Abstract
To investigate key regulatory components and genes with great impact on salt tolerance, near isogenic or mutant lines with distinct salinity tolerance are suitable genetic materials to simplify and dissect the complex genes networks. In this study, we evaluated responses of a barley mutant genotype (73-M4-30), in comparison with its wild-type background (Zarjou) under salt stress. Although the root growth of both genotypes was significantly decreased by exposure to sodium chloride (NaCl), the effect was greater in the wild type. The chlorophyll content decreased under salt stress for the wild type, but no change occurred in the mutant. The mutant maintained the steady-state level of [K+] and significantly lower [Na+] concentrations in roots and higher [K+]/[Na+] ratio in shoots under salt conditions. The catalase (CAT), peroxidase (POD) activity, and proline content were higher in the mutant than those in the wild type under controlled conditions. The soluble proline was higher after 24 h of salt stress in roots of the mutant but was higher after 96 h of salt stress in the wild type. The CAT and POD activity of the mutant increased under salt stress which was as a coincidence to lower levels of hydrogen peroxide (H2O2) and malondialdehyde (MDA) contents. The ratio of dry-to-fresh weight of the roots increased for the mutant under salt stress which was as a result of the higher phenylalanine ammonia-lyase (PAL) gene expression and peroxidase activity and involved in cell wall lignification. Consequently, it seems that ion homeostasis and increased peroxidase activity have led to salt tolerance in the mutant’s genotype.
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Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701
Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiology 141:391–396. doi:10.1104/pp.106.082040
Bates LS, Waldren BP, Teare ID (1973) Rapid determination of free proline of water-stress studies. Plant Soil 39:205–207. doi:10.1007/BF00018060
Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465(1):140–151. doi:10.1016/S0005-2736(00)00135-8
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
Cervilla L, Rosales M, Rubio-Wilhelmi M, Sánchez-Rodríguez E, Blasco B, Ríos J, Romero L, Ruiz J (2009) Involvement of lignification and membrane permeability in the tomato root response to boron toxicity. Plant Sci 176(4):545–552. doi:10.1016/j.plantsci.2009.01.008
Chen ZH, Zhou MX, Newman IA, Mendham NJ, Zhang GP, Shabala S (2007) Potassium and sodium relations in salinised barley tissues as a basis of differential salt tolerance. Funct Plant Biol 34:150–162. doi:10.1071/FP06237
Degl’Innocenti E, Hafsi C, Guidi L, Navari-Izzo F (2009) the effect of salinity on photosynthetic activity in potassium-deficient barley species. J Plant Physiol 166:1968–1981. doi:10.1016/j.jplph.2009.06.013
Frei M (2013) Lignin: characterization of a multifaceted crop component. Sci World J Article ID 436517, 2013:25. doi:10.1155/2013/436517
Ghiazdowska A, Krasuska U, Bogatek R (2010) Dormancy removal in apple embryos by nitric oxide or cyanide involves modifications in ethylene biosynthetic pathway. Planta 232:1397–1407. doi:10.1007/s00425-010-1262-2
Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59(2):309–314. doi:10.1104/pp.59.2.309
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. doi:10.1016/j.plaphy.2010.08.016
Hazman M, Hause B, Eiche E, Nick P, Riemann M (2015) Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked to an increased ROS-scavenging activity. J Exp Bot 66(11):3339–3352. doi:10.1093/jxb/erv142
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. doi:10.1016/0003-9861(68)90654-1
Hemm MR, Rider SD, Ogas J, Murry DJ, Chapple C (2004) Light induces phenylpropanoid metabolism in Arabidopsis roots. Plant J 38(5):765–778. doi:10.1111/j.1365-313X.2004.02089.x
Hoagland DR, Arnon DI (1950) The water culture method for growing plants without soil. Circular (California Agricultural Experiment Station) 347(2):32
Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2015) Salicylic acid in plant salinity stress signaling and tolerance. Plant Growth Regul 76(1):25–40. doi:10.1007/s10725-015-0028-z
Jbir N, Chaïbi W, Ammar SD, Jemmali A, Ayadi A (2001) Root growth and lignification of two wheat species differing in their sensitivity to NaCl, in response to salt stress. Plant Biol Pathol 324:863–868. doi:10.1016/S0764-4469(01)01355-5
Kosová K, Prášil IT, Vítámvás P (2013) Protein contribution to plant salinity response and tolerance acquisition. Int J Mol Sci 14(4):6757–6789. doi:10.3390/ijms14046757
Larkindale JD, Hall JR, Knight M, Vierling E (2007) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermo tolerance. Plant Physiol 138:882–897. doi:10.1104/pp.105.062257
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UVΓ-VIS spectroscopy. Curr Protoc Food Anal Chem. doi:10.1002/0471142913.faf0403s01
Lin KC, Jwo WS, Chandrika N, Wu TM, Lai MH, Wang CS, Hong CY (2016) A rice mutant defective in antioxidant-defense system and sodium homeostasis possess increased sensitivity to salt stress. Biol Plant 60(1):86–94. doi:10.1007/s10535-015-0561-7
Maehly AC (1954) The assay of catalases and peroxidases. In: Glick D (ed) Methods of biochemical analysis. Inter sciences Publishers, New York, p 358
Mahluji M, Mal Verdi Q, Afyuni D, Jafari A, DorchehI MA, Sadeqi D, Yusefi A (2007) Introducing and comparing of salinity tolerant barley lines (4 and 5) to local cultivar in On-farm trial. http://agris.fao.org/agris-search/search.do?recordID=IR2008000425. Accessed 22 Feb 2017
Mandal S, Mallick N, Mitra A (2009) Salicylic acid-induced resistance to Fusarium oxysporum f. sp. lycopersici in tomato. Plant Physiol Biochem 47:642–649. doi:10.1016/j.plaphy.2009.03.001
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250. doi:10.1046/j.0016-8025.2001.00808.x
Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167(3):645–663. doi:10.1111/j.1469-8137.2005.01487.x
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. doi:10.1146/annurev.arplant.59.032607.092911
Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540. doi:10.1016/j.tplants.2004.09.002
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wide comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36. doi:10.1093/nar/30.9.e36
Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8:1757–1764. doi:10.1089/ars.2006.8.1757
Polle A (2001) Dissecting the superoxide dismutase–ascorbate glutathione pathway by metabolic modeling: computer analysis as a step towards flux analysis. Plant Physiol 126:445–462. doi:10.1104/pp.126.1.445
Roshandel P, Flowers T (2009) the ionic effects of NaCl on physiology and gene expression in rice genotypes differing in salt tolerance. Plant Soil 315:35–147. doi:10.1007/s11104-008-9738-6
Runhong G, Ke D, Guimei G, Zhizhao D, Zhiwei C, Liang L, Ting H, Ruiju L, Jianhua H (2013) Comparative transcriptional profiling of two contrasting barley genotypes under salinity stress during the seedling stage. Int J Genom 19 p. Article ID 972852. doi:10.1155/2013/972852
Scebba F, Sebastiani L, Vitaglianpo C (1998) Changes in activity of antioxidantive enzymes in wheat (Triticum aestivum) seedlings under cold acclimation. Physiol Plant 104:747–752. doi:10.1034/j.1399-3054.1998.1040433.x
Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plant 151:257–279. doi:10.1111/ppl.12165
Shabala S, Cuin TA, Prismall L, Nemchinov LG (2007) Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta 227:189–197. doi:10.1007/s00425-007-0606-z
Shavrukov Y (2012) Salt stress or salt shock: which genes are we studying? J Exp Bot 64(1):119–127. doi:10.1093/jxb/ers316
Sorahinobar M, Niknam V, Ebrahimzadeh H, Soltanloo H, Behmanesh M, Enferadi ST (2015) Central role of salicylic acid in resistance of wheat against fusarium graminearum. J Plant Growth Regul 35:477–491. doi:10.1007/s00344-015-9554-1
Vidossich P, Alfonso-Prieto M, Rovira C (2012) Catalases versus peroxidases: DFT investigation of H2O2 oxidation in models systems and implications for heme protein engineering. J Inorg Biochem 117:292–297. doi:10.1016/j.**orgbio.2012.07.002
Vij S, Tyagi AK (2007) Emerging trends in the functional genomics of the abiotic stress response in crop plants: review article. Plant Biotechnol J 5(3):361–380. doi:10.1111/j.1467-7652.2007.00239.x
Walia H, Wilson C, Wahid A, Condamine P, Cui X, Close TJ (2006) Expression analysis of barley (Hordeum vulgare L.) during salinity stress. Funct Integr Genom 6(2):143–156. doi:10.1007/s10142-005-0013-0
Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14(4):7370–7390. doi:10.3390/ijms14047370
Wei W, Bilsborrow PE, Hooley P, Fincham DA, Lombi E, Forster BP (2003) Salinity induced differences in growth, ion distribution and partitioning in barley between the cultivar Maythorpe and its derived mutant Golden Promise. Plant Soil 250(2):183–191. doi:10.1023/A:1022832107999
Williams V, Twine S (1960) Flame photometric method for sodium, potassium and calcium. Mod Methods Plant Anal 5:3–5
Witzel K, Weidner A, Surabhi GK, Börner A, Mock HP (2009) Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. J Exp Bot 60(12):3545–3557. doi:10.1093/jxb/erp198
Zhang H, Han B, Wang T, Chen S, Li H, Zhang Y, Dai S (2012) Mechanisms of plant salt response: insights from proteomics. J Proteome Res 11:49–67. doi:10.1021/pr200861w
Zhang B, Liu K, Zheng Y, Wang Y, Wang J, Liao H (2013) Disruption of AtWNK8 enhances tolerance of arabidopsis to salt and osmotic stresses via modulating proline content and activities of catalase and peroxidase. Int J Mol Sci 14(4):7032. doi:10.3390/ijms14047032
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71. doi:10.1016/S1360-1385(00)01838-0
Ziemann M, Kamboj A, Hove RM, Loveridge S, El-Osta A, Bhave M (2013) Analysis of the barley leaf transcriptome under salinity stress using mRNA-Seq. Acta Physiologiae Plant 35:1915–1924. doi:10.1007/s11738-013-1230-0
Acknowledgements
The authors would like to acknowledge the financial support received from the project via the Faculty of Plant Production, Department of Plant Breeding and Biotechnology, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran. The first author would like to thank the Persian Gulf University, Bushehr, Iran for a scholarship. The authors would like to thank the Seed and Plant Improvement Institute, Karaj, Iran, for the provision of seed material and our deep gratitude goes to Mona Sorahinobar for helpful suggestions on the initial draft of the paper.
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Kiani, D., Soltanloo, H., Ramezanpour, S.S. et al. A barley mutant with improved salt tolerance through ion homeostasis and ROS scavenging under salt stress. Acta Physiol Plant 39, 90 (2017). https://doi.org/10.1007/s11738-017-2359-z
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DOI: https://doi.org/10.1007/s11738-017-2359-z