Bitkilerde Aktif Oksijen Türleri ve Oksidatif Stres

Yıl 2020, Cilt: 3 Sayı: 2, 205 - 226, 15.08.2020

Ali Doğru

https://doi.org/10.38001/ijlsb.691600

Cited By: 3

Öz

Aerobik organizmalar için oksijen vazgeçilmez
bir moleküldür. Biyotik ve abiyotik stres faktörleri altında bitkilerde elektron
taşınımı ile ilgili reaksiyonlar aktif oksijen türlerinin oluşum hızını
artırır. Bu reaksiyonlarda elektronlar stres faktörlerinin etkisiyle asıl hedef
molekül yerine oksijene verilir. Bu şekilde başlayan zincirleme reaksiyonlar
bitki dokularında süperoksit radikali, hidrojen peroksit ve hidroksil radikali
gibi aktif oksijen türlerinin birikim göstermeye başlamasına yol açar.
Antioksidant sistemin yeterince aktive edilememesi durumunda oldukça reaktif
olan aktif oksijen türleri hücresel bileşenlere zarar vermeye başlar. Bu olay
oksidatif stres olarak bilinir. Aktif oksijen türleri bitki hücrelerindeki
birçok organelde oluşabilir. Kloroplastlar bitki hücrelerinde aktif oksijen
türlerini oluşturma kapasitesi bakımından en aktif organellerdir. Bunun dışında
mitokondriler, peroksizomlar, endoplazmik retikulum gibi organellerle
apoplastik bölgede de aktif oksijen oluşumu gözlenir. Stres koşulları altında
sekonder bir stres olarak ortaya çıkan oksidatif stres tarımsal verimliliği
tehdit eden en önemli faktör olarak kabul edilmektedir. Bu derlemede bitki
hücrelerinde aktif oksijen türlerinin oluşumuna neden olan metabolik olaylar,
bu bileşiklerin kimyasal özellikleri ve oksidatif hasar oluşturma mekanizmaları
tartışılmıştır. 

Anahtar Kelimeler

Aktif oksijen türleri, Bitki, Oksidatif stress

Active Oxygen Species and Oxidative Stress in Plants

Öz

Oxygen has been an indispensable molecule for
aerobic organisms. The reactions related to electron transport in plants under
biotic and abiotic stress factors may cause acceleration of the formation rate
of active oxygen species. In these reactions, electrons are delivered to the
oxygen instead of main target molecule as the result of stressful conditions.
Thus, a chain reaction starts and this leads to the accumulation of the active
oxygen species in plant tissues, such as superoxide, hydrogen peroxide and
hydroxyl radical. In the case of lower antioxidant activity, active oxygen
species begin to be harmful to cell components, which is known as oxidative
stress. Active oxygen species may be produced in several cell compartments in
plant cells. Chloroplasts, for example, are known to have the highest potential
to produce active oxygen species in plant cells. In addition, mitochondria,
peroxisomes, endoplasmic reticulum and apoplast are included in the formation
of active oxygen species in plants. Oxidative stress, which appears secondary
stress under stressful conditions, has been accepted as the most serious threat
for agricultural productivity. In this review, metabolic reactions leading to
the formation of active oxygen species in plants, the chemistry of these
reactive compounds and their mechanism to produce oxidative stress are
discussed.

Anahtar Kelimeler

Active oxygen species, Plant, oxidative stress

Kaynakça

• [1] Halliwell, B., Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology, 141, 2, 312-322 (2006).
• [2] Alscher, R.G., Donahue, J.L., Cramer, C.L., Reactive oxygen species and antioxidants: relationship in green cells. Physiologia Plantarum, 100, 2, 224-233, (1997).
• [3] Dat, J., San, S., Vandenabeele, E. Vranova, M. Van Montagu, D. Inze, F. Van Breusegem, Dual action of the active oxygen species during plant stress response. Cell and Molecular Life Science, 57, 5, 779-795, (2000).
• [4] Bray, E.A., Bailey-Serres, J., Weretylnik, E., Biochemistry and Molecular Biology of Plants, 1. Baskı, American Society of Plant Physiologists, (2000).
• [5] Öncel, I., Keleş, Y., Üstün A.S., Interactive effects of temperature and heavy metal stress on the growth and some biochemical compounds in wheat seedlings. Environmental Pollution, 107, 3, 35-320, (2000).
• [6] del Rio, L.A., Sandalio, L.M., Corpas, F.J., Palma, J.M., Barroso, J.B., Activated oxygen-mediated metabolic functions of leaf peroxisomes. Plant Physiology, 104, 4, 673-680, (2006).
• [7] Navrot, N., Rouhier, N., Gelhaye, E., Jaquot, J.P., Reactive oxygen species generation and antioxidant systems in plant mitochondria. Plant Physiology, 129, 1, 185-195, (2007).
• [8] Foyer, C.H., Noctor, G., Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell,17, 1866-1875, (2005).
• [9] Bhattachrjee, S., Reactive oxygen species and oxidative burst: roles in stress senescence and signal transduction in plants. Current Science, 89, 7, 1113-1121, (2005).
• [10] Mittler, R., Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7, 9, 405-410, (2002).
• [11] Apel, K., Hirt, H., Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology, 55, 373-399, (2004).
• [12] Khan, N.A., Singh, S., Abiotic Stress and Plant Responses, 1. Baskı, IK International, (2008).
• [13] Canavar, S., Bazı arpa (Hordeum vulgare L.) genotiplerinde tuz toleransının fizyolojik ve biyokimyasal olarak araştırılması. Yüksek Lisans Tezi, Biyoloji Bölümü, Sakarya Üniversitesi, Sakarya, Türkiye, 2018.
• [14] Guido, V., Fundamentals of physics and chemistry of atmosphere, 1. Baskı, Springer, (2001).
• [15] Demidchik, V., Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. Environmental and Experimental Botany, 109, 212-228, (2015).
• [16] Renda, A., Fenner, Y., Gibson, B.K., Karakas, A.I., Lattanzio, J.C., Campbell, S., Chieffi, A., Cunha, K., Smith, V.V., On the origin of fluorine in milky way. Monthly Notices of Royal Astronomy Society, 354, 575-580, (2004).
• [17] Dowling, D. K., Simmons, L.W., Reactive oxygen species as universal constraints in life-history evolution. Proceeding of the Royal Society Part B Biological Science, 276, 1737-1745, (2009).
• [18] Salin, M.L., Toxic oxygen species and protective systems of the chloroplast. Physiologia Plantarum ,72, 681-689, (1987).
• [19] Edrewa, A., Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approaches. Agriculture, Ecosyststem and Environment ,106, 119-133, (2005).
• [20] Vranova, E., Van Breusegem, F., Dat, J., Belles-Boix, E., Inze, D., Plant Signal Transduction, 1. Baskı, Oxford University Press, (2003).
• [21] Doğru, A., Kolzanın (Brassica napus L. ssp. oleifera) bazı kışlık çeşitlerinde düşük sıcaklık toleransı ile ilgili fizyolojik ve biyokimyasal parametrelerin araştırılması. Doktora Tezi, Biyoloji Bölümü, Hacettepe Üniversitesi, Ankara, Türkiye, (2006).
• [22] Hippeli, S., Heiser, I., Elstner, E.F., Activated oxygen and free oxygen radicals in pathology: new insight and analogies between animals and plants. Plant Physiology and Biochemistry, 37, 167-178, (1999).
• [23] Niyogi, K.K., Photoprotection revisited: geneic and molecular approaches. Annual Review of Plant Physiology and Molecular Biology, 50, 333-359, (1999).
• [24] Kavdia, M., A computational madel for free radicals transport in the microcirculation. Antioxidant Redox Signal, 8, 1103-1111, (2006).
• [25] Halliwell, B., Gutteridge, J.M.C., Free radicals in biology and medicine, 1. Baskı, Oxford University Press, (1999).
• [26] Smirnoff, N., The role of active oxygen in the response of plants to water deficit and desiccaiton. New Phytologist, 125, 27-58, (1993).
• [27] Lesser, M.P., Oxidative stress in marine environments: biochemistry and physiological ecology. Annual Review of Physiology, 68, 253-278, (2006).
• [28] Moller, I.M., Jensen, P.E., Hannson, A., Oxidative modifications to cellular components in plants. Annual Review of Plant Biology, 58, 459-481, (2007).
• [29] Rinalducci, S., Murgiano, L., Zolla, L., Redox proteomics: basic principles and further perspectives for the detection of protein oxidation in plants. Journal of Experimental Botany, 59, 3781-3801, (2008).
• [30] Takahashi, S., Badger, M.R., Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science, 16, 53-60, (2011).
• [31] Moller, I.M., Plant mitochondria and oxidative stress. Electron transport, NADPH turnover and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 561-591, (2001).
• [32] Asada, K., Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology, 141, 391-396, (2006).
• [33] Pospisil, P., Arato, A., Krieger-Liszkay, A., Rutherford, A.W., Hydroxyl radical generation by photosystem II. Biochemistry, 43, 6783-6792, (2004).
• [34] Hirst, J., King, M.S., Pryde, K.R., The production of reactive oxygen species by complex I. Biochemical Society Transaction, 36, 976-980, (2008).
• [35] Ananyev, G.M., Renger, G., Wacker, U., Klimov, V.V., The production of superoxide radicals and the superoxide dismutase activityof photosystem II. The possible involvement of cytochrome b559. Photosynthesis Research, 41, 327-338, (1994).
• [36] Cleland, R.E., Grace, S.C., Voltammetric detection of superoxide production by photosystem II. FEBS Letter, 457, 348-352, (1999).
• [37] Pospisil, P., Snyrychova, I., Kruk, J., Strzalka, K., Naus, J., Evidence that cytochrome b559 is involved in superoxide production in photosystem II. Effect of synthetic short-chain plastoquinones in a cytochrome b559 tobacco mutant. Biochemical Journal, 397, 321-327, (2006).
• [38] Chen, G.X., Kazimir, J., Cheniae, G.M., Photoinhibition of hydroxylamine-extracted photosystem II membranes: studies of the mechanism. Biochemistry, 31, 11072-11083, (1992).
• [39] Chen, G.X., Blubaugh, D.J., Homann, P.H., Goldbeck, J.G., Cheniae, G.M., Superoxide contributes to the rapid inactivation of spesific secondary donors of the photosystem II reaction center during photodamage of manganese-depleted photosystem II membranes. Biochemistry, 34, 2317-2332, (1995).
• [40] Foyer, C. H., Noctor, G., Redox regulation in photosynthetic organisms: signaling, acclimation and practical implications. Antioxidant Redox Signal, 11, 861-710, (2009).
• [41] Asada, K., The water-water cycle in chloroplasts: scavenging of active oxygen species and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 601-639, (1999).
• [42] Reumann, S., Weber, A.P.M., Plant peroxisomes respire in the light: Some gaps of the photorespiratory C2 cycle have become filled. Biochimica et Biophysica Acta, 1763, 1496-1510, (2006).
• [43] del Rio, L.A., Corpas, F.J., Sandalio, L.M., Palma, J.M., Gomez, M., Barroso, J.B., Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. Journal of Experimental Botany, 53, 1255-1272, (2002).
• [44] Lopez-Huertas, E., Charlton, W.L., Johnson, B., Graham, L.A., Baker, A., Stress induces peroxisomes biogenesis genes. EMBO Journal, 19, 6770-6777, (2000).
• [45] Hernandez, J.A., Ferrer, M.A., Jimenez, A., Barcelo, A.R., Sevilla, F., Antioxidant systems and O2.-/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiology, 127, 817-831, (2001).
• [46] Mhamdi, A., Noctor, G., Baker, A., Plant catalases: peroxisomal redox gurdians. Archieves of Biochemistry and Biophysics, 15, 181-194, (2012).
• [47] Dynowsky, M., Schaaf, G., Loque, D., Moran, O., Ludewig, U., Plant plasma membrane water channels conduct the signaling molecule H2O2. Biochemical Journal, 414, 53-61, (2008).
• [48] Bolwell, G.P., Wojtazsek, P., Mechanisms for the generation of reactive oxygen species in plant defence-a broad perspective. Physiological and Molecular Plant Pathology, 51, 347-366, (1997).
• [49] Bindschedler, L.V., Dewdney, J., Blee, K.A., Stone, J.M., Asai, T., Plotnikov, J., Denoux, C., Hayes, T., Gerrish, C., Davies, D.R., Ausubel, F.M., Bolwell, G.P., Peroxidase-dependent apoplastic oxidative burst in Arabidopsis requirred for pathogen resistance. Plant Journal, 47, 851-863, (2006).
• [50] Rodriguez, A.A., Grunberg, K.A., Taleisnik, E., Reactive oxygen species in the elongation zone of maize leaves are necessary for leaf extension. Plant Physiology, 129, 1627-1632, (2002).
• [51] Rodriguez, A.A., Lascano, R., Bustos, D., Taleisnik, E., Salinity-induced decrease in NADPH oxidase activity in the maize leaf blade elongation zone. Journal of Plant Physiology, 164, 223-230, (2007).
• [52] Chang, C.C.C., Slesak, I., Jorda, L., Sotnikov, A., Melzer, M., Miszalski, Z., Mullineaux, P.M., Parker, J.E., Karpinska, B., Karpinski, S., Arabidopsis chloroplastic glutathione peroxidase play a role in crosstalk between photooxidative stress and immune response. Plant Physiology, 150, 670-683, (2009).
• [53] Fry, S.C., Miller, J.G., Dumville, J.C., A proposed role of copper ions in cell wall loosening. Plant and Soil, 247, 57-67, (2002).
• [54] Fry, S.C., Primary cell wall metabolism: tracking the careers of the wall polymers in living plant cells. New Phytologist, 161, 641-675, (2004).
• [55] Demidchik, V., Shabala, S.N., Coutts, K.B., Tester, M.A., Davies, J.M., Free oxygen radicals regulate plasma membrane Ca+2- and K+ permeable channels in plant root cells. Journal of Cell Science, 116, 81-88, (2003).
• [56] Demidchik, V., Reactive oxygen species, oxidative stress and plant ion channels, 1. Baskı, Springer-Verlag, (2010).
• [57] Sies, H., Strategies of antioxidant defence. European Journal of Biochemistry, 215, 213-219, (1993).
• [58] Fenton, H.J.H., Oxidation of tartaric acid in presence of iron. Journal of Chemical Society Transactions, 65, 899-911, (1894).
• [59] Goldstein, S., Meyerstein, D., Czapski, G., The Fenton reagents. Free Radical Biology and Medicine, 15, 435-445, (1993).
• [60] Koppenol, W.H., The Haber-Weiss cycle-70 years later. Redox Reports, 6, 229-234, (2001).
• [61] Haber, F., Weiss, J., On the catalysis of hydroperoxide. Naturwissenschaften, 20, 948-950, (1932).
• [62] Jain, K., Kataria, S., Guruprasad, K.N., Oxyradicals under UV-B stress and their quenching by antioxidant. Journal of Experimental Biology, 42, 884-892, (2004).
• [63] Kataria, S., Jain, K., Guruprasad, K.N., Involvement of oxyradicals in promotion/imhibition of expansion growth in cucumber cotyledons. Journal of Experimental Biology, 43, 910-915, (2005).
• [64] Sersen, F., Kralova, K., EPR spectroscopy-a valuable tool to study photosynthesizing organisms exposed to abiotic stresses, 1. Baskı, Intech, (2013).
• [65] Snyrychova, I., Pospisil, P., Naus, J., Reaction pathways involved int he production of hydroxyl radicals in the thylakoid membrane: EPR spin-trapping study. Photochemical and Photobiologic Science, 5, 472-476, (2006).
• [66] Pospisil, P., Production of reactive oxygen species by photosystem II. Biochimica et Biophysica Acta-Bioenergetics, 1787, 1151-1160, (2009).
• [67] Schweitzer, C., Schmidt, R., Physical mechanisms of generation and deactivation of singlet oxygen. Chemical Reviews, 103, 1685-1757, (2003).
• [68] Trebst, A., Depka, B., Role of carotene in the rapid turnover and assembly of photosystem II in Chlamydomonas reinhardtii. FEBS Letter, 400, 359-362, (1997).
• [69] Kruk, J., Trebst, A., Plastoquinol as a singlet oxygen scavenger in photosystem II. Biochimica et Biophysica Acta-Bioenergetics, 1777, 154-162, (2008).
• [70] Fischer, B.B., Hideg, E., Krieger-Liszkay, A., Production, detection, and signaling of singlet oxygen in photosyhtetic organisms. Antioxidant Redox Signaling, 18, 2145-2162, (2013).
• [71] Fornazari, M., de Paula, J.G., Castilho, R.F., Kowaltowski, A.J., Redox properties of the adenoside triphosphate sensitive K+ channel in brain mitochondria. Journal of Neuroscience Research, 86, 1548-1556, (2008).
• [72] Pryzybla, D., Göbel, C., Imboden, A., Hamberg, M., Feussner, I., Apel, K., Enzymatic, but not non-enzymatic 1O2-mediated peroxidation of polyunsaturated fatty acids forms part of the EXECUTER1-dependent stress response program in the flu mutant of Arabidopsis thaliana. Plant Journal, 54, 236-248, (2008).
• [73] Krasnovsky, A.A.J., Singlet molecular oxygen in photobiochemical systems: IR phosphorescence studies. Membrane Cell Biology, 12, 665-690, (1998).
• [74] Flors, C., Fryer, M.J., Waring, J., Reeder, B., Bechtold, U., Mullineaux, P.M., Nonell, S., Wilson, M.T., Baker, N.R., Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green (R.). Journal of Experimental Botany, 57, 1725-1734, (2006).
• [75] Driever, S.M., Fryer, M.J., Mullineaux, P.M., Baker, N.R., Imaging of reactive oxygen species in vivo. Methods in Molecular Biology, 479, 109-116, (2009).
• [76] Farmer, E.E., Mueller, M.J., ROS mediated lipid peroxidation and RES-activated signaling. Annual Review of Plant Biology, 64, 429-450, (2013).
• [77] Catala, A., An overwiev of lipid peroxidation with emphasis in outer segments of phptpreceptors ant the chemiluminescence assay. International Journal of Biochemistry and Cell Biology, 38, 1482-1495, (2006).
• [78] Krieger-Liszkay, A., Fufezan, C., Trebst, A., Singlet oxygen production in photosystem II and related protection mechanisms. Photosynthesis Research, 98, 551-564, (2008).
• [79] Moller, L.M., Jensen, P.E., Hansson, A., Oxidative modifications to cellular components in plants. Annual Review of Plant Biology, 58, 459-481, (2007).
• [80] Avery, S.V., Molecular targets of oxidative stress. Biochemical Journal, 434, 201-210, (2011).
• [81] Shacter, E., Quantification and sifnificance of protein oxidation in biological samples. Drug Metabolism Reviews, 32, 307-326, (2000).
• [82] Bechtold, U., Murphy, D.J., Mullineaux, P.M., Arabidopsis peptide methionine sulfoxide reductase prevents cellular oxidative damage in long nights. Plant Cell, 16, 908-919, (2004).
• [83] Onda, Y., Oxidative protein-folding systems in plant cells. International Journal of Cell Biology, 585, 431-446, (2013).
• [84] Cecarini, V., Gee, J., Fioretti, E., Amici, M., Angeletti, M., Eleuteri, A.M., Keller J.N., Protein oxidation and cellular homeostasis: emphasis on metabolism. Biochimica et Biophysica Acta, 1773, 93-104, (2007).
• [85] Lounifi, I., Arc, E., Molassiotis, A., Job, D., Rajjou, L., Tanou, G., Interplay between protein carbonylation and nitrosylation in plants. Proteomics, 13, 568-578, (2013).
• [86] Tanou, G., Job, C., Rajjou, L., Arc, E., Belghazi, M., Diamantidis, G., Molassiotis, A., Job D., Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant Journal, 60, 795-804, (2009).
• [87] Bartoli, C.G., Gomez, F., Martinez, D.E., Guiamet, J.J., Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). Journal of Experimental Botany, 55, 1663-1669 (2004).
• [88] Romero-Puertas, M.C., Palma, J.M., Gomez, M., delRio, L.A., Sandalio, L.M., Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell and Environment, 25, 677-686, (2002).
• [89] Becana, M., Klucas, R.V., Transition metals in legume root nodules: iron-dependent free radical production increases during nodule sescence. Proceeding of the National Academy of Science USA, 89, 8958-8962, (1992).
• [90] Moran, J.F., Becana, M., Iturbe-Ormaetxe, I., Frechilla, S., Klucas, R.V., Aparicio-Tejo P., Drought induces oxidative stress in pea plants. Planta, 194, 1994-1999, (1994).
• [91] Couee, I., Sulmon, C., Gouesbet, G., El Amrani, A., Involvement of soluble sugars in reactive oxygen species balance and response to oxidative stress in plants. Journal of Experimental Botany, 57, 449-159, (2006).
• [92] Morelli, R., Russo-Volpe, S., Bruno, N., Lo Scalzo, R., Fenton-dependent damage to carbohydrates: free radical scavenging activity of some simple sugars. Journal of Agriculture and Food Chemistry, 51, 7418-7425, (2003).
• [93] Shen, B., Jensen, R.G., Bohnert, H.J., Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiology, 113, 1177-1183, (1997).
• [94] Britt, A.B., DNA damage and repair in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 47, 75-100, (1996).
• [95] Cooke, M.S., Evans, M.D., Dizdaroğlu, M., Lunec, J., Oxidative DNA damage: mechanisms, mutation and disease. FASEB Journal, 17, 1195-1214, (2003).
• [96] Yoshiyama, K.O., Sakaguchi, K., Kimura, S., DNA damage response in plants: conserved and variable response compared to animals. Biology, 2, 1338-1356, (2013).
• [97] Wang, Z., Rhee, D.B., Lu, J., Bohr, C.T., Zhou, F., Vallabhaneni, H., de Souza-Pinto, N.C., Liu, Y., Characterization of the Arabidopsis heterotrimeric G protein. Journal of Biological Chemistry, 283, 13913-13922, (2008).
• [98] Tuteja, N., Singh, M.B., Misra, M.K., Bhalla, P.L., Tuteja, N., Molecular mechanisms of DNA damage and repair: progress in plants. Critical Review of Biochemistry and Molecular Biology, 36, 337-397, (2001).
• [99] Vanderauwera, S., Suzuki, N., Miller, G., Van de Cotte, B., Morsa, S., Lavanat, J.L., Hegie, A., Triantaphylides, C., Shulaev, V., van Montagu, M.C.E., Van Breusegem, F., Mittler, R., Extranuclear protection of chromosomal DNA from oxidative stress. Proceeding of the National Academy of Science USA, 108, 1711-1716, (2011).