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Programmed cell death in plants: Effect of protein synthesis inhibitors and structural changes in pea guard cells

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Abstract

Pea leaf epidermis incubated with cyanide displayed ultrastructural changes in guard cells that are typical of apoptosis. Cycloheximide, an inhibitor of cytoplasmic protein synthesis, and lincomycin, an inhibitor of protein synthesis in chloroplasts and mitochondria, produced different effects on the dynamics of programmed death of guard cells. According to light microscopy data, cycloheximide reinforced and lincomycin suppressed the CN−-induced destruction of cell nuclei. Lincomycin lowered the effect of cycloheximide in the light and prevented it in the dark. According to electron microscopy data, the most pronounced effects of cycloheximide in the presence of cyanide were autophagy and a lack of apoptotic condensation of nuclear chromatin, the prevention of chloroplast envelope rupturing and its invagination inside the stroma, and the appearance of particular compartments with granular inclusions in mitochondria. Lincomycin inhibited the CN−-induced ultrastructural changes in guard cell nuclei. The data show that programmed death of guard cells may have a combined scenario involving both apoptosis and autophagy and may depend on the action of both cytoplasm synthesized and chloroplast and mitochondrion synthesized proteins.

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Abbreviations

PCD:

programmed cell death

ROS:

reactive oxygen species

References

  1. Golstein, P., Aurby, L., and Levraud, J.-P. (2003) Nature Revs. Mol. Cell Biol., 4, 798–807.

    CAS  Google Scholar 

  2. Samuilov, V. D., Oleskin, A. V., and Lagunova, E. M. (2000) Biochemistry (Moscow), 65, 873–887.

    CAS  Google Scholar 

  3. Vanyushin, B. F. (2001) Usp. Biol. Khim., 41, 3–38.

    CAS  Google Scholar 

  4. Van Loo, G., Saelens, X., van Gurp, M., MacFarlane, M., Martin, S. J., and Vandenabeele, P. (2002) Cell Death Differ., 9, 1031–1042.

    PubMed  Google Scholar 

  5. Newmeyer, D. D., and Ferguson-Viller, S. (2003) Cell, 112, 481–490.

    PubMed  CAS  Google Scholar 

  6. Damial, N. N., and Korsmeyer, S. J. (2004) Cell, 116, 205–219.

    Google Scholar 

  7. Samuilov, V. D., Lagunova, E. M., Beshta, O. E., and Kitashov, A. V. (2000) Biochemistry (Moscow), 65, 696–702.

    CAS  Google Scholar 

  8. Samuilov, V. D., Lagunova, E. M., Dzyubinskaya, E. V., Izyumov, D. S., Kiselevsky, D. B., and Makarova, Ya. V. (2002) Biochemistry (Moscow), 67, 627–634.

    Article  CAS  Google Scholar 

  9. Samuilov, V. D., Lagunova, E. M., Gostimsky, S. A., Timofeev, K. N., and Gusev, M. V. (2003) Biochemistry (Moscow), 68, 912–917.

    CAS  Google Scholar 

  10. Samuilov, V. D., Lagunova, E. M., Kiselevsky, D. B., Dzyubinskaya, E. V., Makarova, Y. V., and Gusev, M. V. (2003) Biosci. Rep., 23, 103–117.

    Article  PubMed  CAS  Google Scholar 

  11. Bakeeva, L. E., Dzyubinskaya, E. V., and Samuilov, V. D. (2005) Biochemistry (Moscow), 70, 972–979.

    Article  CAS  Google Scholar 

  12. Bakeeva, L. E., Skulachev, V. P., Sudarikova, Yu. V., and Tsyplenkova, V. G. (2001) Biochemistry (Moscow), 66, 1335–1341.

    CAS  Google Scholar 

  13. Skulachev, V. P., Bakeeva, L. E., Chernyak, B. V., Domina, L. V., Minin, A. A., Pletjushkina, O. Yu., Saprunova, V. B., Skulachev, I. V., Tsyplenkova, V. G., Vasiliev, J. M., Yaguzinsky, L. S., and Zorov, D. B. (2004) Mol. Cell. Biochem., 256/257, 341–358.

    CAS  Google Scholar 

  14. Mattson, M. P., and Furukawa, K. (1997) Apoptosis, 2, 257–264.

    Article  PubMed  CAS  Google Scholar 

  15. Kuriyama, H. (1999) Plant Physiol., 121, 763–774.

    Article  PubMed  CAS  Google Scholar 

  16. Asai, T., Stone, J. M., Heard, J. E., Kovtun, Y., Yorgey, P., Sheen, J., and Ausubel, F. M. (2000) Plant Cell, 12, 1823–1835.

    Article  PubMed  CAS  Google Scholar 

  17. Mach, J. M., Castillo, A. R., Hoogstraten, R., and Greenberg, J. T. (2001) Proc. Natl. Acad. Sci. USA, 98, 771–776.

    Article  PubMed  CAS  Google Scholar 

  18. Madeo, F., Frohlich, E., Ligr, M., Grey, M., Sigrist, S. J., Wolf, D. H., and Frohlich, K.-U. (1999) J. Cell Biol., 145, 757–767.

    Article  PubMed  CAS  Google Scholar 

  19. Ludovico, P., Sousa, M. J., Silva, M. T., Leao, C., and Corte-Real, M. (2001) Microbiologia, 147, 2409–2415.

    CAS  Google Scholar 

  20. Alessenko, A. V., Boikov, P. Ya., Filippova, G. N., Khrenov, A. V., Loginov, A. S., and Makarieva, E. D. (1997) FEBS Lett., 416, 113–116.

    Article  PubMed  CAS  Google Scholar 

  21. Ning, S.-B., Wang, L., Li, Z.-Y., Jin, W.-W., and Song, Y.-C. (2001) Ann. Bot., 87, 575–583.

    Article  CAS  Google Scholar 

  22. Okada, K., Satoh, K., and Katoh, S. (1991) FEBS Lett., 295, 155–158.

    Article  PubMed  CAS  Google Scholar 

  23. Tyystjarvi, E., and Aro, E.-M. (1996) Proc. Natl. Acad. Sci. USA, 93, 2213–2218.

    Article  PubMed  CAS  Google Scholar 

  24. Allakhverdiev, S. I., Nishiyama, Y., Miyairi, S., Yamamoto, H., Inagaki, N., Kanesaki, Y., and Murata, N. (2002) Plant Physiol., 130, 1443–1453.

    Article  PubMed  CAS  Google Scholar 

  25. Reynolds, E. (1963) J. Cell. Biol., 17, 208–212.

    Article  PubMed  CAS  Google Scholar 

  26. Dat, J. F., Pellinen, R., Beeckman, T., van De Cotte, B., Langebartels, C., Kangasjarvi, J., Inze, D., and van Breusegem, F. (2003) Plant J., 33, 621–632.

    Article  PubMed  CAS  Google Scholar 

  27. Leist, M., Single, B., Castoldi, A. F., Kuhnle, S., and Nicotera, P. (1997) J. Exp. Med., 185, 1481–1486.

    Article  PubMed  CAS  Google Scholar 

  28. Eguchi, Y., Shimizu, S., and Tsujimoto, Y. (1997) Cancer Res., 57, 1835–1840.

    PubMed  CAS  Google Scholar 

  29. Izyumov, D. S., Avetisyan, A. V., Pletjushkina, O. Yu., Sakharov, D. V., Wirtz, K. W., Chernyak, B. V., and Skulachev, V. P. (2004) Biochim. Biophys. Acta, 1658, 141–147.

    PubMed  CAS  Google Scholar 

  30. Yaglom, J. A., Ekhteral, D., Gabai, V. L., and Sherman, M. Y. (2003) J. Biol. Chem., 278, 50483–50496.

    Article  PubMed  CAS  Google Scholar 

  31. Shchepina, L. A., Popova, E. N., Pletjushkina, O. Yu., and Chernyak, B. V. (2002) Biochemistry (Moscow), 67, 222–226.

    Article  CAS  Google Scholar 

  32. Ishida, H., Shimizu, S., Makino, A., and Mae, T. (1998) Planta, 204, 305–309.

    Article  PubMed  CAS  Google Scholar 

  33. Affourtit, C., Albury, M. S., Crichton, P. G., and Moore, A. L. (2002) FEBS Lett., 510, 121–126.

    Article  PubMed  CAS  Google Scholar 

  34. Bendall, D. S., and Manasse, R. S. (1995) Biochim. Biophys. Acta, 1229, 23–38.

    Google Scholar 

  35. Asada, K. (2000) Philos. Trans. R. Soc. Lond. B Biol. Sci., 355, 1419–1430.

    PubMed  CAS  Google Scholar 

  36. Jabs, T. (1999) Biochem. Pharmacol., 57, 231–245.

    Article  PubMed  CAS  Google Scholar 

  37. Kohler, B., Hills, A., and Blatt, M. R. (2003) Plant Physiol., 131, 385–388.

    Article  PubMed  CAS  Google Scholar 

  38. Foreman, J., Demidchik, V., Bothwell, J. H. F., Mylona, P., Miedema, H., Torres, M. A., Linstead, P., Costa, S., Brownlee, C., Jones, J. D. G., Davies, J. M., and Dolan, L. (2003) Nature, 422, 442–446.

    Article  PubMed  CAS  Google Scholar 

  39. Gupta, R., and Luan, S. (2003) Plant Physiol., 132, 1149–1152.

    Article  PubMed  CAS  Google Scholar 

  40. Godon, C., Lagniel, G., Lee, J., Buhler, J.-M., Kieffer, S., Perrot, M., Boucherie, H., Toledano, M. B., and Labarre, J. (1998) J. Biol. Chem., 273, 22480–22489.

    Article  PubMed  CAS  Google Scholar 

  41. Desaint, S., Luriau, S., Aude, J. C., Rousselet, E., and Toledano, M. B. (2004) J. Biol. Chem., 279, 31157–31163.

    Article  PubMed  CAS  Google Scholar 

  42. Levine, A., Tenhaken, R., Dixon, R., and Lamb, C. (1994) Cell, 79, 583–593.

    Article  PubMed  CAS  Google Scholar 

  43. Bethke, P. C., and Jones, R. L. (2001) Plant J., 25, 19–29.

    Article  PubMed  CAS  Google Scholar 

  44. Ratan, R. R., Murphy, T. H., and Baraban, J. M. (1994) J. Neurosci., 14, 4385–4392.

    PubMed  CAS  Google Scholar 

  45. Clarke, P. G. H. (1990) Anat. Embryol., 181, 195–213.

    Article  PubMed  CAS  Google Scholar 

  46. Vierstra, R. D. (1996) Plant Mol. Biol., 32, 275–302.

    Article  PubMed  CAS  Google Scholar 

  47. Reggiori, F., and Klionsky, D. J. (2002) Eukaryot. Cell, 1, 11–21.

    Article  PubMed  CAS  Google Scholar 

  48. Ogier-Denis, E., and Codogno, P. (2003) Biochim. Biophys. Acta, 1603, 113–128.

    PubMed  CAS  Google Scholar 

  49. Moriyasu, Y., and Ohsumi, Y. (1996) Plant Physiol., 111, 1233–1241.

    PubMed  CAS  Google Scholar 

  50. Chen, M. H., Liu, L. F., Chen, Y. R., Wu, H. K., and Yu, S. M. (1994) Plant J., 6, 625–636.

    PubMed  CAS  Google Scholar 

  51. Aubert, S., Gout, E., Bligny, R., Marty-Mazars, D., Barrieu, F., Alabouvette, J., Marty, F., and Douche, R. (1996) J. Cell Biol., 133, 1251–1263.

    Article  PubMed  CAS  Google Scholar 

  52. Moriyasu, Y., and Hillmer, S. (2000) in Vacuolar Compartments (Robinson, D. G., and Rogers, J. C., eds.) Annu. Plant Rev., 5, 71–89.

  53. Hanaoka, H., Noda, T., Shirano, Y., Kato, T., Hayashi, H., Shibata, D., Tabata, S., and Ohsumi, Y. (2002) Plant Physiol., 129, 1181–1193.

    Article  PubMed  CAS  Google Scholar 

  54. Toyooka, K., Okamoto, T., and Minamikawa, T. (2001) J. Cell Biol., 154, 973–982.

    Article  PubMed  CAS  Google Scholar 

  55. Lee, R.-H., and Chen, S.-C. G. (2002) New Phytologist, 155, 25–32.

    Article  CAS  Google Scholar 

  56. Elmore, S. P., Qian, T., Grissom, S. F., and Lemasters, J. J. (2001) FASEB J., 15, 458–474.

    Google Scholar 

  57. Xue, L., Fletcher, G. C., and Tolkovsky, A. M. (2001) Curr. Biol., 11, 361–365.

    Article  PubMed  CAS  Google Scholar 

  58. Brunet, S., Thibault, P., Gagnon, E., Kearney, P., Bergeron, J. J. M., and Desjardins, M. (2003) Trends Cell Biol., 13, 629–638.

    Article  PubMed  CAS  Google Scholar 

  59. Matile, P., Hortensteiner, S., and Thomas, H. (1999) Annu. Rev. Plant Physiol. Mol. Biol., 50, 67–95.

    Article  CAS  Google Scholar 

  60. Ono, K., Hashimoto, H., and Katoh, S. (1995) Plant Cell Physiol., 36, 9–17.

    CAS  Google Scholar 

  61. Minamikawa, T., Toyooka, K., Okamoto, T., Hara-Nishimura, I., and Nishimura, M. (2001) Protoplasma, 218, 144–153.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Physiology of Microorganisms, Biological Faculty, Lomonosov Moscow State University, 119992, Moscow, Russia

    E. V. Dzyubinskaya, D. B. Kiselevsky & V. D. Samuilov

  2. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119992, Moscow, Russia

    L. E. Bakeeva

Authors
  1. E. V. Dzyubinskaya
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  2. D. B. Kiselevsky
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  3. L. E. Bakeeva
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  4. V. D. Samuilov
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Correspondence to V. D. Samuilov.

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Original Russian Text © E. V. Dzyubinskaya, D. B. Kiselevsky, L. E. Bakeeva, V. D. Samuilov, 2006, published in Biokhimiya, 2006, Vol. 71, No. 4, pp. 493–504.

Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM05-121, March 19, 2006.

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Dzyubinskaya, E.V., Kiselevsky, D.B., Bakeeva, L.E. et al. Programmed cell death in plants: Effect of protein synthesis inhibitors and structural changes in pea guard cells. Biochemistry (Moscow) 71, 395–405 (2006). https://doi.org/10.1134/S0006297906040079

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