Abstract
The ultrastructure and functional parameters of the photosynthetic apparatus in leaves of 14-day-old pea seedlings were studied in conditions of laboratory simulated acid rain (SAR). Pea seedlings were sprayed with an aqueous solution containing NaNO3 (0.2 mM) and Na2SO4 (0.2 mM) (pH 5.6, a control variant), or with the same solution, which was acidified to pH 2.5 (acid variant). Functional characteristics were determined by chlorophyll fluorescence analysis. There was reduction in the efficiency of the photosynthetic electron transport by 25% accompanied by an increase in the quantum yield of thermal dissipation of excess light quanta by 85% without significant change in maximum quantum yield of PSII photochemistry (Fv/Fm). Ultrastructural changes in chloroplasts were revealed by transmission electron microscopy (TEM) 2 days after the SAR treatment of pea leaves. In this case, changes in the structure of the grana and heterogeneity of the thylakoids packing in the granum, namely, an increase in thylakoid intraspace widths and thickness of granal thylakoids compared to the control, were found. It was shown also that carbonic anhydrase activity was significantly inhibited in chloroplast preparations isolated from SAR-treated pea leaves. We hypothesize possible involvement of chloroplast carbonic anhydrase in thylakoid granal structure maintenance. The structural disturbances and the inhibition of photochemical activity of chloroplasts are possible consequences of the carbonic anhydrase inactivation by SAR treatment leading to violation of HCO3 −–CO2 equilibrium. The data obtained suggest that acid rains negatively affect the photosynthetic apparatus by disrupting the membrane system of the chloroplast.
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Abbreviations
- AR:
-
acid rain
- SAR:
-
simulated acid rain
- CA:
-
carbonic anhydrase
- TEM:
-
transmission electron microscopy
- PSI:
-
photosystem I
- PSII:
-
photosystem II
- PSA:
-
photosynthetic apparatus
- chl:
-
chlorophyll
References
Alscher, R.G., Donahue, J.L., and Cramer, C.L., Reactive oxygen species and antioxidants: relationships in green cells, Physiol. Plant., 1997, vol. 100, pp. 224–233.
Arnon, D.I., Cooper enzymes in isolated chloroplasts polyphenolase in Beta vulgaris, Plant Physiol., 1949, vol. 24, pp. 149–154.
Avenson, T.J., Kanazawa, A., Cruz, J., Takizava, A.K., Ettinger, W.E., and Kramer, D.M., Integrating the proton circuit into photosynthesis: progress and challenges, Plant Cell Environ., 2005, vol. 28, pp. 97–109.
Avron, M., Photophosphorylation by Swiss-chard chloroplasts, Biochim. Biophys. Acta, 1980, vol. 40, pp. 257–272.
Baker, N.R. and Rosenquist, E., Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities, J. Exp. Bot., 2004, vol. 55, pp. 1607–1621.
Baranov, S.V., Ananyev, G.M., Klimov, V.V., and Dismukes, G.C., Bicarbonate accelerates assembly of the inorganic core of the water-oxidizing complex in manganese-depleted photosystem II: a proposed biogeochemical role for atmospheric carbon dioxide in oxygenic photosynthesis, Biochemistry, 2000, vol. 39, pp. 6060—6065.
Barcelo, J., Vazquez, M.D., and Poschenrieder, C.H., Structural and ultrastructural disorders in cadmium-treated bush bean plants (Phaseolus vulgaris L.), New Phytol., 1988, vol. 108, pp. 37–49.
Bazilevich, N.I., Grebenshchikov, O.S., and Tishkov, A.A., Geograficheskie zakonomernosti struktury i funktsionirovaniya ekosistem (Geographic Patterns in Structure and Function of Ecosystems), Moscow: Nauka, 1986.
Gabara, B., Sklodowska, M., Wyrwicka, A., Glinśka, S., and Gapinśka, M., Changes in the ultrastructure of chloroplasts and mitochondria and antioxidant enzyme activity in Lycopersicon esculentum Mill, leaves sprayed with acid rain, Plant Sci., 2003, vol. 164, pp. 507–516.
Genty, B., Briantais, J.M., and Baker, N.R., The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence, Biochim. Biophys. Acta, 1989, vol. 990, pp. 87–92.
Guadagno, C.R., Virzo, De, Santo, A., and D’Ambrosio, N., A revised energy partitioning approach to assess the yields of non-photochemical quenching components, Biochim. Biophys. Acta, 2010, vol. 1797, pp. 525–530.
Gutknecht, J., Bisson, M.A., and Tosteson, F.C., Diffusion of carbon dioxide through lipid bilayer membranes: effects of carbonic anhydrase, bicarbonate, and unstirred layers, J. Gen. Physiol., 1977, vol. 69, pp. 779–794.
Hecht-Bucholz, C.H., Light and electron microscopic investigations of the reactions of various genotypes to nutritional disorders, Plant Soil, 1983, vol. 72, pp. 151–165.
Isidorov, V.A., Ekologicheskaya khimiya (Ecological Chemistry), St. Petersburg: Khimizdat, 2001.
Ivanov, B.N., Ignatova, L.K., and Romanova, A.K., Diversity in forms and functions of carbonic anhydrase in terrestrial higher plants, Russ. J. Plant Physiol., 2007, vol. 54, no. 2, pp. 143–162.
Krzechowska, M. and Wozny, A., Lead uptake, localisation and changes in cell utrastructure of Funaria hygrometrica protonema, Biol. Plant., 1996, vol. 38, pp. 253–259.
Likens, G.E. and Bormann, F.H., Acid rain: a serious regional environmental problem, Science, 1974, vol. 184, pp. 1176–1179.
Maxwell, K. and Johnson, G.N., Chlorophyll fluorescence—a practical guide, J. Exp. Bot., 2000, vol. 51, pp. 659–668.
Neufeld, H.S., Jernstendt, J.A., and Haines, B.L., Direct foliar effects of simulated acid rain. 1. Damage, growth and gas exchange, New Phytol., 1985, vol. 99, pp. 389–405.
Ouzounidou, G., Ciamparova, M., Moustakas, M., and Karataglis, S., Responses of maize (Zea mays L.) plants to copper stress. I. Growth mineral content and ultrastructure of roots, Environ. Exp. Bot., 1995, vol. 35, pp. 167–176.
Pérez-Bueno, M., Johnson, M.P., Zia, A., Ruban, A.V., and Horton, P., The Lhcb protein and xanthophyll composition of the light harvesting antenna controls the ΔpHdependency of nonphotochemical quenching in Arabidopsis thaliana, FEBS Lett., 2008, vol. 582, pp. 1477–1482.
Schreiber, U., Schliwa, U., and Bilger, W., Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer, Photosynth. Res., 1986, vol. 10, pp. 51–62.
Semenikhin, A.V., Polishchuk, A.V., and Podorvanov, V.V., Effect of heavy metals on carbonic anhydrase activity in pea chloroplasts, Bull. Kharkiv Nat. Agrar. Univ. Ser. Biol., 2014, vol. 32, no. 1, pp. 23–31.
Shaukat, S.S. and Khan, M., Growth and physiological responses of tomato (Lycopersicon esculentum Mill.) to simulated acid rain, Pak. J. Bot., 2008, vol. 40, pp. 2427–2435.
Shutova, T., Kenneweg, H., Buchta, J., Nikitina, J., Terentyev, V., Chernyshov, S., Andersson, B., Allakhverdiev, S.I., Klimov, V.V., Dau, H., Junge, W., and Samuelsson, G., The photosystem II-associated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal, EMBO J., 2008, vol. 27, pp. 782–791.
Stemler, A.J., The bicarbonate effect, oxygen evolution, and the shadow of Otto Warburg, Photosynth. Res., 2002, vol. 73, pp. 177–183.
Stoyanova, D. and Velikova, V., Effects of simulated acid rain on chloroplast ultrastructure of primary leaves of Phaseolus vulgaris, Biol. Plant., 1997, vol. 40, pp. 589–595.
Sun, Z., Wang, L., Chen, M., Wang, L., Liang, C., Zhou, Q., and Huang, X., Interactive effects of cadmium and acid rain on photosynthetic light reaction in soybean seedlings, Ecotoxicol. Environ. Saf., 2012, vol. 79, pp. 62–68.
Tarhanen, S., Ultrastructural responses of the lichen Bryoria fuscesens to simulated acid rain and heavy metal deposition, Ann. Bot., 1998, vol. 82, pp. 735–746.
van Kooten, O. and Snel, J.F.H., The use of chlorophyll fluorescence nomenclature in plant stress physiology, Photosynth. Res., 1990, vol. 25, pp. 147–150.
Vartapetian, B.B. and Zakhmilova, N.A., Ultrastructure of wheat seedling mitochondria under anoxia and postanoxia, Protoplasma, 1990, vol. 156, pp. 39–44.
Velikova, V. and Yordanov, I., Changes in prompt chlorophyll fluorescence and oxygen evolution after bean plant treatment with artificial acid rain, Bulg. J. Plant Physiol., 1996, vol. 22, pp. 14–24.
Velikova, V., Tsonev, T., and Yordanov, I., Light and CO2 responses of photosynthesis and chlorophyll fluorescence characteristics in bean plants after simulated acid rain, Physiol. Plant., 1999, vol. 107, pp. 77–83.
Vodka, M.V., Polishchuk, A.V., Belyavskaya, N.A., and Zolotareva, E.K., Effects of heavy metals, carbonic anhydrase inhibitors, on photosynthetic apparatus of pea leaf chloroplasts. Bull. Kharkiv Nat. Agrar. Univ. Ser. Biol., 2013, vol. 30, no. 1, pp. 46–55.
Wen, K., Liang, C., Wang, L., Hu, G., and Zhou, Q., Combined effects of lanthanum ion and acid rain on growth, photosynthesis and chloroplast ultrastructure in soybean seedlings, Chemosphere, 2011, vol. 84, pp. 601–608.
Wulff, A., Sheppaed, L., and Leith, I., Evaluation of electrolyte leakage, chlorophyll fluorescence and ultrastructural techniques for detecting effects of acid mist on frost hardiness of Sitka spruce shoots, Environ. Exp. Bot., 1994, vol. 34, pp. 261–273.
Zolotareva, E. K., Bound bicarbonate participation in photosynthetic transport, in Plant Physiology: Problems and Perspectives of Development, Kyiv: Logos, 2009, vol. 1, pp. 91–112.
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Original Russian Text © O.V. Polishchuk, M.V. Vodka, N.A. Belyavskaya, A.P. Khomochkin, E.K. Zolotareva, 2016, published in Tsitologiya, 2016, Vol. 58, No. 1, pp. 52–59.
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Polishchuk, O.V., Vodka, M.V., Belyavskaya, N.A. et al. The effect of acid rain on ultrastructure and functional parameters of photosynthetic apparatus in pea leaves. Cell Tiss. Biol. 10, 250–257 (2016). https://doi.org/10.1134/S1990519X16030093
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DOI: https://doi.org/10.1134/S1990519X16030093