Article | . 2018 Vol. 36, Issue. 4
Effect of Sulfur Dioxide on Physiological Responses, Cysteine, and Glutathione in Pepper and Eggplant



Department of Environmental Horticulture, University of Seoul1
National Institute of Agricultural Sciences, Rural Development Administration2




2018.. 478:486


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This study was carried out to investigate the photosynthetic rate, water use efficiency, chlorophyll content, morphological changes, and cysteine and glutathione contents of pepper and eggplant plants treated with 50 μg·kg sulfur dioxide (SO2) in a controlled environment chamber. Plants were treated with 50 μg·kg -1 SO22 for 24 h/day in a naturally irradiated phytotron. After exposure, SO2 damage was examined by evaluating photosynthetic rate, water use efficiency (WUE), chlorophyll and carotenoid content, visible injury, stomata characteristics, and cysteine and glutathione content. The photosynthetic rate was significantly lower in treated plants compared to the control, and WUE increased with the SO2 treatment in both pepper and eggplant compared to untreated plants. The chlorophyll and carotenoid content also decreased in plants treated with SO2. The visible injury to leaves appeared after about 14 d of SO2 exposure in pepper and 18 d after SO2 exposure in eggplant. The leaves had yellow and white spots on their surface in both the pepper and eggplant plants. Over a period of SO2 exposure, necrosis was observed in both pepper and eggplant leaves. Stomatal density and size decreased in response to SO2 exposure in both of pepper and eggplant. The cysteine and glutathione levels significantly increased after SO2 exposure in both pepper and eggplant.



1. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta Vulgaris. Plant Physiol 24:1-15. doi:10.1104/pp. 24.1.1  

2. Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163-190. doi:10.1007/ s11099-013-0021-6  

3. Baek SG, Woo SY (2010) Physiological and biochemical responses of two tree species in urban areas to different air pollution levels. Photosynthetica 48:23-29. doi:10.1007/s11099-010-0005-8  

4. Black CR, BLACK VJ (1979) The effects of low concentrations of sulphur dioxide on stomatal conductance and epidermal cell survival in field bean (Vicia faba L.). J Exp Bot 30:291-298. doi:10.1093/jxb/30.2.291  

5. Brychkova G, Xia Z, Yang G, Yesbergenova Z, Zhang Z, Davydov O, Fluhr R, Sagi M (2007) Sulfite oxidase protects plants against sulfur dioxide toxicity. Plant J 50:696-709. doi:10.1111/j.1365-313X.2007.03080.x  

6. Cheng HC, Woo SY, Lee SH, Baek SG (2010) Photosynthesis, antioxidant enzyme, and anatomical difference of Sedum kamtschaticum and Hosta longipes to ozone. Korean Hortic Sci Technol 28:394-402  

7. Cheng HC, Woo SY, Lee SH, Kwak MJ, Kim KN (2013) Physiological and biochemical responses of Sedum kamtschaticum and Hosta longipes to ozone stress. Korean J Hortic Sci Technol 31:1-7. doi:10.7235/hort.2013.12007  

8. Choi D, Toda H, Kim Y (2014) Effect of sulfur dioxide (SO) on growth and physiological activity in Alnus sieboldiana at Miyakejima Island in Japan. Ecol Res 29:103-110. doi:10.1007/s11284-013-1103-4  

9. Dhir B, Siddiqi TO, Iqbal M (2001) Stomatal and photosynthetic responses of Cichorium intybus leaves to sulfur dioxide treatment at different stages of plant development. J Plant Biol 44:97-102. doi:10.1007/BF03030282  

10. Gheorghe IF, Ion B (2011) The effects of air pollutants on vegetation and the role of vegetation in reducing atmospheric pollution. Intech Publisher, Shanghai, China, pp 256-259  

11. Gigolashvili T, Kopriva S (2014) Transporters in plant sulfur metabolism. Front Plant Sci 5:442. doi:10.3389/fpls.2014.00442  

12. Govindjee (2012) Photosynthesis V2: Development, carbon metabolism, and plant productivity. Elsevier, USA, pp 263-273   

13. Guderian R (2012) Air pollution: phytotoxicity of acidic gases and its significance in air pollution control. Springer Science & Business Media, Berlin, Germany, p 33  

14. Gupta A (2016) Effect of air pollutants on plant gaseous exchange process: effect on stomata and respiration. In Anonymous Plant Responses to Air Pollution, Springer, Singapore, pp 85-92. doi:10.1007/978-981-10-1201-3_8  

15. Haworth M, Elliott-Kingston C, Gallagher A, Fitzgerald A, McElwain JC (2012) Sulphur dioxide fumigation effects on stomatal density and index of non-resistant plants: implications for the stomatal palaeo-[CO] proxy method. Rev Palaeobot Palynol 182:44-54. doi:10.1016/j.revpalbo.2012.06.006  

16. Heather G (2003) Effect of air pollution on agricultural crops. Ministry of Agriculture, Air Pollution on Agricultural Crops, Ontario, Canada, p 85   

17. Hernández-Pérez A, Valdez-Aguilar LA, Villegas-Torres OG, Alía-Tejacal I, Trejo-Téllez LI, Sainz-Aispuro MdJ (2016) Effects of ammonium and calcium on lisianthus growth. Hortic Environ Biotechnol. 57:123-131. doi:10.1007/s13580-016-0004-1  

18. Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901-908. doi:10.1016/j.revpalbo.2012.06.006  

19. Heyneke E, Strauss AJ, Strasser RJ, Krüger GHJ (2012) Open-top chamber facility to study air pollution impacts in South Africa. Part II: SO–drought interactions on yield, photosynthesis and symbiotic nitrogen fixation in soybean. South Afr J Plant Soil 29:9-23. doi:10.1080/02571862.2012.688373  

20. Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18:605-618. doi:10.1111/j.1365-3040.1995.tb00562.x  

21. Hirase K, Molin WT (2003) Sulfur assimilation in plants and weed control: Potential targets for novel herbicides and action sites of certain safeners. Weed Biol Mgt 3:147-157. doi:10.1046/j.1445-6664.2003.00098.x  

22. Je SM, Son SG, Woo SY, Byun KO, Kim CS (2006) Photosynthesis and chlorophyll contents of Chloranthus glaber under different shading treatments. Korean J Agric For Meteorol 8:54-60   

23. Joshi N, Chauhan A, Joshi PC (2009) Impact of industrial air pollutants on some biochemical parameters and yield in wheat and mustard plants. Environmentalist 29:398-404. doi:10.1007/s10669-009-9218-4  

24. Khan MR, Khan MW (1993) The interaction of SO and root-knot nematode on tomato. Environ Pollution 81:91-102. doi:10.1016/ 0269-7491(93)90072-V  

25. Kim JS, Shim IS, Kim IS, Kim MJ (2010) Changes of cysteine, glutathione and ascorbic acid content in Chinese cabbage, head lettuce and spinach by the growth stage. Korean J Hortic Sci Technol 28:186-191   

26. Kim YJ (2006) An investigation on crop gas poisoning and greenhouse heating. J Bio-Environ Control 15:180-186   

27. Kitajima K, Hogan KP (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26:857-865. doi:10.1046/j.1365-3040.2003.01017.x  

28. Knabe W (1976) Effects of sulfur dioxide on terrestrial vegetation. J Human Environ 5:213-218   

29. Kocsy G, von Ballmoos P, Suter M, Rüegsegger A, Galli U, Szalai G, Galiba G, Brunold C (2000) Inhibition of glutathione synthesis reduces chilling tolerance in maize. Planta 211:528-536. doi:10.1007/s004250000308  

30. Kropff MJ (1987) Physiological effects of sulphur dioxide. 1. The effect of SO on photosynthesis and stomatal regulation of Vicia faba L. Plant Cell Environ 10:753-760. doi:10.1111/1365-3040.ep11604762  

31. Kumari S, Prakash I (2015) Changes in micromorphology of plant Sida veronicaefolia in response to air pollution stress in Meerut City. In Proceeding of the UGC Sponsored National Seminar on The Role of Biology in Bringing Second Green Revolution, India, pp 26-32   

32. Lauenroth WK, Dodd JL (1981) Chlorophyll reduction in western wheatgrass (Agropyron smithii Rydb.) exposed to sulfur dioxide. Water Air Soil Pollut 15:309-315. doi:10.1007/BF00285044  

33. Lee HK, Khaine I, Kwak MJ, Jang JH, Lee TY, Lee JK, Kim IR, Kim WI, Oh KS, et al (2017) The relationship between SO exposure and plant physiology: A mini review. Hortic Environ Biotechnol 58:523-529. doi:10.1007/s13580-017-0053-0  

34. Lee JY, Je SM, Lee SH, Woo SY (2013) The effects of ozone on photosynthesis, antioxidative enzyme activity and leaf anatomical response in the indoor plants and Japanese red pine. J Kor For Soc 102:601-607. doi:10.14578/jkfs.2013.102.4.601  

35. Lee SH, Seo SG, Lee YB (2003) Effects of elevated CO, SO, and water stress on photosynthesis and stomatal responses in Perilla frutescens var. japonica. J Kor Soc Hortic Sci 44:625-629   

36. Lee YR, Choi SR, Kwon OK, Huh EJ (2009) Injury symptoms of orchids by sulfur dioxide gases in greenhouse. Flower Res J 17:237-241   

37. Lee YY, Kang YJ, Lee YB (2001) The induction of secondary toxic substances and antioxidative enzymes by SO fumigation in foliage plants. Korean J Environ Agric 20:44-49   

38. MAFRA (Ministry of Agriculture, Food and Rural Affairs) (2015) Vegetable in cultivated greenhouse status and vegetable production. MAFRA, Sejong, Korea (in Korean)   

39. Malhotra SS, Hocking D (1976) Biochemical and cytological effects of sulphur dioxide on plant metabolism. New Phytol 76:227-237. doi:10.1111/j.1469-8137.1976.tb01456.x  

40. McAinsh MR, Evans NH, Montgomery LT, North KA (2002) Calcium signalling in stomatal responses to pollutants. New Phytol 153:441-447. doi:10.1046/j.0028-646X.2001.00336.x  

41. Medrano H, Tomás M, Martorell S, Flexas J, Hernández E, Rosselló J, Pou A, Escalona J, Bota J (2015) From leaf to whole-plant water use efficiency (WUE) in complex canopies: limitations of leaf WUE as a selection target. Crop J 3:220-228. doi:10.1016/j.cj.2015.04.002  

42. Nandi PK, Agrawal M, Agrawal SB, Rao DN (1990) Physiological responses of Vicia faba plants to sulfur dioxide. Ecotoxicol Environ Saf 19:64-71. doi:10.1016/0147-6513(90)90079-K  

43. Nikiforova V, et al (2006) Effect of sulfur availability on the integrity of amino acid biosynthesis in plants. Amino Acids 30:173-183. doi:10.1007/s00726-005-0251-4  

44. Njålsson R (2005) Glutathione synthetase deficiency. Cellular and Molecular Life Sciences (CMLS) 62:1938-1945. doi:10.1007/ s00018-005-5163-7  

45. Noctor G, Mhamdi A, Chaouch S, Han YI, Neukermans J, Marquez‐garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454-484. doi:10.1111/j.1365-3040.2011.02400.x  

46. Novak K, Skelly JM, Schaub M, Kräuchi N, Hug C, Landolt W, Bleuler P (2003) Ozone air pollution and foliar injury development on native plants of Switzerland. Environ Pollution 125:41-52. doi:10.1016/S0269-7491(03)00085-X  

47. Peiser GD, Yang SF (1977) Chlorophyll destruction by the bisulfite-oxygen system. Plant Physiol 60:277-281. doi:10.1016/S0269-7491 (03)00085-X  

48. Singh RP, Tripathi P, Kumar A, Gupta A, Singh K (2013) Effect of SO on chlorophyll content and leaf temperature on leaves of potato (Solanum tuberosum L.) genotypes. Department of Agricultural Meteorology. University of Agriculture and Technology, Kumarganj, India, pp 224-229   

49. Swain SC, Padhi SK (2015) Effect of sulphur dioxide on growth, chlorophyll and sulphur contents of pomegranate. Trop Agric Res Extension 16:21-24. doi:10.4038/tare.v16i1.5269  

50. Upreti DK, Divakar PK, Shukla V, Bajpai R (2015) Recent advances in lichenology: modern methods and approaches in lichen systematics and culture techniques. Springer, India, pp 98-101. doi:10.1007/978-81-322-2235-4  

51. Verma S, Mishra SN (2005) Putrescine alleviation of growth in salt stressed Brassica juncea by inducing antioxidative defense system. J Plant Physiol 162:669-677. doi:10.1016/j.jplph.2004.08.008  

52. Von Caemmerer SV, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376-387. doi:10.1007/BF00384257  

53. Wali B, Iqbal M (2004) Plant growth, stomatal response, pigments and photosynthesis of Althea officinalis as affected by SO stress. Indian J Plant Physiol 9:224-233   

54. Winner WE, Mooney HA, Goldstein RA (1985) Sulfur dioxide and vegetation: physiology, ecology, and policy issues. Stanford University Press, California, USA, pp 1-22   

55. Woo SY, Kwon KW, Lee JC, Choi JH, Kang BS (2003) Recovery of net photosynthetic rate after SO fumigation in Quercus acutissima, Pinus densiflora, Populus alba × glandulosa, and Acanthopanax sessiliflorus. Photosynthetica 41:319-320. doi:10.1023/B:PHOT. 0000011971.85208.8f  

56. Yunus M, Singh N, De Kok LJ (2013) Environmental stress: indication, mitigation and eco-conservation. Springer Science & Business Media, Dorderecht, the Netherlands, pp 28-32  

57. Zhang X, Zang R, Li C (2004) Population differences in physiological and morphological adaptations of Populus davidiana seedlings in response to progressive drought stress. Plant Sci 166:791-797. doi:10.1016/j.plantsci.2003.11.016