Advertisement

Plant Molecular Biology

, Volume 51, Issue 4, pp 509–521 | Cite as

Nuclease activities and DNA fragmentation during programmed cell death of megagametophyte cells of white spruce (Picea glauca) seeds

  • Xu He
  • Allison R. Kermode
Article

Abstract

The haploid megagametophyte of white spruce (Picea glauca) seeds undergoes programmed cell death (PCD) during post-germinative seedling growth. Death of the megagametophyte storage parenchyma cells was preceded by reserve mobilization and vacuolation. TUNEL (terminal deoxynucleotidyltransferase-mediated dUTP nick-end labeling)-positive nuclei indicated that the first megagametophyte cells to die were those closest to the radicle at the micropylar end of the seed as well as those that comprised the most peripheral and innermost layers at the chalazal end of the seed. The death process was accompanied by nuclear fragmentation and internucleosomal DNA cleavage and the sequential activation of several nucleases. The latter comprised at least two groups: those induced relatively early during post-germinative seedling growth, that had pH optima in the neutral range (33, 31, 17 and 15 kDa), and those induced later that had pH optima in the acidic range (73, 62, 48, 43 and 29 kDa). Activities of all of the nucleases were stimulated by Ca2+, Mg2+ and Mn2+; only the nucleases active at neutral pH were inhibited by Zn2+. The temporal pattern of induction of the neutral and acidic nucleases may suggest that the latter function after tonoplast rupture.

DNA fragmentation megagametophyte nucleases Picea glauca programmed cell death 

References

  1. Alam, A. 1992. A method for formulation of protein assay. Ann. Biochem. 208: 121–126.Google Scholar
  2. Aoyagi, S., Sugiyama, M. and Fukuda, H. 1998. BEN1 and ZEN1 cDNAs encoding S1-type DNases that are associated with programmed cell death in plants. FEBS Lett. 429: 134–138.Google Scholar
  3. Beers, E.P. 1997. Programmed cell death during plant growth and development. Cell Death Diff. 4: 649–661.Google Scholar
  4. Beers, E.P., Woffenden, B.J. and Zhao, C. 2000. Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol. Biol. 44: 399–415.Google Scholar
  5. Bethke, P.C. and Jones, R.L. 2001. Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J. 25: 19–29.Google Scholar
  6. 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.Google Scholar
  7. Brown, P.H. and Ho, T. H. 1986. Barley aleurone layers secrete a nuclease in response to gibberellic acid. Plant Physiol. 82: 801–806.Google Scholar
  8. Buckner, B., Johal, G.S. and Janick-Buckner, D. 2000. Cell death in maize. Physiol. Plant. 108: 231–239.Google Scholar
  9. Chen, F.Q. 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.Google Scholar
  10. Counis, M.F. and Torriglia, A. 2000. DNases and apoptosis. Biochem. Cell Biol. 78: 405–414.Google Scholar
  11. 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.Google Scholar
  12. Del Pozo, O. and Lam, E. 1998. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol. 8: 1129–1132.Google Scholar
  13. Dellaporta, S.L., Wood, J. and Hicks, J.B. 1983. The plant DNA minipreparation: version II. Plant Mol. Biol. Rep. 4: 19–21.Google Scholar
  14. Delorme, V.G., 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.Google Scholar
  15. Ellis, R.E, Yuan, J.Y. and Horvitz, H.R., 1991. Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7: 663–698.Google Scholar
  16. Fath, A., Bethke, P.C. and Jones, R.L. 1999. Barley aleurone cell death is not apoptotic: characterization of nuclease activities and DNA degradation. Plant J. 20: 305–315.Google Scholar
  17. Fath, A., Bethke, P., Lonsdale, J., Meza-Romero, R. and Jones, R. 2000. Programmed cell death in cereal aleurone. Plant Mol. Biol. 44: 255–266.Google Scholar
  18. Filonova, L.H., Bozhkov, P.V., Brukhin, V.B., Daniel, G., Zhivotovsky, B. and von Arnold, S. 2000. 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.Google Scholar
  19. Fukuda, H. 2000. Programmed cell death of tracheary elements as a paradigm in plants. Plant Mol. Biol. 44: 245–253.Google Scholar
  20. 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 defense functions. Cell 77: 551–563.Google Scholar
  21. Heath, M.C. 2000. Hypersensitive response-related death. Plant Mol. Biol. 44: 321–334.Google Scholar
  22. 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.Google Scholar
  23. Lam E. and del Pozo, O. 2000. Caspase-like protease involvement in the control of plant cell death. Plant Mol. Biol. 44: 417–428.Google Scholar
  24. LoSchiavo, F., Baldan, B., Compagnin, D., Ganz, R., Mariani, P. and Terzi, M. 2000. Spontaneous and induced apoptosis in embryogenic cell cultures of carrot (Daucus carota L.) in different physiological states. Eur. J. Cell Biol. 79: 294–298.Google Scholar
  25. Mittler, R. 1998. Cell death in plants. In: R.A. Lockshin, Z. Zakeri, Z. and J.L. Tilly (Eds.) When Cells Die: A Comprehensive Evaluation of Apoptosis and Programmed Cell Death, Wiley-Liss, New York, pp. 147–174.Google Scholar
  26. Mittler, R. and Lam, E. 1995. Identification, characterization, and purification of a tobacco endonuclease activity induced upon hypersensitive response cell death. Plant Cell 7: 1951–1962.Google Scholar
  27. Mittler, R. and Lam, E. 1997. Characterization of nuclease activities and DNA fragmentation induced upon hypersensitive response cell death and mechanical stress. Plant Mol. Biol. 34: 209–221.Google Scholar
  28. Mittler, R., del Pozo, O., Meisel, L. and Lam, E. 1997. Pathogeninduced programmed cell death in plants, a possible defense mechanism. Dev. Genet. 21: 279–289.Google Scholar
  29. Orzaez, D. and Granell, A. 1997. DNA fragmentation is regulated by ethylene during carpel senescence in Pisum sativum. Plant J. 11: 137–144.Google Scholar
  30. Owens, J.N., Morris, S.J. and Misra, S. 1992. The ultrastructural, histochemical, and biochemical development of the postfertilization megagametophyte and zygotic embryo of Pseudotsuga menziesii. Can. J. For. Res. 23: 816–827.Google Scholar
  31. Pontier, D., Balague, C. and Roby, D. 1998. The hypersensitive response. A programmed cell death associated with plant resistance. C. R. Acad. Sci. Paris III 321: 721–734.Google Scholar
  32. Quirino, B.F., Noh, Y.S., Himelblau, E. and Amasino, R.M. 2000. Molecular aspects of leaf senescence. Trends Plant Sci. 5: 278–282.Google Scholar
  33. Raven, P.H., Evert, R.F. and Eichhorn, S.E. 1999. Biology of Plants. W.H. Freeman and Worth, New York, pp. 469–483.Google Scholar
  34. 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
  35. Schmid, M., Simpson, D. and Gietl, 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. USA 96: 14159–14164.Google Scholar
  36. Sikorska, M. and Walker, P.R. 1998. Endonuclease activities and apoptosis. In: R.A. Lockshin, Z. Zakeri and J.L. Tilly (Eds.) When Cells Die: A Comprehensive Evaluation of Apoptosis and Programmed Cell Death, Wiley-Liss, New York, pp. 211–242.Google Scholar
  37. Solomon, M., Belenghi, B., Delledonne, M., Menachem, E. 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: 431–444.Google Scholar
  38. Stein, J.C. and Hansen, G. 1999. Mannose induces an endonuclease responsible for DNA laddering in plant cells. Plant Physiol. 121: 71–80.Google Scholar
  39. Sugiyama, M., Ito, J., Aoyagi, S. and Fukuda, H. 2000. Endonucleases. Plant Mol. Biol. 44: 387–397.Google Scholar
  40. Thelen, M.P. and Northcote, D.H. 1989. Identification and purifi-cation of a nuclease from Zinnia elegans L.: a potential marker marker for xylogenesis. Planta 179: 181–195.Google Scholar
  41. Thornberry, N.A. and Lazebnik, Y. 1998. Caspases: enemies within. Science 281: 1312–1316.Google Scholar
  42. Tillman-Sutela, E., Kauppi, A. 2000. Structures contributing to the completion of conifer seed germination. Trees 14: 191–197.Google Scholar
  43. Vierstra, R.D. 1996. Proteolysis in plants: Mechanisms and functions. Plant Mol. Biol. 32: 275–302.Google Scholar
  44. Walker, P.R. and Sikorska, M. 1994. Endonuclease activities, chromatin structure, and DNA degradation in apoptosis. Biochem. Cell. Biol. 72: 615–623.Google Scholar
  45. Walker, P.R., LeBlanc, J. and Sikorska, M. 1993. Detection of the initial stages of DNA fragmentation in apoptosis. Bio/technology 15: 1032–1040.Google Scholar
  46. Wang, H., Li, J., Bostock, B.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
  47. Wang, M., Hoekstra, S., van Bergen, S., Lamers, G.E., Oppedijk, 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.Google Scholar
  48. Wang, M., Oppedijk, B.J., Caspers, M.P.M., Lamers, G.E.M., Boot, M.J., Geerlings, D.N.G., Bakhuizen, B., Meijer, A.H. and van Duijn, B. 1998. Spatial and temporal regulation of DNA fragmentation in the aleurone of germinating barley. J. Exp. Bot. 49: 1293–1301.Google Scholar
  49. Wang, M., Oppedijk, B.J., Lu, X., van Duijn, B. 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
  50. Wu, H.M. and Cheun, A.Y. 2000. Programmed cell death in plant reproduction. Plant Mol. Biol. 44: 267–281.Google Scholar
  51. Xu, Y. and Hanson, M.R. 2000. Programmed cell death during pollination-induced petal senescence in petunia. Plant Physiol. 122: 1323–1333.Google Scholar
  52. Young, T.E. and Gallie, D.R. 1999. Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals. Plant Mol. Biol. 39: 915–926.Google Scholar
  53. Young, T.E. and Gallie, D.R. 2000a. Programmed cell death during endosperm development. Plant Mol. Biol. 44: 283–301.Google Scholar
  54. Young, T.E. and Gallie, D.R. 2000b. Regulation of programmed cell death in maize endosperm by abscisic acid. Plant Mol. Biol. 42: 397–414.Google Scholar
  55. Young, T.E., Gallie, D.R. and DeMason, D.A. 1997. Ethylene mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol. 115: 737–751.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Xu He
    • 1
  • Allison R. Kermode
    • 1
  1. 1.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada

Personalised recommendations