopsis thaliana. Plant Mol Biol 1995; 29: 81–89.

    PubMed  CAS  Article  Google Scholar 

  38. Hara-Nishimura I, Kinoshita T, Hiraiwa N, Nishimura M. Vacuolar processing enzymes in protein-storage vacuoles and lytic vacuoles. J Plant Physiol 1998; 152: 668–674.

    CAS  Google Scholar 

  39. Yamada K, Nishimura M, Hara-Nishimura I. The slow wound-response of γVPE is regulated by endogenous salicylic acid in Arabidopsis. Planta 2004; 218: 599–605.

    PubMed  CAS  Article  Google Scholar 

  40. Hara-Nishimura I, Hatsugai N, Kuroyanagi M, Nakaune S, Nishimura M. Vacuolar processing enzyme: An executor of plant cell death. Curr Opinon Plant Biol 2005: in press.

  41. Shirahama-Noda K, Yamamoto A, Sugihara K, et al. Biosynthetic processing of cathepsins and lysosomal degradation are abolished in asparaginyl endopeptidase-deficient mice. J Biol Chem 2003; 278: 33194–33199.

    PubMed  CAS  Article  Google Scholar 

  42. Goodman RN, Novacky AJ. The Hypersensitive Response Reaction in Plants to Pathogens: A Resistance Phenomenon. American Phytopathological Society Press, MN, 1994.

    Google Scholar 

  43. Greenberg JT. Programed cell death in plant-pathogen interaction. Annu. Rev. Plant Physiol. Plant Mol Biol 1997; 48: 525–545.

    PubMed  CAS  Article  Google Scholar 

  44. 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 1999; 11: 431–443.

    PubMed  CAS  Article  Google Scholar 

  45. Belenghi B, Acconcia F, Trovato M, et al. AtCYS1, a cystatin from Arabidopsis thaliana, suppresses hypersensitive cell death. Eur J Biochem 2003; 270: 2593–2604.

    PubMed  CAS  Article  Google Scholar 

  46. Lam E, delPozo O. Caspase-like protease involvement in the control of plant cell death. Plant Mol Biol 2000; 44: 417–428.

    PubMed  CAS  Article  Google Scholar 

  47. Elbaz M, Avni A, Weil M. Constitutive caspase-like machinery executes programmed cell death in plant cells. Cell Death Differ 2002; 9: 726–733.

    PubMed  CAS  Article  Google Scholar 

  48. Sanmartin M, Jaroszewski L, Raikhel NV, Rojo E. Caspases. Regulating death since the origin of life. Plant Physiol 2005; 137: 841–847.

    PubMed  CAS  Article  Google Scholar 

  49. Wilson KP, Black J-AF, Thomson JA, et al. Structure and mechanism of interleukin-1 beta converting enzyme. Nature 1994; 370: 270–274.

    PubMed  CAS  Article  Google Scholar 

  50. Hiraiwa N, Nishimura M, Hara-Nishimura I. Expression and activation of the vacuolar processing enzyme in Saccharomyces cerevisiae. Plant J 1997; 12: 819–829.

    PubMed  CAS  Article  Google Scholar 

  51. Stennicke HR, Salvesen GS. Properties of the caspases. Biochim Biophys Acta 1998; 1387: 17–31.

    PubMed  CAS  Google Scholar 

  52. Earnshaw WC, Martins LM, Kaufmann SH. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 1999; 68: 383–424.

    PubMed  CAS  Article  Google Scholar 

  53. Hara-Nishimura I. In: Handbook of Proteolytic Enzymes, Barrett AJ, Rawlings ND, Woessner JF, eds. Lonson, UK: Academic Press, 1998; 746–749.

    Google Scholar 

  54. Becker C, Shutov AD, Nong VH, et al. Purification, cDNA cloning and characterization of proteinase B, an asparagine-specific endopeptidase from germinating vetch (Vicia sativa L.) seeds. Eur J Biochem 1995; 228: 456–462.

    PubMed  CAS  Article  Google Scholar 

  55. Holmes FO. Inheritance of resistance to tobacco-mosaic disease in tobacco. Phytopathology 1938; 28: 553–561.

    Google Scholar 

  56. Walton JD. Host-selective toxins: Agents of compatibility. Plant Cell 1996; 8: 1723–1733.

    PubMed  CAS  Article  Google Scholar 

  57. Asai T, Stone JM, Heard JE, et al. Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell 2000; 12: 1823–1836.

    PubMed  CAS  Article  Google Scholar 

  58. Navarre DA, Wolpert TJ. Victorin induction of an apoptotic/senescence-like response in oats. Plant Cell 1999; 11: 237–249.

    PubMed  CAS  Article  Google Scholar 

  59. Gilchrist DG. Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol 1998; 36: 393–414.

    PubMed  CAS  Article  Google Scholar 

  60. Shimada T, Yamada K, Kataoka M, et al. Vacuolar processing enzymes are essential for proper processing of seed storage proteins in Arabidopsis thaliana. J Biol Chem 2003; 278: 32292–32299.

    PubMed  CAS  Article  Google Scholar 

  61. Kinoshita T, Yamada K, Hiraiwa N, Nishimura M, Hara-Nishimura I. Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions. Plant J 1999; 19: 43–53.

    PubMed  CAS  Article  Google Scholar 

  62. Hara-Nishimura, I. Maeshima M. In Robinson ADG Vacuolar Compartments in Plants, Rogers JC, eds. London, UK: Sheffield Academic Press, 2000; 20–42.

    Google Scholar 

  63. Nishimura M, Beevers H. Hydrolysis of protein in vacuoles isolated from higher plant tissues. Nature 1979; 277: 412–413.

    CAS  Article  Google Scholar 

  64. Jones AM. Programmed cell death in development and defense. Plant Physiol 2001; 125: 94–97.

    PubMed  CAS  Article  Google Scholar 

  65. Okamoto T, Minamikawa T. Molecular cloning and characterization of Vigna mungo processing enzyme 1 (VmPE-1), an asparaginyl endopeptidase possibly involved in post-translational processing of a vacuolar cysteine endopeptidase (SH-EP). Plant Mol Biol 1999; 39: 63–73.

    PubMed  CAS  Article  Google Scholar 

  66. Alonso JM, Granell A. A putative vacuolar processing protease is regulated by ethylene and also during fruit ripening in Citrus fruit. Plant Physiol 1995; 109: 541–547.

    PubMed  CAS  Article  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Botany, Graduate School of Science, Kyoto University, Kitashirakawa, Sakyo-ku, Kyoto, 606-8502, Japan

    N. Hatsugai, M. Kuroyanagi & I. Hara-Nishimura

  2. Department of Cell Biology, National Institute for Basic Biology, Okazaki, 444-8585, Japan

    M. Nishimura

Authors
  1. N. Hatsugai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Kuroyanagi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Nishimura
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. Hara-Nishimura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. Hara-Nishimura.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hatsugai, N., Kuroyanagi, M., Nishimura, M. et al. A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11, 905–911 (2006). https://doi.org/10.1007/s10495-006-6601-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10495-006-6601-1

Keywords

  • caspase
  • cysteine protease
  • programmed cell death
  • vacuolar processing enzyme
  • vacuole
  • VPE