Abstract
Acid rain can directly or indirectly affect plant physiological functions, especially photosynthesis. The enzyme ATP synthase is the key in photosynthetic energy conversion, and thus, it affects plant photosynthesis. To clarify the mechanism by which acid rain affects photosynthesis, we studied the effects of acid rain on plant growth, photosynthesis, chloroplast ATP synthase activity and gene expression, chloroplast ultrastructure, intracellular H+ level, and water content of rice seedlings. Acid rain at pH 4.5 remained the chloroplast structure unchanged but increased the expression of six chloroplast ATP synthase subunits, promoted chloroplast ATP synthase activity, and increased photosynthesis and plant growth. Acid rain at pH 4.0 or less decreased leaf water content, destroyed chloroplast structure, inhibited the expression of six chloroplast ATP synthase subunits, decreased chloroplast ATP synthase activity, and reduced photosynthesis and plant growth. In conclusion, acid rain affected the chloroplast ultrastructure, chloroplast ATPase transcription and activity, and P n by changing the acidity in the cells, and thus influencing the plant growth and development. Finally, the effects of simulated acid rain on the test indices were found to be dose-dependent.
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Abbasi T, Poornima P, Kannadasan T, Abbasi SA (2013) Acid rain: past, present, and future. Int J Environ Eng 97:229–272
Bernacchi CJ, Bagley JE, Serbin SP, Ruiz Vera UM, Rosenthal DM, Vanloocke A (2013) Modelling C3 photosynthesis from the chloroplast to the ecosystem. Plant Cell Environ 36:1641–1657
Cao CX, Zhou Q, Han LL, Zhang P, Jiang HD (2010) Effects of simulated acid rain on oilseed rape (Brassica napus) physiological characteristics at flowering stage and yield. J Appl Ecol 21:2057–2062
Chen J, Wang WH, Liu TW, Wu FH, Zheng HL (2013) Photosynthetic and antioxidant responses of liquidambar formosana and schima superba seedlings to sulfuric-rich and nitric-rich simulated acid rain. Plant Physiol Biochem 64:41–51
Del Riego G, Casano LM, Martin M, Sabater B (2006) Multiple phosphorylation sites in the beta subunit of thylakoid ATP synthase. Photosynth Res 89:11–18
Department EoCE (2015) China’s environmental bulletin in 2014.37:1
Dias BB, Leite ML, Farago PV, de Oliveira AV, Beruski GC (2010) Sulfur effect by simulated acid rain on morphophysiological parameters of the bean plant. Acta Sci Agron 32:433–439
Feniouk BA, Suzuki T, Yoshida M (2006) The role of subunit epsilon in the catalysis and regulation of FOF1-ATP synthase. Biochim Biophys Acta Bioenerg 1757:326–338
Ghulam MM, Zghidi Abouzid O, Lambert E, Lerbs-Mache S, Merendino L (2012) Transcriptional organization of the large and the small ATP synthase operons, atpI/H/F/a and atpB/E, in Arabidopsis thaliana chloroplasts. Plant Mol Biol Report 79:259–272
Gravois KA (1998) Optimizing selection for rough rice yield, head rice, and total milled rice. Euphytica 101:151–156
Helliot B, Swennen R, Poumay Y, Frison E, Lepoivre P, Panis B (2003) Ultrastructural changes associated with cryopreservation of banana (Musa spp.) highly proliferating meristems. Plant Cell Rep 21:690–698
Hu H, Wang L, Liao C, Fan C, Zhou Q, Huang X (2014) Combined effects of lead and acid rain on photosynthesis in soybean seedlings. Biol Trace Elem Res 161:136–142
Imran MA, Hussain S, Hussain M, Ch MN, Meo AA (2014) Effect of simulated acid rain (SAR) on some morphochemical aspects of mash (Vigna mungo L.). Pak J Bot 46:245–250
Kartashov IM, Opanasenko VK, Malyan AN (2015) Effects of medium viscosity increasing agents on ATP synthesis in chloroplast thylakoids. Biofizika 60:481–486
Kingsbury RW, Epstein E, Pearcy RW (1984) Physiological responses to salinity in selected lines of wheat. Plant Physiol 74:417–423
Kish Trier E, Briere L, Dunn SD, Wilkens S (2008) The stator complex of the a(1)a(0)-ATP synthase-structural characterization of the E and H subunits. J Mol Biol 375:673–685
Kong R, Zheng X, Huang W, Zhou L, Zhang G (2012) Ion composition and its sources of rainwater from shanghai urban and suburban areas. Urban Environ Urban Ecol 25:22–27
Kong M, Wang F, Yang Z, Mi H (2013) ATPG is required for the accumulation and function of chloroplast ATP synthase in Arabidopsis. Chin Sci Bull 58:3224–3232
Konno H, Nakane T, Yoshida M, Ueoka NH, Hara S, Hisabori T (2012) Thiol modulation of the chloroplast ATP synthase is dependent on the energization of thylakoid membranes. Plant Cell Physiol 53:626–634
Lajtha K, Jones J (2013) Trends in cation, nitrogen, sulfate and hydrogen ion concentrations in precipitation in the United States and Europe from 1978 to 2010: a new look at an old problem. Biogeochemistry 116:303–334
Liang CJ, Ge YQ, Su L, Bu JJ (2015) Response of plasma membrane H+-ATPase in rice (Oryza sativa) seedlings to simulated acid rain. Environ Sci Pollut Res 22:535–545
Liu P, Xia F, Pan J, Chen Y, Peng H, Chen S (2011) Discuss on present situation and countermeasures for acid rain prevention and control in China. Environ Sci Manag 21:4–11
Liu MH, Yi LT, Yu SQ, Yu F, Yin XM (2015) Chlorophyll fluorescence characteristics and the growth response of Elaeocarpus glabripetalus to simulated acid rain. Photosynthetica 53:23–28
Macaulay BM, Enahoro GE (2015) Effects of simulated acid rain on the morphology, phenology and dry biomass of a local variety of maize (Suwan-1) in southwestern Nigeria. Environ Monit Assess 187:1–13
Meng H, Dong DM, Wang J, Yang KN, Tian L, Sun W, Fang CS (2011) Effects of simulated acid rain on main nutritional indicators of three leafy vegetables. Chem Res Chin Univ 27:397–401
Menz FC, Seip HM (2004) Acid rain in Europe and the United States: an update. Environ Sci Pol 7:253–265
Ramlall C, Varghese B, Ramdhani S, Pammenter NW, Bhatt A, Berjak P, Sershen (2015) Effects of simulated acid rain on germination, seedling growth and oxidative metabolism of recalcitrant-seeded Trichilia dregeana grown in its natural seed bank. Physiol Plant 153:149–160
Schmidt M, Luff M, Mollwo A, Kaminski M, Mittag M, Kreimer G (2007) Evidence for a specialized localization of the chloroplast ATP-synthase subunits alpha, beta, and gamma in the eyespot apparatus of Chlamydomonas reinhardtii (Chlorophyceae). J Phycol 43:284–294
Sena L, Chandel N (2012) Physiological roles of mitochondrial reactive oxygen species. Mol Cell 48:158–167
Shirakihara Y, Shiratori A, Tanikawa H, Nakasako M, Yoshida M, Suzuki T (2015) Structure of a thermophilic F-1-ATPase inhibited by an epsilon-subunit: deeper insight into the epsilon-inhibition mechanism. FEBS J 282:2895–2913
Sun Z, Wang L, Chen M, Wang L, Liang C, Zhou Q, Huang X (2012) Interactive effects of cadmium and acid rain on photosynthetic light reaction in soybean seedlings. Ecotoxicol Environ Saf 79:62–68
Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401:914–917
Undem C, Rios EJ, Maylor J, Shimoda LA (2012) Endothelin-1 augments Na+/H+ exchange activity in murine pulmonary arterial smooth muscle cells via rho kinase. PLoS One 7:1602–1603
Walker JE (2013) The ATP synthase: the understood, the uncertain and the unknown. Biochem Soc Trans 41:1–16
Wang LH, Wang W, Zhou Q, Huang XH (2014) Combined effects of lanthanum (III) chloride and acid rain on photosynthetic parameters in rice. Chemosphere 112:355–361
Wen KJ, Liang CJ, Wang LH, Hu G, Zhou Q (2011) Combined effects of lanthanumion and acid rain on growth, photosynthesis and chloroplast ultrastructure in soybean seedlings. Chemosphere 84:601–608
Wyrwicka A, Skłodowska M (2006) Influence of repeated acid rain treatment on antioxidative enzyme activities and on lipid peroxidation in cucumber leaves. Environ Exp Bot 56:198–204
Xie Z, Du Y, Zeng Y, Li Y, Yan M, Jiao S (2009) Effects of precipitation variation on severe acid rain in southern China. J Geogr Sci 19:489–501
Zhang H, Chen TT, Liu LJ, Wang ZQ, Yang JC, Zhang JH (2013) Performance in grain yield and physiological traits of rice in the Yangtze river basin of China during the last 60 yr. Integr Agric 12:57–66
Zhang J, Jiang XD, Li TL, Cao XJ (2014) Photosynthesis and ultrastructure of photosynthetic apparatus in tomato leaves under elevated temperature. Photosynthetica 52:430–436
Zhang YK, Zhu DF, Zhang YP, Chen HZ, Xiang J, Lin XQ (2015) Low pH-induced changes of antioxidant enzyme and ATPase activities in the roots of rice (Oryza sativa L.) seedlings. PLoS One 10:2–6
Zhao Z (2014) Effects of simulated acid rain on photosynthetic physiology characteristics of Ipomoea cairica seedling. Ecotoxicol Environ Sci 19:13–21
Zhao Y, Hou Q (2010) Characteristics of the acid rain variation in China during 1993–2006 and associated causes. Acta Meteorol Sin 24:239–250
Zhu Y, Di T, Xu G, Chen X, Zeng H, Yan F, Shen Q (2009) Adaptation of plasma membrane H+-ATPase of rice roots to low pH as related to ammonium nutrition. Plant Cell Environ 32:1428–1440
Zhu X, Feng Y, Liang G, Liu N, Zhu JK (2013) Aequorin-based luminescence imaging reveals stimulus and tissue-specific Ca2+ dynamics in Arabidopsis plants. Mol Plant 6:444–455
Acknowledgments
The authors are grateful for the financial support of the Natural Science Foundation of China (31170477, 21371100, 21501068), the National Water Pollution Control and Management Technology Major Project (2012ZX07101_013), the Research and Innovation Project for Postgraduate of Higher Education Institutions of Jiangsu Province in 2014 (KYLX_1160), and Ph.D. Programs Foundation of Ministry of Education of China (20130093120006). We thank the LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
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Sun, J., Hu, H., Li, Y. et al. Effects and mechanism of acid rain on plant chloroplast ATP synthase. Environ Sci Pollut Res 23, 18296–18306 (2016). https://doi.org/10.1007/s11356-016-7016-3
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DOI: https://doi.org/10.1007/s11356-016-7016-3