Acid Rain Deposition Modulates Photosynthesis, Enzymatic and Non-enzymatic Antioxidant Activities in Tomato

  • Biswojit Debnath
  • Muhammad Irshad
  • Sangeeta Mitra
  • Min Li
  • Hafiz Muhammad Rizwan
  • Shuang Liu
  • Tenfei Pan
  • Dongliang Qiu
Research paper


Acid rain is one of the serious environmental issues causing morphological and physiological changes in plants. However, the impact of acid rain to vegetable crops remains indescribable. This study explored the effects of two pH levels of simulated acid rain (SAR) on photosynthesis and activity of different enzymatic and non-enzymatic key antioxidant compounds compared with control in two different tomato cultivars. With the increasing levels of acidity of SAR, decreased significantly the plant growth, chlorophyll, carotenoids, soluble protein and soluble sugar contents in leaves of both tomato cultivars but decreased percentages were more in Red Rain than Micro-Tom cultivar of tomato. Different enzymatic antioxidant key compounds accumulation was the maximum at pH 3.5 and degraded at pH 2.5 of SAR treatment for both tomato cultivars. In contrast, the growth of hydrogen peroxide (H2O2), malondialdehyde (MDA) and proline content was increased by SAR treatment which depends on the level of pH value of SAR. In addition, marked increase in phenolic, flavonoid and reducing antioxidant activity was found at pH 3.5 followed by pH 2.5 of SAR and control in both tomato cultivars. Our findings suggested that the tomato seedlings produced more reactive oxygen species (ROS) scavenging enzymatic and non-enzymatic antioxidant compounds to SAR stress at 3.5 pH level. Meanwhile, the inhibition of growth as well as photosynthesis of tomato seedlings and the severity of oxidative damage were found at pH 2.5 of SAR which might be depend on the types of cultivar.


Simulated acid rain Solanum lycopersicum Reactive oxygen species Photosynthesis Antioxidant compound 



We are thankful to Yueting Sun, Xiaocao Lu for their helpful assistance in purchasing reagents. This study was supported by the National Natural Science Grant of China (Award no. 30400061), Natural Science Foundation of Fujian Province, China (2011J01082) and Special Fund for Science and Technology Innovation of FAFU (CXZX2016107).


  1. Ahmed IM, Cao F, Zhang M, Chen X, Zhang G, Wu F (2013) Difference in yield and physiological features in response to drought and salinity combined stress during anthesis in Tibetan wild and cultivated barleys. PLoS ONE 8(10):e77869CrossRefGoogle Scholar
  2. Al Hassan M, Fuertes MM, Sanchez FJR, Vicente O, Boscaiu M (2015) Effects of salt and water stress on plant growth and on accumulation of osmolytes and antioxidant compounds in cherry tomato. Not Bot Horti Agrobot Cluj-Napoca 43(1):1Google Scholar
  3. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50(1):601–639CrossRefGoogle Scholar
  4. Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207CrossRefGoogle Scholar
  5. Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76CrossRefGoogle Scholar
  6. Bettaieb I, Hamrouni-Sellami I, Bourgou S, Limam F, Marzouk B (2011) Drought effects on polyphenol composition and antioxidant activities in aerial parts of Salvia officinalis L. Acta Physiol Plant 33(4):1103–1111CrossRefGoogle Scholar
  7. Bhattacharjee S (2005) Reactive oxygen species and oxidative burst: roles in stress, senescence and signal transduction in plants. Curr Sci 89:1113–1121Google Scholar
  8. Bouwman AF, Vuuren DPV, Derwent RG, Posch M (2002) A global analysis of acidification and eutrophication of terrestrial ecosystems. Water Air Soil Pollut 141(1–4):349–382CrossRefGoogle Scholar
  9. Bradford MM (1976) A rapid method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72((s 1–2)):248–254CrossRefGoogle Scholar
  10. Chen J, Li W, Gao F (2010) Biogeochemical effects of forest vegetation on acid precipitation-related water chemistry: a case study in southwest China. J Environ Monit Jem 12(10):1799–1806CrossRefGoogle Scholar
  11. Chen J, Wang W-H, Liu T-W, Wu F-H, Zheng H-L (2013) Photosynthetic and antioxidant responses of Liquidambar formosana and Schima superba seedlings to sulfuric-rich and nitric-rich simulated acid rain. Plant Physiol Biochem 64:41–51CrossRefGoogle Scholar
  12. Croft H, Chen J, Zhang Y (2014) The applicability of empirical vegetation indices for determining leaf chlorophyll content over different leaf and canopy structures. Ecol Complexity 17:119–130CrossRefGoogle Scholar
  13. Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers Environ Sci 2(53):53Google Scholar
  14. Dolatabadian A, Sanavy SAMM, Gholamhoseini M, Joghan AK, Majdi M, Kashkooli AB (2013) The role of calcium in improving photosynthesis and related physiological and biochemical attributes of spring wheat subjected to simulated acid rain. Physiol Mol Biol Plants 19(2):189–198CrossRefGoogle Scholar
  15. Evans LS (1984) Botanical aspects of acidic precipitation. Bot Rev 50(4):449–490CrossRefGoogle Scholar
  16. Eyidogan F, Öz MT (2007) Effect of salinity on antioxidant responses of chickpea seedlings. Acta Physiol Plant 29(5):485CrossRefGoogle Scholar
  17. Gapińska M, Skłodowska M, Gabara B (2008) Effect of short-and long-term salinity on the activities of antioxidative enzymes and lipid peroxidation in tomato roots. Acta Physiol Plant 30(1):11CrossRefGoogle Scholar
  18. Garg N, Manchanda G (2009) ROS generation in plants: boon or bane? Plant Biosys 143(1):81–96CrossRefGoogle Scholar
  19. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930CrossRefGoogle Scholar
  20. Halman JM, Schaberg PG, Hawley GJ, Eagar C (2008) Calcium addition at the Hubbard Brook Experimental Forest increases sugar storage, antioxidant activity and cold tolerance in native red spruce (Picea rubens). Tree Physiol 28(6):855–862CrossRefGoogle Scholar
  21. Hamid N, Jawaid F (2009) Effect of short-term exposure of two different concentrations of sulphur dioxide and nitrogen dioxide mixture on some biochemical parameter of soybean (Glycine max (L.) Merr.). Pak J Bot 41(5):2223-2228Google Scholar
  22. Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207(4):604–611CrossRefGoogle Scholar
  23. 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(1):136–142CrossRefGoogle Scholar
  24. Kholová J, Sairam R, Meena R, Srivastava G (2009) Response of maize genotypes to salinity stress in relation to osmolytes and metal-ions contents, oxidative stress and antioxidant enzymes activity. Biol Plant 53(2):249–256CrossRefGoogle Scholar
  25. Kita I, Sato T, Kase Y, Mitropoulos P (2004) Neutral rains at Athens, Greece: a natural safeguard against acidification of rains. Sci Total Environ 327(1):285–294CrossRefGoogle Scholar
  26. Kováčik J, Klejdus B, Bačkor M, Stork F, Hedbavny J (2011) Physiological responses of root-less epiphytic plants to acid rain. Ecotoxicology 20(2):348–357CrossRefGoogle Scholar
  27. Kováčik J, Klejdus B, Štork F, Hedbavny J (2012) Physiological responses of Tillandsia albida (Bromeliaceae) to long-term foliar metal application. J Hazard Mater 239:175–182CrossRefGoogle Scholar
  28. Li Y (2009) Physiological responses of tomato seedlings (Lycopersicon esculentum) to salt stress. Mod Appl Sci 3(3):171CrossRefGoogle Scholar
  29. Liang C, Wang W (2013) Antioxidant response of soybean seedlings to joint stress of lanthanum and acid rain. Environ Sci Pollut Res 20(11):8182–8191CrossRefGoogle Scholar
  30. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Limited, London, UKGoogle Scholar
  31. Liu J, Zhou G, Yang C, Ou Z, Peng C (2007) Responses of chlorophyll fluorescence and xanthophyll cycle in leaves of Schima superba Gardn. & Champ. and Pinus massoniana Lamb. to simulated acid rain at Dinghushan Biosphere Reserve, China. Acta Physiol Plant 29(1):33–38CrossRefGoogle Scholar
  32. Liu T-W, Wu F-H, Wang W-H, Chen J, Li Z-J, Dong X-J, Patton J, Pei Z-M, Zheng H-L (2011) Effects of calcium on seed germination, seedling growth and photosynthesis of six forest tree species under simulated acid rain. Tree Physiol 31(4):402–413CrossRefGoogle Scholar
  33. Liu TW, Niu L, Fu B, Chen J, Wu FH, Chen J, Wang WH, Hu WJ, He JX, Zheng HL (2013) A transcriptomic study reveals differentially expressed genes and pathways respond to simulated acid rain in Arabidopsis thaliana. Genome 56(1):49–60CrossRefGoogle Scholar
  34. Løvdal T, Olsen KM, Slimestad R, Verheul M, Lillo C (2010) Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. Phytochemistry 71(5):605–613CrossRefGoogle Scholar
  35. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51(345):659–668CrossRefGoogle Scholar
  36. Moyle L (2008) Ecological and evolutionary genomics in the wild tomatoes (Solanum sect. Lycopersicon). Evolution 62(12):2995–3013CrossRefGoogle Scholar
  37. Neves NR, Oliva MA, Da CCD, Costa AC, Ribas RF, Pereira EG (2009) Photosynthesis and oxidative stress in the restinga plant species Eugenia uniflora L. exposed to simulated acid rain and iron ore dust deposition: potential use in environmental risk assessment. Sci Total Environ 407(12):3740–3745Google Scholar
  38. Ordonez A, Gomez J, Vattuone M (2006) Antioxidant activities of Sechium edule (Jacq.) Swartz extracts. Food Chem 97(3):452–458CrossRefGoogle Scholar
  39. Pan T, Li Y, Ma C, Qiu D (2015) Calcium affecting protein expression in longan under simulated acid rain stress. Environ Sci Pollut Res 22(16):12215–12223CrossRefGoogle Scholar
  40. Polishchuk AV, Vodka MV, Belyavskaya NA, Khomochkin AP, Zolotareva EK (2016) The effect of acid rain on ultrastructure and functional parameters of photosynthetic apparatus in pea leaves. Cell Tissue Biol 10(3):250–257CrossRefGoogle Scholar
  41. Posmyk M, Kontek R, Janas K (2009) Antioxidant enzymes activity and phenolic compounds content in red cabbage seedlings exposed to copper stress. Ecotoxicol Environ Saf 72(2):596–602CrossRefGoogle Scholar
  42. Quan LJ, Zhang B, Shi WW, Li HY (2008) Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. J Integ Plant Biol 50(1):2–18CrossRefGoogle Scholar
  43. Shereefa LAH, Kumaraswamy M (2016) Reactive oxygen species and ascorbate–glutathione interplay in signaling and stress responses in Sesamum orientale L. against Alternaria sesami (Kawamura) Mohanty and Behera. J Saudi Soc Agril Sci 15(1):48-56Google Scholar
  44. Shi Q, Bao Z, Zhu Z, Ying Q, Qian Q (2006) Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regul 48(2):127–135CrossRefGoogle Scholar
  45. Škerget M, Kotnik P, Hadolin M, Hraš AR, Simonič M, Knez Ž (2005) Phenols, proanthocyanidins, flavones and flavonols in some plant materials and their antioxidant activities. Food Chem 89(2):191–198CrossRefGoogle Scholar
  46. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. Chlorophyll a Fluorescence 19:321–362Google Scholar
  47. 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(4):62CrossRefGoogle Scholar
  48. Tausz M, Hietz P, Briones O (2001) The significance of carotenoids and tocopherols in photoprotection of seven epiphytic fern species of a Mexican cloud forest. Funct Plant Biol 28(8):775–783CrossRefGoogle Scholar
  49. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151(1):59–66CrossRefGoogle Scholar
  50. Wen K, Liang C, Wang L, Hu G, Zhou Q (2011) Combined effects of lanthanumion and acid rain on growth, photosynthesis and chloroplast ultrastructure in soybean seedlings. Chemosphere 84(5):601–608CrossRefGoogle Scholar
  51. 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(2):198–204CrossRefGoogle Scholar
  52. Xu RK, Ji GL (2001) Effects of H2SO4 and HNO3 on soil acidification and aluminum speciation in variable and constant charge soils. Water Air Soil Pollut 129(1–4):33–43CrossRefGoogle Scholar
  53. Yemm E, Willis A (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57(3):508CrossRefGoogle Scholar
  54. Yuan X, Yang Z, Li Y, Liu Q, Han W (2016) Effects of different levels of water stress on leaf photosynthetic characteristics and antioxidant enzyme activities of greenhouse tomato. Photosynthetica 54(1):28–39CrossRefGoogle Scholar
  55. Zhang J, Wang J, Zhao Z, Chen Y, Dou W (2005) Effects of simulated acid rain on physiological and biochemical characters of eggplant, the host plant of Tetranychus cinnabarinus. Ying yong sheng tai xue bao. J Appl Ecol 16(3):450–454Google Scholar
  56. Zhang Y, Zhang L, Hu X-H (2014) Exogenous spermidine-induced changes at physiological and biochemical parameters levels in tomato seedling grown in saline-alkaline condition. Bot Stud 55(1):58CrossRefGoogle Scholar

Copyright information

© University of Tehran 2018

Authors and Affiliations

  • Biswojit Debnath
    • 1
    • 2
  • Muhammad Irshad
    • 1
  • Sangeeta Mitra
    • 1
  • Min Li
    • 1
  • Hafiz Muhammad Rizwan
    • 1
  • Shuang Liu
    • 1
  • Tenfei Pan
    • 1
  • Dongliang Qiu
    • 1
  1. 1.College of HorticultureFujian Agriculture and Forestry UniversityFuzhouChina
  2. 2.Department of HorticultureSylhet Agricultural UniversitySylhetBangladesh

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