Advertisement

Biochemistry (Moscow)

, Volume 77, Issue 13, pp 1452–1464 | Cite as

Programmed cell death in plants

  • A. S. Fomicheva
  • A. I. Tuzhikov
  • R. E. Beloshistov
  • S. V. Trusova
  • R. A. Galiullina
  • L. V. Mochalova
  • N. V. Chichkova
  • A. B. VartapetianEmail author
Review

Abstract

The modern concepts of programmed cell death (PCD) in plants are reviewed as compared to PCD (apoptosis) in animals. Special attention is focused on considering the potential mechanisms of implementation of this fundamental biological process and its participants. In particular, the proteolytic enzymes involved in PCD in animals (caspases) and plants (phytaspases) are compared. Emphasis is put on elucidation of both common features and substantial differences of PCD implementation in plants and animals.

Key words

apoptosis caspase programmed cell death phytaspase 

Abbreviations

AFC

7-amino-4-trifluoromethyl-coumarin

AMC

7-amino-4-methylcoumarin

AtMC

Arabidopsis thaliana metacaspase

CHO

aldehyde group

CMK

chloromethylketone

FMK

fluoromethylketone

HR

hypersensitive response

PCD

programmed cell death

TMV

tobacco mosaic virus

VPE

vacuolar processing enzyme

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Kerr, J. F., Wyllie, A. H., and Currie, A. R. (1972) Br. J. Cancer, 26, 239–257.PubMedCrossRefGoogle Scholar
  2. 2.
    Nicholson, D. W., and Thornberry, N. A. (1997) Trends Biochem. Sci., 22, 299–306.PubMedCrossRefGoogle Scholar
  3. 3.
    Williams, B., and Dickman, M. (2008) Mol. Plant Pathol., 9, 531–544.PubMedCrossRefGoogle Scholar
  4. 4.
    Reape, T. J., Molony, E. M., and McCabe, P. F. (2008) J. Exp. Bot., 59, 435–444.PubMedCrossRefGoogle Scholar
  5. 5.
    Reape, T. J., and McCabe, P. F. (2010) Apoptosis, 15, 249–256.PubMedCrossRefGoogle Scholar
  6. 6.
    Bonneau, L., Ge, Y., Drury, G. E., and Gallois, P. (2008) J. Exp. Bot., 59, 491–499.PubMedCrossRefGoogle Scholar
  7. 7.
    Degterev, A., Boyce, M., and Yuan, J. (2003) Oncogene, 22, 8543–8567.PubMedCrossRefGoogle Scholar
  8. 8.
    Walker, N. P., Talanian, R. V., Brady, K. D., Dang, L. C., Bump, N. J., Ferenz, C. R., Franklin, S., Ghayur, T., Hackett, M. C., Hammill, L. D., et al. (1994) Cell, 78, 343–352.PubMedCrossRefGoogle Scholar
  9. 9.
    Thornberry, N. A., Rano, T. A., Peterson, E. P., Rasper, D. M., Timkey, T., Garcia-Calvo, M., Houtzager, V. M., Nordstrom, P. A., Roy, S., Vaillancourt, J. P., Chapman, K. T., and Nicholson, D. W. (1997) J. Biol. Chem., 272, 17907–17911.PubMedCrossRefGoogle Scholar
  10. 10.
    Talanian, R. V., Quinlan, C., Trautz, S., Hackett, M. C., Mankovich, J. A., Banach, D., Ghayur, T., Brady, K. D., and Wong, W. W. (1997) J. Biol. Chem., 272, 9677–9682.PubMedCrossRefGoogle Scholar
  11. 11.
    Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998) Cell, 94, 481–490.PubMedCrossRefGoogle Scholar
  12. 12.
    Li, H., Zhu, H., Xu, C. J., and Yuan, J. (1998) Cell, 94, 491–501.PubMedCrossRefGoogle Scholar
  13. 13.
    Liu, X., Zou, H., Slaughter, C., and Wang, X. (1997) Cell, 89, 175–184.PubMedCrossRefGoogle Scholar
  14. 14.
    Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A., and Nagata, S. (1998) Nature, 391, 43–50.PubMedCrossRefGoogle Scholar
  15. 15.
    Sakahira, H., Enari, M., and Nagata, S. (1998) Nature, 391, 96–99.PubMedCrossRefGoogle Scholar
  16. 16.
    Timmer, J. C., and Salvesen, G. S. (2007) Cell Death Differ., 14, 66–72.PubMedCrossRefGoogle Scholar
  17. 17.
    Juo, P., Kuo, C. J., Yuan, J., and Blenis, J. (1998) Curr. Biol., 8, 1001–1008.PubMedCrossRefGoogle Scholar
  18. 18.
    Slee, E. A., Harte, M. T., Kluck, R. M., Wolf, B. B., Casiano, C. A., Newmeyer, D. D., Wang, H. G., Reed, J. C., Nicholson, D. W., Alnemri, E. S., Green, D. R., and Martin, S. J. (1999) J. Cell Biol., 144, 281–292.PubMedCrossRefGoogle Scholar
  19. 19.
    Chun, H. J., Zheng, L., Ahmad, M., Wang, J., Speirs, C. K., Siegel, R. M., Dale, J. K., Puck, J., Davis, J., Hall, C. G., Skoda-Smith, S., Atkinson, T. P., Straus, S. E., and Lenardo, M. J. (2002) Nature, 419, 395–399.PubMedCrossRefGoogle Scholar
  20. 20.
    Salmena, L., Lemmers, B., Hakem, A., Matysiak-Zablocki, E., Murakami, K., Au, P. Y., Berry, D. M., Tamblyn, L., Shehabeldin, A., Migon, E., Wakeham, A., Bouchard, D., Yeh, W. C., McGlade, J. C., Ohashi, P. S., and Hakem, R. (2003) Genes Dev., 17, 883–895.PubMedCrossRefGoogle Scholar
  21. 21.
    Beisner, D. R., Ch’en, I. L., Kolla, R. V., Hoffmann, A., and Hedrick, S. M. (2005) J. Immunol., 175, 3469–3473.PubMedGoogle Scholar
  22. 22.
    Su, H., Bidere, N., Zheng, L., Cubre, A., Sakai, K., Dale, J., Salmena, L., Hakem, R., Straus, S., and Lenardo, M. (2005) Science, 307, 1465–1468.PubMedCrossRefGoogle Scholar
  23. 23.
    Kang, T. B., Ben-Moshe, T., Varfolomeev, E. E., Pewzner-Jung, Y., Yogev, N., Jurewicz, A., Waisman, A., Brenner, O., Haffner, R., Gustafsson, E., Ramakrishnan, P., Lapidot, T., and Wallach, D. (2004) J. Immunol., 173, 2976–2984.PubMedGoogle Scholar
  24. 24.
    Fernando, P., Kelly, J. F., Balazsi, K., Slack, R. S., and Megeney, L. A. (2002) Proc. Natl. Acad. Sci. USA, 99, 11025–11030.PubMedCrossRefGoogle Scholar
  25. 25.
    Miura, M., Chen, X. D., Allen, M. R., Bi, Y., Gronthos, S., Seo, B. M., Lakhani, S., Flavell, R. A., Feng, X. H., Robey, P. G., Young, M., and Shi, S. (2004) J. Clin. Invest., 114, 1704–1713.PubMedGoogle Scholar
  26. 26.
    Howard, A. D., Kostura, M. J., Thornberry, N., Ding, G. J., Limjuco, G., Weidner, J., Salley, J. P., Hogquist, K. A., Chaplin, D. D., Mumford, R. A., et al. (1991) J. Immunol., 147, 2964–2969.PubMedGoogle Scholar
  27. 27.
    Sleath, P. R., Hendrickson, R. C., Kronheim, S. R., March, C. J., and Black, R. A. (1990) J. Biol. Chem., 265, 14526–14528.PubMedGoogle Scholar
  28. 28.
    Zhang, Y., Center, D. M., Wu, D. M., Cruikshank, W. W., Yuan, J., Andrews, D. W., and Kornfeld, H. (1998) J. Biol. Chem., 273, 1144–1149.PubMedCrossRefGoogle Scholar
  29. 29.
    Riedl, S. J., and Shi, Y. (2004) Nat. Rev. Mol. Cell. Biol., 5, 897–907.PubMedCrossRefGoogle Scholar
  30. 30.
    Lavrik, I., Golks, A., and Krammer, P. H. (2005) J. Cell Sci., 118, 265–267.PubMedCrossRefGoogle Scholar
  31. 31.
    Varfolomeev, E. E., Schuchmann, M., Luria, V., Chiannilkulchai, N., Beckmann, J. S., Mett, I. L., Rebrikov, D., Brodianski, V. M., Kemper, O. C., Kollet, O., Lapidot, T., Soffer, D., Sobe, T., Avraham, K. B., Goncharov, T., Holtmann, H., Lonai, P., and Wallach, D. (1998) Immunity, 9, 267–276.PubMedCrossRefGoogle Scholar
  32. 32.
    Hockenbery, D., Nunez, G., Milliman, C., Schreiber, R. D., and Korsmeyer, S. J. (1990) Nature, 348, 334–336.PubMedCrossRefGoogle Scholar
  33. 33.
    Boise, L. H., Gonzalez-Garcia, M., Postema, C. E., Ding, L., Lindsten, T., Turka, L. A., Mao, X., Nunez, G., and Thompson, C. B. (1993) Cell, 74, 597–608.PubMedCrossRefGoogle Scholar
  34. 34.
    Adams, J. M., and Cory, S. (1998) Science, 281, 1322–1326.PubMedCrossRefGoogle Scholar
  35. 35.
    Oltvai, Z. N., Milliman, C. L., and Korsmeyer, S. J. (1993) Cell, 74, 609–619.PubMedCrossRefGoogle Scholar
  36. 36.
    Chittenden, T., Harrington, E. A., O’Connor, R., Flemington, C., Lutz, R. J., Evan, G. I., and Guild, B. C. (1995) Nature, 374, 733–736.PubMedCrossRefGoogle Scholar
  37. 37.
    Kiefer, M. C., Brauer, M. J., Powers, V. C., Wu, J. J., Umansky, S. R., Tomei, L. D., and Barr, P. J. (1995) Nature, 374, 736–739.PubMedCrossRefGoogle Scholar
  38. 38.
    Yang, E., Zha, J., Jockel, J., Boise, L. H., Thompson, C. B., and Korsmeyer, S. J. (1995) Cell, 80, 285–291.PubMedCrossRefGoogle Scholar
  39. 39.
    Wang, K., Yin, X. M., Chao, D. T., Milliman, C. L., and Korsmeyer, S. J. (1996) Genes Dev., 10, 2859–2869.PubMedCrossRefGoogle Scholar
  40. 40.
    Chipuk, J. E., and Green, D. R. (2008) Trends Cell Biol., 18, 157–164.PubMedCrossRefGoogle Scholar
  41. 41.
    Riedl, S. J., and Salvesen, G. S. (2007) Nat. Rev. Mol. Cell. Biol., 8, 405–413.PubMedCrossRefGoogle Scholar
  42. 42.
    Zou, H., Henzel, W. J., Liu, X., Lutschg, A., and Wang, X. (1997) Cell, 90, 405–413.PubMedCrossRefGoogle Scholar
  43. 43.
    Liu, X., Kim, C. N., Yang, J., Jemmerson, R., and Wang, X. (1996) Cell, 86, 147–157.PubMedCrossRefGoogle Scholar
  44. 44.
    Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S., and Wang, X. (1997) Cell, 91, 479–489.PubMedCrossRefGoogle Scholar
  45. 45.
    Yuan, S., Yu, X., Topf, M., Ludtke, S. J., Wang, X., and Akey, C. W. (2010) Structure, 18, 571–583.PubMedCrossRefGoogle Scholar
  46. 46.
    Lakhani, S. A., Masud, A., Kuida, K., Porter, G. A., Jr., Booth, C. J., Mehal, W. Z., Inayat, I., and Flavell, R. A. (2006) Science, 311, 847–851.PubMedCrossRefGoogle Scholar
  47. 47.
    Shi, Y. (2002) Mol. Cell, 9, 459–470.PubMedCrossRefGoogle Scholar
  48. 48.
    Wang, S., Miura, M., Jung, Y., Zhu, H., Gagliardini, V., Shi, L., Greenberg, A. H., and Yuan, J. (1996) J. Biol. Chem., 271, 20580–20587.PubMedCrossRefGoogle Scholar
  49. 49.
    Lin, X. Y., Choi, M. S., and Porter, A. G. (2000) J. Biol. Chem., 275, 39920–39926.PubMedCrossRefGoogle Scholar
  50. 50.
    Eckhart, L., Ban, J., Fischer, H., and Tschachler, E. (2000) Biochem. Biophys. Res. Commun., 277, 655–659.PubMedCrossRefGoogle Scholar
  51. 51.
    Cardone, M. H., Roy, N., Stennicke, H. R., Salvesen, G. S., Franke, T. F., Stanbridge, E., Frisch, S., and Reed, J. C. (1998) Science, 282, 1318–1321.PubMedCrossRefGoogle Scholar
  52. 52.
    Allan, L. A., Morrice, N., Brady, S., Magee, G., Pathak, S., and Clarke, P. R. (2003) Nat. Cell. Biol., 5, 647–654.PubMedCrossRefGoogle Scholar
  53. 53.
    Deveraux, Q. L., and Reed, J. C. (1999) Genes Dev., 13, 239–252.PubMedCrossRefGoogle Scholar
  54. 54.
    Fesik, S. W., and Shi, Y. (2001) Science, 294, 1477–1478.PubMedCrossRefGoogle Scholar
  55. 55.
    Shiozaki, E. N., Chai, J., Rigotti, D. J., Riedl, S. J., Li, P., Srinivasula, S. M., Alnemri, E. S., Fairman, R., and Shi, Y. (2003) Mol. Cell, 11, 519–527.PubMedCrossRefGoogle Scholar
  56. 56.
    Chai, J., Shiozaki, E., Srinivasula, S. M., Wu, Q., Datta, P., Alnemri, E. S., and Shi, Y. (2001) Cell, 104, 769–780.PubMedCrossRefGoogle Scholar
  57. 57.
    Yang, Q. H., Church-Hajduk, R., Ren, J., Newton, M. L., and Du, C. (2003) Genes Dev., 17, 1487–1496.PubMedCrossRefGoogle Scholar
  58. 58.
    Srinivasula, S. M., Gupta, S., Datta, P., Zhang, Z., Hegde, R., Cheong, N., Fernandes-Alnemri, T., and Alnemri, E. S. (2003) J. Biol. Chem., 278, 31469–31472.PubMedCrossRefGoogle Scholar
  59. 59.
    Bump, N. J., Hackett, M., Hugunin, M., Seshagiri, S., Brady, K., Chen, P., Ferenz, C., Franklin, S., Ghayur, T., Li, P., et al. (1995) Science, 269, 1885–1888.PubMedCrossRefGoogle Scholar
  60. 60.
    Xue, D., and Horvitz, H. R. (1995) Nature, 377, 248–251.PubMedCrossRefGoogle Scholar
  61. 61.
    Zhou, Q., Snipas, S., Orth, K., Muzio, M., Dixit, V. M., and Salvesen, G. S. (1997) J. Biol. Chem., 272, 7797–7800.PubMedCrossRefGoogle Scholar
  62. 62.
    Drew, M. C., He, C. J., and Morgan, P. W. (2000) Trends Plant Sci., 5, 123–127.PubMedCrossRefGoogle Scholar
  63. 63.
    Gunawardena, A. H. (2008) J. Exp. Bot., 59, 445–451.PubMedCrossRefGoogle Scholar
  64. 64.
    Rubinstein, B. (2000) Plant Mol. Biol., 44, 303–318.PubMedCrossRefGoogle Scholar
  65. 65.
    Fukuda, H. (1996) Annu. Rev. Plant Physiol. Plant Mol. Biol., 47, 299–325.PubMedCrossRefGoogle Scholar
  66. 66.
    Greenberg, J. T. (1996) Proc. Natl. Acad. Sci. USA, 93, 12094–12097.PubMedCrossRefGoogle Scholar
  67. 67.
    Van Doorn, W. G., Beers, E. P., Dangl, J. L., Franklin-Tong, V. E., Gallois, P., Hara-Nishimura, I., Jones, A. M., Kawai-Yamada, M., Lam, E., Mundy, J., Mur, L. A., Petersen, M., Smertenko, A., Taliansky, M., Van Breusegem, F., Wolpert, T., Woltering, E., Zhivotovsky, B., and Bozhkov, P. V. (2011) Cell Death Differ., 18, 1241–1246.PubMedCrossRefGoogle Scholar
  68. 68.
    Curtis, M. J., and Wolpert, T. J. (2004) Plant J., 38, 244–259.PubMedCrossRefGoogle Scholar
  69. 69.
    Dangl, J. L., and Jones, J. D. (2001) Nature, 411, 826–833.PubMedCrossRefGoogle Scholar
  70. 70.
    Lam, E., Kato, N., and Lawton, M. (2001) Nature, 411, 848–853.PubMedCrossRefGoogle Scholar
  71. 71.
    Hammond-Kosack, K. E., and Jones, J. D. (1997) Annu. Rev. Plant Physiol. Plant Mol. Biol., 48, 575–607.PubMedCrossRefGoogle Scholar
  72. 72.
    Hutcheson, S. W. (1998) Annu. Rev. Phytopathol., 36, 59–90.PubMedCrossRefGoogle Scholar
  73. 73.
    Hara-Nishimura, I., and Hatsugai, N. (2011) Cell Death Differ., 18, 1298–1304.PubMedCrossRefGoogle Scholar
  74. 74.
    Hatsugai, N., Kuroyanagi, M., Nishimura, M., and Hara-Nishimura, I. (2006) Apoptosis, 11, 905–911.PubMedCrossRefGoogle Scholar
  75. 75.
    Hatsugai, N., Iwasaki, S., Tamura, K., Kondo, M., Fuji, K., Ogasawara, K., Nishimura, M., and Hara-Nishimura, I. (2009) Genes Dev., 23, 2496–2506.PubMedCrossRefGoogle Scholar
  76. 76.
    Kisselev, A. F., Garcia-Calvo, M., Overkleeft, H. S., Peterson, E., Pennington, M. W., Ploegh, H. L., Thornberry, N. A., and Goldberg, A. L. (2003) J. Biol. Chem., 278, 35869–35877.PubMedCrossRefGoogle Scholar
  77. 77.
    Gu, C., Kolodziejek, I., Misas-Villamil, J., Shindo, T., Colby, T., Verdoes, M., Richau, K. H., Schmidt, J., Overkleeft, H. S., and van der Hoorn, R. A. (2010) Plant J., 62, 160–170.PubMedCrossRefGoogle Scholar
  78. 78.
    Lincoln, J. E., Richael, C., Overduin, B., Smith, K., Bostock, R., and Gilchrist, D. G. (2002) Proc. Natl. Acad. Sci. USA, 99, 15217–15221.PubMedCrossRefGoogle Scholar
  79. 79.
    Del Pozo, O., and Lam, E. (2003) Mol. Plant Microbe Interact., 16, 485–494.PubMedCrossRefGoogle Scholar
  80. 80.
    Hansen, G. (2000) Mol. Plant Microbe Interact., 13, 649–657.PubMedCrossRefGoogle Scholar
  81. 81.
    Danon, A., Rotari, V. I., Gordon, A., Mailhac, N., and Gallois, P. (2004) J. Biol. Chem., 279, 779–787.PubMedCrossRefGoogle Scholar
  82. 82.
    Dickman, M. B., Park, Y. K., Oltersdorf, T., Li, W., Clemente, T., and French, R. (2001) Proc. Natl. Acad. Sci. USA, 98, 6957–6962.PubMedCrossRefGoogle Scholar
  83. 83.
    Shaw, E. (1990) Adv. Enzymol., 63, 271–347.PubMedGoogle Scholar
  84. 84.
    Del Pozo, O., and Lam, E. (1998) Curr. Biol., 8, 1129–1132.PubMedCrossRefGoogle Scholar
  85. 85.
    Uren, A. G., O’Rourke, K., Aravind, L. A., Pisabarro, M. T., Seshagiri, S., Koonin, E. V., and Dixit, V. M. (2000) Mol. Cell, 6, 961–967.PubMedGoogle Scholar
  86. 86.
    Aravind, L., and Koonin, E. V. (2002) Proteins, 46, 355–367.PubMedCrossRefGoogle Scholar
  87. 87.
    Tsiatsiani, L., Van Breusegem, F., Gallois, P., Zavialov, A., Lam, E., and Bozhkov, P. V. (2011) Cell Death Differ., 18, 1279–1288.PubMedCrossRefGoogle Scholar
  88. 88.
    Vercammen, D., van de Cotte, B., De Jaeger, G., Eeckhout, D., Casteels, P., Vandepoele, K., Vandenberghe, I., Van Beeumen, J., Inze, D., and Van Breusegem, F. (2004) J. Biol. Chem., 279, 45329–45336.PubMedCrossRefGoogle Scholar
  89. 89.
    Watanabe, N., and Lam, E. (2011) J. Biol. Chem., 286, 10027–10040.PubMedCrossRefGoogle Scholar
  90. 90.
    Bozhkov, P. V., Filonova, L. H., Suarez, M. F., Helmersson, A., Smertenko, A. P., Zhivotovsky, B., and von Arnold, S. (2004) Cell Death Differ., 11, 175–182.PubMedCrossRefGoogle Scholar
  91. 91.
    Suarez, M. F., Filonova, L. H., Smertenko, A., Savenkov, E. I., Clapham, D. H., von Arnold, S., Zhivotovsky, B., and Bozhkov, P. V. (2004) Curr. Biol., 14, R339–R340.PubMedCrossRefGoogle Scholar
  92. 92.
    Bozhkov, P. V., Suarez, M. F., Filonova, L. H., Daniel, G., Zamyatnin, A. A., Jr., Rodriguez-Nieto, S., Zhivotovsky, B., and Smertenko, A. (2005) Proc. Natl. Acad. Sci. USA, 102, 14463–14468.PubMedCrossRefGoogle Scholar
  93. 93.
    Watanabe, N., and Lam, E. (2005) J. Biol. Chem., 280, 14691–14699.PubMedCrossRefGoogle Scholar
  94. 94.
    Vercammen, D., Belenghi, B., van de Cotte, B., Beunens, T., Gavigan, J. A., De Rycke, R., Brackenier, A., Inze, D., Harris, J. L., and Van Breusegem, F. (2006) J. Mol. Biol., 364, 625–636.PubMedCrossRefGoogle Scholar
  95. 95.
    Vercammen, D., Declercq, W., Vandenabeele, P., and Van Breusegem, F. (2007) J. Cell Biol., 179, 375–380.PubMedCrossRefGoogle Scholar
  96. 96.
    Carmona-Gutierrez, D., Frohlich, K. U., Kroemer, G., and Madeo, F. (2010) Cell Death Differ., 17, 377–378.PubMedCrossRefGoogle Scholar
  97. 97.
    Enoksson, M., and Salvesen, G. S. (2010) Cell Death Differ., 17, 1221.PubMedCrossRefGoogle Scholar
  98. 98.
    He, R., Drury, G. E., Rotari, V. I., Gordon, A., Willer, M., Farzaneh, T., Woltering, E. J., and Gallois, P. (2008) J. Biol. Chem., 283, 774–783.PubMedCrossRefGoogle Scholar
  99. 99.
    Watanabe, N., and Lam, E. (2011) Plant J., 66, 969–982.PubMedCrossRefGoogle Scholar
  100. 100.
    Coll, N. S., Vercammen, D., Smidler, A., Clover, C., Van Breusegem, F., Dangl, J. L., and Epple, P. (2010) Science, 330, 1393–1397.PubMedCrossRefGoogle Scholar
  101. 101.
    Sundstrom, J. F., Vaculova, A., Smertenko, A. P., Savenkov, E. I., Golovko, A., Minina, E., Tiwari, B. S., Rodriguez-Nieto, S., Zamyatnin, A. A., Jr., Valineva, T., Saarikettu, J., Frilander, M. J., Suarez, M. F., Zavialov, A., Stahl, U., Hussey, P. J., Silvennoinen, O., Sundberg, E., Zhivotovsky, B., and Bozhkov, P. V. (2009) Nat. Cell. Biol., 11, 1347–1354.PubMedCrossRefGoogle Scholar
  102. 102.
    Hiraiwa, N., Nishimura, M., and Hara-Nishimura, I. (1999) FEBS Lett., 447, 213–216.PubMedCrossRefGoogle Scholar
  103. 103.
    Kuroyanagi, M., Nishimura, M., and Hara-Nishimura, I. (2002) Plant Cell Physiol., 43, 143–151.PubMedCrossRefGoogle Scholar
  104. 104.
    Hatsugai, N., Kuroyanagi, M., Yamada, K., Meshi, T., Tsuda, S., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2004) Science, 305, 855–858.PubMedCrossRefGoogle Scholar
  105. 105.
    Rojo, E., Martin, R., Carter, C., Zouhar, J., Pan, S., Plotnikova, J., Jin, H., Paneque, M., Sanchez-Serrano, J. J., Baker, B., Ausubel, F. M., and Raikhel, N. V. (2004) Curr. Biol., 14, 1897–1906.PubMedCrossRefGoogle Scholar
  106. 106.
    Kuroyanagi, M., Yamada, K., Hatsugai, N., Kondo, M., Nishimura, M., and Hara-Nishimura, I. (2005) J. Biol. Chem., 280, 32914–32920.PubMedCrossRefGoogle Scholar
  107. 107.
    Bosch, M., Poulter, N. S., Perry, R. M., Wilkins, K. A., and Franklin-Tong, V. E. (2010) Plant Mol. Biol., 74, 381–393.PubMedCrossRefGoogle Scholar
  108. 108.
    Hara-Nishimura, I., Hatsugai, N., Nakaune, S., Kuroyanagi, M., and Nishimura, M. (2005) Curr. Opin. Plant Biol., 8, 404–408.PubMedCrossRefGoogle Scholar
  109. 109.
    Chichkova, N. V., Kim, S. H., Titova, E. S., Kalkum, M., Morozov, V. S., Rubtsov, Y. P., Kalinina, N. O., Taliansky, M. E., and Vartapetian, A. B. (2004) Plant Cell, 16, 157–171.PubMedCrossRefGoogle Scholar
  110. 110.
    Chichkova, N. V., Shaw, J., Galiullina, R. A., Drury, G. E., Tuzhikov, A. I., Kim, S. H., Kalkum, M., Hong, T. B., Gorshkova, E. N., Torrance, L., Vartapetian, A. B., and Taliansky, M. (2010) EMBO J., 29, 1149–1161.PubMedCrossRefGoogle Scholar
  111. 111.
    Chichkova, N. V., Galiullina, R. A., Taliansky, M. E., and Vartapetian, A. B. (2008) Plant Stress, 2, 89–95.Google Scholar
  112. 112.
    Pitzschke, A., and Hirt, H. (2010) EMBO J., 29, 1021–1032.PubMedCrossRefGoogle Scholar
  113. 113.
    Howard, E. A., Zupan, J. R., Citovsky, V., and Zambryski, P. C. (1992) Cell, 68, 109–118.PubMedCrossRefGoogle Scholar
  114. 114.
    Reavy, B., Bagirova, S., Chichkova, N. V., Fedoseeva, S. V., Kim, S. H., Vartapetian, A. B., and Taliansky, M. E. (2007) Plant Cell Rep., 26, 1215–1219.PubMedCrossRefGoogle Scholar
  115. 115.
    Schaller, A. (2004) Planta, 220, 183–197.PubMedCrossRefGoogle Scholar
  116. 116.
    Ottmann, C., Rose, R., Huttenlocher, F., Cedzich, A., Hauske, P., Kaiser, M., Huber, R., and Schaller, A. (2009) Proc. Natl. Acad. Sci. USA, 106, 17223–17228.PubMedCrossRefGoogle Scholar
  117. 117.
    Rautengarten, C., Steinhauser, D., Bussis, D., Stintzi, A., Schaller, A., Kopka, J., and Altmann, T. (2005) PLoS Comput. Biol., 1, e40.PubMedCrossRefGoogle Scholar
  118. 118.
    Tripathi, L. P., and Sowdhamini, R. (2006) BMC Genomics, 7, 200.PubMedCrossRefGoogle Scholar
  119. 119.
    Steiner, D. F. (1998) Curr. Opin. Chem. Biol., 2, 31–39.PubMedCrossRefGoogle Scholar
  120. 120.
    Seidah, N. G., Mayer, G., Zaid, A., Rousselet, E., Nassoury, N., Poirier, S., Essalmani, R., and Prat, A. (2008) Int. J. Biochem. Cell. Biol., 40, 1111–1125.PubMedCrossRefGoogle Scholar
  121. 121.
    Coffeen, W. C., and Wolpert, T. J. (2004) Plant Cell, 16, 857–873.PubMedCrossRefGoogle Scholar
  122. 122.
    Curtis, M. J., and Wolpert, T. J. (2002) Plant J., 29, 295–312.PubMedCrossRefGoogle Scholar
  123. 123.
    Navarre, D. A., and Wolpert, T. J. (1999) Plant Cell, 11, 237–249.PubMedGoogle Scholar
  124. 124.
    Vartapetian, A. B., Tuzhikov, A. I., Chichkova, N. V., Taliansky, M., and Wolpert, T. J. (2011) Cell Death Differ., 18, 1289–1297.PubMedCrossRefGoogle Scholar
  125. 125.
    Chichkova, N. V., Tuzhikov, A. I., Taliansky, M., and Vartapetian, A. B. (2012) Physiol. Plant., 145, 77–84.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2012

Authors and Affiliations

  • A. S. Fomicheva
    • 1
  • A. I. Tuzhikov
    • 2
  • R. E. Beloshistov
    • 1
  • S. V. Trusova
    • 2
  • R. A. Galiullina
    • 2
  • L. V. Mochalova
    • 2
  • N. V. Chichkova
    • 2
  • A. B. Vartapetian
    • 2
    Email author
  1. 1.Faculty of Bioengineering and BioinformaticsLomonosov Moscow State UniversityMoscowRussia
  2. 2.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia

Personalised recommendations