Eff ect of polysaccharide from Enteromorpha prolifera on maize seedlings under NaCl stress

  • Song Liu
  • Bing Li
  • Xiaolin Chen
  • Yukun Qin
  • Pengcheng LiEmail author


In this study, a polysaccharide from Enteromorpha prolifera (EP) was extracted and its eff ect on maize seedlings under NaCl stress was investigated. Firstly, the components and structure of the EP were determined. We found that EP is a sulfated polysaccharide of high-molecular weight (Mw, 1 840 KDa) heteropolysaccharides and the main monosaccharide is rhamnose. The polysaccharide was applied to explore its eff ect on the growth of maize seedlings and its defense response under a salt stress. The results show that EP could promote the growth of maize seedlings under the salt stress. In addition, EP was shown able to signifi cantly regulate membrane permeability and adjustment of osmotic substances such as soluble protein, soluble sugar, and proline, antioxidant enzymes containing superoxide dismutase, catalase, peroxidase, and ascorbate peroxidase. Therefore, EP is an eff ective salt-resistant substance for the growth of maize seedlings under NaCl stress.

Key word

polysaccharides Enteromorpha prolifera maize seedling NaCl stress 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abdel–Basset R. 1998. Calcium channels and membrane disorders induced by drought stress in Vicia faba plants supplemented with calcium. Acta Physiol. Plant., 20 (2): 149–153.Google Scholar
  2. Bates L S. 1973. Rapid determination of free proline for waterstress studies. Plant Soil, 39 (1): 205–207.Google Scholar
  3. Battacharyya D, Babgohari M Z, Rathor P, Prithiviraj B. 2015. Seaweed extracts as biostimulants in horticulture. Sci. Hortic., 196: 39–48.Google Scholar
  4. Beauchamp C, Fridovich I. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem., 44 (1): 276–287.Google Scholar
  5. Bi F, Iqbal S, Arman M, Ali A, Hassan M U. 2011. Carrageenan as an elicitor of induced secondary metabolites and its effects on various growth characters of chickpea and maize plants. J. Saudi Chem. Soc., 15 (3): 269–273.Google Scholar
  6. Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal. Biochem., 72 (1–2): 248–254.Google Scholar
  7. Cho M, Yang C, Kim Y S, You S G. 2010. Molecular characterization and biological activities of watersoluble sulfated polysaccharides from Enteromorpha prolifera. Food Sci. Biotechnol., 19 (2): 525–533.Google Scholar
  8. DuBois M, Gilles K A, Hamilton J K, Rebers P A, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem., 28 (3): 350–356.Google Scholar
  9. Dzung N A, Khanh V T P, Dzung T T. 2011. Research on impact of chitosan oligomers on biophysical characteristics, growth, development and drought resistance of coffee. Carbohyd r. Polym., 84 (2): 751–755.Google Scholar
  10. Farhangi–Abriz S, Torabian S. 2017. Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress. Ecotox. Environ. Saf., 137: 64–70.Google Scholar
  11. Foyer C H, Noctor G. 2005. Oxidant and antioxidant signalling in plants: a re–evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ., 28 (8): 1 056–1 071.Google Scholar
  12. Glosek–Sobieraj M, Cwalina–Ambroziak B, Hamouz K. 2018. The effect of growth regulators and a biostimulator on the health status, yield and yield components of potatoes (Solanum tuber o sum L.). Gesunde Pflanz., 70 (1): 1–11.Google Scholar
  13. Gunes A, Inal A, Alpaslan M, Eraslan F, Bagci E G, Cicek N. 2007. Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J. Plant Physiol., 164 (6): 728–736.Google Scholar
  14. Heath R L, Packer L. 1968. Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch. Biochem. Biophys., 125 (1): 189–198.Google Scholar
  15. Jaulneau V, Lafitte C, Jacquet C, Fournier S, Salamagne S, Briand X, Esquerré–Tugayé M T, Dumas B. 2010. Ulvan, a sulfated polysaccharide from green algae, activates plant immunity through the jasmonic acid signaling pathway. J. Biomed. Biotechnol., 2010: 525 291, Scholar
  16. Jiao L L, Jiang P, Zhang L P, Wu M J. 2010. Antitumor and immunomodulating activity of polysaccharides from Enteromorpha intestinalis. Biotechnol. Bioproc. E ng., 15: 421–428.Google Scholar
  17. Kawai Y, Seno N, Anno K. 1969. A modified method for chondrosulfatase assay. Anal. Biochem., 32 (2): 314–321.Google Scholar
  18. Khatkar D, Kuhad M S. 2000. Short–term salinity induced changes in two wheat cultivars at different growth stages. Biol. Plant., 43 (4): 629–632.Google Scholar
  19. Klarzynski O, Descamps V, Plesse B, Yvin J C, Kloareg B, Fritig B. 2003. Sulfated fucan oligosaccharides elicit defense responses in tobacco and local and systemic resistance against tobacco mosaic virus. Mol. Plant Microbe In t., 16 (2): 115–122.Google Scholar
  20. Li B, Liu S, Xing R E, Li K C, Li R F, Qin Y K, Wang X Q, Wei Z H, Li P C. 2013. Degradation of sulfated polysaccharides from Enteromorpha prolifera and their antioxidant activities. Carbohyd r. Polym., 92 (2): 1 991–1 996.Google Scholar
  21. Liu L P, Long X H, Shao H B, Liu Z P, Tao Y, Zhou Q S, Zong J Q. 2015. Ameliorants improve saline–alkaline soils on a large scale in northern Jiangsu Province, China. Ecol. Eng., 81: 328–334.Google Scholar
  22. Lü H T, Gao Y J, Shan H, Lin Y T. 2014. Preparation and antibacterial activity studies of degraded polysaccharide selenide from Enteromorpha prolifera. Carbohyd r. Polym., 107: 98–102.Google Scholar
  23. Lu Z Q, Liu D L, Liu S K. 2007. Two rice cytosolic ascorbate peroxidases differentially improve salt tolerance in transgenic Arabidopsis. Plant Cell Rep., 26 (10): 1 909–1 917.Google Scholar
  24. Luan L Q, Nagasawa N, Ha V T T, Hien N Q, Nakanishi T M. 2009. Enhancement of plant growth stimulation activity of irradiated alginate by fractionation. Radiat. Phys. Chem., 78 (9): 796–799.Google Scholar
  25. Mejía–Espejel L, Robledo–Paz A, Lozoya–Gloria E, Peña–Valdivia C B, Carrillo–Salazar J A. 2018. Elicitors on steviosides production in Stevia rebaudiana Bertoni calli. Sci. Hortic., 242: 95–102.Google Scholar
  26. Mekhedov S L, Kende H. 1996. Submergence enhances expression of a gene encoding 1–aminocyclopropane–1–carboxylate oxidase in deepwater rice. Plant Cell Physiol., 37 (4): 531–537.Google Scholar
  27. Meloni D A, Oliva M A, Martinez C A, Cambraia J. 2003. Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ. Exp. Bot., 49 (1): 69–76.Google Scholar
  28. Michalak I, Dmytryk A, Śmieszek A, Marycz K. 2017. Chemical characterization of Enteromorpha prolifera extract obtained by enzyme–assisted extraction and its influence on the metabolic activity of Caco–2. Int. J. Mol. Sci., 18 (3): 479.Google Scholar
  29. Michalak I, Górka B, Wieczorek P P, Rój E, Lipok J, Łęska B, Messyasz B, Wilk R, Schroeder G, Dobrzyńska–Inger A, Chojnacka K. 2016. Supercritical fluid extraction of algae enhances levels of biologically active compounds promoting plant growth. Eur. J. Phycol., 51 (3): 243–252.Google Scholar
  30. Michalak I, Tuhy Ł, Chojnacka K. 2015. Seaweed extract by microwave assisted extraction as plant growth biostimulant. Open Chem., 13 (1): 1 183–1 195.Google Scholar
  31. Mittal S, Kumari N, Sharma V. 2012. Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol. Biochem., 54: 17–26.Google Scholar
  32. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci., 7 (9): 405–410.Google Scholar
  33. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol., 59: 651–681.Google Scholar
  34. Pacholczak A, Nowakowska K, Mika N, Borkowska M. 2016. The effect of the biostimulator Goteo on the rooting of ninebark stem cuttings. Folia Hort ic., 28 (2): 109–116.Google Scholar
  35. Rodriguez H G, Roberts J K M, Jordan W R, Drew M C. 1997. Growth, water relations, and accumulation of organic and inorganic solutes in roots of maize seedlings during salt stress. Plant Physiol., 113(3): 881–893.Google Scholar
  36. Ruiz–Lozano J M, Porcel R, Azcón C, Aroca R. 2012. Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J. Exp. Bot., 63 (11): 4 033–4 044.Google Scholar
  37. Sánchez F J, Manzanares M, De Andres E F, Tenorio J L, Ayerbe L. 1998. Turgor maintenance, osmotic adjustment and soluble sugar and proline accumulation in 49 pea cultivars in response to water stress. Field Crop s Res., 59 (3): 225–235.Google Scholar
  38. Seckin B, Sekmen A H, Türkan I. 2009. An enhancing effect of exogenous mannitol on the antioxidant enzyme activities in roots of wheat under salt stress. J. Plant Growth Regul., 28 (1): 12–20.Google Scholar
  39. Sharp J K, Valent B, Albersheim P. 1984. Purification and partial characterization of a β–glucan fragment that elicits phytoalexin accumulation in soybean. J. Biol. Chem., 259 (18): 11 312–11 320.Google Scholar
  40. Song L, Chen X L, Liu X D, Zhang F B, Hu L F, Yue Y, Li K C, Li P C. 2016. Characterization and comparison of the structural features, immune–modulatory and anti–avian influenza virus activities conferred by three algal sulfated polysaccharides. Mar. Drugs, 14 (1): 4.Google Scholar
  41. Sudhakar C, Lakshmi A, Giridarakumar S. 2001. Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morus alba L.) under NaCl salinity. Plant Sci., 161 (3): 613–619.Google Scholar
  42. Szabados L, Savouré A. 2010. Proline: a multifunctional amino acid. Trends Plant Sc i., 15 (2): 89–97.Google Scholar
  43. Volkmar K M, Hu Y, Steppuhn H. 1998. Physiological responses of plants to salinity: a review. Can. J. Plant Sci., 78 (1): 19–27.Google Scholar
  44. Wang Z L, Pote J, Huang B R. 2003. Responses of cytokinins, antioxidant enzymes, and lipid peroxidation in shoots of creeping bentgrass to high root–zone temperatures. J. Am. Soc.. Hortic. Sci., 128: 648–655.Google Scholar
  45. Xu D L, Huang X C, Ou C R, Xue C H, Yang W G, Wang H H. 2005. In vitro study on polysaccharides in Enteromorpha with non–specific immunity. Food Sci., 26: 232–235.Google Scholar
  46. Xu J, Xu L L, Zhou Q W, Hao S X, Zhou T, Xie H J. 2015. Isolation, purification, and antioxidant activities of degraded polysaccharides from Enteromorpha prolifera. Int. J. Biol. Macromol., 81: 1 026–1 030.Google Scholar
  47. Yang X L, Guo J Y. 2010. Effect of sodium alginate on H. annuus L. seedling to salt–tolerance. Northern Hortic., (23): 37–39. (in Chinese with English abstract)Google Scholar
  48. Yang X L, Guo Y D. 2011. Effect of sodium alginate on Raphanus sativus L. seedlings in adaptation to salttolerance. Chin. Veget., 1 (2): 81–84. (in Chinese with English abstract)Google Scholar
  49. Zhang J J, Zhang Q B, Wang J, Shi X L, Zhang Z S. 2009. Analysis of the monosaccharide composition of fucoidan by precolumn derivation HPLC. Chin. J. Oceanol. Limn ol., 27 (3): 578–582.Google Scholar
  50. Zhang X Q, Li K C, Liu S, Zou P, Xing R E, Yu H H, Chen X L, Qin Y K, Li P C. 2017a. Relationship between the degree of polymerization of chitooligomers and their activity affecting the growth of wheat seedlings under salt stress. J. Agric. Food Chem., 65 (2): 501–509.Google Scholar
  51. Zhang X Q, Li K C, Xing R E, Liu S, Chen X L, Yang H Y, Li P C. 2017b. miRNA and mRNA expression profiles reveal insight into chitosan–mediated regulation of plant growth. J. Agr ic. Food Chem., 66 (15): 3 810–3 822.Google Scholar
  52. Zhou H P, Jiang X T, Wang S R, Chen Q H. 1995. Effect of polysaccharide from Enteromorpha prolifera on lipemia, SOD activity and LPO content. Chin. J. Biochem. Mol. Biol., 11 (2): 161–165. (in Chinese with English abstract)Google Scholar
  53. Zhu J K. 2000. Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol., 124 (3): 941–948.Google Scholar
  54. Zou P, Lu X L, Jing C L, Yuan Y, Lu Y, Zhang C S, Meng L, Zhao H T, Li Y Q. 2018. Low–molecular–weight polysaccharides from Pyropia yezoensis enhance tolerance of wheat seedlings(Triticum aestivum L.) to salt stress. Front. Plant Sci., 9: 427, Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Song Liu
    • 1
    • 2
    • 3
  • Bing Li
    • 4
  • Xiaolin Chen
    • 1
    • 2
    • 3
  • Yukun Qin
    • 1
    • 2
    • 3
  • Pengcheng Li
    • 1
    • 2
    • 3
    Email author
  1. 1.CAS Key Laboratory of Experimental Marine Biology, Institute of OceanologyChinese Academy of SciencesQingdaoChina
  2. 2.Laboratory for Marine Drugs and BioproductsQingdao National Laboratory for Marine Science and TechnologyQingdaoChina
  3. 3.Center for Ocean Mega-ScienceChinese Academy of SciencesQingdaoChina
  4. 4.Marine Science and Engineering CollegeQingdao Agriculture UniversityQingdaoChina

Personalised recommendations