Skip to main content

Advertisement

Log in

A comparative metabolomics analysis of the halophyte Suaeda salsa and Salicornia europaea

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

Suaeda salsa and Salicornia europaea are both annual herbaceous species belonging to the Chenopodiaceae family, and often grow together through our observations in the Yellow River Delta Nature Reserve, and could be used as raw material to produce food and beverages in food industry due to its high nutritional value. In this study, we adopted widely targeted metabolomics to identify 822 and 694 metabolites in the leaves of S. salsa and S. europaea, respectively, to provide a basic data for the future development and utilization of these two species. We found that these two plants were rich in metabolic components with high medical value, such as flavonoids, alkaloids and coumarins. The high contents of branched chain amino acid in these two species may be an important factor for their adaptation to saline-alkali environments. In addition, the contents of glucosamine (FC = 7.70), maltose (FC = 9.34) and d-(+)-sucrose (FC = 7.19) increased significantly, and the contents of d-(+)-glucose, 2-propenyl (sinigrin) and fructose 1-phosphate were significantly increased in the leaves of S. salsa compared to S. europaea, indicating that some certain compounds in different plants have different sensitivity to salt stress. Our work provides new perspectives about important second metabolism pathways in salt tolerance between these two plants, which could be helpful for studying the tolerance mechanisms of wetland plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdelhafez, O. M., Amin, K. M., Batran, R. Z., Maher, T. J., Nada, S. A., & Sethumadhavan, S. (2010). Synthesis, anticoagulant and PIVKA-II induced by new 4-hydroxycoumarin derivatives. Bioorganic & Medicinal Chemistry, 18, 3371–3378.

    CAS  Google Scholar 

  • Ali, B. H., Wabel, N. A., & Blunden, G. (2005). Phytochemical, pharmacological and toxicological aspects of Hibiscus sabdariffa L.: a review. Phytotherapy Research, 19(3), 369–375.

    CAS  Google Scholar 

  • Amin, K. M., Rahman, D. E. A., & Al-Eryani, Y. A. (2008). Synthesis and preliminary evaluation of some substituted coumarins as anticonvulsant agents. Bioorganic & Medicinal Chemistry, 16, 5377–5388.

    CAS  Google Scholar 

  • Anandam, S., & Selvamuthukumar, S. (2014). Fabrication of cyclodextrin nanosponges for quercetin delivery: physicochemical characterization, photostability, and antioxidant effects. Journal of Materials Science, 49, 8140–8153.

    CAS  Google Scholar 

  • Anwar, J., Spanevello, R. M., Pimentel, V. C., Gutierres, J., Thome, G., Cardoso, A., et al. (2013). Caffeic acid treatment alters the extracellular adenine nucleotide hydrolysis in platelets and lymphocytes of adult rats. Food and Chemical Toxicology, 56, 459–466.

    CAS  Google Scholar 

  • Arakawa, Y., Chiji, H., & Izawa, M. (1983). Structural elucidation of 2 new chromones isolated from glasswort (Salicornia europaea L). Agricultural and Biological Chemistry, 47(9), 2029–2033.

    CAS  Google Scholar 

  • Bagdas, D., Cinkilic, N., Ozboluk, H. Y., Ozyigit, M. O., & Gurun, M. S. (2013). Antihyperalgesic activity of chlorogenic acid in experimental neuropathic pain. Journal of Natural Medicines, 67, 698–704.

    CAS  Google Scholar 

  • Bai, J. H., Wang, X., Jia, J., Zhang, G. L., Wang, Y. Y., & Zhang, S. (2017). Denitrification of soil nitrogen in coastal and inland salt marshes with different flooding frequencies. Physics and Chemistry of the Earth, 97, 31–36.

    Google Scholar 

  • Behl, R. K., Moawad, A. M., & Achtnich, W. (1991). Amino acid and protein profile changes in a spring wheat mutant under prolonged heat stress. Annals of Biology, 7, 63–68.

    Google Scholar 

  • Bendaly, A., Messedi, D., Smaoui, A., Ksouri, R., Bouchereau, A., & Abdelly, C. (2016). Physiological and leaf metabolome changes in the xerohalophyte species Atriplex halimus induced by salinity. Plant Physiology and Biochemistry, 103, 208–218.

    CAS  Google Scholar 

  • Birt, D. F., & Jeffery, E. (2013). Flavonoids. Advances in Nutrition, 4, 576–577.

    Google Scholar 

  • Borate, A. R., Suralkar, A. A., Birje, S. S., Malusare, P. V., & Bangale, P. A. (2011). Antihyperlipidemic effect of protocatechuic acid in fructose induced hyperlipidemia in rats. International Journal of Pharma and Bio Sciences, 2(4), 456.

    CAS  Google Scholar 

  • Chao, C. Y., & Yin, M. C. (2009). Antibacterial effects of roselle calyx extracts and protocatechuic acid in ground beef and apple juice. Foodborne Pathogens and Disease, 6(2), 201–206.

    CAS  Google Scholar 

  • Chen, W., Gong, L., Guo, Z. L., Wang, W. S., Zhang, H. Y., Liu, X. Q., et al. (2013). A novel integrated method for large-scale detection, identification, and quantification of widely targeted metabolites: application in the study of rice metabolomics. Molecular Plant, 6, 1769–1780.

    CAS  Google Scholar 

  • Chen, H. Y., & Yang, X. B. (2006). Protective effect of hyperin on focal cerebral ischemia reperfusion injury in rats. Journal of Integrative Medicine, 4, 526–529.

    CAS  Google Scholar 

  • Cheng, X., Siow, R. C. M., & Mann, G. E. (2011). Impaired redox signaling and antioxidant gene expression in endothelial cells in diabetes: a role for mitochondria and the nuclear factor-E2-related factor 2-Kelch-like ECH-associated protein 1 defense pathway. Antioxidants & Redox Signaling, 14(3), 469.

    CAS  Google Scholar 

  • Cho, A. S., Jeon, S. M., Kim, M. J., Yeo, J., Seo, K. I., Choi, M. S., et al. (2010). Chlorogenic acid exhibits anti-obesity property and improves lipid metabolism in high-fat diet-induced-obese mice. Food and Chemical Toxicology, 48, 937–943.

    CAS  Google Scholar 

  • Chung, Y. C., Chun, H. K., Yang, J. Y., Kim, J. Y., & Han, E. H. (2005). Tungtungmadic acid, a novel antioxidant, from Salicornia herbacea. Archives of Pharmacal Research, 28, 1122–1126.

    CAS  Google Scholar 

  • Cinkilic, N., Cetintas, S. K., Zorlu, T., Vatan, O., Yilmaz, D., Cavas, T., et al. (2013). Radioprotection by two phenolic compounds: chlorogenic and quinic acid, on X-ray induced DNA damage in human blood lymphocytes in vitro. Food and Chemical Toxicology, 53, 359–363.

    CAS  Google Scholar 

  • Clifford, M. N. (2000). Chlorogenic acids and other cinnamates-nature, occurrence, dietary burden, absorption and metabolism. Journal of the Science of Food and Agriculture, 80(7), 1033–1043.

    CAS  Google Scholar 

  • Daglia, M., Di Lorenzo, A., Nabavi, S. F., Talas, Z. S., & Nabavi, S. M. (2014). Polyphenols: well beyond the antioxidant capacity: gallic acid and related compounds as neuroprotective agents: you are what you eat! Current Pharmaceutical Biotechnology, 15(4), 362–372.

    CAS  Google Scholar 

  • Delogu, G. L., Serra, S., Quezada, E., Uriarte, E., Vilar, S., Tatonetti, N. P., et al. (2014). Monoamine oxidase (MAO) inhibitory activity: 3-phenylcoumarins versus 4-hydroxy-3- phenylcoumarins. Chem. Med. Chem, 9, 1–5.

    Google Scholar 

  • Di Pierro, F., Orsi, R., & Settembre, R. (2015). Role of betaine in improving the antidepressant effect of S-adenosyl-methionine in patients with mild-to-moderate depression. Journal of Multidisciplinary Healthcare, 8(1), 39–45.

    Google Scholar 

  • Ding, H. R., Hong, L. Z., Yang, Z. Q., Wang, M. W., Wang, K., & Zhu, X. M. (2008). Progress of study on halophyte Suaeda salsa. Jiangxi Nongye Daxue Xuebao, 20, 35–37. (in Chinese).

    CAS  Google Scholar 

  • Dueñas, M., González-Manzano, S., González-Paramás, A., & Santos-Buelga, C. (2010). Antioxidant evaluation of O-methylated metabolites of catechin, epicatechin and quercetin. Journal of Pharmaceutical and Biomedical Analysis, 51, 443–449.

    Google Scholar 

  • Fiehn, O. (2002). Metabolomics—The link between genotypes and phenotypes. Plant Molecular Biology, 48, 155–171.

    CAS  Google Scholar 

  • Gao, Y., Sun, Q., Liu, D., Ma, B., Zhao, H., Fang, Z., et al. (2016). A sensitive LC–MS/MS method to quantify methylergonovine in human plasma and its application to a pharmacokinetic study. Journal of Chromatography B-analytical Technologies in the Biomedical and Life Sciences, 1011, 62–68.

    CAS  Google Scholar 

  • Geng, M., Wang, J. H., Chen, H., Yang, X. B., & Huang, Z. M. (2009). Effects of hyperin on the cccDNA of duck hepatitis B virus and its immunological regulation. Acta Pharmaceutica Sinaca, 44, 1440–1444.

    CAS  Google Scholar 

  • Gong, Q., Li, P., Ma, S., Indu Rupassara, S., & Bohnert, H. J. (2005). Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant Journal, 44, 826–839.

    CAS  Google Scholar 

  • Ha, B. J., Lee, S. H., Kim, H. J., & Lee, J. (2006). The role of Salicornia herbacea in ovariectomy-induced oxidative stress. Biological and Pharmaceutical Bulletin, 29, 1305–1309.

    CAS  Google Scholar 

  • Hall, R. D. (2006). Plant metabolomics: From holistic hope, to hype, to hot topic. New Phytologist, 169, 453–468.

    CAS  Google Scholar 

  • Hall, R., Beale, M., Fiehn, O., Hardy, N., Sumner, L., & Bino, R. (2002). Plant metabolomics: The missing link in functional genomics strategies. Plant Cell, 14, 1437–1440.

    CAS  Google Scholar 

  • He, Q., Altieri, A. H., & Cui, B. S. (2015). Herbivory drives zonation of stress-tolerant marsh plant. Ecology, 96(5), 1318–1328.

    Google Scholar 

  • Hertog, M. G. L., Peter, C. H. H., & Martijn, B. K. (1992). Content of potentially anticarcinogenic flavonoids of 28 vegetables and 9 fruits commonly used in the Netherlands. Journal of Agricultural and Food Chemistry, 40, 2379–2383.

    CAS  Google Scholar 

  • Hua, C., Jiang, H. T., Zhou, F., Ding, C. X., Zhao, M. D., & Wang, R. L. (2014). Antioxidant activity of halophyte Salicornia europaea L. Jiangsu Agricultural Sciences, 42(10), 295–297. (Chinese).

    Google Scholar 

  • Jorge, T. F., Rodrigues, J. A., Caldana, C., Schmidt, R., Van Dongen, J. T., Thomas-Oates, J., et al. (2016). Mass spectrometry-based plant metabolomics: Metabolite responses to abiotic stress(Review). Mass Spectrometry Reviews, 47(9), 620–649.

    Google Scholar 

  • Joshi, V., Joung, J. Q., Fei, Z. J., & Jander, G. (2010). Interdependence of threonine, methionine and isoleucine metabolism in plants: Accumulation and transcriptional regulation under abiotic stress. Amino Acids, 39, 933–947.

    CAS  Google Scholar 

  • Kesh, S. B., Sikder, K., Manna, K., Das, D. K., Khan, A., Das, N., et al. (2013). Promising role of ferulic acid, atorvastatin and their combination in ameliorating high fat diet-induced stress in mice. Life Science, 92, 938–949.

    CAS  Google Scholar 

  • Kim, B. H., Choi, J. S., Yi, E. H., Lee, J. K., Won, C., Ye, S. K., et al. (2013). Relative antioxidant activities of quercetin and its structurally related substances and their effects on NF-κB/CRE/AP-1 signaling in murine macrophages. Molecules and Cells, 35, 410–420.

    CAS  Google Scholar 

  • Kore, K. J., Bramhakule, P. P., Rachhadiya, R. M., & Shete, R. V. (2011). Evaluation of antiulcer activity of protocatechuic acid ethyl ester in rats. International Journal of Pharmacy & Life Sciences, 2(7), 909.

    CAS  Google Scholar 

  • Lee, K. W., Bode, A. M., & Dong, Z. (2011). Molecular targets of phytochemicals for cancer prevention. Nature Reviews Cancer, 11, 211–218.

    CAS  Google Scholar 

  • Lee, S. J., Jeong, E. M., Ki, A. Y., Oh, K. S., Kwon, J., Jeong, J. H., et al. (2016). Oxidative defense metabolites induced by salinity stress in roots of Salicornia herbacea. Journal of Plant Physiology, 206, 133–142.

    CAS  Google Scholar 

  • Lee, K., Lee, J. S., Jang, H. J., Kim, S. M., Chang, M. S., Park, S. H., et al. (2012a). Chlorogenic acid ameliorates brain damage and edema by inhibiting matrix metalloproteinase-2 and 9 in a rat model of focal cerebral ischemia. European Journal of Pharmacology, 689, 85–95.

    Google Scholar 

  • Lee, Y. S., Lee, S., Lee, H. S., Kim, B. K., Ohuchi, K., & Shin, K. H. (2005). Inhibitory effects of isorhamnetin-3-O-beta-D-glucoside from Salicornia herbacea on rat lens aldose reductase and sorbitol accumulation in streptozotocin-induced diabetic rat tissues. Biological & Pharmaceutical Bulletin, 28(8), 916–918.

    CAS  Google Scholar 

  • Lee, D. Y., Shrestha, S., Seo, W. D., Lee, M. H., Jeong, T. S., Cho, J. H., et al. (2012b). Structural and quantitative analysis of antioxidant and low-density lipoprotein-antioxidant flavonoids from the grains of sugary rice. Journal of Medicinal Food, 15, 399–405.

    CAS  Google Scholar 

  • Li, C. M., Jiang, W. L., Zhu, H. B., & Hou, J. (2012a). Antifibrotic effects of protocatechuic aldehyde on experimental liver fibrosis. Pharmaceutical Biology, 50(4), 413–419.

    CAS  Google Scholar 

  • Li, Z., & Vance, D. E. (2008). Phosphatidylcholine and choline homeostasis. Journal of Lipid Research, 49, 1187–1194.

    CAS  Google Scholar 

  • Li, F. R., Yu, F. X., Yao, S. T., Si, Y. H., Zhang, W., & Gao, L. L. (2012b). Hyperin extracted from manchurian rhododendron leaf induces apoptosis in human endometrial cancer cells through a mitochondrial pathway. Asian Pacific Journal of Cancer Prevention, 13, 3653–3656.

    Google Scholar 

  • Li, Y., Zhang, Y. Z., Guo, L., Wang, Y., & Wang, X. H. (2015). Study on extraction and antioxidant activity of flavonoids from heteroptera saline seepweed. Food Research and Development, 36, 38–41. (Chinese).

    CAS  Google Scholar 

  • Lopez-Lazaro, M. (2014). Distribution and biological activities of the flavonoid luteolin. Mini-Reviews in Medicinal Chemistry, 9(1), 31–59.

    Google Scholar 

  • Matsuda, F., Okazaki, Y., Oikawa, A., Kusano, M., Nakabayashi, R., Kikuchi, J., et al. (2012). Dissection of genotype-phenotype associations in rice grains using metabolome quantitative trait loci analysis. The Plant Journal, 70, 624–636.

    CAS  Google Scholar 

  • Miyagi, Y., Om, A. S., Chee, K. M., & Bennink, M. R. (2000). Inhibition of azoxymethane-induced colon cancer by orange juice. Nutrition and Cancer, 36, 224–229.

    CAS  Google Scholar 

  • Nabavi, S. F., Russo, G. L., Daglia, M., & Nabavi, S. M. (2015). Role of quercetin as an alternative for obesity treatment: You are what you eat! Food Chemistry, 179, 305–310.

    CAS  Google Scholar 

  • Nićiforović, N., & Abramovič, H. (2014). Sinapic acid and its derivatives: Natural sources and bioactivity. Comprehensive Reviews in Food Science and Food Safety, 13, 34–51.

    Google Scholar 

  • Niño-Maldonado, A. I., Caballero-García, G., Mercado-Bochero, W., Rico-Villademoros, F., & Calandre, E. P. (2009). Efficacy and tolerability of intravenous methylergonovine in migraine female patients attending the emergency department: a pilot open-label study. Head & Face Medicine, 5, 21.

    Google Scholar 

  • Olomola, T. O., Mosebi, S., Klein, R., Traut-Johnstone, T., Coates, J., Hewer, R., et al. (2014). Novel furocoumarins as potential HIV-1 integrase inhibitors. Bioorganic Chemistry, 57, 1–4.

    CAS  Google Scholar 

  • Orhan, I. E., Daglia, M., Nabavi, S. F., Loizzo, M. R., Sobarzo-Snchez, E., & Nabavi, S. M. (2015). Flavonoids and dementia: an update. Current Medicinal Chemistry, 22, 1004–1015.

    CAS  Google Scholar 

  • Patel, K. S., Patel, J. C., Dholariya, H. R., Patel, V. K., & Patel, K. D. (2012). Synthesis of Cu (II), Ni (II), Co (II), and Mn (II) complexes with ciprofloxacin and their evaluation of antimicrobial, antioxidant and anti-tubercular activity. Open Journal of Metal, 2, 49–59.

    CAS  Google Scholar 

  • Phillips, P. A., Sangwan, V., Borja-Cacho, D., Dudeja, V., Vickers, S. M., & Saluja, A. K. (2011). Myricetin induces pancreatic cancer cell death via the induction of apoptosis and inhibition of the phosphatidylinositol 3-kinase (PI3K) signaling pathway. Cancer Letters, 308, 181–188.

    CAS  Google Scholar 

  • Piazzon, A., Vrhovsek, U., Masuero, D., Mattivi, F., Mandoj, F., & Nardini, M. (2012). Antioxidant activity of phenolic acids and their metabolites: synthesis and antioxidant properties of the sulfate derivatives of ferulic and caffeic acids and of the acyl glucuronide of ferulic acid. Journal of Agricultural and Food Chemistry, 60, 12312–12323.

    CAS  Google Scholar 

  • Prasad, A. N., Rupar, C. A., & Prasad, C. (2011). Methylenetetrahydrofolate reductase (MTHFR) deficiency and infantile epilepsy. Brain and Development, 33(9), 758–769.

    Google Scholar 

  • Pu, W., Lin, Y., Zhang, J., Wang, F., Wang, C., & Zhang, G. (2014). 3-Arylcoumarins: Synthesis and potent anti-inflammatory activity. Bioorganic & Medicinal Chemistry Letters, 24, 5432–5434.

    CAS  Google Scholar 

  • Rattanachaikunsopon, P., & Phumkhachorn, P. (2010). Contents and antibacterial activity of flavonoids extracted from leaves of Psidium guajava. Journal of Midicinal Plants Research, 4, 393–396.

    CAS  Google Scholar 

  • Rhee, M. H., Park, H. J., & Cho, J. Y. (2009). Salicornia herbacea: Botanical, chemical and harmacological review of halophyte marsh plant. Journal of Medicinal Plants Research, 3(8), 548–555.

    CAS  Google Scholar 

  • Sahoo, J., Mekap, S. K., & Kumar, P. S. (2015). Synthesis, Spectral characterization of some new 3-heteroaryl azo 4-hydroxy coumarin derivatives and their antimicrobial evaluation. Journal of Taibah University for Science, 9, 187–195.

    Google Scholar 

  • Sanchez, D. H., Lippold, F., Redestig, H., Hannah, M. A., Erban, A., Krämer, U., et al. (2008). Integrative functional genomics of salt acclimatization in the model legume Lotus japonicus. Plant Journal, 53, 973–987.

    CAS  Google Scholar 

  • Sanchez, D. H., Pieckenstain, F. L., Escaray, F., Erban, A., Kraemer, U., Udvardi, M. K., et al. (2011a). Comparative ionomics and metabolomics in extremophile and glycophytic Lotus species under salt stress challenge the metabolic pre-adaptation hypothesis. Plant Cell Environment, 34, 605–617.

    CAS  Google Scholar 

  • Sanchez, D. H., Pieckenstain, F. L., Szymanski, J., Erban, A., Bromke, M., Hannah, M. A., et al. (2011b). Comparative functional genomics of salt stress in related model and cultivated plants identifies and overcomes limitations to translational genomics. PLoS ONE, 6, e17094.

    CAS  Google Scholar 

  • Scazzocchio, B., Vari, R., Filesi, C., D’Archivio, M., Santangelo, C., Giovannini, C., et al. (2011). Cyanidin-3-O-beta-Glucoside and protocatechuic acid exert insulin-like effects by upregulating PPARgamma activity in human omental adipocytes. Diabetes, 60(9), 2234–2244.

    CAS  Google Scholar 

  • Seema, P. (2016). Salicornia: evaluating the halophytic extremophile as a food and a pharmaceutical candidate. 3 BIOTECH, 6, 104.

    Google Scholar 

  • Shao, H. M., Sun, S. Q., & Xu, H. J. (1996). The determination of seven water-soluble vitamins and eighteen amino acids in Suaeda salsa (L.) Pall. juice by high performance liquid chromatography. Se Pu, 14, 235. (in Chinese).

    CAS  Google Scholar 

  • Shi, G. F., An, L. J., Jiang, B., Guan, S., & Bao, Y. M. (2006). Alpinia protocatechuic acid protects against oxidative damage in vitro and reduces oxidative stress in vivo. Neuroscience Letters, 403(3), 206–210.

    CAS  Google Scholar 

  • So, F. V., Guthrie, N., Chambers, A. F., Moussa, M., & Carroll, K. K. (1996). Inhibition of human breast cancer cell proliferation and delay of mammary tumorigenesis by flavonoids and citrus juices. Nutrition and Cancer, 262, 167–181.

    Google Scholar 

  • Srikrishna, D., Godugu, C., & Dubey, P. K. (2018). A review on pharmacological properties of coumarins. Mini Reviews in Medicinal Chemistry., 18, 113–141.

    CAS  Google Scholar 

  • Tanaka, T., Tanaka, T., & Tanaka, M. (2011). Potential cancer chemopreventive activity of protocatechuic acid. Journal of Experimental and Clinical Medicine, 3(1), 27–33.

    CAS  Google Scholar 

  • Theoharides, T. C., Stewart, J. M., Hatziagelaki, E., & Kolaitis, G. (2015). Brain fog, inflammation and obesity: Key aspects of neuropsychiatric disorders improved by luteolin. Frontiers in Neuroscience, 9, 225.

    Google Scholar 

  • Trombino, S., Cassano, R., Ferrarelli, T., Barone, E., Picci, N., & Mancuso, C. (2013). Trans-ferulic acid-based solid lipid nanoparticles and their antioxidant effect in rat brain microsomes. Colloids and Surfaces B-Biointerfaces, 109, 273–279.

    CAS  Google Scholar 

  • Varatharajalu, R., Garige, M., Leckey, L. C., Arellanes-Robledo, J., Reyes-Gordillo, K., Shah, R., et al. (2014). Adverse signaling of scavenger receptor class B1 and PGCls in alcoholic hepatosteatosis and steatohepatitis and protection by betaine in rat. American Journal of Pathology, 184(7), 2036–2044.

    Google Scholar 

  • Verma, N., Amresh, G., Sahu, P. K., Mishra, N., Singh, A. P., & Rao, Ch V. (2012). Antihyperglycemic activity, antihyperlipedemic activity, haematological effects and histopathological analysis of Sapindus mukorossi gaerten fruits in streptozotocin induced diabetic rats. Asian Pacific Journal of Tropical Medicine, 5, 518–522.

    Google Scholar 

  • Wang, Z. J. (2009). Studies on separation purification and antioxidant activity of a water-soluble polysaccharide SPA from Suaeda spp. Journal of Liaoning University of TCM, 11, 168–169. (in Chinese).

    CAS  Google Scholar 

  • Wang, L. (2014). Study on functional constituents of Suaeda. Masterthesis. Dalian Polytechnic University, Liaoning, China.

  • Wang, P., Bai, H. W., & Zhu, B. T. (2012). Structural basis for certain naturally occurring bioflavonoids to function as reducing cosubstrates of cyclooxygenase I and II. PLoS ONE, 5, e12316.

    Google Scholar 

  • Wang, X. Y., Feng, X., Wang, M., Chen, Y., Dong, Y. F., Zhao, Y. Y., et al. (2011). Studies on the Chemical Constituents of Salicornia europaea. Journal of Chinese Medicinal Materials, 34(1), 67–69. (in Chinese).

    Google Scholar 

  • Wang, C. Q., Zhao, J. Q., Chen, M., & Wang, B. S. (2006). Identification of betacyanin and effects of environmental factors on its accumulation in halophyte Suaeda salsa. Journal of Plant Physiology and Molecular Biology, 32, 195–201. (in Chinese).

    CAS  Google Scholar 

  • Widodo, Patterson, J. H., Newbigin, E., Tester, M., Bacic, A., & Roessner, U. (2009). Metabolic responses to salt stress of barley (Hordeum vulgare L) cultivars, Sahara and Clipper, which differ in salinity tolerance. Journal of Experimental Botany, 60(14), 4089–4103.

    CAS  Google Scholar 

  • Wu, D., Cai, S., Chen, M., Ye, L., Chen, Z., Zhang, H., et al. (2013). Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS ONE, 8, e55431.

    CAS  Google Scholar 

  • Xi, J. B., Zhang, F. S., & Mao, D. R. (2003). The utilization of halophytes for traditional medicine in Xinjiang. Review of China Agricultural Science and Technology, 5(1), 43–48. (in Chinese).

    Google Scholar 

  • Xu, H. J. (2006). Determination of 9 trace elements in Suaeda salsa. Chinese Journal of Pest Control, 22, 459. (in Chinese).

    Google Scholar 

  • Xu, H. J. (2008). Determination of 18 amino acids in Suaeda salsa. Chinese Journal of Pest Control, 24, 161. (in Chinese).

    Google Scholar 

  • Yamada, J., & Tomita, Y. (1996). Antimutagenic activity of caffeic acid and related compounds. Bioscience, Biotechnology, and Biochemistry, 60, 328–329.

    CAS  Google Scholar 

  • Yang, J. H., Kim, S. C., & Shin, B. Y. (2013a). O-Methylated flavonol isorhamnetin prevents acute inflammation through blocking of NF-kB activation. Food and Chemical Toxicology, 59, 362–372.

    CAS  Google Scholar 

  • Yang, M., Tanaka, T., Hirose, Y., Deguchi, T., Mori, H., & Kawada, Y. (1997). Chemopreventive effects of diosmin and hesperidin on N-butyl-N-(4 hydroxybutyl) nitrosamine-induced urinary-bladder carcinogenesis in male ICR mice. International Journal of Cancer, 73, 719–724.

    CAS  Google Scholar 

  • Yang, Z. G., Wen, X. F., Li, Y. H., Matsuzaki, K., & Kitanaka, S. (2013b). Inhibitory effects of the constituents of Hippophae rhamnoides on 3T3-L1 cell differentiation and nitric oxide production in RAW264.7 cells. Chemcial and Pharmaceutical Bulletin, 61, 279–285.

    CAS  Google Scholar 

  • Yang, X., Zhang, X., Yuan, Z., Li, X., Zhang, L., & Fan, L. (2009). Simultaneous determination of myricitrin, hyperin, quercitroside, and quercetin in Folium Rhododendri Micranthi by RP-HPLC. Journal of Chromatographic Science, 47, 714–717.

    CAS  Google Scholar 

  • Zhang, J. Y., Li, M. H., Xu, L. M., & Wang, Z. J. (2008). Effect of Suaeda seed oil on blood-fat and immunologic function of mouse. Occupational Health, 24, 1529–1530. (In Chinese).

    CAS  Google Scholar 

  • Zhang, C. X., Pan, M. X., Li, B., Wang, L., Mo, X. F., Chen, Y. M., et al. (2014). Choline and betaine intake is inversely associated with breast cancer risk: a two-stage case-control study in China. Cancer Science, 104(2), 250–258.

    Google Scholar 

  • Zhao, M. D. (2012). Study on nutritional components, antioxidant activity and antimicrobial effect of sea vegetable Salicornia europaea L. Master thesis, Nanjing Normal University.

  • Zheng, P., Liu, J., Mai, S., Yuan, Y., Wang, Y., & Dai, G. (2014). Regulation of signal transducer and activator of transcription 3 and apoptotic pathways by betaine attenuates isoproterenol-induced acute myocardial injury in rats. Human and Experimental Toxicology, 1, 1–10.

    Google Scholar 

  • Zhou, Z., Zhang, Y., Ding, X. R., Chen, S. H., Yang, J., Wang, X. J., et al. (2007). Protocatechuic aldehyde inhibits hepatitis B virus replication both in vitro and in vivo. Antiviral Research, 74(1), 59–64.

    CAS  Google Scholar 

Download references

Acknowledgements

This study was financially supported by the National Key R&D Program of China (No. 2017YFC0505906). We thank Wuhan Metware Biotechnology Co., Ltd. for widely targeted metabolomics.

Author information

Authors and Affiliations

Authors

Contributions

JB managed the project; XW designed the experiments and analyzed the raw data; SY, XW, GZ, WW, DW collected the plant materials; XW and JB wrote the manuscript.

Corresponding author

Correspondence to Junhong Bai.

Ethics declarations

Conflict of interest

We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, and there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Bai, J., Wang, W. et al. A comparative metabolomics analysis of the halophyte Suaeda salsa and Salicornia europaea. Environ Geochem Health 43, 1109–1122 (2021). https://doi.org/10.1007/s10653-020-00569-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-020-00569-4

Keywords

Navigation