Abstract
Salt tolerance in plants is a complex trait involving multiple mechanisms. Understanding these mechanisms and their regulation will assist in developing novel strategies to engineer salt-tolerant crops. In the current study, we investigated salt-tolerant mechanisms in soybean (Glycine max) cultivar WF-7 in comparison to salt-sensitive Union. In vivo and in vitro salt assays demonstrated the salt tolerance of WF-7 at the seedling stage and during germination. After a 10-day 200 mM NaCl treatment, chlorophyll content in Union was reduced by 50 % compared to a 17 % reduction in WF-7. WF-7 was also less affected by abscisic acid (ABA) and NaCl during germination than Union. Upon ABA and NaCl treatment, the ABA-responsive genes SCOF1, ASN1, bZIP44, and AAPK1 are differentially expressed in WF-7 and Union seedlings. These results suggest that salt tolerance in WF-7 is in part regulated through an ABA-dependent pathway. In addition, following a 4-day 200 mM NaCl treatment, WF-7 produced more H2O2 than Union indicating the involvement of reactive oxygen species (ROS) in regulating salt tolerance in WF-7. Yet another mechanism WF-7 employs is withholding toxic chloride (Cl−) ions from aerial tissues. Following 200 mM NaCl treatment, Cl− accumulation was mostly localized to the roots of WF-7. In contrast, most of the Cl− in Union was transported into the stems and leaves. Taken together, our results demonstrated a role of ABA and ROS in regulating salt tolerance in WF-7, and the critical role of Cl− in NaCl-induced mortality in soybean.
Key message Withholding toxic Cl− ions from leaves and, to a lesser extent, stems, confers salt tolerance to soybean WF-7. In addition, ABA and ROS may be involved in salt-stress signal transduction.
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References
Abel GH, MacKenzie AJ (1964) Salt tolerance of soybean varieties (Glycine max L. Merrill) during germination and later growth. Crop Sci 4:157–161
Amarowicz R, Pegg RB (2008) Legumes as a source of natural antioxidants. Eur J Lipid Sci Technol 110:865–878
Bahmaniar MA, Sepanlou MG (2008) Influence of saline irrigation water and gypsum on leaf nutrient accumulation, protein, and oil seed in soybean cultivars. J Plant Nutr 31:485–495
Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochimica et Biophysica Acta 1465:140–151
Böhmer M, Schroeder JI (2011) Quantitative transcriptomic analysis of abscisic acid-induced and reactive oxygen species-dependent expression changes and proteomic profiling in Arabidopsis suspension cells. Plant J 67:105–118
Boschin G, Arnoldi A (2011) Legumes are valuable sources of tocopherols. Food Chem 127:1199–1203
Conde A, Chaves MM, Gerós H (2011) Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol 52:1583–1602
Cui Z, Carter TE, Gai J, Qiu J, Nelson RL (1999) Origin, description, and pedigree of Chinese soybean cultivars from 1923 to 1995. U.S. Department of Agriculture, Agricultural Research Service, Technical Bulletin No. 1871
Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795
de Carvalho MHC (2008) Drought stress and reactive oxygen species. Plant Signal Behav 3:156–165
Delgado MJ, Ligero F, Lluch C (1994) Effects of salt stress on growth and nitrogen fixation by pea, faba-bean, common bean and soybean plants. Soil Biol Biochem 26:371–376
Desikan R, Clarke A, Hancock JT, Neill SJ (1999) H2O2 activates a MAP kinase-like enzyme in Arabidopsis thaliana suspension cultures. J Exp Bot 50:1863–1866
Desikan R, Neill SJ, Hancock JT (2000) Hydrogen peroxide-induced gene expression in Arabidopsis thaliana. Free Radic Biol Med 28:773–778
Epstein E, Norlyn JD, Rush DW, Kings RW, Kelly DB (1980) Saline culture of crops. A general approach. Science 210:399–404
Essa TA (2002) Effect of salinity stress on growth and nutrient composition of three soybean (Glycine max L. Merrill) cultivars. J Agron Crop Sci 188:86–93
Fedina IS, Nedeva D, Çiçek N (2009) Pre-treatment with H2O2 induces salt tolerance in barley seedlings. Biol Plant 53:321–324
Gao JP, Chao DY, Lin HX (2007) Understanding abiotic stress tolerance mechanisms: recent studies on stress response in rice. J Integr Plant Biol 49:742–750
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930
Guan RX, Tian L, Liu ZX, Chang RZ, Ren SX, Qiu LJ (2008) Development of a codominant SCAR marker linked to salt tolerant gene in soybean. In: Proceedings of World Soybean Research Conference VIII, 2008, Beijing, China. p 17
Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proc Natl Acad Sci USA 103:11206–11210
Ishibashi Y, Yamaguchi H, Yuasa T, Iwaya-Inoue M, Arima S, Zheng SH (2011) Hydrogen peroxide spraying alleviates drought stress in soybean plants. J Plant Physiol 168:1562–1567
Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357
Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci USA 97:2940–2945
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidases AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633
Lee GJ, Boerma HR, Villagrcia MR, Zhou X, Carter TE Jr, Li Z (2004) A major QTL conditioning salt tolerance in S-100 soybean and descendent cultivars. Theor Appl Genet 109:1610–1619
Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008) Soybean GmbZIP44, GmbZIP62, and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240
Lu KX, Cao BH, Feng XP, He Y, Jiang DA (2009) Photosynthetic response of salt-tolerant and sensitive soybean varieties. Photosynthesis 47:281–387
Luo Q, Yu B, Liu Y (2005) Differential sensitivity to chloride and sodium ions in seedlings of Glycine max and G. soja under NaCl stress. J Plant Physiol 162:1003–1012
Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247
Palta JP (1990) Leaf chlorophyll content. Remote Sens Rev 5:207–227
Phang T, Shao G, Lam H (2008) Salt tolerance in soybean. J Integr Plant Biol 50:1196–1212
Wang D, Shannon MC, Grieve CM (2001) Salinity reduces radiation absorption and use efficiency in soybean. Field Crop Res 69:267–277
Xia XJ, Wang YJ, Zhou YH, Tao Y, Mao WH, Shi K, Asami T, Chen Z, Yu JQ (2009) Reactive oxygen species are involved in Brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150:801–814
Zhu JK (2002) Salt and drought stress signal transduction in plants. Rev Plant Biol 53:247–273
Acknowledgments
This work was supported in part by USDA Evans Allen Funds to SR, and by the grants 2009CB119000 and 2009-2-06 to YG. Authors would also like to thank reviewers for their valuable comments. This article is a contribution of the Virginia State University, Agricultural Research Station (journal series No. 288).
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Communicated by B. Li.
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Ren, S., Weeda, S., Li, H. et al. Salt tolerance in soybean WF-7 is partially regulated by ABA and ROS signaling and involves withholding toxic Cl− ions from aerial tissues. Plant Cell Rep 31, 1527–1533 (2012). https://doi.org/10.1007/s00299-012-1268-2
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DOI: https://doi.org/10.1007/s00299-012-1268-2