Article | 10. 2015 Vol. 33, Issue. 5
Proline, Sugars, and Antioxidant Enzymes Respond to Drought Stress in the Leaves of Strawberry Plants



College of Life Science, Jiangsu Normal University1




2015.10. 625:632


PDF XML




Drought is a severe abiotic stress that affects global crop production. A drought model was created for ‘Toyonoka’ Fragaria × ananassa, and the effects of drought stress on contents of proline, sugars, and antioxidant enzyme activities were investigated. Strawberry transplants with identical growth were chosen for the experiments and the randomized design included four replications (10 plants per block). The experimental sets differed in the moisture level of the culture medium relative to the range of moisture content as follows: control, 70-85%; mild drought stress, 50-60%; moderate drought stress, 40-50%; and severe drought stress, 30-40%. Drought stress was imposed by limiting irrigation. Plants were sampled and physiological parameters were measured on 0, 2, 4, 6, 8, and 10 days after the commencement of drought stress. The water potential of strawberry leaves decreased in the plants under mild, moderate, and severe stress during the course of the water stress treatment and exhibited a significant difference from the control. Strawberry leaves subjected to drought stress had higher accumulation of proline, sugars, and malondialdehyde, and higher activities of superoxide dismutase, peroxidase, and catalase than leaves of control plants. Malondialdehyde levels increased in parallel with the severity and duration of drought stress. By contrast, antioxidant enzyme activity displayed dynamic responses to drought stress, first increasing and subsequently decreasing as the severity and duration of drought stress increased. These results suggest that strawberry plants respond to drought stress by altering the activities of antioxidant enzymes and the levels of osmotically active metabolites. These biochemical response changes may confer adaptation to drought stress and improve the capacity of plants to withstand water-deficit conditions.



1. Aebi, H. 1984. Isolation, purification, characterization and assay of antioxygenic enzymes: catalase in vitro. Method. Enzymol. 105:121-126.  

2. Ashraf, M. and P.J.C. Harris. 2008. Physiological and biochemical adaptations of Cynodon dactylon (L.) Pers. from the salt range (Pakistan) to salinity stress. Flora 203:683-694.  

3. Bacelar, E.A., D.L. Santos, J.M. Moutinho-Pereira, B.C. Gonçalves, H.F. Ferreira, and C.M. Correia. 2006. Immediate responses and adaptive strategies of three olive cultivars under contrasting water availability regimes: changes on structure and chemical composition of foliage and oxidative damage. Plant Sci. 170: 596-605.  

4. Baily, C., A. Benamar, F. Corbineau, and D. Dôme. 1996. Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seed as related to deterioration during accelerated aging. Physiol. Plant 97:104-110.  

5. Blanke, M.M. and D.T. Cooke. 2006. Water channels in strawberry and their role in the plant’s response to water stress. Acta Hortic.708:65-68.  

6. Bohnert, H.J. and R.G. Jensen. 1996. Strategies for engineering water stress tolerance in plants. Trends Biotechnol. 14:89-97.  

7. Bordonaba, J.G. and L.A. Terry. 2010. Manipulating the taste- related composition of strawberry fruits (Fragaria × ananassa) from different cultivars using deficit irrigation. Food Chem. 122:1020-1026.  

8. Chance, B. and A.C. Maehly. 1995. Assay of catalases and peroxidases, p. 764-775. In: Colowick S.P. and N.O. Kaplan (eds): Methods Enzymol. Acad. Press, New York, USA.  

9. Claussen, W. 2005. Proline as a measure of stress in tomato plants. Plant Sci. 168:241-248.  

10. Devi, R., N. Kaur, and A.K. Gupta. 2012. Potential of antioxidant enzymes in depicting drought tolerance of wheat (Triticum aestivum L.). Indian J. Biochem. Biophys. 49:257-265.   

11. Grant, O.M., A.W. Johnson, M.J. Davies, C.M. James, and D.W. Simpson. 2010. Physiological and morphological diversity of cultivated strawberry (Fragaria × ananassa) in response to water deficit. Environ. Exp. Bot. 68:264-272.  

12. Hare, P.D., W.A. Cress, and J. Van Staden. 1998. Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 21:535-553.  

13. Hessini, K., M. Ghandour, A.A. Albouchi, H.W. Soltani Koyro, and C. Abdelly. 2008. Biomass production, photosynthesis, and leaf water relations of Spartina alterniflora under moderate water stress. J. Plant Res. 121:311-318.  

14. Howarth, C.J. 2005. Genetic improvements of tolerance to high temperature, p: 277-280. In: M. Ashraf, P.J.C. Harris (eds.). Abiotic Stresses: Plant Resistance Through Breeding and Molecular Approaches. Howarth Press Inc., New York, USA.  

15. Kim, S.K., R.N. Bae, and C.H. Chun. 2011. Changes in bioactive compounds contents of ‘Maehyang’ and ‘Seolhyang’ strawberry fruits by UV light illumination. Kor. J. Hort. Sci. Technol. 29:172-180.  

16. Kim, K.S., S.H. Park, and M.A. Jenks. 2007. Changes in leaf cuticular waxes of sesame (Sesamum indicum L.) plants exposed to water deficit. J. Plant Physiol. 164:1134-1143.  

17. Klamkowski, K. and W. Treder. 2006. Morphological and physiological responses of strawberry plants to water stress. Agric. Conspec. Sci. 71:159-165.  

18. Krüger, E., G. Schmidt, and S. Rasim. 2002. Effect of irrigation on yield, fruit size and firmness of strawberry cv. Elsanta. Acta Hortic. 567:471-474.  

19. Li, D.D., Z.S. Luo, W.S. Mou, Y.S. Wang, T.J. Ying, and L.C. Mao. 2014. ABA and UV-C effects on quality, antioxidant capacity and anthocyanin contents of strawberry fruit (Fragaria × ananassa Duch.). Postharvest Biol. Technol. 90:56-62.  

20. Liu, F., C.S. Savi´, C.R. Jensen, A. Shahnazari, S.E. Jacobsen, C.R.Stiki´, and M.N. Andersen. 2007. Water relations and yield of lysimeter-grown strawberries under limited irrigation. Sci. Hortic. 111:128-132.  

21. Luo X.L. and Q.F. Huang. 2011. Relationships between Leaf and Stem Soluble Sugar Content and Tuberous Root Starch Accu-mulation in Cassava. J. Agric. Sci. 3:64.  

22. Martinez, J.P., S. Lutts, A. Schanck, M. Baji, and J.M. Kinet. 2004. Is osmotic adjustment required for water stress resistance in the mediterranean shrub Atriplex halimus L. J. Plant Physiol. 161:1041-1051.  

23. Meloni, D.A., M.A. Oliva, C.A. Martinez, and J. Cambraia. 2003. Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ. Exp. Bot. 49:69-76.  

24. Morgan, J.M. 1984. Osmoregulation and water stress in higher plants. Annual Rev. Plant Physiol. 35:299-319.  

25. Mishra, R.K. and G.S. Singhal. 1992. Function of photosynthetic apparatus of intact wheat leaves under high light and heat stress and its relationship with peroxidation of thylakoid lipids. Plant Physiol. 98:1-6.  

26. Murshed, R., F. Lopez-Lauri, and H. Sallanon. 2013. Effect of water stress on antioxidant systems and oxidative parameters in fruits of tomato (Solanum lycopersicon L, cv. Micro-tom). Physiol. Mol. Biol. Plant. 19:363-378.  

27. Na, Y.W., H.J. Jeong, S.Y. Lee, H.G. Choi, S.H. Kim, and I.R. Rho. 2014. Chlorophyll fluorescence as a diagnostic tool for abiotic stress tolerance in wild and cultivated strawberry species. Hortic. Environ. Biotechnol. 55:280-286.  

28. Nanjo, T., M. Kobayashi, Y. Yoshiba, Y. Sanada, K. Wada, H. Tsukaya, Y. Kakubari, K. Yanaguchi-Shinozaki, and K. Shinozaki. 1999. Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. Plant J.18:185-193.   

29. Petridis, A., Therios, I., Samouris, G., Koundouras, S., and A. Giannakoul. 2012. Effect of water deficit on leaf phenolic composition, gas exchange, oxidativedamage and antioxidant activity of four Greek olive (Olea europaea L.) cultivars. Plant Physiol. Biochem. 60:1-11.  

30. Pourtaghi, A., F. Darvish, D. Habibi, G. Nourmohammadi, and J. Daneshian. 2011. Effect of irrigation water deficit on antioxidant activity and yield of some sunflower hybrids. Aust. J. Crop Sci. 5:197-204.  

31. Rahnama, H. and H. Ebrahimzadeh. 2005. The effect of NaCl on antioxidant enzyme activities in potato seedlings. Biol. Plant. 49:93-97.   

32. Remorini, D., J.C. Melgar, L. Guidi, E. Degl’Innocenti, S. Castelli, M.L. Traversi, R. Massai, and M. Tattini. 2009. Interaction effects of root-zone salinity and solar irradiance on the physiology and biochemistry of Olea europaea. Environ. Exp. Bot. 65: 210-219.  

33. Samaras, Y., R.A. Bressan, L.N. Csonka, M.G. Garci´a-Ri´os, M. Paino D’Urzo, and D. Rhodes. 1995. Proline accumulation during drought and salinity, p. 161-187. In: N Smirnoff (ed.). Environment and plant metabolism. Bios Scientific Publishers, Oxford, USA.   

34. Sánchez-Rodríguez, E., M. Rubio-Wilhelmi, B. Blasco, R. Leyva, L. Romero, and J.M. Ruiz. 2012 Antioxidant response resides in the shoot in reciprocal grafts of drought-tolerant and drought- sensitive cultivars in tomato under water stress. Plant Sci. 188:89-96.  

35. Shigeoka S., T. Ishikawa, M. Tamoi, Y. Miyagawa, T. Takeda, Y. Yabuta, and K.J. Yoshimura. 2002. Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 53:1305-1319.  

36. Sofo, A., B. Dichio, C. Xiloyannis, and A. Masia. 2004. Effects of different irradiance levels on some antioxidant enzymes and on malondialdehyde content during rewatering in olive tree. Plant Sci. 166:293-302.  

37. Sun, C.H., D. Wang, Y.L. Hu, X.H. Li, W.D. Zhang, J. Sun, and X.L. Gao. 2013. Effects of salicylic acid on physiological characteristics of strawberry leaves under drought stress. Eur. J. Hortic. Sci. 78:106-111.  

38. Terry L, G.A. Chope, and J.G. Bordonaba. 2007. Effect of water deficit irrigation and inoculation with Botrytis cinerea on strawberry (Fragaria × ananassa) fruit quality. J Agric. Food Chem. 55::10812-10819.  

39. Wang, H. and J.Y. Jin. 2005. Photosynthetic rate, chlorophyll fluorescence parameters and lipid peroxidation of maize leaves as affected by zinc deficiency. Photosynthetica 43:591-596.  

40. Yang, X.G, H. Fu, H.R. Zhang, and J.D. Zhao. 2006. Effect of soil water stress on leaf water potential and biomass of Zygophyllum xanthoxylum during seedling stage. Acta Pratac. Sin. 15(2): 37-41.  

41. Yin, D., S. Chen, F. Chen, Z. Guan, and W. Fang. 2009. Morphological and physiological responses of two chrysanthemum cultivars differing in their tolerance to water logging. Environ. Exp. Bot. 67:87-93.