Seasonal and diurnal changes in photochemistry and antioxidant responses, and phenolic metabolism in evergreen Jasminum fruticans
Subject Areas : Environmental physiology
1 - Department of Biology, Payame Noor University (PNU), Iran
Keywords: Seasonal changes, carotenoids, Flavonoids, Antioxidant system, Chlorophyll fluorescence, Jasminum fruticans, diurnal changes,
Abstract :
In this study, seasonal and diurnal changes in photosynthesis and phenolic metabolism in evergreen jasmin (Jasminum fruticans L.) were examined over a 12-month period. We found the differences in pigment and phenolic contents between the values determined during the autumn and winter months and the values determined during the spring and summer months. During the autumn and winter months, the low seasonality of Chla was accompanied by increases in both carotenoids and phenol levels which play a major role in photoprotection processes. While the maximal quantum efficiency of PSII (Fv/Fm) showed diurnal changes during the winter months, such diurnal changes were not observed for the other seasons. These diurnal changes reflected dynamic photoinhibition, as an adaptation mechanism, which may actually protect the leaves against photodamage under cold conditions. During the winter months, increased O–J phase (from the OJIP chlorophyll fluorescence curve) and decreased I–P phase in parallel with the reduction of Fv/Fm, revealed that the cold stress influenced both the donor and acceptor sides of PSII. Interestingly, we found the relationship between diurnal changes of Fv/Fm and those of hydrogen peroxide (H2O2) levels and catalase (CAT) activity during the winter months. Diurnal changes in CAT activity represented the differences between the values determined in warm and cold seasons. Compared with the diurnal changes during the spring and summer months, the maximum activity of CAT was observed at 15:00 h during the winter months, which indicated that CAT may play an effective role in protection of photosystems under a high photosynthetically active radiation (PAR) during cold days.
Ashraf, M.H.P.J.C. and Harris, P.J. (2013) Photosynthesis under stressful environments: an overview. Photosynthetica, 51: 163-190.
Azzabi, G., Pinnola, A., Betterle, N., Bassi, R. and Alboresi, A. (2012) Enhancement of non-photochemical quenching in the Bryophyte physcomitrella patens during acclimation to salt and osmotic stress. Plant Cell Physiology, 53: 1815-1825.
Boominathan, R. and Doran, P.M. (2002) Ni induced oxidative stress in roots of the Ni hyperaccumlator, Alyssum bertoloni. New Phytologist, 156: 202-205.
Bradford, M.M. (1976) A rapid & sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248-254.
Cazzonelli, C. I. and Pogson, B. J. (2010). Source to sink: regulation of carotenoid biosynthesis in plants. Trends in Plant Science, 15: 266-274.
Chen, L., Jia, H., Tian, Q., Du, L. and Gao, Y. (2012) Protecting effect of phosphorylation on oxidative damage of D1 protein by down-regulating the production of superoxide anion in photosystem II membranes under high light. Photosynth Research, 112: 141-148.
Cheng, L., Ma, F. (2004) Diurnal operation of the xanthophyll cycle and the antioxidant system in apple peel. Journal of the American Society for Horticultural Science, 129(3): 313-320.
Ehlert, B. and Hincha, D.K. (2008) Chlorophyll fluorescence imaging accurately quantifies freezing damage and cold acclimation responses in Arabidopsis leaves. Plant Methods, 4(1): 12.
Fischer, B.B., Hideg, E. and Krieger-Liszkay, A. (2013) Production, detection and redox signaling of singlet oxygen in photosynthetic organisms. Antioxidants Redox Signaling, 18: 2145-2162.
Giannopolitis, C.N. and Ries, S.K. (1977) Superoxide dismutase: occurrence in higher plants. Plant Physiology, 59: 309-314.
Ivanov, A.G., Allakhverdiev, S.I., Huner, N.P.A. and Murata, N. (2012) Genetic decrease in fatty acid unsaturation of phosphatidylglycerol increased photoinhibition of photosystem I at low temperature in tobacco leaves. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1817: 1374-1379.
Habibi, G. and Ajory, N. (2015) The effect of drought on photosynthetic plasticity in Marrubium vulgare plants growing at low & high altitudes. Plant Research, 128: 987-994
Habibi, G. (2020) Comparison of CAM expression, photochemistry and antioxidant responses in Sedum album and Portulaca oleracea under combined stress. Physiologia Plantarum , 170(4): 550-568.
Habibi, G., Elyaghi, S., Abedini, M. and sabourmoghaddam, N. (2018) Benefit of iodine soil application for alleviating detrimental effects of salinity stress in strawberry. Iranian Journal of Plant Biology 10(2): 57-72.
Habibi, G. (2014) Hydrogen Peroxide (H2O2) Generation, Scavenging & Signaling in Plants. In: Ahmad P, (eds.), Oxidative Damage to Plants: Antioxidant Networks and Signaling. Elsevier, USA, 557-574.
Habibi, G. (2017a) Physiological, photochemical and ionic responses of sunflower seedlings to exogenous selenium supply under salt stress. Acta Physiologiae Plantarum, 39(10): 213.
Habibi, G., Servataian, N. and Abedini, M. (2017b) Photoprotection mechanisms in wheat plants under high light and cold temperature conditions. Iranian Journal of Plant Biology, 9(1): 59-72.
Kalaji, H. M., Bosa, K., Kościelniak, J. and Żuk-Gołaszewska, K. (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environmental and Experimental Botany, 73: 64-72.
Lichtenthaler, H.K. and Wellburn, A.R. (1985) Determination of total carotenoids & chlorophylls a & b of leaf in different solvents. Biochemical Society Transactions , 11: 591-592.
Li, Y.N., Li, Y.T., Ivanov, A.G., Jiang, W.L., Che, X.K., Liang, Y., Zhang, Z.S., Zhao, S.J. and Gao, H.Y. (2019) Defective photosynthetic adaptation mechanism in winter restricts the introduction of overwintering plant to high latitudes. BioRxiv, p.613117.
Luna, C.M., Pastori, G.M., Driscoll, S., Groten, K., Bernard, S. and Foyer, C.H. (2005) Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat. Journal of Experimental Botany, 56: 417-423.
Mavi, A., Terzi, Z. and Ozgen, U. (2004) Antioxidant properties of some medicinal plants: Prangos ferulacea (Apiaceae), Sedum sempervivoides (Crassulaceae), Malva neglecta (Malvaceae), Cruciata taurica (Rubiaceae), Rosa pimpinellifolia (Rosaceae), Galium verum subsp. Verum (Rubiaceae), Urtica dioica (Urticaceae). Biological & Pharmaceutical Bulletin ,27: 702-705.
Míguez, F., Fernández‐Marín, B., Becerril, J.M. and García‐Plazaola, J.I. (2015) Activation of photoprotective winter photoinhibition in plants from different environments: a literature compilation and meta-analysis. Physiologia Plantarum, 155: 414-423.
Míguez, F., Fernández-Marín, B., Becerril, J.M. and García-Plazaola, J.I. (2017) Diversity of winter photoinhibitory responses: a case study in co-occurring lichens, mosses, herbs and woody plants from subalpine environments. Physiologia Plantarum, 160: 282-296.
Miura, K. and Tada, Y. (2014). Regulation of water, salinity, and cold stress responses by salicylic acid. Frontiers in Plant Science, 5: 4-12.
Rousseau, C., Belin, E., Bove, E., Rousseau, D., Fabre, F. and Berruyer, R. (2013) High throughput quantitative phenotyping of plant resistance using chlorophyll fluorescence image analysis. Plant Methods, 9: 17.
Russell, R.B., Lei, T.T. and Nilsen, E.T. (2009) Freezing induced leaf movements and their potential implications to early spring carbon gain: Rhododendron maximum as exemplar. Functional Ecology, 23: 463-471.
Sarikurkcu, C., Tepe, B. and Yamac, M., 2008. Evaluation of the antioxidant activity of four edible mushrooms from the Central Anatolia, Eskisehir - Turkey: Lactarius deterrimus, Suillus collitinus, Boletus edulis, Xerocomus chrysenteron. Bioresource Technology, 99: 6651-6655.
Savitch, L.V., Ivanov, A.G., Krol, M., Sprott, D.P., Öquist, G. and Huner, N.P. (2010) Regulation of energy partitioning and alternative electron transport pathways during cold acclimation of lodgepole pine is oxygen dependent. Plant, Cell & Environment 51: 1555-1570.
Scheller, H. and Haldrup, A. (2005) Photoinhibition of photosystem I. Planta, 221: 5-8.
Silva‐Cancino, M.C., Esteban, R., Artetxe, U. and Plazaola, J.I.G. (2012) Patterns of spatio-temporal distribution of winter chronic photoinhibition in leaves of three evergreen Mediterranean species with contrasting acclimation responses. Physiologia Plantarum, 144: 289-301.
Simon, L.M., Fatrai, Z., Jonas, D.E. and Matkovics, B. (1974) Study of peroxide metabolism enzymes during the development of Phaseolus vulgaris. Biochemie und Physiologie der Pflanzen, 166: 387-392.
Strasser, R.J., Tsimilli-Michael, M. and Srivastava, A. (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou, G.C., Govindjee (Eds.), Chlorophyll a Fluorescence: A Signature of Photosynthesis. Springer, Dordrecht, 321-362.
Suetsugu, N. and Wada, M. (2007) Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biological Chemistry 388: 927-935.
Takahashi, S. and Badger, M.R. (2011) Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science, 16: 1-10.
Takahashi, S. (2010) The solar action spectrum of photosystem II damage. Plant Physiology, 153: 988-993.
Takahashi, D., Kawamura, Y. and Uemura, M. (2016) Cold acclimation is accompanied by complex responses of glycosylphosphatidylinositol (GPI)-anchored proteins in Arabidopsis. Journal of Experimental Botany, 67: 5203-5215.
Telfer, A. (2014) Singlet oxygen production by PSII under light stress: mechanism, detection & the protective role of b-Carotene. Plant Cell Physiology, 55(7): 1216-1223.
Tholen, D. (2008) The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves. Plant Cell Environment 31: 1688-1700.
Velikova, V., Yordanov, I. and Edreva, A. (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants-protective role of exogenous polyamines. Plant Science 151: 59-66.
Van Heerden, P.D.R., Swanepoel, J.W. and Krüger, G.H.J. (2007) Modulation of photosynthesis by drought in two desert scrub species exhibiting C3-mode CO2 assimilation. Environmental and Experimental Botany 61(2): 124-136.
Winkel-Shirley, B. (2002) Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5: 18-223.
Wong, C.Y. and Gamon, J.A. (2015) The photochemical reflectance index provides an optical indicator of spring photosynthetic activation in evergreen conifers. New Phytologist 206: 196-208.
Yamori, W., Sakata, N., Suzuki, Y., Shikanai, T. and Makino, A. (2011) Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. The Plant Journal 68: 966-976.
Xu, H.G., Liu, G.J., Liu, G.T., Yan, B.F., Duan, W. and Wang L.J. (2014) Comparison of investigation methods of heat injury in grapevine (Vitis) & assessment to heat tolerance in different cultivars & species. BMC Plant Biology 14: 156.
Zucker, M. (1965) Induction of phenylalanine deaminase by light, its relation to chlorogenic acid synthesis in potato tuber tissue. Physiologia Plantarum 40: 779-784.
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Ashraf, M.H.P.J.C. and Harris, P.J. (2013) Photosynthesis under stressful environments: an overview. Photosynthetica, 51: 163-190.
Azzabi, G., Pinnola, A., Betterle, N., Bassi, R. and Alboresi, A. (2012) Enhancement of non-photochemical quenching in the Bryophyte physcomitrella patens during acclimation to salt and osmotic stress. Plant Cell Physiology, 53: 1815-1825.
Boominathan, R. and Doran, P.M. (2002) Ni induced oxidative stress in roots of the Ni hyperaccumlator, Alyssum bertoloni. New Phytologist, 156: 202-205.
Bradford, M.M. (1976) A rapid & sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72: 248-254.
Cazzonelli, C. I. and Pogson, B. J. (2010). Source to sink: regulation of carotenoid biosynthesis in plants. Trends in Plant Science, 15: 266-274.
Chen, L., Jia, H., Tian, Q., Du, L. and Gao, Y. (2012) Protecting effect of phosphorylation on oxidative damage of D1 protein by down-regulating the production of superoxide anion in photosystem II membranes under high light. Photosynth Research, 112: 141-148.
Cheng, L., Ma, F. (2004) Diurnal operation of the xanthophyll cycle and the antioxidant system in apple peel. Journal of the American Society for Horticultural Science, 129(3): 313-320.
Ehlert, B. and Hincha, D.K. (2008) Chlorophyll fluorescence imaging accurately quantifies freezing damage and cold acclimation responses in Arabidopsis leaves. Plant Methods, 4(1): 12.
Fischer, B.B., Hideg, E. and Krieger-Liszkay, A. (2013) Production, detection and redox signaling of singlet oxygen in photosynthetic organisms. Antioxidants Redox Signaling, 18: 2145-2162.
Giannopolitis, C.N. and Ries, S.K. (1977) Superoxide dismutase: occurrence in higher plants. Plant Physiology, 59: 309-314.
Ivanov, A.G., Allakhverdiev, S.I., Huner, N.P.A. and Murata, N. (2012) Genetic decrease in fatty acid unsaturation of phosphatidylglycerol increased photoinhibition of photosystem I at low temperature in tobacco leaves. Biochimica et Biophysica Acta (BBA) – Bioenergetics, 1817: 1374-1379.
Habibi, G. and Ajory, N. (2015) The effect of drought on photosynthetic plasticity in Marrubium vulgare plants growing at low & high altitudes. Plant Research, 128: 987-994
Habibi, G. (2020) Comparison of CAM expression, photochemistry and antioxidant responses in Sedum album and Portulaca oleracea under combined stress. Physiologia Plantarum , 170(4): 550-568.
Habibi, G., Elyaghi, S., Abedini, M. and sabourmoghaddam, N. (2018) Benefit of iodine soil application for alleviating detrimental effects of salinity stress in strawberry. Iranian Journal of Plant Biology 10(2): 57-72.
Habibi, G. (2014) Hydrogen Peroxide (H2O2) Generation, Scavenging & Signaling in Plants. In: Ahmad P, (eds.), Oxidative Damage to Plants: Antioxidant Networks and Signaling. Elsevier, USA, 557-574.
Habibi, G. (2017a) Physiological, photochemical and ionic responses of sunflower seedlings to exogenous selenium supply under salt stress. Acta Physiologiae Plantarum, 39(10): 213.
Habibi, G., Servataian, N. and Abedini, M. (2017b) Photoprotection mechanisms in wheat plants under high light and cold temperature conditions. Iranian Journal of Plant Biology, 9(1): 59-72.
Kalaji, H. M., Bosa, K., Kościelniak, J. and Żuk-Gołaszewska, K. (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environmental and Experimental Botany, 73: 64-72.
Lichtenthaler, H.K. and Wellburn, A.R. (1985) Determination of total carotenoids & chlorophylls a & b of leaf in different solvents. Biochemical Society Transactions , 11: 591-592.
Li, Y.N., Li, Y.T., Ivanov, A.G., Jiang, W.L., Che, X.K., Liang, Y., Zhang, Z.S., Zhao, S.J. and Gao, H.Y. (2019) Defective photosynthetic adaptation mechanism in winter restricts the introduction of overwintering plant to high latitudes. BioRxiv, p.613117.
Luna, C.M., Pastori, G.M., Driscoll, S., Groten, K., Bernard, S. and Foyer, C.H. (2005) Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat. Journal of Experimental Botany, 56: 417-423.
Mavi, A., Terzi, Z. and Ozgen, U. (2004) Antioxidant properties of some medicinal plants: Prangos ferulacea (Apiaceae), Sedum sempervivoides (Crassulaceae), Malva neglecta (Malvaceae), Cruciata taurica (Rubiaceae), Rosa pimpinellifolia (Rosaceae), Galium verum subsp. Verum (Rubiaceae), Urtica dioica (Urticaceae). Biological & Pharmaceutical Bulletin ,27: 702-705.
Míguez, F., Fernández‐Marín, B., Becerril, J.M. and García‐Plazaola, J.I. (2015) Activation of photoprotective winter photoinhibition in plants from different environments: a literature compilation and meta-analysis. Physiologia Plantarum, 155: 414-423.
Míguez, F., Fernández-Marín, B., Becerril, J.M. and García-Plazaola, J.I. (2017) Diversity of winter photoinhibitory responses: a case study in co-occurring lichens, mosses, herbs and woody plants from subalpine environments. Physiologia Plantarum, 160: 282-296.
Miura, K. and Tada, Y. (2014). Regulation of water, salinity, and cold stress responses by salicylic acid. Frontiers in Plant Science, 5: 4-12.
Rousseau, C., Belin, E., Bove, E., Rousseau, D., Fabre, F. and Berruyer, R. (2013) High throughput quantitative phenotyping of plant resistance using chlorophyll fluorescence image analysis. Plant Methods, 9: 17.
Russell, R.B., Lei, T.T. and Nilsen, E.T. (2009) Freezing induced leaf movements and their potential implications to early spring carbon gain: Rhododendron maximum as exemplar. Functional Ecology, 23: 463-471.
Sarikurkcu, C., Tepe, B. and Yamac, M., 2008. Evaluation of the antioxidant activity of four edible mushrooms from the Central Anatolia, Eskisehir - Turkey: Lactarius deterrimus, Suillus collitinus, Boletus edulis, Xerocomus chrysenteron. Bioresource Technology, 99: 6651-6655.
Savitch, L.V., Ivanov, A.G., Krol, M., Sprott, D.P., Öquist, G. and Huner, N.P. (2010) Regulation of energy partitioning and alternative electron transport pathways during cold acclimation of lodgepole pine is oxygen dependent. Plant, Cell & Environment 51: 1555-1570.
Scheller, H. and Haldrup, A. (2005) Photoinhibition of photosystem I. Planta, 221: 5-8.
Silva‐Cancino, M.C., Esteban, R., Artetxe, U. and Plazaola, J.I.G. (2012) Patterns of spatio-temporal distribution of winter chronic photoinhibition in leaves of three evergreen Mediterranean species with contrasting acclimation responses. Physiologia Plantarum, 144: 289-301.
Simon, L.M., Fatrai, Z., Jonas, D.E. and Matkovics, B. (1974) Study of peroxide metabolism enzymes during the development of Phaseolus vulgaris. Biochemie und Physiologie der Pflanzen, 166: 387-392.
Strasser, R.J., Tsimilli-Michael, M. and Srivastava, A. (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou, G.C., Govindjee (Eds.), Chlorophyll a Fluorescence: A Signature of Photosynthesis. Springer, Dordrecht, 321-362.
Suetsugu, N. and Wada, M. (2007) Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biological Chemistry 388: 927-935.
Takahashi, S. and Badger, M.R. (2011) Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science, 16: 1-10.
Takahashi, S. (2010) The solar action spectrum of photosystem II damage. Plant Physiology, 153: 988-993.
Takahashi, D., Kawamura, Y. and Uemura, M. (2016) Cold acclimation is accompanied by complex responses of glycosylphosphatidylinositol (GPI)-anchored proteins in Arabidopsis. Journal of Experimental Botany, 67: 5203-5215.
Telfer, A. (2014) Singlet oxygen production by PSII under light stress: mechanism, detection & the protective role of b-Carotene. Plant Cell Physiology, 55(7): 1216-1223.
Tholen, D. (2008) The chloroplast avoidance response decreases internal conductance to CO2 diffusion in Arabidopsis thaliana leaves. Plant Cell Environment 31: 1688-1700.
Velikova, V., Yordanov, I. and Edreva, A. (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants-protective role of exogenous polyamines. Plant Science 151: 59-66.
Van Heerden, P.D.R., Swanepoel, J.W. and Krüger, G.H.J. (2007) Modulation of photosynthesis by drought in two desert scrub species exhibiting C3-mode CO2 assimilation. Environmental and Experimental Botany 61(2): 124-136.
Winkel-Shirley, B. (2002) Biosynthesis of flavonoids and effects of stress. Current Opinion in Plant Biology 5: 18-223.
Wong, C.Y. and Gamon, J.A. (2015) The photochemical reflectance index provides an optical indicator of spring photosynthetic activation in evergreen conifers. New Phytologist 206: 196-208.
Yamori, W., Sakata, N., Suzuki, Y., Shikanai, T. and Makino, A. (2011) Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. The Plant Journal 68: 966-976.
Xu, H.G., Liu, G.J., Liu, G.T., Yan, B.F., Duan, W. and Wang L.J. (2014) Comparison of investigation methods of heat injury in grapevine (Vitis) & assessment to heat tolerance in different cultivars & species. BMC Plant Biology 14: 156.
Zucker, M. (1965) Induction of phenylalanine deaminase by light, its relation to chlorogenic acid synthesis in potato tuber tissue. Physiologia Plantarum 40: 779-784.