Plant Molecular Biology Reporter

, Volume 30, Issue 3, pp 590–598 | Cite as

Salinity-Induced Effects in the Halophyte Suaeda salsa Using NMR-based Metabolomics

  • Huifeng Wu
  • Xiaoli Liu
  • Liping You
  • Linbao Zhang
  • Junbao Yu
  • Di Zhou
  • Jianmin Zhao
  • Jianghua Feng


Suaeda salsa is a native halophyte in saline soils. Salinity is the most important environmental constraint for plant productivity in the Yellow River Delta. In this work, we investigated the salt-induced effects in root of S. salsa exposed to two environmentally relevant salinities for 1 week and 1 month using nuclear magnetic resonance-based metabolomics. Our results indicated that salt stress inhibited the growth of S. salsa and induced significant metabolic responses including decreased amino acids, lactate, 4-aminobutyrate, malate, choline, phosphocholine, and increased betaine, sucrose, and allantoin in root tissues of S. salsa. In addition, salinity exposures upregulated the activities of superoxide dismutase, glutathione S-transferases, peroxidase, catalase, and glutathione peroxidase in the aboveground part of seedlings of S. salsa after exposures. Overall, these results demonstrated the osmotic and oxidative stresses, disturbances in protein biosynthesis/degradation, and energy metabolism in S. salsa exposed to salinities.


Suaeda salsa Salinity Metabolic response NMR Metabolomics Antioxidant enzyme activity 



Analysis of variance


Betaine aldehyde dehydrogenase




Choline monooxygenase


False discovery rate


Glutathione peroxidase


Glutathione S-transferases


Nuclear magnetic resonance


Principal component


Principal components analysis




Pattern recognition


Reactive oxygen species


Significance analysis of microarray


Superoxide dismutase


Tricarboxylic acid


Sodium 3-trimethlysilyl [2,2,3,3-D4] propionate



We thank Dr. Mark Viant (School of Bioscience, The University of Birmingham) for use of the software ProMetab. This research was supported by the Project of National Science & Technology Pillar Program in “12th Five Year” Period (2011BAC02B01), The 100 Talents Program of the Chinese Academy of Sciences, Innovation Programs of the Chinese Academy of Sciences (KZCX2-YW-223 and KZCX2-YW-225) and Technology Development Program Projects of Shandong Province (2008GG20005006 and 2008GG3NS0700), and in part by the CAS/SAFEA International Partnership Program for Creative Research Teams.


  1. Aliferis KA, Materzok S, Paziotou GN, Chrysayi-Tokousbalides M (2009) Lemna minor L. as a model organism for ecotoxicological studies performing 1H NMR fingerprinting. Chemosphere 76:967–973PubMedCrossRefGoogle Scholar
  2. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341PubMedCrossRefGoogle Scholar
  3. Askari H, Edqvist J, Hajheidari M, Kafi M, Salekdeh GH (2006) Effects of salinity levels on proteome of Suaeda aegyptiaca leaves. Proteomics 6:2542–2554PubMedCrossRefGoogle Scholar
  4. Bailey NJC, Oven M, Holmes E, Nicholson JK, Zenk MH (2003) Metabolomic analysis of the consequences of cadmium exposure in Silene cucubalus cell cultures via 1H NMR spectroscopy and chemometrics. Phytochemistry 62:851–858PubMedCrossRefGoogle Scholar
  5. Bao Y, Zhao R, Li F, Tang W, Han L (2011) Simultaneous expression of Spinacia oleracea chloroplast choline monooxygenase (CMO) and betaine aldehyde dehydrogenase (BADH) genes contribute to dwarfism in transgenic Lolium perenne. Plant Mol Biol Rep 29:379–388CrossRefGoogle Scholar
  6. Basyuni M, Kinjo Y, Baba S, Shinzato N, Iwasaki H, Siregar EBM, Oku H (2011) Isolation of salt stress tolerance genes from roots of mangrove plant, Rhizophora stylosa Griff., using PCR-based suppression subtractive hybridization. Plant Mol Biol Rep 29:533–543CrossRefGoogle Scholar
  7. Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126:1024–1030PubMedCrossRefGoogle Scholar
  8. Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  9. Bundy JG, Davey MP, Viant MR (2009) Environmental metabolomics: a critical review and future perspectives. Metabolomics 5:3–21CrossRefGoogle Scholar
  10. Chen H, Jiang JG, Wu GH (2009) Effects of salinity changes on the growth of Dunaliella salina and its isozyme activities of glycerol-3-phosphate dehydrogenase. J Agric Food Chem 57:6178–6182PubMedCrossRefGoogle Scholar
  11. Choi HK, Choi YH, Verberne MC, Lefeber AWM, Erkelens C, Verpoorte R (2004) Metabolic fingerprinting of wild type and transgenic tobacco plants by 1HNMR and multivariate analysis technique. Phytochemistry 65:857–864PubMedCrossRefGoogle Scholar
  12. Cui BS, He Q, Zhao XS (2008) Ecological thresholds of Suaeda salsa to the environmental gradients of water table depth and soil salinity. Acta Ecol Sin 28:1408–1418CrossRefGoogle Scholar
  13. Dai H, Xiao C, Liu H, Hao F, Tang H (2010) Combined NMR and LC-DAD-MS analysis reveals comprehensive metabonomic variations for three phenotypic cultivars of Salvia miltiorrhiza Bunge. J Proteome Res 9:1565–1578PubMedCrossRefGoogle Scholar
  14. Davis B (2005) Growing pains for metabolomics. The Scientist 19:25–28Google Scholar
  15. Dendooven L, Alcántara-Hernández RJ, Valenzuela-Encinas C, Luna-Guido M, Perez-Guevara F, Marsch R (2010) Dynamics of carbon and nitrogen in an extreme alkaline saline soil: a review. Soil Biol Biochem 42:865–877CrossRefGoogle Scholar
  16. Fan WMT (1996) Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog Nucl Magn Reson Spectros 28:161–219Google Scholar
  17. Fiehn O (2002) Metabolomics: the link between genotypes and phenotypes. Plant Mol Biol 48:155–171PubMedCrossRefGoogle Scholar
  18. Greenway H, Osmond CB (1972) Salt responses of enzymes from species differing in salt tolerance. Plant Physiol 49:256–259PubMedCrossRefGoogle Scholar
  19. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Station Circ 347:1–32Google Scholar
  20. Jellouli N, Jouira HB, Daldoul S, Chenennaoui S, Ghorbel A, Salem AB, Gargouri A (2011) Proteomic and transcriptomic analysis of grapevine PR10 expression during salt stress and functional characterization in yeast. Plant Mol Biol Rep 28:1–8CrossRefGoogle Scholar
  21. Katsiadaki I, Williams TD, Ball JS, Bean TP, Sanders MB, Wu H, Santos EM, Brown MM, Baker P, Ortega F, Falciani F, Craft JA, Tyler CR, Viant MR, Chipman JK (2009) Hepatic transcriptomic and metabolomic responses in the Stickleback (Gasterosteus aculeatus) exposed to ethinyl-estradiol. Aquat Toxicol 97:174–187PubMedCrossRefGoogle Scholar
  22. Kim HK, Verpoorte R (2010) Sample preparation for plant metabolomics. Phytochem Anal 21:4–13PubMedCrossRefGoogle Scholar
  23. Lee MB, Blunt JW, Lever M, Georgea PM (2004) A nuclear-magnetic-resonance-based assay for betaine-homocysteine methyltransferase activity. Anal Biochem 330:199–205PubMedCrossRefGoogle Scholar
  24. Li PH, Chen M, Wang BS (2002) Effect of K+ nutrition on growth and activity of leaf tonoplast V-H+-ATPase and V-H+-PPase of Suaeda salsa under NaCl stress. Acta Bot Sin 44:433–440Google Scholar
  25. Li W, Wang D, Jin T, Chang Q, Yin D, Xu S, Liu B, Liu L (2011) The vacuolar Na+/H+ antiporter gene SsNHX1 from the halophyte Salsola soda confers salt tolerance in transgenic alfalfa (Medicago sativa L.). Plant Mol Biol Rep 29:278–290CrossRefGoogle Scholar
  26. Lindon JC, Nicholson JK, Everett JR (1999) NMR spectroscopy of biofluid. Ann Rep NMR Spectrosc 381–388Google Scholar
  27. Liu X, Yang C, Zhang L, Li L, Liu S, Yu J, You L, Zhou D, Xia C, Zhao J, Wu H (2011a) Metabolic profiling of cadmium-induced effects in one pioneer intertidal halophyte Suaeda salsa by NMR-based metabolomics. Ecotoxicology 20:1422–1432PubMedCrossRefGoogle Scholar
  28. Liu X, Zhang L, You L, Wu H, Zhao J, Cong M, Li F, Wang Q, Li L, Li C, Han G, Wang G, Xia C, Yu J (2011b) Metabolomic study on the halophyte Suaeda salsa in the Yellow River Delta. Clean-Soil Air Water 39:720–727CrossRefGoogle Scholar
  29. Liu X, Zhang L, You L, Yu J, Cong M, Wang Q, Li F, Li L, Zhao J, Li C, Wu H (2011c) Assessment of clam Ruditapes philippinarum as heavy metal bioindicators using NMR-based metabolomics. Clean-Soil Air Water 39:759–766CrossRefGoogle Scholar
  30. Liu X, Zhang L, You L, Yu J, Zhao J, Li L, Wang Q, Li F, Liu D, Wu H (2011d) Differential toxicological effects induced by mercury in gills from three pedigrees of Manila clam Ruditapes philippinarum by NMR-based metabolomics. Ecotoxicology 20:177–186PubMedCrossRefGoogle Scholar
  31. Liu X, Zhang L, You L, Cong M, Zhao J, Wu H, Li C, Liu D, Yu J (2011e) Toxicological responses to acute mercury exposure for three species of Manila clam Ruditapes philippinarum by NMR-based metabolomics. Environ Toxicol Pharmacol 31:323–332PubMedCrossRefGoogle Scholar
  32. Moghaieb REA, Saneoka H, Fujita K (2004) Effect of salinity on osmotic adjustment, glycinebetaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophytic plants, Salicornia europaea and Suaeda maritime. Plant Sci 166:1345–1349CrossRefGoogle Scholar
  33. Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250PubMedCrossRefGoogle Scholar
  34. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663PubMedCrossRefGoogle Scholar
  35. Nuccio ML, Rhodes D, McNeil SD, Hanson AD (1999) Metabolic engineering of plants for osmotic stress resistance. Curr Opin Plant Biol 2:128–134PubMedCrossRefGoogle Scholar
  36. Parsons HM, Ludwig C, Gunther UL, Viant MR (2007) Improved classification accuracy in 1- and 2-dimensional NMR metabolomics data using the variance stabilising generalised logarithm transformation. BMC Bioinform 8:234CrossRefGoogle Scholar
  37. Pedras MSC, Zheng QA (2010) Metabolic responses of Thellungiella halophila/salsuginea to biotic and abiotic stresses: Metabolite profiles and quantitative analyses. Phytochemistry 71:581–589PubMedCrossRefGoogle Scholar
  38. Peel GJ, Mickelbart MV, Rhodes D (2010) Choline metabolism in glycine betaine accumulating and non-accumulating near-isogenic lines of Zea mays and Sorghum bicolor. Phytochemistry 71:404–414PubMedCrossRefGoogle Scholar
  39. Song J, Fan H, Zhao YY, Jia YH, Du XH, Wang BS (2008) Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an intertidal zone and on saline inland. Aquat Bot 88:331–337CrossRefGoogle Scholar
  40. Sonjak S, Udovic M, Wraber T, Likar M, Marjana Regvar M (2009) Diversity of halophytes and identification of arbuscular mycorrhizal fungi colonising their roots in an abandoned and sustained part of Secovlje salterns. Soil Biol Biochem 41:1847–1856CrossRefGoogle Scholar
  41. Sun X, Zhang J, Zhang H, Ni Y, Zhang Q, Chen J, Guan Y (2010) The responses of Arabidopsis thaliana to cadmium exposure explored via metabolite profiling. Chemosphere 78:840–845PubMedCrossRefGoogle Scholar
  42. Wang BS, Luttge U, Ratajczak R (2001) Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J Exp Bot 52:2355–2365PubMedCrossRefGoogle Scholar
  43. Wang CQ, Chen M, Wang BS (2007) Betacyanin accumulation in the leaves of C3 halophyte Suaeda salsa L. is induced by watering roots with H2O2. Plant Sci 172:1–7CrossRefGoogle Scholar
  44. Xiao C, Dai H, Liu H, Wang Y, Tang H (2008) Revealing the metabonomic variation of rosemary extracts using 1H NMR spectroscopy and multivariate data analysis. J Agric Food Chem 56:10142–10153PubMedCrossRefGoogle Scholar
  45. Xu L (2004) Methods of chemometrics. Science Press, Beijing, pp 221–227Google Scholar
  46. Xu C, Zheng L, Gao C, Wang C, Liu G, Jiang J, Wang Y (2011) Ovexpression of a vacuolar H+−ATPase c subunit gene mediates physiological changes leading to enhanced salt tolerance in transgenic tobacco. Plant Mol Biol Rep 29:424–430CrossRefGoogle Scholar
  47. Yang G, Zhou R, Tang T, Chen X, Ouyang J, He L, Li W, Chen S, Guo M, Li X, Zhong C, Shi S (2011) Gene expression profiles in response to salt stress in Hibiscus tiliaceus. Plant Mol Biol Rep 29:609–617CrossRefGoogle Scholar
  48. Zhang L, Ma XL, Zhang Q, Ma CL, Wang PP, Sun YF, Zhao YX, Zhang H (2001) Expressed sequence tags from a NaCl-treated Suaeda salsa cDNA library. Gene 267:193–200PubMedCrossRefGoogle Scholar
  49. Zhang JY, Li MH, Xu LM, Wang ZJ (2008) Effect o f Suaeda seed oil on blood-fat and immunologic function of mouse (In Chinese). Occup Health 24:1529–1530Google Scholar
  50. Zhang JT, Zhang Y, Du YY, Chen SY, Tang HR (2011) Dynamic metabonomic responses of tobacco (Nicotiana tabacum) plants to salt stress. J Proteome Res 10:1904–1914PubMedCrossRefGoogle Scholar
  51. Zhang L, Liu X, You L, Zhou D, Wang Q, Li F, Cong M, Li L, Zhao J, Liu D, Yu J, Wu H (2011a) Benzo(a)pyrene-induced metabolic responses in Manila clam Ruditapes philippinarum by proton nuclear magnetic resonance (1H NMR) based metabolomics. Environ Toxicol Pharmacol 32:218–225PubMedCrossRefGoogle Scholar
  52. Zhang L, Liu X, You L, Zhou D, Wu H, Li L, Zhao J, Feng J, Yu J (2011b) Metabolic responses in gills of Manila clam Ruditapes philippinarum exposed to copper using NMR-based metabolomics. Mar Environ Res 72:33–39PubMedCrossRefGoogle Scholar
  53. Zhang X, Zhen J, Li Z, Kang D, Yang Y, Kong J, Hua J (2011) Expression profile of early responsive genes under salt stress in upland cotton (Gossypium hirsutum L.). Plant Mol Biol Rep 29:626–637CrossRefGoogle Scholar
  54. Zhao KF (1991) Desalinization of saline soils by Suaeda salsa. Plant Soil 135:303–305CrossRefGoogle Scholar
  55. Zhao HL, Ma YZ, Li JX, Piao L (2010) Study on edible value of Suaeda salsa (In Chinese). J Anhui Agric Sci 38:14350–14351Google Scholar
  56. Zhou G, Yang L, Li Y, Zou C, Huang L, Qiu L, Huang X, Srivastava MK (2011) Proteomic analysis of osmotic stress-responsive proteins in sugarcane leaves. Plant Mol Biol Rep. doi: 10.1007/s11105-011-0343-0

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Huifeng Wu
    • 1
  • Xiaoli Liu
    • 1
    • 2
  • Liping You
    • 1
    • 2
  • Linbao Zhang
    • 1
    • 2
  • Junbao Yu
    • 1
  • Di Zhou
    • 1
    • 2
  • Jianmin Zhao
    • 1
  • Jianghua Feng
    • 3
  1. 1.Key Laboratory of Coastal Zone Environment Processes, CAS, Shandong Provincial Key Laboratory of Coastal Zone Environment Processes, Yantai Institute of Coastal Zone ResearchChinese Academy of SciencesYantaiPeople’s Republic of China
  2. 2.The Graduate School of Chinese Academy of SciencesBeijingPeople’s Republic of China
  3. 3.Department of Electronic Science, Fujian Key Laboratory of Plasma and Magnetic Resonance, State Key Laboratory of Physical Chemistry of Solid SurfacesXiamen UniversityXiamenPeople’s Republic of China

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