Abstract
Salinity toxicity has become a major threat to the yield of highland barley in Tibet due to severe soil salinization. This research disclosed the effects of low-dose γ-irradiation on the physio-biochemical and transcriptional responses to NaCl stress in highland barley seedlings. The results revealed that 50-Gy gamma irradiation pretreatment could markedly stimulate highland barley growth under NaCl stress and alleviate the salt-induced oxidative stress (evidenced by lower malondialdehyde and hydrogen peroxide contents in irradiated seedlings) through elevating the antioxidant enzyme activities and proline level. Moreover, transmission electron microscopy results revealed that irradiation pretreatment could alleviate the salt damage to chloroplasts ultrastructure. Notably, transcriptional analysis showed that γ-irradiation pretreatment could enhance the expression of salt stress related genes. Overall, our results show that gamma ray pretreatment can improve the salt tolerance of barley seedlings.
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Ahmed IM, Cao FB, Han Y, Nadira UA, Zhang GP, Wu FB (2013) Differential changes in grain ultrastructure, amylase, protein and amino acid profiles between Tibetan wild and cultivated barleys under drought and salinity alone and combined stress. Food Chem 141:2743–2750. https://doi.org/10.1016/j.foodchem.2013.05.101
Akshatha Chandrashekar KR, Somashekarappa HM, Souframanien J (2014) Effect of gamma irradiation on germination, growth, and biochemical parameters of Terminalia arjuna Roxb. Radiat Prot Environ 36:38–44. https://doi.org/10.4103/0972-0464.121826
Arora A, Sairam RK, Srivastava GC (2002) Oxidative stress and antioxidative system in plants. Curr Sci 82:1227–1238. https://www.researchgate.net/publication/237817932. Accessed 1 November 2001
Barbato R, Trotta A, Redondo-Gómez S, Pagliano C (2012) Chloroplast ultrastructure and thylakoid polypeptide composition are affected by different salt concentrations in the halophytic plant Arthrocnemum macrostachyum. J Plant Physiol 169:111–116. https://doi.org/10.1016/j.jplph.2011.11.001
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Bergmeyer N (1970) Methoden der enzymatischen analyse. Akademie–Verlag, Berlin
Beyaz R, Kahramanogullari CT, Yildiz C, Darcin ES, Yildiz M (2016) The effect of gamma radiation on seed germination and seedling growth of Lathyrus chrysanthus Boiss. under invitro conditions. J Environ Radioactiv 162–163:129–133. https://doi.org/10.1016/j.jenvrad.2016.05.006
Bose JK, Xie YJ, Shen WB, Shabala S (2013) Haem oxygenase modifies salinity tolerance in Arabidopsis by controlling K+ retention via regulation of the plasma membrane H+–ATPase and by altering SOS1 transcript levels in roots. J Exp Bot 64:471–481. https://doi.org/10.1093/jxb/ers343
Cheng J, Lu HX, Huang Y, Li K, Huang R, Zhou JH, Cen KF (2016) Enhancing growth rate and lipid yield of Chlorella with nuclear irradiation under high salt and CO2 stress. Bioresour Technol 203:220–227. https://doi.org/10.1016/j.biortech.2015.12.032
Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226. https://doi.org/10.1042/BJ20080625
Du ST, Liu Y, Zhang P, Liu HJ, Zhang XQ, Zhang RR (2015) Atmospheric application of trace amounts of nitric oxide enhances tolerance to salt stress and improves nutritional quality in spinach (Spinacia oleracea L.). Food Chem 173:905–911. https://doi.org/10.1016/j.foodchem.2014.10.115
El-Beltagi HS, Mohamed HI, Mohammed AH (2013) Physiological and biochemical effects of γ-irradiation on cowpea plants (Vigna sinensis) under salt stress. Not Bot Hortic Agrobot 41:104–114. https://doi.org/10.15835/nbha4118927
Esnault MA, Legue F, Chenal C (2010) Ionizing radiation: advances in plant response. Environ Exp Bot 68:231–237. https://doi.org/10.1016/j.envexpbot.2010.01.007
Farooq M, Siddique KHM, Schubert S (2013) Role of nitric oxide in improving plant resistance against salt stress. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 413–424
Gama PBS, Inanaga S, Tanaka K, Nakazawa R (2007) Physiological response of common bean (Phaseolus vulgaris L.) seedlings to salinity stress. Afr J Biotechnol 6:79–88
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314. https://doi.org/10.1104/pp.59.2.309
Helaly MNM, El-Hosieny AMR (2011) Effectiveness of gamma irradiated protoplasts on improving salt tolerance of lemon (Citrus limon L. Burm. f.). Am J Plant Physiol 6:190–208. https://doi.org/10.3923/ajpp.2011.190.208
Krupinska K (2006) Fate and activities of plastids during leaf senescence. In: Wise RR, Hoober JK (eds) The structure and function of plastids. Springer, Dordrecht, pp 433–449
Kurowska M, Labocha-Pawłowska A, Gnizda D, Maluszynski M, Szarejko I (2012) Molecular analysis of point mutations in a barley genome exposed to MNU and gamma rays. Mutat Res 739:52–70. https://doi.org/10.1016/j.mrfmmm.2012.08.008
Li HZ, Zhou WJ, Zhang ZJ, Gu HH, Takeuchi Y, Yoneyama KY (2005) Effect of γ-radiation on development, yield and quality of microtubers in vitro Solanum tuberosum L. Biol Plant 49:625–628. https://doi.org/10.1007/s10535-005-0062-1
Li QY, Niu HB, Yin J, Wang MB, Shao HB, Deng DZ, Chen XX, Ren JP, Li YC (2008) Protective role of exogenous nitric oxide against oxidative-stress induced by salt stress in barley (Hordeum vulgare). Colloids Surf B 65:220–225. https://doi.org/10.1016/j.colsurfb.2008.04.007
Ligaba A, Katsuhara M (2010) Insights into the salt tolerance mechanism in barley (Hordeum vulgare) from comparisons of cultivars that differ in salt sensitivity. J Plant Res 123:105–118. https://doi.org/10.1007/s10265-009-0272-2
Luckey TD (2003) Radiation hormesis overview. RSO Mag 8:22–41
Macovei A, Garg B, Raikwar S, Balestrazzi A, Carbonera D, Buttafava A, Bremont JFJ, Gill SS, Tuteja N (2014) Synergistic exposure of rice seeds to different doses of γ-ray and salinity stress resulted in increased antioxidant enzyme activities and genespecific modulation of TC-NER pathway. BioMed Res Int 676934:15. https://doi.org/10.1155/2014/676934
Maity JP, Mishra D, Chakraborty A (2005) Modulation of some quantitative and qualitative characteristics in rice (Oryza sativa L.) and mung (Phaseolus mungo L.) by ionizing radiation. Radiat Phys Chem 74:391–394. https://doi.org/10.1016/j.radphyschem.2004.08.005
Marcu D, Cristea V, Daraban L (2013a) Dose-dependent effects of gamma radiation on lettuce (Lactuca sativa var. capitata) seedlings. Int J Radiat Biol 89:219–223. https://doi.org/10.3109/09553002.2013.734946
Marcu D, Damian G, Cosma C, Cristea V (2013b) Gamma radiation effects on seed germination, growth and pigment content, and ESR study of induced free radicals in maize (Zea mays). J Biol Phys 39:625–634. https://doi.org/10.1007/s10867-013-9322-z
Melki M, Dahmani T (2009) Gamma Irradiation Effects on Durum Wheat (Triticum durum Desf.) under Various Conditions. Pak J Biol Sci 12:1531–1534. https://doi.org/10.3923/pjbs.2009.1531.1534
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mohammed AH, Mohamed HI, Zaki LM (2012) Pre-exposure to gamma rays alleviates the harmful effect of salinity on cowpea plants. J Stress Physiol Biochem 8:199–217
Moussa HR (2011) Low dose of gamma irradiation enhanced drought tolerance in soybean. Acta Agron Hung 17:63–72. https://doi.org/10.1556/AAgr.59.2011.1.1
Naeem MS, Jin ZL, Wan GL, Liu D, Liu HB, Yoneyama K, Zhou WJ (2010) 5-Aminolevulinic acid improves photosynthetic gas exchange capacity and ion uptake under salinity stress in oilseed rape (Brassica napus L.). Plant Soil 332:405–415. https://doi.org/10.1007/s11104-010-0306-5
Naeem MS, Warusawitharana H, Liu H, Liu D, Ahmad R (2012) 5-Aminolevulinic acid alleviates the salinity-induced changes in Brassica napus as revealed by the ultrastructural study of chloroplast. Plant Physiol Biochem 57:84–92. https://doi.org/10.1016/j.plaphy.2012.05.018
Paramonova NV, Shevyakova NI, Kuznetsov VlV (2004) Ultrastructure of chloroplasts and their storage inclusions in the primary leaves of Mesembryanthemum crystallinum affected by putrescine and NaCl. Russ J Plant Physiol 51:86–96. https://doi.org/10.1023/B:RUPP.0000011307.95130.8f
Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492. https://doi.org/10.1016/0003-2697(84)90039-3
Qi WC, Zhang L, Xu HB, Wang L, Jiao Z (2014) Physiological and molecular characterization of the enhanced salt tolerance induced by low-dose gamma irradiation in Arabidopsis seedlings. Biochem Bioph Res Commun 450:1010–1015. https://doi.org/10.1016/j.bbrc.2014.06.086
Qi WC, Zhang L, Feng W, Xu HB, Wang L, Jiao Z (2015) ROS and ABA signaling are involved in the growth stimulation induced by low-dose gamma irradiation in Arabidopsis seedling. Appl Biochem Biotec 175:1490–1506. https://doi.org/10.1007/s12010-014-1372-6
Qiu QS, Guo Y, Quintero FJ, Pardo JM, Schumaker KS, Zhu JK (2004) Regulation of vacuolar Na+/H+ exchange in Arabidopsis thaliana by the salt-overly -sensitive (SOS) pathway. J Biol Chem 279:207–215. https://doi.org/10.1074/jbc.M307982200
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108. https://doi.org/10.1038/nprot.2008.73
Shalata A, Neumann PM (2001) Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. J Exp Bot 52:2207–2211. https://doi.org/10.1093/jexbot/52.364.2207
Shereen A, Ansari R, Mumtaz S et al (2009) Impact of gamma irradiation induced changes on growth and physiological responses of rice under saline conditions. Pak J Bot 41:2487–2495
Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance Gene SOS1 encodes a putative Na+/H+ Antiporter. Proc Natl Acad Sci 97:6896–6901. https://doi.org/10.1073/pnas.120170197
Singh B, Datta PS (2010) Gamma irradiation to improve plant vigour, grain development, and yield attributes of wheat. Radiat Phys Chem 79:139–143. https://doi.org/10.1016/j.radphyschem.2009.05.025
Smirnoff N, Cumbes QJ (1989) Hydroxyl radial scavenging activity of compatible solutes. Phytochemistry 28:1057–1060. https://doi.org/10.1016/0031-9422(89)80182-7
Virgin HI (1993) The chloroplast as site of chlorophyll formation and photosynthesis: a short history. Pigment Protein Complexes Plast. https://doi.org/10.1016/B978-0-12-676960-9.50006-7
Wang J, Li HR, Li YH, Yu JP, Yang LS, Feng FJ, Chen Z (2013) Speciation, distribution, and bioavailability of soil selenium in the Tibetan Plateau kashin-beck disease area-a case study in Songpan County, Sichuan Province, China. Biol Trace Elem Res 156:367–375. https://doi.org/10.1007/s12011-013-9822-5
Wi SG, Chung BY, Kim JS, Kim JH, Baek MH, Lee JW, Kim YS (2007) Effects of gamma irradiation on morphological changes and biological responses in plants. Micron 38:553–564. https://doi.org/10.1016/j.micron.2006.11.002
Zhang J, Kirkham MB (1994) Drought-stress-induced changes in activities of superoxide dismutase, catalase, and peroxidase in wheat species. Plant Cell Physiol 35:785–791. https://doi.org/10.1093/oxfordjournals.pcp.a078658
Acknowledgements
This work was supported by the National Natural Science Fund of China (11605159, 11704343 and 11405147), Chinese Postdoctoral Science Foundation (2017M612412), the Foundation for University Key Teachers of Henan Province.
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Wang, X., Ma, R., Cao, Q. et al. Enhanced tolerance to salt stress in highland barley seedlings (Hordeum vulgare ssp. vulgare) by gamma irradiation pretreatment. Acta Physiol Plant 40, 174 (2018). https://doi.org/10.1007/s11738-018-2736-2
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DOI: https://doi.org/10.1007/s11738-018-2736-2