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The differences in physiological responses, ultrastructure changes, and Na+ subcellular distribution under salt stress among the barley genotypes differing in salt tolerance

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Abstract

Plants adopt several strategies to maintain cellular ion homeostasis, including physiological, biochemical, cellular, subcellular, and molecular mechanisms for fighting against salt stress. We investigated the responses of tolerant Tibetan wild barley (XZ16), tolerant (CM72) and sensitive (Gairdner) barley cultivars at physiological, cellular, and molecular levels. The results revealed that salinity induced a significantly greater reduction in total root length, surface area, diameter, and total volume in Gairdner than in CM72 and XZ16. Analysis of gene expression using quantitative RT-PCR showed that transcripts of vacuolar H+-ATPase and inorganic pyrophosphatase (HvHVA/68 and HvHVP1) were more abundant in leaves and roots of XZ16 and CM72 than those of Gairdner. Observation of electron microscopy detected the difference in the damage of leaf and root ultrastructure among the three genotypes under salt stress, with XZ16 and Gairdner being least and most affected, respectively. Subcellular study showed that a primary strategy to protect the cytosol against sodium toxicity was compartmentalization of sodium ions into soluble fraction (vacuoles). Gairdner showed drastically stronger sodium-specific fluorescence visualized by CoroNa-Green, a sodium-specific fluorophore, than CM72 and XZ16.

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Abbreviations

SPB:

Sodium phosphate buffer

TEM:

Transmission electron microscopy

ICP–OES:

Inductively coupled plasma–optical emission spectrometry

References

  • Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Lett 581:2247–2254

    Article  CAS  PubMed  Google Scholar 

  • Apse MP, Aharon GS, Sneddon WA, Blumwald E (1999) Salt tolerance conferred by over expression of a vacuolar Na+/H+ antiport in Arabidopsis. Sci 285:1256–1258

    Article  CAS  Google Scholar 

  • Ayala F, Leary JW, Schumaker KS (1996) Increased vacuolar and plasma membrane H+-ATPase activities in Salicornia bigelovii Torr in response to NaCl. J Exp Bot 47:25–32

    Article  CAS  Google Scholar 

  • Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochim Biophys Acta 1465:140–151

    Article  CAS  PubMed  Google Scholar 

  • Brini F, Hanin M, Mezghani I, Berkowitz GA, Masmoudi K (2007) Overexpression of wheat Na+/H+ antiporter NHX1 and H+- pyrophosphatase TVP1 improve salt- and drought-stress tolerance in Arabidopsis thaliana plants. J Exp Bot 58:301–308

    Article  CAS  PubMed  Google Scholar 

  • Dong Hh, Eduardo L, Quan Z, Sung-M H, Youzhi L, Francisco JQ, **ngyu J, Matilde PDU, Sang YL, Yanxiu Z, Jeong DB, Ray AB, Dae JY, Jose MP, Hans JB (2009) Loss of halophytism by interference with SOS1 expression. Plant Physiol 151:210–222

    Article  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55(396):307–319

    Article  CAS  PubMed  Google Scholar 

  • Flowers TJ, Colmer TO (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  CAS  PubMed  Google Scholar 

  • Flowers TJ, Hajibagheri MA (2001) Salinity tolerance in Hordeum vulgare ion concentrations in root cells of cultivars differing in salt tolerance. Plant Soil 231:1

    Article  CAS  Google Scholar 

  • Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 45:146–159

    CAS  PubMed  Google Scholar 

  • Gao F, Gao Q, Duan XG, Yue GD, Yang AF, Zhang JR (2006) Cloning of an H+-PPase gene from Thellungiella halophila and its heterologous expression to improve tobacco salt tolerance. J Exp Bot 57:3259–3270

    Article  CAS  PubMed  Google Scholar 

  • Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214

    Article  CAS  PubMed  Google Scholar 

  • Golldack D, Dietz KJ (2001) Salt-induced expression of the vacuolar H+-ATPase in the common ice plant is developmentally controlled and tissue specific. Plant Physiol 125:1643–1654

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    CAS  PubMed  Google Scholar 

  • He XL, Huan X, Shen YZ, Huang ZJ (2014) Wheat V-H+-ATPase subunit genes significantly affect salt tolerance in Arabidopsis thaliana. PLoS ONE 9(8):e86982

    Article  PubMed Central  PubMed  Google Scholar 

  • Kohei H, Megumi N, Katsuhisa Y, Miwa O, Yoshihisa O, Tomohiro U, Go Tatsuaki, Masa HS, Miyo TM, Masao T, Sei-ichiro HAN, Ikuko HN, Masayoshi M, Hidehiro F, Tetsuro M (2009) Dynamic aspects of ion accumulation by vesicle traffic under salt stress in Arabidopsis. Plant Cell Physiol 50(12):2023–2033

    Google Scholar 

  • Krebs M, Beyhl D, Gorlich E, Al-Rasheid AS, Marten I, Stierhof YD, Hedrich R, Schumacher K (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci USA 107:3251–3256

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Maser P, Gierth M, Schroeder JI (2002) Molecular mechanisms of potassium and sodium uptake in plants. Plant Soil 247:43–54

    Article  Google Scholar 

  • Mehea P, Hyosuk L, Jung SL, Ok Myung, Beom-Gi B, Kim MP (2009) In planta measurements of Na+ using fluorescent dye CoroNa Green. J Plant Biol 52:298–302

    Article  Google Scholar 

  • Mitsuya S, Takeoka Y, Miyake H (2000) Effects of sodium chloride on foliar ultrastructure of sweet potato (Ipomoea batatas Lam) plantlets grown under light and dark conditions in vitro. J Plant Physiol 157:661–667

    Article  CAS  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Physiol 59:651–681

    CAS  Google Scholar 

  • Okamura H, Aoyama I (1994) Interactive toxic effect and distribution of heavy metals in phytoplankton. Environ Toxicol Water Qual 9:7–15

    Article  CAS  Google Scholar 

  • Pajerowski JD, Dahl KN, Zhong FL, Sammak PJ, Discher DE (2007) Physical plasticity of the nucleus in stem cell differentiation. Proc Natl Acad Sci USA 104:15619–15624

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Parida AK, Das AB (2004) Effects of NaCl stress on nitrogen and phosphorus metabolism in a true mangrove Bruguiera parviflora grown under hydroponic culture. J Plant Physiol 161:921–928

    Article  CAS  PubMed  Google Scholar 

  • Peng HY, Yang XE, Tian SK (2005) Accumulation and ultrastructural distribution of copper in Elasholtzia splendens. J Zhejiang Univ Sci B 6:311–318

  • Qiu L, Wu DZ, Ali S, Cai SG, Dai F, Zhang GP (2011) Evaluation of salinity tolerance and analysis of allelic function of HvHKT1 and HvHKT2 in Tibetan wild barley. Theor Appl Genet 122:695–703

    Article  CAS  PubMed  Google Scholar 

  • Shuang W, Tobias B, Kimberly LG (2012) Mechanical fixation techniques for processing and orienting delicate samples, such as the root of Arabidopsis thaliana, for light or electron microscopy. Nat Protoc 7:1113–1124

    Article  Google Scholar 

  • Suzuki A, Vergnet C, Morot-Gaudry JF, Zehnacker C, Grosclaude J (1994) Immunological characterization of ferredoxin and methyl viologen interaction domains of glutamate synthase using monoclonal antibodies. Plant Physiol Biochem 32:619–626

    CAS  Google Scholar 

  • Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, Donald Mc (2011) Additive effects of Na+ and Cl− ions on barley growth under salinity stress. J Exp Bot 62:2189–2203

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tester M, Davenport RJ (2003) Na+ transport and Na+ tolerance in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  Google Scholar 

  • Vera-Estrella R, Barkla BJ, Garcia-Ramirez L, Pantoja O (2005) Salt stress in Thellungiella halophila activates Na+ transport mechanisms required for salinity tolerance. Plant Physiol 139:1507–1517

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang XC, Chang LL, Wang BC, Wang D, Li PH, Wang LM, Yi XP, Huang QX, Peng M, Guo AP (2013) Comparative Proteomics of Thellungiella halophila leaves from plants subjected to salinity reveals the importance of chloroplastic starch and soluble sugars in halophyte salt tolerance. Mol Cell Proteomics 12:2174–2195

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu DZ, Qiu L, Xu L, Ye LZ, Chen MX, Zhang GP (2011) Genetic variation of HvCBF genes and their association with salinity tolerance in Tibetan annual wild barley. PLoS One 6:e22938

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu D, Cai SG, Chen M, Ye LZ, Chen ZG, Wu FB, Zhang GP (2013) Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS One 8:e55431

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • **a FC, Jiang GQ, Lu JM (2002) Development of the study on Halophyte’s structure of resisting saline-alkali. J TongHua Teach Coll 23(2):67–69

    Google Scholar 

  • Yamane K, Mitsuya S, Taniguchi W, Miyake H (2012) Salt-induced chloroplast protrusionis the process of exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts into cytoplasm in leaves of rice. Plant Cell Environ 35:1663–1671

    Article  CAS  PubMed  Google Scholar 

  • Zeng F, Zhou W, Qiu B, Ali S, Wu F, Zhang G (2011) Subcellular distribution and chemical forms of chromium in rice plants suffering from different levels of chromium toxicity. J Plant Nutr Soil Sci 174:249–256

    CAS  Google Scholar 

  • Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Sun HY, Dai HX, Zhang GP, Wu FB (2010) Difference in response to drought stress among Tibet wild barley genotypes. Euphytica 172:395–403

    Article  CAS  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by National Natural Science Foundation of China (No. 31330055, 31301246 and 31171544), China Agriculture Research System (CARS-05).

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Authors and Affiliations

  1. Agronomy Department, Key Laboratory of Crop Germplasm Resource of Zhejiang Province, Institute of Crop Science, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, China

    Zahra Jabeen, Nazim Hussain, Yong Han, Munawar Jawad Shah, Fanrong Zeng, Jianbin Zeng & Guo** Zhang

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  1. Zahra Jabeen
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  2. Nazim Hussain
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  3. Yong Han
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  4. Munawar Jawad Shah
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  6. Jianbin Zeng
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  7. Guo** Zhang
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Correspondence to Guo** Zhang.

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Communicated by J. V. Jorrin-Novo.

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Jabeen, Z., Hussain, N., Han, Y. et al. The differences in physiological responses, ultrastructure changes, and Na+ subcellular distribution under salt stress among the barley genotypes differing in salt tolerance. Acta Physiol Plant 36, 2397–2407 (2014). https://doi.org/10.1007/s11738-014-1613-x

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