Abstract
Antioxidative mechanisms are important to protect cells from the hazardous effects of reactive oxygen species (ROS). Salt stress is one of the environmental stress factors that leads to accumulation of ROS at toxic levels. In this study, we analyzed the responses of two rice (Oryza sativa L.) cultivars against NaCl stress at enzymatic and transcriptional levels. In 14 day-old-seedlings, different antioxidant enzyme activities were observed. These findings were also supported by transcriptional analyses of the responsible genes. According to the results, Cyt-APX, CAT A, Cyt-GR1 and proline metabolism-related genes were differentially expressed between two rice varieties under different salt concentrations. Their regulational differences cause different salt sensitivities of the varieties. By this study, we provided an insight into understanding of the correlation between antioxidant defence genes and ROS enzymes under salt stress.
Similar content being viewed by others
References
Abdul Qados AMS (2011) Effect of salt stress on plant growth and metabolism of bean plant Vicia faba (L.). J Saudi Soc Agric Sci 10(1):7–15. https://doi.org/10.1016/j.jssas.2010.06.002
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126
Ara N, Nakkanong K, Lv W, Yang J, Hu Z, Zhang M (2013) Antioxidant enzymatic activities and gene expression associated with heat tolerance in the stems and roots of two cucurbit species (“Cucurbita maxima” and “Cucurbita moschata”) and their interspecific inbred line “Maxchata”. Int J Mol Sci 14(12):24008–24028. https://doi.org/10.3390/ijms141224008
Azevedo Neto AD, Prisco JT, Enéas-Filho J, Abreu CEBd, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56(1):87–94. https://doi.org/10.1016/j.envexpbot.2005.01.008
Barkla BJ et al (2013) Elucidation of salt stress defense and tolerance mechanisms of crop plants using proteomics–current achievements and perspectives. Proteomics 13(12–13):1885–1900. https://doi.org/10.1002/pmic.201200399
Barrera-Figueroa BE, Wu Z, Liu R (2013) Abiotic stress-associated microRNAs in plants: discovery, expression analysis, and evolution. Front Biol 8(2):189–197
Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44(1):276–287
Belghith I, Senkler J, Hildebrandt T, Abdelly C, Braun H-P, Debez A (2018) Comparative analysis of salt-induced changes in the root proteome of two accessions of the halophyte Cakile maritima. Plant Physiol Biochem 130:20–29. https://doi.org/10.1016/j.plaphy.2018.06.029
Bian S, Jiang Y (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Sci Hortic 120(2):264–270. https://doi.org/10.1016/j.scienta.2008.10.014
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(1):77–84. https://doi.org/10.1016/S0168-9452(02)00338-2
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1):248–254
Celik O, Atak Ç (2012) Evaluation of proline accumulation and Δ1-pyrroline-5-carboxylate synthetase (P5CS) gene expression during salinity stress in two soybean (Glycine max L. Merr.) varieties. Pol J Environ Stud 21:559–564
Çelik Ö, Atak C (2012) The effect of salt stress on antioxidative enzymes and proline content of two Turkish tobacco varieties. Turk J Biol 36:339–356
Chakraborty A, Bhattacharjee S (2015) Differential competence of redox-regulatory mechanism under extremes of temperature determines growth performances and cross tolerance in two indica rice cultivars. J Plant Physiol 176:65–77. https://doi.org/10.1016/j.jplph.2014.10.016
Cock J, Yoshida S, Forno DA (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute, Manila
Compton M (2006) Use of statistics in plant biotechnology. In: Loyola-Vargas V, Vázquez-Flota F (eds) Plant cell culture protocols, vol 318. Methods in Molecular Biology™. Humana Press, New York, pp 145–163
Demiral T, Türkan İ (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53(3):247–257. https://doi.org/10.1016/j.envexpbot.2004.03.017
Ding S et al (2012) Enhanced sensitivity and characterization of photosystem II in transgenic tobacco plants with decreased chloroplast glutathione reductase under chilling stress. Biochem Biophys Acta 1817(11):1979–1991. https://doi.org/10.1016/j.bbabio.2012.06.003
Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11(1):1–42. https://doi.org/10.2307/3001478
Fernández-Ocaña A et al (2011) Functional analysis of superoxide dismutases (SODs) in sunflower under biotic and abiotic stress conditions. Identification of two new genes of mitochondrial Mn-SOD. J Plant Physiol 168(11):1303–1308. https://doi.org/10.1016/j.jplph.2011.01.020
Foyer C, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133(1):21–25. https://doi.org/10.1007/BF00386001
Hao ZN, Wang LP, Tao RX (2009) Expression patterns of defence genes and antioxidant defence responses in a rice variety that is resistant to leaf blast but susceptible to neck blast. Physiol Mol Plant P 74(2):167–174. https://doi.org/10.1016/j.pmpp.2009.11.003
Jung Y et al (2010) Expression analysis of proline metabolism-related genes from halophyte arabis stelleri under osmotic stress conditions. J Integr Plant Biol 52(10):891–903
Kim J-H et al (2005) Expression of antioxidant isoenzyme genes in rice under salt stress and effects of jasmonic acid and γ-radiation. Agric Chem Biotechnol 48:1–6
Kim D et al (2007) Gene transcription in the leaves of rice undergoing salt-induced morphological changes (Oryza sativa L.). Mol Cells 24(1):45
Lee DH, Kim YS, Lee CB (2001) The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.). J Plant Physiol 158(6):737–745
Lee S-H et al (2007) Simultaneous overexpression of both CuZn superoxide dismutase and ascorbate peroxidase in transgenic tall fescue plants confers increased tolerance to a wide range of abiotic stresses. J Plant Physiol 164(12):1626–1638. https://doi.org/10.1016/j.jplph.2007.01.003
Lee MH et al (2013) Divergences in morphological changes and antioxidant responses in salt-tolerant and salt-sensitive rice seedlings after salt stress. Plant Physiol Biochem 70:325–335. https://doi.org/10.1016/j.plaphy.2013.05.047
Liu J, Li J, Su X, Xia Z (2014) Grafting improves drought tolerance by regulating antioxidant enzyme activities and stress-responsive gene expression in tobacco. Environ Exp Bot 107:173–179. https://doi.org/10.1016/j.envexpbot.2014.06.012
Luo H, Li H, Zhang X, Fu J (2011) Antioxidant responses and gene expression in perennial ryegrass (Lolium perenne L.) under cadmium stress. Ecotoxicology (London, England) 20(4):770–778. https://doi.org/10.1007/s10646-011-0628-y
Lutts S, Majerus V, Kinet JM (1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiol Plant 105(3):450–458
Menezes-Benavente L, Teixeira FK, Alvim Kamei CL, Margis-Pinheiro M (2004) Salt stress induces altered expression of genes encoding antioxidant enzymes in seedlings of a Brazilian indica rice (Oryza sativa L.). Plant Sci 166(2):323–331
Morita S, Nakatani S, Koshiba T, Masumura T, Ogihara Y, Tanaka K (2011) Differential expression of two cytosolic ascorbate peroxidases and two superoxide dismutase genes in response to abiotic stress in rice. Rice Sci 18(3):157–166. https://doi.org/10.1016/S1672-6308(11)60023-1
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880
Pfaffl MW, Gerstmayer B, Bosio A, Windisch W (2003) Effect of zinc deficiency on the mRNA expression pattern in liver and jejunum of adult rats: monitoring gene expression using cDNA microarrays combined with real-time RT-PCR. J Nutr Biochem 14(12):691–702
Rabbani MA et al (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133(4):1755–1767
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161(11):1189–1202
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 osmolyte concentration. Plant Sci 163(5):1037–1046. https://doi.org/10.1016/S0168-9452(02)00278-9
Scandalios J (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38(7):995–1014
Seevers P, Daly J, Catedral F (1971) The role of peroxidase isozymes in resistance to wheat stem rust disease. Plant Physiol 48(3):353–360
Shu DF, Wang LY, Duan M, Deng YS, Meng QW (2011) Antisense-mediated depletion of tomato chloroplast glutathione reductase enhances susceptibility to chilling stress. Plant Physiol Biochem 49(10):1228–1237. https://doi.org/10.1016/j.plaphy.2011.04.005
Silva-Ortega CO, Ochoa-Alfaro AE, Reyes-Agüero JA, Aguado-Santacruz GA, Jiménez-Bremont JF (2008) Salt stress increases the expression of p5cs gene and induces proline accumulation in cactus pear. Plant Physiol Biochem 46(1):82–92. https://doi.org/10.1016/j.plaphy.2007.10.011
Stewart RR, Bewley JD (1980) Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 65(2):245–248
Su J, Wu R (2004) Stress-inducible synthesis of proline in transgenic rice confers faster growth under stress conditions than that with constitutive synthesis. Plant Sci 166(4):941–948
Sytar O et al (2017) Applying hyperspectral imaging to explore natural plant diversity towards improving salt stress tolerance. Sci Total Environ 578:90–99. https://doi.org/10.1016/j.scitotenv.2016.08.014
Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218(1):1–14. https://doi.org/10.1007/s00425-003-1105-5
Wang Y, Ying Y, Chen J, Wang X (2004) Transgenic Arabidopsis overexpressing Mn-SOD enhanced salt-tolerance. Plant Sci 167(4):671–677
Wu H (2018) Plant salt tolerance and Na+ sensing and transport. Crop J 6(3):215–225. https://doi.org/10.1016/j.cj.2018.01.003
Wu TM et al (2013) Identification and characterization of a novel chloroplast/mitochondria co-localized glutathione reductase 3 involved in salt stress response in rice. Plant Mol Biol 83(4–5):379–390. https://doi.org/10.1007/s11103-013-0095-3
Yin G et al (2014) Activity levels and expression of antioxidant enzymes in the ascorbate–glutathione cycle in artificially aged rice seed. Plant Physiol Biochem 80:1–9. https://doi.org/10.1016/j.plaphy.2014.03.006
Zeng L, Shannon MC (2000) Salinity effects on seedling growth and yield components of rice. Crop Sci 40:996–1003
Zhang M, Fang Y, Ji Y, Jiang Z, Wang L (2013) Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. South Afr J Bot 85:1–9. https://doi.org/10.1016/j.sajb.2012.11.005
Zhang M, Huang H, Dai S (2014) Isolation and expression analysis of proline metabolism-related genes in Chrysanthemum lavandulifolium. Gene 537(2):203–213. https://doi.org/10.1016/j.gene.2014.01.002
Zhu B, Su J, Chang M, Verma DPS, Fan Y-L, Wu R (1998) Overexpression of a Δ < sup > 1 </sup > -pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water-and salt-stress in transgenic rice. Plant Sci 139(1):41–48
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Çelik, Ö., Çakır, B.C. & Atak, Ç. Identification of the antioxidant defense genes which may provide enhanced salt tolerance in Oryza sativa L.. Physiol Mol Biol Plants 25, 85–99 (2019). https://doi.org/10.1007/s12298-018-0618-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-018-0618-0