Abstract
Our previous work revealed that the soybean GmsSOS1 enhances salt tolerance in Arabidopsis. In this work, we studied the physiological mechanisms by which the GmsSOS1 confers salt and oxidative stress tolerance in Arabidopsis and yeast cells. Under salt stress condition, the GmsSOS1-expressing Arabidopsis plants displayed larger leaf area, lower leaf relative electrolytic leakage, less accumulation of H2O2, superoxide anion radicals (O2 −), and malondialdehyde compared with wild type. In consistent with these observations, the activities of antioxidant enzymes catalase, ascorbate peroxide, and peroxidase in the GmsSOS1-expressing plants were higher than those in wild type under salt stress. Combined salt and oxidative stresses caused more damage and higher accumulation of H2O2 and Na+ than single stress condition in both wild type and the GmsSOS1-expressing plants. However, the GmsSOS1-expressing Arabidopsis plants could maintain significantly lower levels of H2O2 and Na+ and exhibited better growth than wild type under either single or combined stress. The GmsSOS1 complemented the yeast plasma membrane-localized Na+/H+ antiporter and enhanced salt tolerance by reducing Na+ accumulation in yeast cells. Our results suggest that the soybean GmsSOS1 can alleviate the primary Na+ toxicity by limiting Na+ accumulation and mitigate the secondary oxidative stress through improving antioxidant enzyme activity.
Similar content being viewed by others
References
Adem GD, Roy SJ, Zhou M, Bowman JP, Shabala S (2014) Evaluating contribution of ionic, osmotic and oxidative stress components towards salinity tolerance in barley. BMC Plant Biol 14:113
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. doi:10.1016/S0076-6879(84)05016-3
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. doi:10.1016/0003-2697(71)90370-8
Chung J-S, Zhu J-K, Bressan RA, Hasegawa PM, Shi H (2008) Reactive oxygen species mediate Na+-induced SOS1 mRNA stability in Arabidopsis. Plant J 53:554–565. doi:10.1111/j.1365-313X.2007.03364.x
de Oliveira AB, Alencar NL, Gomes-Filho E (2013) Comparison between the water and salt stress effects on plant growth and development. InTech Open. doi:10.5772/54223
Feki K, Quintero FJ, Khoudi H, Leidi EO, Masmoudi K, Pardo JM, Brini F (2014) A constitutively active form of a durum wheat Na+/H+ antiporter SOS1 confers high salt tolerance to transgenic Arabidopsis. Plant Cell Rep 33:277–288. doi:10.1007/s00299-013-1528-9
Fujibe T, Saji H, Arakawa K, Yabe N, Takeuchi Y, Yamamoto KT (2004) A methyl viologen-resistant mutant of Arabidopsis, which is allelic to ozone-sensitive rcd1, is tolerant to supplemental ultraviolet-B irradiation. Plant Physiol 134:275–285. doi:10.1104/pp.103.033480
Gajewska E, Sklodowska M (2007) Effect of nickel on ROS content and antioxidative enzyme activities in wheat leaves. Biometals 20:27–36. doi:10.1007/s10534-006-9011-5
Gao J, Sun J, Cao P, Ren L, Liu C, Chen S, Chen F, Jiang J (2016) Variation in tissue Na+ content and the activity of SOS1 genes among two species and two related genera of Chrysanthemum. BMC Plant Biol 16:98. doi:10.1186/s12870-016-0781-9
Gietz RD (2014) Yeast transformation by the LiAC/SS carrier DNA/PEG method. In: Xiao W (ed) Yeast protocols, methods in molecular biology, vol 1163, pp 33–44. doi:10.1007/978-1-4939-0799-1_4
Halley JE, Kaplan T, Wang AY, Kobor MS, Rine J (2010) Roles for H2A.Z and its acetylation in GAL1 transcription and gene induction, but not GAL1-transcriptional memory. PLoS Biol 8(6):e1000401. doi:10.1371/journal.pbio.1000401
He Y, Fu J, Yu C, Wang X, Jiang Q, Hong J, Lu K, Xue G, Yan C, James A, Xu L, Chen J, Jiang D (2015) Increasing cyclic electron flow is related to Na+ sequestration into vacuoles for salt tolerance in soybean. J Exp Bot 66:6877–6889. doi:10.1093/jxb/erv392
Jiang J, Shi H (2008) Signaling control of SOS1 mRNA stability. Plant Signal Behav 3:687–688
Jouve L, Jacques D, Douglas GC, Hoffmann L, Hausman J-F (2007) Biochemical characterization of early and late bud flushing in common ash (Fraxinus excelsior L.). Plant Sci 172:962–969. doi:10.1016/j.plantsci.2007.02.008
Katiyar-Agarwal S, Zhu J, Kim K, Agarwal M, Fu X, Huang A, Zhu J-K (2006) The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. PNAS 103:18816–18821. doi:10.1073/pnas.0604711103
Li J, Cai W (2015) A ginseng PgTIP1 gene whose protein biological activity related to Ser128 residue confers faster growth and enhanced salt stress tolerance in Arabidopsis. Plant Sci 234:74–85. doi:10.1016/j.plantsci
Li ZQ, Li JX, Li HJ, Shi ZH, Zhang GF (2015) Overexpression of TsApx1 from Thellungiella salsuginea improves abiotic stress tolerance in transgenic Arabidopsis thaliana. Biol Plant 2015(59):497–506. doi:10.1007/s10535-015-0533-y
Liu M, Wang T-Z, Zhang W-H (2015) Sodium extrusion associated with enhanced expression of SOS1 underlies different salt tolerance between Medicago falcata and Medicago truncatula seedlings. Environ Exp Bot 110:46–55. doi:10.1016/j.envexpbot
Ma D-M, Xu W-R, Li H-W, Jin F-X, Guo L-N, Wang J, Dai H-J, Xu X (2014a) Co-expression of the Arabidopsis SOS genes enhances salt tolerance in transgenic tall fescue (Festuca arundinacea Schreb.). Protoplasma 251:219–231. doi:10.1007/s00709-013-0540-9
Ma Q, Li Y-X, Yuan H-J, Hu J, Wei L, Bao A-K, Zhang J-L, Wang S-M (2014b) ZxSOS1 is essential for long-distance transport and spatial distribution of Na+ and K+ in the xerophyte Zygophyllum xanthoxylum. Plant Soil 374:661–676. doi:10.1007/s11104-013-1891-x
Maloof JN, Nozue K, Mumbach MR, Palmer CM (2013) LeafJ: an ImageJ plugin for semi-automated leaf shape measurement. J Vis Exp 71:e50028. doi:10.3791/50028
Manchanda G, Garg N (2008) Salinity and its effects on the functional biology of legumes. Acta Physiol Plant 30:595–618. doi:10.1007/s11738-008-0173-3
Martínez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu J-K, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012. doi:10.1104/pp.106.092635
Meng J-F, Xu T-F, Wang Z-Z, Fang Y-L, Xi Z-M, Zhang Z-W (2014) The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology. J Pineal Res 57:200–212. doi:10.1111/jpi.12159
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Nie W, Xu L, Yu B (2015) A putative soybean GmsSOS1 confers enhanced salt tolerance to transgenic Arabidopsis sos1-1 mutant. Protoplasma 252:127–134. doi:10.1007/s00709-014-0663-7
Oh DH, Lee SY, Bressan RA, Yun DJ, Bohnert HJ (2010) Intracellular consequences of SOS1 deficiency during salt stress. J Exp Bot 61:1205–1213. doi:10.1093/jxb/erp391
Olías R, Eljakaoui Z, Li J, De Morales PA, Marín-Manzano MC, Pardo JM, Belver A (2009a) The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant Cell Environ 32:904–916. doi:10.1111/j.1365-3040.2009.01971.x
Olías R, Eljakaoui Z, Pardo JM, Belver A (2009b) The Na+/H+ exchanger SOS1 controls extrusion and distribution of Na+ in tomato plants under salinity conditions. Plant Signal Behav 4:973–976
Qiu ZB, Guo JL, Zhu AJ, Zhang L, Zhang MM (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotox Environ Safe 104:202–208. doi:10.1016/j.ecoenv
Quintero FJ, Ohta M, Shi H, Zhu J-K, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. PNAS 99:9061–9066. doi:10.1073/pnas.132092099
Sanadhya P, Agarwal P, Agarwal PK (2015) Ion homeostasis in a salt-secreting halophytic grass. AoB Plants 7:plv055. doi:10.1093/aobpla/plv055
Schmidt R, Mieulet D, Hubberten H-M, Obata T, Hoefgen R, Fernie AR, Fisahn J, Segundo BS, Guiderdoni E, Schippers JHM, Mueller-Roeber B (2013) Salt-responsive ERF1 regulates reactive oxygen species–dependent signaling during the initial response to salt stress in rice. Plant Cell 25:2115–2131. doi:10.1105/tpc.113.113068
Shi H, Quintero FJ, Pardo JM, Zhu Jian-Kang (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477. doi:10.1105/tpc.010371
Shi H, Lee BH, Wu SJ, Zhu JK (2003) Overexpressing of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85. doi:10.1038/nbt766
Song A, Lu J, Jiang J, Chen S, Guan Z, Fang W, Chen F (2012) Isolation and characterisation of Chrysanthemum crassum SOS1, encoding a putative plasma membrane Na+/H+ antiporter. Plant Biol 14:706–713. doi:10.1111/j.1438-8677.2011.00560.x
Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu J-K, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709. doi:10.1104/pp.104.039909
Tian F, Jia TJ, Yu BJ (2014) Physiological regulation of seed soaking with soybean isoflavones on drought tolerance of Glycine max and Glycine soja. Plant Growth Regul 74:229–237. doi:10.1007/s10725-014-9914-z
Volkov V (2015) Salinity tolerance in plants. Quantitative approach to ion transport starting from halophytes and stepping to genetic and protein engineering for manipulating ion fluxes. Front Plant Sci 6:873. doi:10.3389/fpls.2015.00873
Wei P, Chen D, Jing R, Zhao C, Yu B (2015) Ameliorative effects of foliar methanol spraying on salt injury to soybean seedlings differing in salt tolerance. Plant Growth Regul 75:133–141. doi:10.1007/s10725-014-9938-4
Wu H, Shabala L, Liu X, Azzarello E, Zhou M, Pandolfi C, Chen Z-H, Bose J, Mancuso S, Shabala S (2015) Linking salinity stress tolerance with tissue-specific Na+ sequestration in wheat roots. Front Plant Sci 6:71
Xue Z, Zhao S, Gao H, Sun S (2014) The salt resistance of wild soybean (Glycine soja Sieb. et Zucc. ZYD 03262) under NaCl stress is mainly determined by Na+ distribution in the plant. Acta Physiol Plant 36:61–70. doi:10.1007/s11738-013-1386-7
Yadav NS, Shukla PS, Jha A, Agarwal PK, Jha B (2012) The SbSOS1 gene from the extreme halophyte Salicornia brachiata enhances Na+ loading in xylem and confers salt tolerance in transgenic tobacco. BMC Plant Biol 12:188
Zhang JL, Shi H (2013) Physiological and molecular mechanisms of plant salt tolerance. Photosynth Res 115:1–22
Zhang XK, Zhou QH, Cao JH, Yu BJ (2011) Differential Cl−/salt tolerance and NaCl-induced alternations of tissue and cellular ion fluxes in Glycine max, Glycine soja and their hybrid seedlings. J Agron Crop Sci 197:329–339
Zhou H, Lin H, Chen S, Becker K, Yang Y, Zhao J, Kudla J, Schumaker KS, Guo Y (2014) Inhibition of the Arabidopsis salt overly sensitive pathway by 14-3-3 proteins. Plant Cell 26:1166–1182. doi:10.1105/tpc.113.117069
Zhou Y, Yin X, Duan R (2015) SpAHA1 and SpSOS1 coordinate in transgenic yeast to improve salt tolerance. PLoS One 10(9):e0137447. doi:10.1371/journal.pone.0137447
Acknowledgements
This work was funded by the National Natural Science Foundation of China (Nos. 30871462, U1603111).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by H Peng.
X. Zhao and P. Wei contributed equally to this work.
Rights and permissions
About this article
Cite this article
Zhao, X., Wei, P., Liu, Z. et al. Soybean Na+/H+ antiporter GmsSOS1 enhances antioxidant enzyme activity and reduces Na+ accumulation in Arabidopsis and yeast cells under salt stress. Acta Physiol Plant 39, 19 (2017). https://doi.org/10.1007/s11738-016-2323-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2323-3