Biologia plantarum 62:201-210, 2018 | DOI: 10.1007/s10535-018-0782-7
Regulation of the key antioxidant enzymes by developmental processes and environmental stresses in the dark
- 1 Department of Plant Biology, University of Szeged, Szeged, Hungary
- 2 Doctoral School in Biology, Faculty of Science and Informatics, University of Szeged, Szeged, Hungary
The presence of solar radiation is one of the most important environmental factors, which is required for the optimal growth and development of plants. The absence of it (e.g. in the night period or artificially prolonged darkness) can alter the light-dependent signalling and regulation pathways and may induce new defence responses. Antioxidant enzymes as components of the plant defence system play a crucial role in the detoxification of reactive oxygen species (ROS) induced by several stressors; however, their regulation can be different in the light or in the dark. In this review we summarize the current knowledge about the physiological and molecular aspects of dark-modulated key antioxidant enzymes (superoxide dismutase, catalase, and ascorbate peroxidase) in different plant species and discuss their roles in different developmental processes (seedling growth and development or senescence) and in responses to environmental stresses (cold, chilling, heat, and biotic stress). Moreover, the hormonal regulation of respective gene transcription and the changes in activity of various isoenzymes at subcellular level are also summarized. Based on this knowledge, modification of these antioxidant enzymes may be used to increase the yield and stress tolerance of cultivated plants in the changing environment.
Keywords: ascorbate peroxidase; catalase; reactive oxygen species; superoxide dismutase
Subjects: antioxidants; ascorbate peroxidase; catalase; superoxide dismutase; reactive oxygen species; diurnal course; dark-induced senescence; auxin; cytokinin; ethylene; gibberelins
Received: July 4, 2017; Revised: October 13, 2017; Accepted: November 16, 2017; Published: June 1, 2018Show citation
ACS | AIP | APA | ASA | Harvard | Chicago | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
References
- Alscher, R.G., Erturk, N., Heath, L.S.: Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. - J. exp. Bot. 53: 1331-1341, 2002. Go to original source...
- Anderson, J.A.: Catalase activity, hydrogen peroxide content and thermotolerance of pepper leaves. - Sci. Hort. 95: 277-284, 2002. Go to original source...
- Asada, K.: The role of ascorbate peroxidase and monodehydroascorbate reductase in H2O2 scavenging in plants. - Cold Spring Harbor Monograph Archive 34: 715-735, 1997.
- Bafeel, S.O., Ibrahim, M.M.: Antioxidants and accumulation of α-tocopherol induce chilling tolerance in Medicago sativa. - Int. J. Agr. Biol. 10: 593-598, 2008.
- Bagnoli, F., Danti, S., Magherini, V., Cozza, R., Innocenti, A.M., Racchi, M.L.: Molecular cloning, characterisation and expression of two catalase genes from peach. - Funct. Plant Biol. 31: 349-357, 2004. Go to original source...
- Bailly, C., Bogatek-Leszczynska, R., Côme, D., Corbineau, F.: Changes in activities of antioxidant enzymes and lipoxygenase during growth of sunflower seedlings from seeds of different vigour. - Seed Sci. Res. 12: 47-55, 2002. Go to original source...
- Ballaré, C.L.: Light regulation of plant defense. - Annu. Rev. Plant Biol. 65: 335-363, 2014. Go to original source...
- Boldt, R., Scandalios, J.G.: Circadian regulation of the Cat3 catalase gene in maize (Zea mays L.): entrainment of the circadian rhythm of Cat3 by different light treatments. - Plant J. 7: 989-999, 1995. Go to original source...
- Bora, K.K., Ganesh, R., Mathur, S.R.: Paclobutrazol delayed dark-induced senescence of mung bean leaves. - Biológia 62: 185-188, 2007. Go to original source...
- Camejo, D., Martí, M.D.C., Nicolás, E., Alarcón, J.J., Jiménez, A., Sevilla, F.: Response of superoxide dismutase isoenzymes in tomato plants (Lycopersicon esculentum) during thermo-acclimation of the photosynthetic apparatus. - Physiol. Plant. 131: 367-377, 2007. Go to original source...
- Cavaiuolo, M., Cocetta, G., Spadafora, N. D., Müller, C. T., Rogers, H. J., Ferrante, A.: Gene expression analysis of rocket salad under pre-harvest and postharvest stresses: a transcriptomic resource for Diplotaxis tenuifolia. - PloS ONE 12: e0178119, 2017. Go to original source...
- Caverzan, A., Passaia, G., Rosa, S.B., Ribeiro, C.W., Lazzarotto, F., Margis-Pinheiro, M.: Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. - Genet. mol. Biol. 35: 1011-1019, 2012. Go to original source...
- Chen, H.J., Wu, S.D., Huang, G.J., Shen, C.Y., Afiyanti, M., Li, W.J., Lin, Y.H.: Expression of a cloned sweet potato catalase SPCAT1 alleviates ethephon-mediated leaf senescence and H2O2 elevation. - J. Plant Physiol. 169: 86-97, 2012. Go to original source...
- Chen, M., Chory, J., Fankhauser, C.: Light signal transduction in higher plants. - Annu. Rev. Genet. 38: 87-117, 2004. Go to original source...
- Cheng, L., Ma, F.: Diurnal operation of the xanthophyll cycle and the antioxidant system in apple peel. - J. amer. Soc. hort. Sci. 129: 313-320, 2004. Go to original source...
- Comparot, S.M., Graham, C.M., Reid, D.M.: Methyl jasmonate elicits a differential antioxidant response in light-and darkgrown canola (Brassica napus) roots and shoots. - Plant Growth Regul. 38: 21-30, 2002. Go to original source...
- Del Rio, L.A., Sandalio, L.M., Altomare, D.A., Zilinskas, B.A.: Mitochondrial and peroxisomal manganese superoxide dismutase: differential expression during leaf senescence. - J. exp. Bot. 54: 923-933, 2003. Go to original source...
- Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chétrit, P., Foyer, C.H., De Paepe, R.: Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. - Plant Cell 15: 1212-1226, 2003. Go to original source...
- Esfandiari, E., Alavi-Kia, S.S., Bahmani, A., Aazami, M.A.: The effect of light on ROS-scavenging systems and lipid peroxidation under cold conditions in saffron (Crocus sativus L.). - Afr. J. agr. Res. 4: 378-382, 2009.
- Foyer, C. H., Noctor, G.: Oxygen processing in photosynthesis: regulation and signaling. - New Phytol. 146: 359-388, 2000. Go to original source...
- Foyer, C.H., Noctor, G.: Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. - Antioxid. Redox Signal. 11: 861-905, 2009. Go to original source...
- Gao, H.J., Zhao, F., Yang, J.X., Yang, H.Q.: Nitric oxide alleviates lipid peroxidation induced by osmotic stress during senescence of detached leaves of Malus hupehensis Rehd. - J. hort. Sci. Biotechnol. 85: 367-373, 2010. Go to original source...
- Ghorbanpour, M., Hatami, M.: Spray treatment with silver nanoparticles plus thidiazuron increases anti-oxidant enzyme activities and reduces petal and leaf abscission in four cultivars of geranium (Pelargonium zonale) during storage in the dark. - J. hort. Sci. Biotechnol. 89: 712-718, 2014. Go to original source...
- Giannino, D., Condello, E., Bruno, L., Testone, G., Tartarini, A., Cozza, R., Mariotti, D.: The gene geranylgeranyl reductase of peach (Prunus persica [L.] Batsch) is regulated during leaf development and responds differentially to distinct stress factors. - J. exp. Bot. 55: 2063-2073, 2004. Go to original source...
- Habibi, G., Hajiboland, R.: Comparison of photosynthesis and antioxidative protection in Sedum album and Sedum stoloniferum (Crassulaceae) under water stress. - Photosynthetica 50: 508-518, 2012. Go to original source...
- Hernández-Jiménez, M.J., Lucas, M.M., de Felipe, M.R.: Antioxidant defence and damage in senescing lupin nodules. - Plant Physiol. Biochem. 40: 645-657, 2002. Go to original source...
- Huang, J., Han, B., Xu, S., Zhou, M., Shen, W.: Heme oxygenase-1 is involved in the cytokinin-induced alleviation of senescence in detached wheat leaves during dark incubation. - J. Plant Physiol. 168: 768-775, 2011. Go to original source...
- Iwamoto, M., Higo, H., Higo, K.: Differential diurnal expression of rice catalase genes: the 5'-flanking region of CatA is not sufficient for circadian control. - Plant Sci. 151: 39-46, 2000. Go to original source...
- Joo, J., Lee, Y.H., Song, S.I.: Rice CatA, CatB, and CatC are involved in environmental stress response, root growth, and photorespiration, respectively. - J. Plant Biol. 57: 375-382, 2014. Go to original source...
- Josse, E.M., Halliday, K.J.: Skotomorphogenesis: the dark side of light signalling. - Curr. Biol. 18: 1144-1146, 2008. Go to original source...
- Kabir, M.H., Wang, M.H.: Functional studies on two catalase genes from tomato (Solanum lycopersicum L.). - J. hort. Sci. Biotechnol. 86: 84-90, 2011. Go to original source...
- Kanazawa, S., Sano, S., Koshiba, T., Ushimaru, T.: Changes in antioxidative enzymes in cucumber cotyledons during natural senescence: comparison with those during darkinduced senescence. - Physiol. Plant. 109: 211-216, 2000. Go to original source...
- Kangasjärvi, S., Neukermans, J., Li, S., Aro, E.M., Noctor, G.: Photosynthesis, photorespiration, and light signalling in defence responses. - J. exp. Bot. 63: 1619-1636, 2012. Go to original source...
- Karatas, I., Oztürk, L., Ersahin, Y., Okatan, Y.: Effects of auxin on photosynthetic pigments and some enzyme activities during dark-induced senescence of Tropaeolum leaves. - Pak. J. Bot. 42: 1881-1888, 2010.
- Karpinski, S., Gabtys, H., Mateo, A., Karpinska, B., Mullineaux, P.M.: Light perception in plant disease defence signalling. - Curr. Opin. Plant Biol. 6: 390-396, 2003. Go to original source...
- Kaur, H., Gupta, A.K., Kaur, N., Sandhu, J.S.: Differential response of the antioxidant system in wild and cultivated genotypes of chickpea. - Plant Growth Regul. 57: 109-114, 2009. Go to original source...
- Kazan, K., Manners, J.M.: The interplay between light and jasmonate signalling during defence and development. - J. exp. Bot. 62: 4087-4100, 2011. Go to original source...
- Kerdnaimongkol, K., Bhatia, A., Joly, R.J., Woodson, W.R.: Oxidative stress and diurnal variation in chilling sensitivity of tomato seedlings. - J. amer. Soc. hort. Sci. 122: 485-490, 1997. Go to original source...
- Khorshidi, M., Nojavan, A.M.: The effects of abscisic acid and CaCl2 on the activities of antioxidant enzymes under cold stress in maize seedlings in the dark. - Pak. J. biol. Sci. 9: 54-59, 2006.
- Kocsy, G., Tari, I., Vanková, R., Zechmann, B., Gulyás, Z., Poór, P., Galiba, G.: Redox control of plant growth and development. - Plant Sci. 211: 77-91, 2013. Go to original source...
- Kubo, A., Saji, H., Tanaka, K., Kondo, N.: Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide. - Plant mol. Biol. 29: 479-489, 1995. Go to original source...
- Kuzniak, E.: Ascorbate and ascorbate-dependent enzymes in detached tomato leaves under conditions modulating the ascorbate pool. - Acta Physiol. Plant. 26: 327-333, 2004. Go to original source...
- Kwon, S.I., An, C.S.: Molecular cloning, characterization and expression analysis of a catalase cDNA from hot pepper (Capsicum annuum L.). - Plant Sci. 160: 961-969, 2001. Go to original source...
- Leivar, P., Quail, P.H.: PIFs: pivotal components in a cellular signaling hub. - Trends Plant Sci. 16: 19-28, 2011. Go to original source...
- Li, J., Matsui, S.: Effects of chilling on antioxidative enzymes in leaves of Cattleya and Cymbidium. - J. jap. Soc. hort. Sci. 70: 360-365, 2001. Go to original source...
- Libik, M., Konieczny, R., Surówka, E., Miszalski, Z.: Superoxide dismutase activity in organs of Mesembryanthemum crystallinum L. at different stages of CAM development. - Acta biol. cracov. Ser. Bot. 47: 199-204, 2005.
- Luna, C.M., Pastori, G.M., Driscoll, S., Groten, K., Bernard, S., Foyer, C.H.: Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat. - J. exp. Bot. 56: 417-423, 2005.
- Luschin-Ebengreuth, N., Zechmann, B.: Compartment-specific investigations of antioxidants and hydrogen peroxide in leaves of Arabidopsis thaliana during dark-induced senescence. - Acta Physiol. Plant. 38: 1-15, 2016. Go to original source...
- Michael, T.P., McClung, C.R.: Phase-specific circadian clock regulatory elements in Arabidopsis. - Plant Physiol. 130: 627-638, 2002. Go to original source...
- Mhamdi, A., Queval, G., Chaouch, S., Vanderauwera, S., Van Breusegem, F., Noctor, G.: Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. - J. exp. Bot. 61: 4197-4220, 2010. Go to original source...
- Mhamdi, A., Noctor, G., Baker, A.: Plant catalases: peroxisomal redox guardians. - Arch. Biochem. Biophys. 525: 181-194, 2012. Go to original source...
- Moussa, H.R., Ahmed, A.E.F.M.: Protective role of selenium on development and physiological responses of Vicia faba. - Int. J. veg. Sci. 16: 174-183, 2010. Go to original source...
- Niewiadomska, E., Miszalski, Z.: Partial characterization and expression of leaf catalase in the CAM-inducible halophyte Mesembryanthemum crystallinum L. - Plant Physiol. Biochem. 46: 421-427, 2008. Go to original source...
- Novák, A., Boldizsár, Á., Ádám, É., Kozma-Bognár, L., Majláth, I., Båga, M., Tóth, B., Chibbar, R., Galiba, G.: Light-quality and temperature-dependent CBF14 gene expression modulates freezing tolerance in cereals. - J. exp. Bot. 67: 1285-1295, 2015.
- Panchuk, I.I., Zentgraf, U., Volkov, R.A.: Expression of the Apx gene family during leaf senescence of Arabidopsis thaliana. - Planta 222: 926-932, 2005. Go to original source...
- Peltzer, D., Polle, A.: Diurnal fluctuations of antioxidative systems in leaves of field-grown beech trees (Fagus sylvatica): Responses to light and temperature. - Physiol. Plant. 111: 158-164, 2001. Go to original source...
- Pignocchi, C., Fletcher, J.M., Wilkinson, J.E., Barnes, J.D., Foyer, C.H.: The function of ascorbate oxidase in tobacco. - Plant Physiol. 132: 1631-1641, 2003. Go to original source...
- Poór, P., Takács, Z., Bela, K., Czékus, Z., Szalai, G., Tari, I.: Prolonged dark period modulates the oxidative burst and enzymatic antioxidant systems in the leaves of salicylic acid-treated tomato. - J. Plant Physiol. 213: 216-226, 2017. Go to original source...
- Radyukina, N.L., Shashukova, A.V., Shevyakova, N.I., Kuznetsov, V.V.: Proline involvement in the common sage antioxidant system in the presence of NaCl and paraquat. - Russ. J. Plant Physiol. 55: 649-656, 2008. Go to original source...
- Ranwala, A.P., Miller, W.B.: Preventive mechanisms of gibberellin 4+7 and light on low-temperature-induced leaf senescence in Lilium cv. Stargazer. - Postharvest Biol. Technol. 19: 85-92, 2000. Go to original source...
- Shah, F., Huang, J., Cui, K., Nie, L., Shah, T., Wu, W., Chen, C.: Physiological and biochemical changes in rice associated with high night temperature stress and their amelioration by exogenous application of ascorbic acid (vitamin C). - Aust. J. Crop. Sci. 5: 1810-1816, 2011.
- Sheokand, S., Swaraj, K.: Natural and dark-induced nodule senescence in chickpea: nodule functioning and H2O2 scavenging enzymes. - Biol. Plant. 38: 545-554, 1996. Go to original source...
- Ślesak, I., Miszalski, Z., Karpinska, B., Niewiadomska, E., Ratajczak, R., Karpinski, S.: Redox control of oxidative stress responses in the C3-CAM intermediate plant Mesembryanthemum crystallinum. - Plant Physiol. Biochem. 40: 669-677, 2002.
- Sunohara, Y., Matsumoto, H.: Oxidative injury induced by the herbicide quinclorac on Echinochloa oryzicola Vasing. and the involvement of antioxidative ability in its highly selective action in grass species. - Plant Sci. 167: 597-606, 2004. Go to original source...
- Van Aken, O., Van Breusegem, F.: Licensed to kill: mitochondria, chloroplasts, and cell death. - Trends Plant Sci. 20: 754-766, 2015. Go to original source...
- Vranová, E., Inzé, D., Van Breusegem, F.: Signal transduction during oxidative stress. - J. exp. Bot. 53: 1227-1236, 2002. Go to original source...
- Wada, K., Tada, T., Nakamura, Y., Ishikawa, T., Yabuta, Y., Yoshimura, K., Shigeoka, S., Nishimura, K.: Crystal structure of chloroplastic ascorbate peroxidase from tobacco plants and structural insights into its instability. - J. Biochem. 134: 239-244, 2003. Go to original source...
- Wojciechowska, R., Hanus-Fajerska, E.J., Kolton, A., Kaminska, I., Grabowska, A., Kunicki, E.: The effect of seedling chilling on glutathione content, catalase and peroxidase activity in Brassica oleracea L. var. italica. - Acta Soc. Bot. Polon. 82: 243-248, 2013. Go to original source...
- Wojtyla, Ł., Lechowska, K., Kubala, S., Garnczarska, M.: Different modes of hydrogen peroxide action during seed germination. - Front. Plant Sci. 7: 66, 2016. Go to original source...
- Yang, J.D., Yun, J.Y., Zhang, T.H., Zhao, H.L.: Presoaking with nitric oxide donor SNP alleviates heat shock damages in mung bean leaf discs. - Bot. Stud. 47: 129-136, 2006.
- Yang, X., Wen, X., Gong, H., Lu, Q., Yang, Z., Tang, Y., Lu, C.: Genetic engineering of the biosynthesis of glycine-betaine enhances thermotolerance of photosystem II in tobacco plants. - Planta 225: 719-733, 2007. Go to original source...
- Zavaleta-Mancera, H.A., López-Delgado, H., Loza-Tavera, H., Mora-Herrera, M., Trevilla-García, C., Vargas-Suárez, M., Ougham, H.: Cytokinin promotes catalase and ascorbate peroxidase activities and preserves the chloroplast integrity during dark-senescence. - J. Plant Physiol. 164: 1572-1582, 2007. Go to original source...
- Zhang, J., Li, H., Xu, B., Li, J., Huang, B.: Exogenous melatonin suppresses dark-induced leaf senescence by activating the superoxide dismutase-catalase antioxidant pathway and down-regulating chlorophyll degradation in excised leaves of perennial ryegrass (Lolium perenne L.). - Front. Plant Sci. 7: 1500, 2016. Go to original source...
- Zhong, H.H., McClung, C.R.: The circadian clock gates expression of two Arabidopsis catalase genes to distinct and opposite circadian phases. - Mol. gen. Genet. 251: 196-203, 1996. Go to original source...
- Zhong, H.H., Resnick, A.S., Straume, M., McClung, C.R.: Effects of synergistic signaling by phytochrome A and cryptochrome1 on circadian clock-regulated catalase expression. - Plant Cell 9: 947-955, 1997. Go to original source...