Programmed Cell Death in Plants

Year 2018, Volume: 30 Issue: 1, 61 - 70, 31.03.2018

Filiz Vardar , Fatma Yanık Aslıhan Çetinbaş Genç

https://doi.org/10.7240/marufbd.303836

Abstract

Cell death which is one of the basic characteristics
of both prokaryotic and eukaryotic cells is encountered within the whole
organism. Programmed cell death (PCD) is a genetically controlled mechanism,
allows retired, dysfunctional, overproduced, irregularly developed or
genetically damaged cells to be destroyed safely for organism. It has been
first used in 1964 by Lockshin
and Williams. Animal apoptosis which is best characterized form of
PCD is used first in 1972 by Kerr et al. According to the recent biochemical and molecular studies PCD is
categorized in three basic groups: apoptosis, autophagy and necrosis. Plants do
not undergo apoptotic cell death, and cell death is classified into two groups
as vacuolar and necrotic cell death. In vacuolar cell death, alterations in
nucleus morphology, chromatin condensation, DNA fragmentation, protoplast
condensation, vacuolization, generation of reactive oxygen species, alterations
in the cytoskeleton and caspase like enzymatic activities are observed, as in
animal cells. Necrotic cell death has different features from vacuolar cell
death such as ATP depletion, cell and mitochondria swelling. PCD appears in
different organs and tissues of plants during vegetative-generative organ
development and under biotic-abiotic stress conditions. It occurs during the
development of plants such as regeneration of root cap cells, formation of
tracheal elements, formation of aerenchyma in hydrophytes, trichome
development, leaf senescence, sex determination and male-female organ development.
Biotic stress factors such as virus, bacteria, fungus and abiotic stress
factors such as UV light, drought, salinity, temperature, freezing, flood,
heavy metals, pesticides lead to PCD. Under biotic and abiotic stress factors,
the balance between antioxidant enzymes and generation of reactive oxygen
species (ROS) changes. ROS are free radicals and cause lipid peroxidation,
protein oxidation, nucleic acid damage and enzyme inhibition. These alterations
in the cellular structures lead to oxidative stress. ROS accumulation also
causes caspase-like activities by activating vacuolar processing enzymes,
metacaspases, saspases and phytaspases. These proteolytic enzymes execute cell
death and cut their substrates from specific amino acid residues such as
aspartic acid. PCD can be visualized by light, fluorescence and electron
microscopy. Besides DNA fragmentation during cell death is determined by TUNEL,
comet assay and gel electrophoresis. Moreover, cytoplasmic cytochrome c
identification, caspase like activities and alterations of mitochondrial
membrane potential can be identified by biochemical analyses. Although a lot of
morphological characteristic features are identified, plant cell death is still
not clear with regard to molecular aspects. Molecular
characterization of PCD will lead in the future to a better understanding of
the mechanisms of plant development and stress tolerance for developing high quality
plants.

Keywords

Necrotic cell death, programmed cell death, reactive oxygen species, vacuolar cell death

Bitkilerde Programlı Hücre Ölümü

Abstract

Programlı hücre ölümü (PHÖ) yaşlanmış, görevini yitirmiş, fazla
üretilmiş, düzensiz gelişmiş veya genetik olarak hasarlı hücrelerin, organizma
için güvenli bir şekilde yok edilmesini sağlayan, genetik olarak kontrol altında
olan bir ölüm mekanizmasıdır. PHÖ vejetatif-generatif organ gelişimi sırasında
ve biyotik-abiyotik stres şartları altında bitkilerin farklı organ ve
dokularında görülür. Bitkilerde gelişim sırasında hücre ölümü; kök şapkası
hücrelerinin değişimi, trakeal elementlerin oluşumu, su bitkilerinde
havalandırma parankimasının oluşumu, trikom gelişimi, yaprak senesensi, eşey
belirlenmesi ve üreme organlarının gelişimi sırasında ortaya çıkar. Bunun
yanında virüs, bakteri, mantar gibi biyotik ve UV ışık, kuraklık, tuzluluk,
sıcaklık, donma, sel, ağır metaller, pestisitler gibi birçok abiyotik stres
faktörü bitkilerde PHÖ’e yol açar. Bitkilerdeki PHÖ mekanizması hayvan
hücrelerindekine benzer şekilde nukleus morfolojisindeki değişiklikler,
kromatin yoğunlaşması, DNA fragmentasyonu, protoplastta büzülme, hücre
iskeletinde değişikler ve kaspaz benzeri enzimatik aktiviteler ile gelişir.
Bitkilerdeki PHÖ, vakuoler ve nekrotik hücre ölümü olmak üzere iki gruba
ayrılır. Vakuoler hücre ölümü, hidrolitik enzimleri içeren litik vakuollerin
hacminin artması ve tonoplastın parçalanarak hidrolitik enzimlerin sitoplazmaya
salınması ile gerçekleşir. Nekrotik hücre ölümünde ise hücre ve hücre organelleri
şişer, plazma zarı erken bozulma gösterir. Nekrotik ölümde mitokondri yapısı
bozulduğu için hücre solunumu gerçekleşemez, hücrede reaktif oksijen türleri
artar ve ATP azalır.

Keywords

Nekrotik hücre ölümü, programlı hücre ölümü, reaktif oksijen türleri

References

• [1] Lockshin, R.A., Williams, C.M. (1964). Programmed cell death. II. Endocrine potentiation of the breakdown of the intersegmental muscles of silkmoths. J. Insect Physiol., 10, 643-649.
• [2] Greenberg, J.T. (1996). Programmed cell death: A way of life for plants. PNAS, 93, 12094-12097.
• [3] Bayles, K.W. (2014). Bacterial programmed cell death: Making sense of a paradox. Nat. Rev. Microbiol., 12, 63-69.
• [4] Wang, J., Bayles, K.W. (2013). Programmed cell death in plants: Lessons from bacteria? Trends Plant Sci., 18(3), 133-139.
• [5] Kerr, J.F.R., Wyllie, A.H., Currie, A.R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging ımplications in tissue kinetics. Brit J of Cancer, 26, 239-257.
• [6] Galluzzi, L., Vitale, I., Abrams, J.M., Alnemri, E.S., Baehrecke, E.H., Blagosklonny, M.V., Dawson, T.M., Dawson, V.L., El-Deiry, W.S., Fulda, S., Gottlieb, E., Green, D.R., Hengartner, M.O., Kepp, O., Knight, R.A., Kumar, S., Lipton, S.A., Lu, X., Madeo, F., Malorni, W., Mehlen, P., Nuñez, G., Peter, M.E., Piacentini, M., Rubinsztein, D.C., Shi, Y., Simon, H.U., Vandenabeele, P., White, E., Yuan, J., Zhivotovsky, B., Melino, G., Kroemer, G. (2012). Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ., 19(1), 107-120.
• [7] Green D.R., Galluzzi L., Kroemer G. (2011). Mitochondria and the autophagy–inflammation–cell death axis in organismal aging. Science, 333(6046), 1109-1112.
• [8] Hengartner, M.O. (2000). The biochemistry of apoptosis. Nature, 407, 770-776.
• [9] Elmore, S. (2007). Apoptosis: a review of programmed cell death. Toxicol Pathol, 35(4), 495-516.
• [10] Jacobsen, M.D., Weil, M., Raff, M.C. (1997). Programmed cell death in animal development. Cell, 88, 347-354.
• [11] McCall, K., Steller, H. (1997). Facing death in the fly: Genetic analysis of apoptosis in Drosophila. Trends Genet., 13, 222-226.
• [12] Earnshaw, W.C., Martins, L.M., Kaufmann, S.H. (1999). Mammalian caspases: Structure, activation, substrates and functions during apoptosis. Ann.Rev. Biochem., 68, 383-424.
• [13] Denault, J.B., Salvesen, G.S. (2002). Caspases: Keys in the ignition of cell death. Chem. Rev., 102, 4489-4499.
• [14] Öz-Arslan, D., Korkmaz, G., Gözüaçık, D. (2009). Otofaji: Bir hücresel stres yanıtı ve ölüm mekanizması. Acıbadem Üni. Sağ. Bil. Der., 2, 184-194.
• [15] Ouyang, W., Liao, W., Luo, C.T., Yin, N., Huse, M., Kim, M.V., Peng, M., Chan, P., Ma, Q., Mo, Y., Meijer, D., Zhao, K., Rudensky, A.Y., Atwal, G., Zhang, M.Q., Li, M.O. (2012). Novel foxo1-dependent transcriptional programs control T(reg) cell function. Nature, 22, 491(7425), 554-559.
• [16] Clarke, P.G. (1990). Developmental cell death: Morphological diversity and multiple mechanisms. Anat. Embryol., 181, 195-213.
• [17] Leist, M., Jaattela, M. (2001). Four deaths and a funeral: From caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol., 2(8), 589-98.
• [18] Wu, J.J, Poon, K.Y., Channual, J.C., Shen, A.Y. (2012). Association between tumor necrosis factor inhibitor therapy and myocardial infarction risk in patients with psoriasis. Arch. Dermatol., 148(11), 1244-50.
• [19] McCall, K. (2010). Genetic control of necrosis - another type of programmed cell death. Curr. Opin. Cell Biol., 22(6), 882-888.
• [20] Galluzzi, L., Vitale, I., Kroemer, G. (2011). Cell death signaling and anticancer therapy. Front. Oncol., 1, 1-18.
• [21] Woltering, E.J., Van der Bent, A., Hoeberichts, F.A. (2002). Do plant caspases exist? Plant Physiol., 130, 1764-1769.
• [22] Danon, A., Rotari, V.I., Gordon A., Mailhac N., Gallois, P. (2004). Ultraviolet-C overexposure induces programmed cell death in Arabidopsis which is mediated by caspase-like activities and which can be suppressed by caspase ınhibitors, p35 and defender against apoptotic death. J. Biol. Chem., 279, 779-787.
• [23] 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., Bozhkov, P.V. (2011). Morphological classification of plant cell deaths. Cell Death Differ., 18(8), 1241-1246.
• [24] Gunawardena, A.H. (2008). Programmed cell death and tissue remodelling in plants. J. Exp. Bot, 59(3), 445-51.
• [25] Huang, S., Mira, M.M., Stasolla, C. (2016). Dying with style: Death decision in plant embryogenesis. In: In vitro embryogenesis in higher plants, M.A. Germaná, M. Lambardi, (eds), Springer, NewYork, USA. s. 101-115.
• [26] Fukuda, H.F. (1994). Redifferentiation of single mesophyll cells into tracheary elements. Int. J. Plant Sci., 155, 262-271.
• [27] Smart, C.M. (1994). Gene expression during leaf senescence. New Phytol., 126, 419-448.
• [28] Gan, S., Amasino, R.M. (1997). Inhibition of leaf senescence by autoregulated production of cytokinin. Science, 270, 1986-1988.
• [29] Hülskamp, M. (2004). Plant trichomes: A model for cell differentiation. Nature Rev. Mol. Cell Biol., 5(6), 471-480.
• [30] Vardar, F., Ünal, M. (2012). Ultrastructural aspects and programmed cell death in the tapetal cells of Lathyrus undulatus Boiss. Acta Biol. Hung., 63(1), 52-66.
• [31] Çetinbaş-Genç A. (2016). Türkiye endemiği olan Crataegus tanacetifolia (Lam.) Pers. (Alıç)' in üreme biyolojisinin analizi. Doktora Tezi, Marmara Üniversitesi, Türkiye, s. 106-107.
• [32] Wang, M., Oppedijk, B.J., Lu, X., van Dujin, V., Schilperoort, R.A. (1996). Apoptosis: A functional paradigm for programmed cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell, 8, 375-391.
• [33] Wu, H.M., Cheung, A.Y. (2000). Programmed cell death in plant reproduction. Development, 44, 267-281.
• [34] Wei, C.X., Lan, S.Y., Xu, Z.X. (2002). Ultrastructural features of nucleus degradation during programmed cell death of starchy endosperm cells in rice. Acta Bot. Sin., 44, 1396-1402.
• [35] Van Hautegem, T., Waters, A.J., Goodrich, J., Nowack, M.K. (2015). Only in dying, life: programmed cell death during plant development. Trends Plant Sci., 20: 102-113.
• [36] Van Durme, M., Nowack, M.K. (2016). Mechanisms of developmentally controlled cell death in plants. Curr. Op. Plant Biol., 29, 29-37.
• [37] Drew, M.C., He, C.J., Morgan, P.W. (2000). Programmed cell death and aerenchyma formation in root. Trends Plant Sci., 5, 123-127.
• [38] Ross, A.F. (1961). Systemic acquired resistance induced by localized virus infections in plants. Virology, 14, 340-358.
• [39] Jones, A.M., Dangl, J.L. (1996). Logjam at the styx: Programmed cell death in plants. Trends Plant Sci., 1, 1360-1385.
• [40] Dietrich, R.A., Delaney, T.P., Uknes, S.J., Ward, E.R., Ryals, J.A., Dangl, J.L. (1994). Arabidopsis mutants simulating disease resistance response. Cell, 77, 565-577.
• [41] Smirnoff, N. (1993). The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol., 125, 27-58.
• [42] Sgherry, C.L.M., Pinzino, C., Navari-Izzo, F. (1996). Sunflower seedlings subjected to increasing water stress by water deficit: Changes in O2-production related to the composition of thylakoid membranes. Physiol. Plant, 96, 446-452.
• [43] Büyük, İ., Soydam-Aydın, S., Aras, S. (2012). Bitkilerin stres koşullarına verdiği moleküler cevaplar. Türk Hij. Den. Biy. Der., 69, 2, 97-100.
• [44] Van Breusegem, F., Dat, J. F. (2006). Reactive oxygen species in plant cell death. Plant Physiol., 141, 384-390.
• [45] Levitt, J. (1972). Responses of plants to environmental stresses. New York, London.
• [46] Flora, S. J. (2007). Role of free radicals and antioxidants in health and disease. Cell. Mol. Biol., 53, 1-2.
• [47] Halliwell, B., Gutteridge, J. M. (1990). Role of free radicals and catalytic metal ions in human disease. Methods Enzymol., 186, 1-85.
• [48] Gill, S.S., Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stres tolerance in crop plants. Plant Physiol. Biochem., 48, 909-930.
• [49] Gechev, T. S., Van Breusegem, F., Stone, J. M., Denev, I., Laloi, C. (2006). Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays, 28, 1091-1101.
• [50] Noctor, G., Foyer, C. H. (1998). Ascorbate and glutathione: keeping active oxygen under control. Ann. Rev. Plant Biol., 49, 249-279.
• 51] Zaefyzadeh, M., Quliyev, R., Babayeva, S., Abbasov, M. (2009). The effect of the interaction between genotypes and drought stress on the superoxide dismutase and chlorophyll content in durum wheat landraces. Turk. J. Biol., 33, 1-7.
• [52] Chen, Q., Zhang, M., Shen, S. (2010). Effect of salt on malondialdehyde and antioxidant enzymes in seedling roots of Jerusalem artichoke (Helianthus tuberosus L.). Acta Physiol. Plant., 33, 273-278.
• [53] Apel, K., Hirt, H. (2004).Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Ann. Rev. Plant Biol., 55, 373-399.
• [54] Sharma, P., Jha, A.B., Dubey, R.S., Pessarakli, M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot., Article ID 217037, 26.
• [55] Hatsugai, N., Yamada, K., Goto-Yamada, S., Hara-Nishimura, I. (2015). Vaculolar processing enzyme in plant programmed cell death. Front. Plant Sci., 6, 234.
• [56] Grudkowska, M., Zagdańska, B. (2004). Multifunctional role of plant cysteine proteinases. Acta Biochim. Pol., 51, 609-624.
• [57] Coffeen, W.C., Wolpert, T.J. (2004). Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell, 16, 857-873.
• [58] Del Pozo, O., Lam, E. (1998). Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol., 8(20), 1129-1132.
• [59] 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, 961-967.
• [60] Suarez, M.F., Filonova, L.H., Smertenko, E.I., Clapham, D.H., von Arnold, S., Zhivotovsky, B., Bozhkov, P.V. (2004). Metacaspase dependent programmed cell death is essential for plant embryogenesis. Curr. Biol., 14, 339-340.
• [61] Hatsugai, N., Kuroyanagi, M., Yamada, K., Meshi, T., Tsuda, S., Kondo, M., (2004). A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell eath. Science, 305, 855-858.
• [62] Ayturk, O., Vardar, F. (2014). Aluminum-induced caspase-like activities in some Gramineae species. Adv. Food Sci., 37(2), 71-75.
• [63] Yanik, F., Ayturk, O., Vardar, F. (2017). Programmed cell death evidence in wheat (Triticum aestivum L.) roots induced by aluminum oxide (Al2O3) nanoparticles. Caryologia, http://dx.doi.org/10.1080/00087114.2017.1286126.
• [64] Tsiatsiani, L., van Breusegem, F., Gallois, P., Zavialov, A., Lam, E., Bozhkov, P.V. (2011). Metacaspases. Cell Death Differ., 18, 1279-1288.
• [65] Güleş, Ö., Eren, Ü. (2008). Apoptozun belirlenmesinde kullanılan yöntemler. Y.Y.Ü. Vet. Fak. Der., 2, 73-
• [66] Fidan, A.F. (2005) DNA Hasar tespitinde tek hücre jel elektroforezi. AKU Fen Bil. Der., 8(1), 41-52.
• [67] Vardar, F., Çabuk, E., Aytürk, Ö., Aydın, Y. (2016). Determination of aluminum induced programmed cell death characterized byDNA fragmentation in Gramineae species. Caryologia 69, 111-115
• [68] Yanık, F., Vardar, F. (2015). Toxic effects of aluminum oxide Al2O3 nanoparticleson root growth and development in Triticum aestivum. Water Air Soil Poll., 226, 296-309.
• [70] Panda, S.K., Yamamoto Y., Kondo H., Matsumoto H. (2008). Mitochondrial alterations related to programmed cell death in tobacco cells under aluminum stress. Comptes Rendus Biologies, 331, 597-610.