Plant Molecular Biology

, Volume 44, Issue 3, pp 245–253 | Cite as

Programmed cell death of tracheary elements as a paradigm in plants

  • Hiroo Fukuda


Plant development involves various programmed cell death (PCD) processes. Among them, cell death occurring during differentiation of procambium into tracheary elements (TEs), which are a major component of vessels or tracheids, has been studied extensively. Recent studies of PCD during TE differentiation mainly using an in vitro differentiation system of Zinnia have revealed that PCD of TEs is a plant-specific one in which the vacuole plays a central role. Furthermore, there are recent findings of several factors that may initiate PCD of TEs and that act at autonomous degradation of cell contents. Herein I summarize the present knowledge about cell death program during TE differentiation as an excellent example of PCD in plants.

nuclease programmed cell death protease tracheary element vacuole Zinnia 


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  1. Aoyagi, S., Sugiyama, M. and Fukuda, H. 1998. BEN1 and ZEN1 cDNAs encoding S1-type DNases that are involved in programmed cell death in plants. FEBS Lett. 429: 134–138.Google Scholar
  2. Bachmair, A., Becker, F., Masterson, 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: 4543–4550.Google Scholar
  3. Beers, E.P. and Freeman, T.B. 1997. Protease activity during tracheary element differentiation in Zinnia mesophyll cultures. Plant Physiol. 113: 873–880.Google Scholar
  4. Brown, P.H. and Ho, T.H.D. 1986. Barley (Hordeum vulgare cultivar Himalaya) aleurone layers secrete a nuclease in response to gibberellic acid: purification and partial characterization of the associated RNase, DNase, and 3′-nucleotidase activities. Plant Physiol. 82: 801–806.Google Scholar
  5. Brown, P.H. and Ho, T.H.D. 1987. Biochemical properties and hormonal regulation of barley nuclease. Eur. J. Biochem. 168: 357–364.Google Scholar
  6. Burgess, J. and Linstead, P. 1984. In vitro tracheary element formation: structural studies and the effect of triiodobenzoic acid. Planta 160: 481–489.Google Scholar
  7. Church, D.L. and Galston, A.W. 1988. Kinetics of determination in the differentiation of isolated mesophyll cells of Zinnia elegans to tracheary elements. Plant Physiol. 88: 92–96.Google Scholar
  8. Demura, T. and Fukuda, H. 1993. Molecular cloning and characterization of cDNAs associated with tracheary element differentiation in cultured Zinnia cells. Plant Physiol. 103: 815–821.Google Scholar
  9. Demura, T. and Fukuda, H. 1994. Novel vascular cell-specific genes whose expression is regulated temporally and spatially during vascular system development. Plant Cell 6: 967–981.Google Scholar
  10. Ellis, R.E., Yuan, J. and Horvitz, H.R. 1991. Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7: 663–698.Google Scholar
  11. Esau, K. and Charvat, I. 1978. On vessel member differentiation in the bean (Phaseolus vulgaris L.). Ann Bot. 42: 665–677.Google Scholar
  12. Fukuda, H. 1996. Xylogenesis: initiation, progression and cell death. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 299–325.Google Scholar
  13. Fukuda, H. 1997a. Tracheary element differentiation. Plant Cell 9: 1147–1156.Google Scholar
  14. Fukuda, H. 1997b. Programmed cell death during vascular system formation. Cell Death Differ. 4: 684–688.Google Scholar
  15. Fukuda, H. 1998. Developmentally programmed cell death in plants: death of xylem cells as a paradigm. In: T. Yamada and Y. Hashimoto (Eds.), Apoptosis: Its role and mechanism, Business Center for Academic Societies Japan, Tokyo, pp. 113–127.Google Scholar
  16. Fukuda, H. and Komamine, A. 1980a. 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.Google Scholar
  17. Fukuda, H. and Komamine, A. 1980b. Direct evidence for cytodifferentiation to tracheary elements without intervening mitosis in a culture of single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol. 65: 61–64.Google Scholar
  18. Gavrieli, Y., Sherman, Y. and Ben-Sasson, S.A. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119: 493–501.Google Scholar
  19. Granell, A., Harris, N., Pisabarro, A.G. and Carbonell, J. 1992. Temporal and spatial expression of a thiolprotease gene during pea ovary senescence, and its regulation by gibberellin. Plant J. 2: 907–915.Google Scholar
  20. Greenberg, J.T. 1996. Programmed cell death: a way of life for plants. Proc. Natl. Acad. Sci. USA 93: 12094–12097.Google Scholar
  21. Greenberg, J.T. 1997. Programmed cell death in plant-pathogen interactions. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 525–545.Google Scholar
  22. Groover, A., DeWitt, N., Heidel, A. and Jones, A. 1997. Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma 196: 197–211.Google Scholar
  23. Groover, A. and Jones, A. 1999. Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol. 119: 375–384.Google Scholar
  24. 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.Google Scholar
  25. Jacobson, M.D. 1996. Reactive oxygen species and programmed cell death. Trends Biochem. Sci. 21: 83–86.Google Scholar
  26. Jones, A.M. and Dangl, J. 1996. Logjam at the Styx: programmed cell death in plants. Trends Plant Sci. 1: 114–119.Google Scholar
  27. Katsuhara, K. 1997. Apoptosis-like cell death in barley roots under salt stress. Plant Cell Physiol. 38: 1087–1090.Google Scholar
  28. Kerr, J. F. R. and Harmon, B. V. 1991. Definition and incidence of apoptosis: a historical perspective. In: L.D. Tomei and F.O. Cope (Eds.), Apoptosis: The Molecular Basis of Cell Death, Cold Spring Harbor Lab. Press, Plainview, NY, pp. 5–29.Google Scholar
  29. Kobayashi, H. and Fukuda, H. 1994. Involvement of calmodulin and calmodulin-binding proteins in the differentiation of tracheary elements in Zinnia cells. Planta 194: 388–394.Google Scholar
  30. 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.Google Scholar
  31. Kuriyama, H. 1999. Loss of tonoplast integrity programmed in tracheary element differentiation. Plant Physiol. 121, in press.Google Scholar
  32. Lai, V. and Srivastava, L.M. 1976. Nuclear changes during differentiation of xylem vessel elements. Cytobiologie 12: 220–243.Google Scholar
  33. Lamb, C. and Dixon, R.A. 1997. The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48: 251–275.Google Scholar
  34. Minami, A. and Fukuda, H. 1995. Transient and specific expression of a cysteine endopeptidase during autolysis in differentiating tracheary elements from Zinnia mesophyll cells. Plant Cell Physiol. 36: 1599–1606.Google Scholar
  35. 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.Google Scholar
  36. O'Brien, T.P. and Thimann, K.V. 1967. Observation on the fine structure of the oat coleoptile III. Correlated light and electron microscopy of the vascular tissues. Protoplasma 63: 443–478.Google Scholar
  37. Pennell, R.I. and Lamb, C. 1997. Programmed cell death in plants. Plant Cell 9: 1157–1168.Google Scholar
  38. Roberts, A.W. and Haigler, C.H. 1989. Rise in chlortetracycline accompanies tracheary element differentiation in suspension cultures of Zinnia. Protoplasma 152: 37–45.Google Scholar
  39. Roberts, A.W. and Haigler, C.H. 1990. Tracheary-element differentiation in suspension-cultured cells of Zinnia requires uptake of extracellular calcium ion: experiments with calcium-channel blockers and calmodulin inhibitors. Planta 180: 502–509.Google Scholar
  40. Roberts, A.W. and Haigler, C.H. 1992. Methylxanthines reversibly inhibit tracheary-element differentiation in suspension cultures of Zinnia elegans L. Planta 186: 586–592.Google Scholar
  41. Rogers, J.C., Dean, D. and Heck, G.R. 1985. Aleurain: a barley thiol protease closely related to mammalian cathepsin H. Proc. Natl. Acad. Sci. USA 82: 6512–6516.Google Scholar
  42. 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.Google Scholar
  43. Smart, C.M. 1994. Gene expression during leaf senescence. New Phytol. 126: 419–448.Google Scholar
  44. Srivastava, L.M. and Singh, A.P. 1972. Certain aspects of xylem differentiation in corn. Can J. Bot. 50: 1795–1804.Google Scholar
  45. Stephenson, P., Collins, B.A., Reid, P.D. and Rubinstein, B. 1996. Localization of ubiquitin to differentiating vascular tissues. Am. J. Bot. 83: 140–147.Google Scholar
  46. Sugiyama, M., Ito, J., Aoyagi, S. and Fukuda, H. 2000. Endonuclease. Plant Mol. Biol. this issue.Google Scholar
  47. Thelen, M.P. and Northcote, D.H. 1989. Identification and purification of a nuclease from Zinnia elegans L.: a potential molecular marker for xylogenesis. Planta 179: 181–195.Google Scholar
  48. Vercher, Y., Molowny, A. and Carbonell, J. 1987. Gibberellic acid effects on the ultrastructure of endocarp cells of unpollinated ovaries of Pisum sativum. Physiol. Plant. 71: 302–308.Google Scholar
  49. Wang, H., Li, J., Bostock, R.M. and 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.Google Scholar
  50. Wang, M., Oppedijk, B.J., Lu, X., Duijn, B.V. and Schilperoort, R.A. 1996b. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol. Biol. 32: 1125–1134.Google Scholar
  51. Watanabe, H., Abe, K., Emori, Y., Hosoyama, H. and Arai, S. 1991. Molecular cloning and gibberellin-induced expression of multiple cysteine proteases of rice seeds (Oryzains). J. Biol. Chem. 266: 16897–16907.Google Scholar
  52. 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.Google Scholar
  53. Yamada, T. and Hashimoto Y. 1998. Apoptosis its roles and mechanism. Business Center for Academic Societies, Japan, Tokyo.Google Scholar
  54. 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.Google Scholar
  55. Ye, Z.-H. and Droste, D.L. 1996. Isolation and characterization of cDNAs encoding xylogenesis-associated and wound-induced ribonucleases in Zinnia elegans. Plant Mol. Biol. 30: 697–709.Google Scholar
  56. 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.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Hiroo Fukuda
    • 1
  1. 1.Department of Biological Sciences, Graduate School of ScienceUniversity of Tokyo, HongoTokyoJapan

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