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Evidences for the presence of caspase-like activities in plants

Year 2011, Volume: 23 Issue: 2, 57 - 69, 04.12.2011

Abstract

Organizing the activation of cell division and cell death in animals and plants may lead a variety of developmental processes for instance determining of cells, tissues and organs.  But, cell death also is used in a number of other processes such as control of cell populations and defense against invading microbes. Beyond the similarities between plant and animal programmed cell death (PCD), the molecular mechanisms underlying the cellular changes in plant remain unclear. In particular there is no indication in plant genomes for genes orthologous to caspases. Proteases not connected to caspases are thought to be related in PCD in plant cells in recent years there are numerous studies showing that caspase inhibitors can suppress cell death in plants. The aim of this review is to focus on recent advances in PCD molecular mechanisms in plants.

References

  • Nagata, S. (2000). Apoptotic DNA fragmentation. Exp. Cell Res., 256, 12-18.
  • Studzinski, G.P. (1999). Overview of Apoptosis. In.: Apoptosis. A Practical Approach.
  • Ed. G.P. Studzinski, Oxford University Press, p. 1-17. Ellis, R.E. and Horvitz, R.H. (1986). Genetic control of programmed cell death in the nematode C. Elegans. Cell, 44, 817-829.
  • Raff, M.C. (1992). Social control on cell survival and cell death. Nature, 356, 397-400.
  • Greenberg, J.T. (1996). Programmed cell death: a way of life for plants. Proc. Natl. Acad. Sci. USA, 93, 12094-12097.
  • Jones, A.M. and Dangl, J.L. (1996). Logjam at Styx:Programmed cell death in plants. Trends Plant Sci., 1, 114-119.
  • Mittler, R., and Lam, E. (1996). Sacrifice in the face of foes: Pathogen- induced programmed cell death in plants. Trends Microbiol., 4, 10–15.
  • Zhivotovsky,. B and Orrenius, S. (2003). Defects in the apoptotic machinery of cancer cells. Role in drug resistance Seminars in Cancer Biology, 13, 125-134.
  • Nicholson, D.W. (1999) Caspase structure, proteolytic substrates, and function during apoptotic cell death” Cell Death Diff., 6,1028–1042 .
  • Lamkanfi, M. Declercq, W. Kalai, M. Saelens X. and Vandenabeele P. (2002). Alice in caspase land. A phylogenetic analysis of caspases from worm to man” Cell Death Differ., 9, –361.
  • Earnshaw WC, Martins LM and Kaufmann SH (1999) Mammalian caspases: structure, activation, substrates and functions during apoptosis. Annu Rev Biochem., 68, 383–424.
  • Palavan-Unsal, N. Buyuktuncer, E.D. and Tufekci, M.A. (2005). Programmed Cell
  • Death in Plants. Journal of Cell and Molecular Biology, 4, 9-23. Dickman, M.B. and Reed, J.C. (2003). Paradigms for Programmed Cell Death in
  • Animals and Plants. In: When Plant Cells Die. Gray, J. Ed. Chapter 2 pp. 26-43. Blackwell Publishing, UK Van Doorn W.G. and Woltering E.J. (2004). Senescence and Programmed Cell Death: substance or semantics? Journal of Experimental Botany, 55, 2147–2153.
  • Rotari, V.I., He, R. and Galloi, P. (2005). Death by proteases in plants: whodunit.
  • Physiol Plantarum, 123, 376–385. Hoeberichts, F.A., Woltering, E.J. (2002). Multiple mediators of plant PCD: interplay of conserved cell death mechanisms and plant-specific regulators” Bioassays, 25, 47–57.
  • Konin, E. V. and Aravind, L.(2002). Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Diff., 9, 394–404.
  • Beers, E.P.,Woffenden, B.J., Zhao, C.(2000). Plant proteolytic enzymes: possible roles during programmed cell death” Plant Mol Biol., 44, 399–415.
  • Woffenden, B.J., Freeman, T.B., Beers, E.P. (1998). Proteasome inhibitors prevent tracheary element differentiation in Zinnia mesophyll cell cultures. Plant Physiol., 118, 419–
  • Groover, A., Jones, A.M. (1999). Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol., 119, 375-378.
  • Sasabe, M., Takeuchi, K., Kamoun, S., Ichinose, Y., Govers, F., Toyoda, K., Shiraishi, T., Yamada, T. (2000). Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture. Eur J Biochem., 267, 5005–5013.
  • Solomon, M., Belenghi, B., Delledonne, M., Menachem, E., Levine, A. (1999). The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell, 11, 431–443.
  • Stennicke, H.R., Salvesen, G.S. (1999). Caspases: preparation and characterization” Methods, 17, 313–319
  • Bozhkov, P.V., Filonova, L.H., Suarez, M.F., Helmersson, A., Smertenko, A.P., Zhivotovsky, B., Von Arnold, S. (2004). VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Diff ., 11, 175–182.
  • Chichkova, N.V., Kim, S.H., Titova, E.S., Kalkum, M., Morozov, V.S., Rubtsov, Y.P., Kalinina, N.O., Taliansky, M.E., Vartapetian, A.B. (2004). A plant caspase-like protease activated during the hypersensitive response. Plant Cell, 16,157–171.
  • Belenghi, B., Romero-Puertas, M. C., Vercammen, D., Brackenier, A., Inze, D., Delledonne, M. and Van Breusegem, F. (2007). Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J. Biol. Chem., 282, 1352-1358.
  • De Jong, A.J., Hoeberichts, F.A., Yakimova, E.T., Maximova, E., Woltering, E.J. (2000)
  • Chemical-induced apoptotic cell death in tomato cells: involvement of caspase-like proteases. Planta, 211, 656-658. Korthout, H.A., Berecki, G., Bruin, W., Van Duijn, B., Wang, M. (2000). The presence and subcellular localization of caspase 3-like proteinases in plant cells. FEBS Lett., 475, 139
  • Sun, Y.L., Zhao, Y., Hong, X., Zhai, Z.H. (1999). Cytochrome c release and caspase activation during menadione-induced apoptosis in plants. FEBS Lett, 462, 317–321.
  • Tian, R., Zhang, G., Yan, C., Dai, Y.: (2000). Involvement of poly(ADP-ribose) polymerase and activation of caspase-3- like protease in heat shock-induced apoptosis in tobacco suspension cells. FEBS Let., 474, 11.
  • D'Silva, I., Poirier, G.G., and Heath, M.C. (1998). Activation of cysteine proteases in cowpea plants during the hypersensitive response: A form of programmed cell death. Exp. Cell Res., 245, 389–399.
  • Hansen G. (2000). Evidence for Agrobacterium-induced apoptosis in maize cells” Mol
  • Plant Microbe Interact., 13, 649–657. Madeo, F. Herker, E. Maldener, C. Wissing, S. Lachelt, S. Herlan, M. Fehr, M. Lauber, K. Sigrist, S.J. Wesselborg, S. Frohlich K.U. (2000). A caspase-related protease regulates apoptosis in yeast. Mol Cell., 9, 911.
  • Suarez, M.F., L.H. Filonova, A. Smertenko, E.I. Savenkov, D.H. Clapham, S. von Arnold, B. Zhivotovsky, and P.V. Bozhkov. (2004). Metacaspase-dependent programmed cell death is essential for plant embryogenesis. Curr. Biol., 14, R339–R340.
  • Vercammen, D.B., Belenghi, B., van de Cotte, T., Beunens, J.-A., Gavigan, R., De Rycke, A., Brackenier, Inzé, D, Harris, J.L. and Van Breusegem, F. (2006). Serpin1 of
  • Arabidopsis thaliana is a suicide inhibitor for metacaspase 9. J. Mol. Bio.,. 364, 625–636. Watanabe, N., Lam, E. (2005). Recent advances in the study of caspase-like proteases and Bax inhibitor-1 in plants: their possible roles as regulators of programmed cell death. Mol Plant Path., 5, 65–70.
  • He, R., Drury ,G.E., Rotari, V.I., Gordon, A., Willer ,M., Tabasum, F., Woltering, E.J., Gallois, P. (2007). Metacaspase-8 modulates programmed cell death induced by UV and H2O2 in Arabidopsis. Journal of Biological Chemistry , 283, 774–783.
  • Bozhkov, P.V., M.F. Suarez, L.H. Filonova, G. Daniel, A.A. Zamyatnin, S. Rodriguez- Nieto Jr., B. Zhivotovsky, and A. Smertenko. (2005). Cysteine protease mcII-Pa executes programmed cell death during plant organogenesis. Proc. Natl. Acad. Sci. USA. 102, 14463–
  • Uren, A.G., O’Rourke, K., Aravind, L., Pisabarro, M.T., Seshagiri, S., Koonin, E.V., Dixit V.M. (2000). Identification of paracaspases and metacaspases. Two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell., 6, 961.
  • Koonin, E.V., and Aravind. L. (2000). Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Diffr., 394–404.
  • Woltering, EJ. (2002). Arie van der Bent and Frank A. Hoeberichts Do Plant Caspases
  • Exist? Plant Physiology, 130, 1764-1769.
  • Woltering, E.J. (2004). Death proteases come alive. Trends Plant Sci., 9, 469–472.
  • Müntz, K., Shutov , A.D., (2002). Legumains and their functions in plants” Trends Plant Sci. , 7, 340–344.
  • Kinoshita, .T, Yamada, K., Hiraiwa ,N., Kondo, M., Nishimura, M., Hara-Nishimura, I. (1999). Vacuolar processing enzyme is up-regulated n the lytic vacuoles of vegetative tissues during senescence and under various stress conditions. Plant J., 19, 43–53.
  • Hayashi, Y., Yamada Shimada, T., Matsushima, R., Nishizawa, N.K., Nishimura, M., Hara-Nishimura, I. (2001). A proteinase-storing body that prepares for cell death or stresses in the epidermal cells of Arabidopsis. Plant Cell Physiol., 42, 894–899.
  • Hatsugai, N., Kuroyanagi, M., Yamada, K., Meshi, T., Tsuda, S., Kondo.M., Nishimura, M., Hara-Nishimura, I. (2004). A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science, 305, 855–858.
  • Meichtry, J., Amrhein, N., Schaller, A. (1999). Characterization of the subtilase gene family in tomato. Lycopersicon esculentum Mill. Plant Molecular Biology, 39, 749–760.
  • Coffeen,W.C., Wolpert, T.J. (2004). Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with PCD in Avena sativa. The Plant Cell, 16, 857–873.
  • Granell, A., Cerco´ s, M., Carbonell, J.(1998). Plant cysteine proteinases in germination and senescence. In: Barrett AJ, Rawlings ND, Woessner JF (Eds) Handbook of Proteolytic
  • Enzymes. Academic Press, London, pp 578–583. Matile, P. (1978). Biochemistry and function of vacuoles. Ann Rev Plant Physiol . 29, –213.
  • Baehrecke, E.H. (2002). How death shapes life during development. Nat Rev Mol Cell Biol., 3, 779–787.
  • Schmid, M., Simpson, D., Giet,l 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.
  • Wan, L., Xia, Q., Qui, X., Selvaraj, G. (2002). Early stages of seed development in
  • Brassica napus: a seed coat-specific cysteine proteinese associated with programmed cell death of the inner integument. Plant .,J 30, 1–10. Balk, J., Leaver, C.J., McCabe, P.F. (1999). Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants” FEBS Lett., 463, 151–154.
  • Xie, Z., Chen, Z. (2000). Harpin-induced hypersensitive cell death is associated with altered mitochondrial functions in tobacco cells. Mol Plant Microbe, Interact., 13, 183–190.
  • Xu, Y., Hanson, M.R. (2000). Programmed cell death during pollination-induced petal senescence in Petunia. Plant Physiol., 122, 1323–1334.
  • Jones A. (2000). Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci., 5, 225–230.
  • Dickman, M.B., Park, Y.K., Oltersdorf ,T., Li, W., Clemente, T., French, R. (2001).
  • Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci USA. 98, 6957–6962.
  • Lam, E., Del Pozo, O., Pontier, D. (1999). BAXing in the hypersensitive response” Trends Plant Sci., 4, 419–421.

Kaspaz benzeri aktivitelerin bitkilerdeki varlığına ilişkin kanıtlar

Year 2011, Volume: 23 Issue: 2, 57 - 69, 04.12.2011

Abstract

Hayvanlarda ve bitkilerde hücre bölünmesi ve ölümü olayları ile ilgili aktivitelerin organizasyonu hücrelerin, dokuların ve organların belirlenmesi gibi farklı olaylara neden olabilir.  Fakat hücre ölümü aynı zamanda hücre sayısının kontrolü ve mikropların saldırısından korunma gibi daha birçok olaylarda kullanılmaktadır. Bitki ve hayvanlarda programlı hücre ölümünde benzerlikler olmasına rağmen bitkilerde meydana gelen hücresel değişikliklerin moleküler mekanizması hala açıklık kazanmamıştır.  Özellikle bitki genomunda kaspazlarla ortoloji gösteren genler belirlenememiştir. Bitkilerdeki programlı hücre ölümü ile ilgili olduğu düşünülen proteazlar kaspazlarla ilişkili değildir. Birçok araştırma kaspaz ket vurucularının bitkilerde programlı hücre ölümünü baskıladığını ortaya koymuştur.  Bu makalenin amacı bitkilerde meydana gelen programlı hücre ölümünün moleküler mekanizmasına ilişkin son gelişmeleri derleyebilmektir.

References

  • Nagata, S. (2000). Apoptotic DNA fragmentation. Exp. Cell Res., 256, 12-18.
  • Studzinski, G.P. (1999). Overview of Apoptosis. In.: Apoptosis. A Practical Approach.
  • Ed. G.P. Studzinski, Oxford University Press, p. 1-17. Ellis, R.E. and Horvitz, R.H. (1986). Genetic control of programmed cell death in the nematode C. Elegans. Cell, 44, 817-829.
  • Raff, M.C. (1992). Social control on cell survival and cell death. Nature, 356, 397-400.
  • Greenberg, J.T. (1996). Programmed cell death: a way of life for plants. Proc. Natl. Acad. Sci. USA, 93, 12094-12097.
  • Jones, A.M. and Dangl, J.L. (1996). Logjam at Styx:Programmed cell death in plants. Trends Plant Sci., 1, 114-119.
  • Mittler, R., and Lam, E. (1996). Sacrifice in the face of foes: Pathogen- induced programmed cell death in plants. Trends Microbiol., 4, 10–15.
  • Zhivotovsky,. B and Orrenius, S. (2003). Defects in the apoptotic machinery of cancer cells. Role in drug resistance Seminars in Cancer Biology, 13, 125-134.
  • Nicholson, D.W. (1999) Caspase structure, proteolytic substrates, and function during apoptotic cell death” Cell Death Diff., 6,1028–1042 .
  • Lamkanfi, M. Declercq, W. Kalai, M. Saelens X. and Vandenabeele P. (2002). Alice in caspase land. A phylogenetic analysis of caspases from worm to man” Cell Death Differ., 9, –361.
  • Earnshaw WC, Martins LM and Kaufmann SH (1999) Mammalian caspases: structure, activation, substrates and functions during apoptosis. Annu Rev Biochem., 68, 383–424.
  • Palavan-Unsal, N. Buyuktuncer, E.D. and Tufekci, M.A. (2005). Programmed Cell
  • Death in Plants. Journal of Cell and Molecular Biology, 4, 9-23. Dickman, M.B. and Reed, J.C. (2003). Paradigms for Programmed Cell Death in
  • Animals and Plants. In: When Plant Cells Die. Gray, J. Ed. Chapter 2 pp. 26-43. Blackwell Publishing, UK Van Doorn W.G. and Woltering E.J. (2004). Senescence and Programmed Cell Death: substance or semantics? Journal of Experimental Botany, 55, 2147–2153.
  • Rotari, V.I., He, R. and Galloi, P. (2005). Death by proteases in plants: whodunit.
  • Physiol Plantarum, 123, 376–385. Hoeberichts, F.A., Woltering, E.J. (2002). Multiple mediators of plant PCD: interplay of conserved cell death mechanisms and plant-specific regulators” Bioassays, 25, 47–57.
  • Konin, E. V. and Aravind, L.(2002). Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Diff., 9, 394–404.
  • Beers, E.P.,Woffenden, B.J., Zhao, C.(2000). Plant proteolytic enzymes: possible roles during programmed cell death” Plant Mol Biol., 44, 399–415.
  • Woffenden, B.J., Freeman, T.B., Beers, E.P. (1998). Proteasome inhibitors prevent tracheary element differentiation in Zinnia mesophyll cell cultures. Plant Physiol., 118, 419–
  • Groover, A., Jones, A.M. (1999). Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol., 119, 375-378.
  • Sasabe, M., Takeuchi, K., Kamoun, S., Ichinose, Y., Govers, F., Toyoda, K., Shiraishi, T., Yamada, T. (2000). Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture. Eur J Biochem., 267, 5005–5013.
  • Solomon, M., Belenghi, B., Delledonne, M., Menachem, E., Levine, A. (1999). The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell, 11, 431–443.
  • Stennicke, H.R., Salvesen, G.S. (1999). Caspases: preparation and characterization” Methods, 17, 313–319
  • Bozhkov, P.V., Filonova, L.H., Suarez, M.F., Helmersson, A., Smertenko, A.P., Zhivotovsky, B., Von Arnold, S. (2004). VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Diff ., 11, 175–182.
  • Chichkova, N.V., Kim, S.H., Titova, E.S., Kalkum, M., Morozov, V.S., Rubtsov, Y.P., Kalinina, N.O., Taliansky, M.E., Vartapetian, A.B. (2004). A plant caspase-like protease activated during the hypersensitive response. Plant Cell, 16,157–171.
  • Belenghi, B., Romero-Puertas, M. C., Vercammen, D., Brackenier, A., Inze, D., Delledonne, M. and Van Breusegem, F. (2007). Metacaspase activity of Arabidopsis thaliana is regulated by S-nitrosylation of a critical cysteine residue. J. Biol. Chem., 282, 1352-1358.
  • De Jong, A.J., Hoeberichts, F.A., Yakimova, E.T., Maximova, E., Woltering, E.J. (2000)
  • Chemical-induced apoptotic cell death in tomato cells: involvement of caspase-like proteases. Planta, 211, 656-658. Korthout, H.A., Berecki, G., Bruin, W., Van Duijn, B., Wang, M. (2000). The presence and subcellular localization of caspase 3-like proteinases in plant cells. FEBS Lett., 475, 139
  • Sun, Y.L., Zhao, Y., Hong, X., Zhai, Z.H. (1999). Cytochrome c release and caspase activation during menadione-induced apoptosis in plants. FEBS Lett, 462, 317–321.
  • Tian, R., Zhang, G., Yan, C., Dai, Y.: (2000). Involvement of poly(ADP-ribose) polymerase and activation of caspase-3- like protease in heat shock-induced apoptosis in tobacco suspension cells. FEBS Let., 474, 11.
  • D'Silva, I., Poirier, G.G., and Heath, M.C. (1998). Activation of cysteine proteases in cowpea plants during the hypersensitive response: A form of programmed cell death. Exp. Cell Res., 245, 389–399.
  • Hansen G. (2000). Evidence for Agrobacterium-induced apoptosis in maize cells” Mol
  • Plant Microbe Interact., 13, 649–657. Madeo, F. Herker, E. Maldener, C. Wissing, S. Lachelt, S. Herlan, M. Fehr, M. Lauber, K. Sigrist, S.J. Wesselborg, S. Frohlich K.U. (2000). A caspase-related protease regulates apoptosis in yeast. Mol Cell., 9, 911.
  • Suarez, M.F., L.H. Filonova, A. Smertenko, E.I. Savenkov, D.H. Clapham, S. von Arnold, B. Zhivotovsky, and P.V. Bozhkov. (2004). Metacaspase-dependent programmed cell death is essential for plant embryogenesis. Curr. Biol., 14, R339–R340.
  • Vercammen, D.B., Belenghi, B., van de Cotte, T., Beunens, J.-A., Gavigan, R., De Rycke, A., Brackenier, Inzé, D, Harris, J.L. and Van Breusegem, F. (2006). Serpin1 of
  • Arabidopsis thaliana is a suicide inhibitor for metacaspase 9. J. Mol. Bio.,. 364, 625–636. Watanabe, N., Lam, E. (2005). Recent advances in the study of caspase-like proteases and Bax inhibitor-1 in plants: their possible roles as regulators of programmed cell death. Mol Plant Path., 5, 65–70.
  • He, R., Drury ,G.E., Rotari, V.I., Gordon, A., Willer ,M., Tabasum, F., Woltering, E.J., Gallois, P. (2007). Metacaspase-8 modulates programmed cell death induced by UV and H2O2 in Arabidopsis. Journal of Biological Chemistry , 283, 774–783.
  • Bozhkov, P.V., M.F. Suarez, L.H. Filonova, G. Daniel, A.A. Zamyatnin, S. Rodriguez- Nieto Jr., B. Zhivotovsky, and A. Smertenko. (2005). Cysteine protease mcII-Pa executes programmed cell death during plant organogenesis. Proc. Natl. Acad. Sci. USA. 102, 14463–
  • Uren, A.G., O’Rourke, K., Aravind, L., Pisabarro, M.T., Seshagiri, S., Koonin, E.V., Dixit V.M. (2000). Identification of paracaspases and metacaspases. Two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol Cell., 6, 961.
  • Koonin, E.V., and Aravind. L. (2000). Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Diffr., 394–404.
  • Woltering, EJ. (2002). Arie van der Bent and Frank A. Hoeberichts Do Plant Caspases
  • Exist? Plant Physiology, 130, 1764-1769.
  • Woltering, E.J. (2004). Death proteases come alive. Trends Plant Sci., 9, 469–472.
  • Müntz, K., Shutov , A.D., (2002). Legumains and their functions in plants” Trends Plant Sci. , 7, 340–344.
  • Kinoshita, .T, Yamada, K., Hiraiwa ,N., Kondo, M., Nishimura, M., Hara-Nishimura, I. (1999). Vacuolar processing enzyme is up-regulated n the lytic vacuoles of vegetative tissues during senescence and under various stress conditions. Plant J., 19, 43–53.
  • Hayashi, Y., Yamada Shimada, T., Matsushima, R., Nishizawa, N.K., Nishimura, M., Hara-Nishimura, I. (2001). A proteinase-storing body that prepares for cell death or stresses in the epidermal cells of Arabidopsis. Plant Cell Physiol., 42, 894–899.
  • Hatsugai, N., Kuroyanagi, M., Yamada, K., Meshi, T., Tsuda, S., Kondo.M., Nishimura, M., Hara-Nishimura, I. (2004). A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science, 305, 855–858.
  • Meichtry, J., Amrhein, N., Schaller, A. (1999). Characterization of the subtilase gene family in tomato. Lycopersicon esculentum Mill. Plant Molecular Biology, 39, 749–760.
  • Coffeen,W.C., Wolpert, T.J. (2004). Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with PCD in Avena sativa. The Plant Cell, 16, 857–873.
  • Granell, A., Cerco´ s, M., Carbonell, J.(1998). Plant cysteine proteinases in germination and senescence. In: Barrett AJ, Rawlings ND, Woessner JF (Eds) Handbook of Proteolytic
  • Enzymes. Academic Press, London, pp 578–583. Matile, P. (1978). Biochemistry and function of vacuoles. Ann Rev Plant Physiol . 29, –213.
  • Baehrecke, E.H. (2002). How death shapes life during development. Nat Rev Mol Cell Biol., 3, 779–787.
  • Schmid, M., Simpson, D., Giet,l 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.
  • Wan, L., Xia, Q., Qui, X., Selvaraj, G. (2002). Early stages of seed development in
  • Brassica napus: a seed coat-specific cysteine proteinese associated with programmed cell death of the inner integument. Plant .,J 30, 1–10. Balk, J., Leaver, C.J., McCabe, P.F. (1999). Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants” FEBS Lett., 463, 151–154.
  • Xie, Z., Chen, Z. (2000). Harpin-induced hypersensitive cell death is associated with altered mitochondrial functions in tobacco cells. Mol Plant Microbe, Interact., 13, 183–190.
  • Xu, Y., Hanson, M.R. (2000). Programmed cell death during pollination-induced petal senescence in Petunia. Plant Physiol., 122, 1323–1334.
  • Jones A. (2000). Does the plant mitochondrion integrate cellular stress and regulate programmed cell death? Trends Plant Sci., 5, 225–230.
  • Dickman, M.B., Park, Y.K., Oltersdorf ,T., Li, W., Clemente, T., French, R. (2001).
  • Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc Natl Acad Sci USA. 98, 6957–6962.
  • Lam, E., Del Pozo, O., Pontier, D. (1999). BAXing in the hypersensitive response” Trends Plant Sci., 4, 419–421.
There are 61 citations in total.

Details

Primary Language English
Journal Section Research Articles
Authors

Narcin Palavan-unsal

E. Damla Arısan This is me

Publication Date December 4, 2011
Published in Issue Year 2011 Volume: 23 Issue: 2

Cite

APA Palavan-unsal, N., & Arısan, E. D. (2011). Evidences for the presence of caspase-like activities in plants. Marmara Fen Bilimleri Dergisi, 23(2), 57-69. https://doi.org/10.7240/mufbed.99746
AMA Palavan-unsal N, Arısan ED. Evidences for the presence of caspase-like activities in plants. MFBD. December 2011;23(2):57-69. doi:10.7240/mufbed.99746
Chicago Palavan-unsal, Narcin, and E. Damla Arısan. “Evidences for the Presence of Caspase-Like Activities in Plants”. Marmara Fen Bilimleri Dergisi 23, no. 2 (December 2011): 57-69. https://doi.org/10.7240/mufbed.99746.
EndNote Palavan-unsal N, Arısan ED (December 1, 2011) Evidences for the presence of caspase-like activities in plants. Marmara Fen Bilimleri Dergisi 23 2 57–69.
IEEE N. Palavan-unsal and E. D. Arısan, “Evidences for the presence of caspase-like activities in plants”, MFBD, vol. 23, no. 2, pp. 57–69, 2011, doi: 10.7240/mufbed.99746.
ISNAD Palavan-unsal, Narcin - Arısan, E. Damla. “Evidences for the Presence of Caspase-Like Activities in Plants”. Marmara Fen Bilimleri Dergisi 23/2 (December 2011), 57-69. https://doi.org/10.7240/mufbed.99746.
JAMA Palavan-unsal N, Arısan ED. Evidences for the presence of caspase-like activities in plants. MFBD. 2011;23:57–69.
MLA Palavan-unsal, Narcin and E. Damla Arısan. “Evidences for the Presence of Caspase-Like Activities in Plants”. Marmara Fen Bilimleri Dergisi, vol. 23, no. 2, 2011, pp. 57-69, doi:10.7240/mufbed.99746.
Vancouver Palavan-unsal N, Arısan ED. Evidences for the presence of caspase-like activities in plants. MFBD. 2011;23(2):57-69.

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