Abstract
It has been shown that salicylic acid (SA) acts as an endogenous signal molecule responsible for inducing abiotic stress tolerance in plants. The effect of SA and sodium chloride (NaCl) on growth, metabolite accumulation, oxidative stress and enzymatic and non-enzymatic antioxidant responses on common bean plants (Phaseolus vulgaris, cv. F-15) was studied. Results revealed that either SA or NaCl decrease, shoot, root and total plant dry weights. SA treatments decreased the contents of proline, and reduced forms of ascorbate and glutathione, however, the content of soluble sugars (TSS), thiobarbituric acid-reactive substances (TBARs) and oxidized ascorbate remained unaffected. On the other hand, salinity significantly reduced the levels of endogenous SA but increased the content of proline, soluble sugars, TBARs, ascorbate and glutathione, as well as all increasing the levels of antioxidant enzyme activities assayed, except CAT. The application of SA improved the response of common bean plants to salinity by increasing plant dry weight and decreasing the content of organic solutes (proline and TSS) and damage to the membrane (TBARs). Moreover, SA application under saline conditions decreased the levels of antioxidant enzyme activities POX, APX and MDHAR which could indicate successful acclimatization of these plants to saline conditions.
Similar content being viewed by others
Abbreviations
- APX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- DHA:
-
Dehydroascorbate
- DHAR:
-
Dehydroascorbate reductase
- GR:
-
Glutathione reductase
- POX:
-
Guaiacol peroxidase
- MDHAR:
-
Monodehydroascorbate reductase
- GSSG:
-
Oxidized glutathione
- ROS:
-
Reactive oxygen species
- AsA:
-
Reduced ascorbate
- GSH:
-
Reduced glutathione
- SA:
-
Salicylic acid
- TBARs:
-
Thiobarbituric acid-reactive substances
- TCA:
-
Trichloroacetic acid
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. doi:10.1016/S0076-6879(84)05016-3
Agarwal S, Sairam RK, Srivastava GC, Tyagi A, Meena RC (2005) Role of ABA, salicylic acid, calcium and hydrogen peroxide on antioxidant enzymes induction in wheat seedlings. Plant Sci 169:559–570. doi:10.1016/j.plantsci.2005.05.004
Al-Hakimi AMA, Hamada AM (2001) Counteraction of salinity stress on wheat plants by grain soaking in ascorbic acid, thiamin or sodium salicylate. Biol Plant 44:253–261. doi:10.1023/A:1010255526903
Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233. doi:10.1111/j.1399-3054.1997.tb04778.x
Ananieva EA, Christov KN, Popova LP (2004) Exogenous treatment with salicylic acid leads to increased antioxidant capacity in leaves of barley plants exposed to paraquat. J Plant Physiol 161:319–328. doi:10.1078/0176-1617-01022
Bor M, Özdemir F, Türkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Sci 164:77–84. doi:10.1016/S0168-9452(02)00338-2
Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030. doi:10.1104/pp.126.3.1024
Dalton DA, Baird LM, Langeberg L, Taugher CY, Anyan WA, Vance CP, Sarath G (1993) Subcellular localization of oxygen defense enzymes in soybean (Glycine max (L.) Merr) root nodules. Plant Physiol 102:481–489
Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (2000) Effects of salicylic acid on oxidative stress and termotolerance in tobacco. J Plant Physiol 156:659–665
Edwars EA, Rawsthorne S, Mullineux PM (1990) Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180:278–284
El-Tayeb MA (2005) Response of barley grains to the interactive effect of salinity and salicylic acid. Plant Growth Regul 45:215–224. doi:10.1007/s10725-005-4928-1
Enyedi A, Yalpani N, Silverman P, Raskin I (1992) Localization, conjugation and function of salicylic acid in tobacco during the hypersensitive reaction to tabacco mosaic virus. Proc Natl Acad Sci USA 89:2480–2489. doi:10.1073/pnas.89.6.2480
Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442. doi:10.1016/j.pbi.2006.05.014
Ghoulam C, Foursy A, Fares K (2002) Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five beet cultivars. Environ Exp Bot 47:39–50. doi:10.1016/S0098-8472(01)00109-5
Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212. doi:10.1016/0003-2697(80)90139-6
Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci EG, Cicek N (2007) Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J Plant Physiol 164:728–736. doi:10.1016/j.jplph.2005.12.009
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 207:604–611. doi:10.1007/s004250050524
Horváth E, Szalai G, Janda T (2007) Induction of abiotic stress tolerance by salicylic acid signaling. J Plant Growth Regul 26:290–300. doi:10.1007/s00344-007-9017-4
Hossain MA, Asada A (1984) Inactivation of ascorbate peroxidase in spinach chloroplasts on dark addition of hydrogen peroxide: its protection by ascorbate. Plant Cell Physiol 25:1285–1295
Hossain M, Nakano Y, Asada K (1984) Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol 25:385–395
Irigoyen JJ, Emerich DW, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugar in nodulated alfalfa (Medicago sativa) plants. Physiol Plant 84:55–60. doi:10.1111/j.1399-3054.1992.tb08764.x
Janda T, Szalai G, Tari I, Páldi E (1999) Hydroponic treatment with salicylic acid decreases the effects of chilling injury in maize (Zea mays L.) plants. Planta 208:175–180. doi:10.1007/s004250050547
Jiménez-Bremont JF, Becerra-Flora A, Hernández-Lucero E, Rodríguez-Kessler M, Acosta-Gallegos JA, Ramírez-Pimentel JG (2006) Proline accumulation in two bean cultivars under salt stress and the effect of polyamines and ornithine. Biol Plant 50:763–766. doi:10.1007/s10535-006-0126-x
Kato M, Shimizu S (1987) Chlorophyll metabolism in higher plants. VII. Chlorophyll degradation in senescing tobacco leaves: phenolic dependent peroxidative degradation. Can J Bot 65:729–735. doi:10.1139/b87-097
Khadri M, Tejera NA, Lluch C (2006) Alleviation of salt stress in common bean (Phaseolus vulgaris) by exogenous abscisic acid supply. J Plant Growth Regul 25:110–119. doi:10.1007/s00344-005-0004-3
Khadri M, Tejera NA, Lluch C (2007) Sodium chloride–ABA interaction in two common bean (Phaseolus vulgaris) cultivars differing in salinity tolerance. Environ Exp Bot 60:211–218. doi:10.1016/j.envexpbot.2006.10.008
Khodary SEA (2004) Effect of salicylic acid on the growth, photosynthesis and carbohydrate metabolism in salt-stressed maize plants. Int J Agric Biol 6:5–8
Klessig DF, Malamy J (1994) The salicylic acid signal in plants. Plant Mol Biol 26:1439–1458. doi:10.1007/BF00016484
Law MY, Charles SA, Halliwell B (1992) Glutathione and ascorbic acid in spinach (Spinacea oleracea) chloroplast. The effect of hydrogen peroxide and paraquat. Biochem J 210:899–903
Malamy J, Hennig J, Klessig DF (1992) Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 4:359–366
Mateo A, Funck D, Mühlenbock P, Kular B, Mullineaux PM, Karpinski S (2006) Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J Exp Bot 57:1795–1807. doi:10.1093/jxb/erj196
Mishra A, Choudhuri MA (1999) Effects of salicylic acid on heavy metal-induced membrane deterioration mediated by lipoxygenase in rice. Biol Plant 42:409–415. doi:10.1023/A:1002469303670
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. doi:10.1016/S1360-1385(02)02312-9
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663. doi:10.1111/j.1469-8137.2005.01487.x
Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279. doi:10.1146/annurev.arplant.49.1.249
Popova L, Ananieva E, Hristova V, Christov K, Georgieva K, Alexieva V, Stoinova Z (2003) Salicylic acid- and methyl jasmonate-induced protection on photosynthesis to paraquat oxidative stress. Bulg J Plant Physiol Special Issue:133–152
Rigaud J, Puppo A (1975) Indole-3-acetic acid catabolism by soybean bacteroids. J Gen Microbiol 88:223–228
Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819
Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421
Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinity stress in relation to oxidative stress, antioxidant activity and osmolytic concentration. Plant Sci 163:1037–1046. doi:10.1016/S0168-9452(02)00278-9
Shakirova FM, Sakhabutdinova AR, Bezrukova MV, Fatkhutdinova RA, Fatkhutdinova DR (2003) Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci 164:317–322. doi:10.1016/S0168-9452(02)00415-6
Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39:137–141. doi:10.1023/A:1022556103536
Tari I, Csiszár J, Szalai G, Horváth F, Pécsváradi A, Kiss G, Szepesi Á, Szabó M, Erdei L (2002) Acclimation of tomato plants to salinity after a salicylic acid pre-treatment. Acta Biol Szeged 46:55–56
Tejera NA, Campos R, Sanjuan J, Lluch C (2004) Nitrogenase and antioxidant enzyme activities in Phaseolus vulgaris nodules formed by Rhizobium tropici isogenic strains with varying tolerance to salt stress. J Plant Physiol 161:329–338. doi:10.1078/0176-1617-01050
Tejera NA, Iribarne C, Palma F, Lluch C (2007) Inhibition of the catalase activity from Phaseolus vulgaris and Medicago sativa by sodium chloride. Plant Physiol Biochem 45:535–541. doi:10.1016/j.plaphy.2007.04.008
Tissa S, Darren D, Eric B, Kinsley D (2000) Acetyl salicylic acid (aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:157–161. doi:10.1023/A:1006386800974
Yemm EW, Cocking EC (1955) The determination of amino acids with ninhydrin. Analystic 80:209–213. doi:10.1039/an9558000209
Acknowledgments
This work was financially supported by the Spanish Ministry of Science and Technology (AGL2006-01279/AGR). The authors are grateful Dr. Pieter Van Dillewijn for the English correction of the paper. We also thank to anonymous reviewers for making valuable suggestions to earlier drafts of this study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Palma, F., Lluch, C., Iribarne, C. et al. Combined effect of salicylic acid and salinity on some antioxidant activities, oxidative stress and metabolite accumulation in Phaseolus vulgaris . Plant Growth Regul 58, 307–316 (2009). https://doi.org/10.1007/s10725-009-9380-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-009-9380-1