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Effects of alginate oligosaccharides with different molecular weights and guluronic to mannuronic acid ratios on glyceollin induction and accumulation in soybeans

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Abstract

Alginate oligosaccharides (AOs) are linear oligosaccharides with alternating sequences of mannuronic acid (M) and guluronic acid (G) residues. AOs can be used as a safe elicitor to induce glyceollins, which have many human health benefits, in soybean seeds. In this research, four AO fractions with different chemical structures and molecular weights were separated, purified, and then characterized by NMR spectroscopy and ESI–MS. With a 4,5-unsaturated hexuronic acid residue (△) at the non-reducing terminus, the structures of these four AO fractions were △G, △MG, △GMG and △MGGG, which exhibited glyceollin-inducing activities of 1.2339, 0.3472, 0.6494 and 1.0611 (mg/g dry weight) in soybean seeds, respectively. The results demonstrated that a larger molecular weight or a higher G/M ratio might correlate with a higher glyceollin-inducing activity. Moreover, the alginate disaccharide △G could be introduced as relatively safe and efficient elicitor of high glyceollin content in soybeans.

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Abbreviations

AO:

Alginate oligosaccharide

G:

Guluronic acid

M:

Mannuronic acid

HPLC:

High-performance liquid chromatography

NMR:

Nuclear magnetic resonance

ESI–MS:

Electrospray ionization–mass spectrometry

SPE:

Solid phase extraction

TFA:

Trifluoroacetic acid

△:

O-(4-deoxy-α-l-erythro-hex-4-enopyranosyluronic acid)-(1→

-G-:

→4)-O-(α-l-gulopyranosyluronic acid)-(1→

-G:

→4)-O-β-l-gulopyranuronic acid

-M-:

→4)-O-(β-d-mannopyranuronic acid)-(1→

References

  • Akimoto C, Aoyagi H, Dicosmo F, Tanaka H (2000) Synergistic effect of active oxygen species and alginate on chitinase production by Wasabia japonica cells and its application. J Biosci Bioeng 89:131–137

    Article  CAS  Google Scholar 

  • Angelova Z, Georgiev S, Roos W (2006) Elicitation of plants. Biotechnol Biotechnol Equip 20:72–83

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Bhattacharyya MK, Ward EWB (1986) Resistance, susceptibility and accumulation of glyceollins I–III in soybean organs inoculated with Phytophthora megasperma f. sp. glycinea. Physiol Mol Plant Pathol 29:227–237

    Article  CAS  Google Scholar 

  • Boue SM, Cleveland TE, Carter-Wientjes C, Shih BY, Bhatnagar D, McLachlan JM, Burow ME (2009) Phytoalexin-enriched functional foods. J Agric Food Chem 57:2614–2622

    Article  CAS  Google Scholar 

  • Boué SM, Carter CH, Ehrlich KC, Cleveland TE (2000) Induction of the soybean phytoalexins coumestrol and glyceollin by Aspergillus. J Agric Food Chem 48:2167–2172

    Article  Google Scholar 

  • Chaki T, Kakimi H, Shibata A, Baba T (2006) Detection of alginate oligosaccharides from mollusks. Biosci Biotechnol Biochem 70:2793–2796

    Article  CAS  Google Scholar 

  • Chandía NP, Matsuhiro B, Mejías E, Moenne A (2004) Alginic acids in Lessonia vadosa: partial hydrolysis and elicitor properties of the polymannuronic acid fraction. J Appl Phycol 16:127–133

    Article  Google Scholar 

  • Eromosele O, Shi B, Liang P (2013) Induction of phytochemical glyceollins accumulation in soybean following treatment with biotic elicitor (Aspergillus oryzae). J Funct Foods 5:1039–1048

    Article  CAS  Google Scholar 

  • Fett WF, Zacharius RM (1982) Bacterially-induced glyceollin production in soybean cell suspension cultures. Plant Sci Lett 24:303–309

    Article  CAS  Google Scholar 

  • Hai D, Huang Y, Tang Y (2010) Genetic and metabolic engineering of isoflavonoid biosynthesis. Appl Microbiol Biotechnol 86:1293–1312

    Article  Google Scholar 

  • Holtan S, Zhang Q, Strand WI, Skjåk-Braek G (2006) Characterization of the hydrolysis mechanism of polyalternating alginate in weak acid and assignment of the resulting MG-oligosaccharides by NMR spectroscopy and ESI–mass spectrometry. Biomacromolecules 7:2108–2121

    Article  CAS  Google Scholar 

  • Iwasaki KI, Matsubara Y (2000) Purification of pectate oligosaccharides showing root-growth-promoting activity in lettuce using ultrafiltration and nanofiltration membranes. J Biosci Bioeng 89:495–497

    Article  CAS  Google Scholar 

  • Jenkins DJ, Mirrahimi A, Srichaikul K, Berryman CE, Wang L, Carleton A, Abdulnour S, Sievenpiper JL, Kendall CW, Kris-Etherton PM (2010) Soy protein reduces serum cholesterol by both intrinsic and food displacement mechanisms. J Nutr 140:2302–2311

    Article  Google Scholar 

  • Jia H, Shi B, Eromosele O, Liang P, Li J (2012) Effects of alginate oligosaccharides on the accumulation of glyceollins in soybean. China Agric Sci 45:1576–1586

    Google Scholar 

  • Jochum M, Bakry R, Wartusch I, Huck CW, Engelhardt H, Bonn GK (2002) Analysis of carbohydrates using different quaternized polystyrene-divinylbenzene particles and pulsed amperometric detection. Chromatographia 56:263–268

    Article  CAS  Google Scholar 

  • Kawada A, Hiura N, Shiraiwa M, Tajima S, Hiruma M, Hara K, Ishibashi A, Takahara H (1997) Stimulation of human keratinocyte growth by alginate oligosaccharides, a possible co-factor for epidermal growth factor in cell culture. FEBS Lett 408:43–46

    Article  CAS  Google Scholar 

  • Kawada A, Hiura N, Tajima S, Takahara H (1999) Alginate oligosaccharides stimulate VEGF-mediated growth and migration of human endothelial cells. Arch Dermatol Res 291:542–547

    Article  CAS  Google Scholar 

  • Küpper FC, Müller DG, Peters AF, Kloareg B, Potin P (2002) Oligoalginate recognition and oxidative burst play a key role in natural and induced resistance of sporophytes of Laminariales. J Chem Ecol 28:2057–2081

    Article  Google Scholar 

  • Landini S, Graham MY, Graham TL (2003) Lactofen induces isoflavone accumulation and glyceollin elicitation competency in soybean. Phytochemistry 62:865–874

    Article  CAS  Google Scholar 

  • Ma LJ, Zhang Y, Bu N, Wang SH (2010) Alleviation Effect of alginate-derived oligosaccharides on vicia faba root tip cells damaged by cadmium. Bull Environ Contam Toxicol 84:161–164

    Article  CAS  Google Scholar 

  • Moesta P, Grisebach H (1980) Effects of biotic and abiotic elicitors on phytoalexin metabolism in soybean. Nature 49:710–711

    Article  Google Scholar 

  • Nagasawa N, Mitomo H, Yoshii F, Kume T (2000) Radiation-induced degradation of sodium alginate. Polym Degrad Stabil 69:279–285

    Article  CAS  Google Scholar 

  • Natsume M, Kamo Y, Hirayama M, Adachi T (1994) Isolation and characterization of alginate-derived oligosaccharides with root growth-promoting activities. Carbohydr Res 258:187–197

    Article  CAS  Google Scholar 

  • Pitta Alvarez SI, Spollansky TC, Giulietti AM (2000) The influence of different biotic and abiotic elicitors on the production and profile of tropane alkaloids in hairy root cultures of Brugmansia candida. Enzyme Microb Technol 26:252–258

    Article  CAS  Google Scholar 

  • Salvo VA, Boué SM, Fonseca JP, Elliott S, Corbitt C, Collins-Burow BM, Curiel TJ, Srivastav SK, Shih BY, Carterwientjes C (2006) Antiestrogenic glyceollins suppress human breast and ovarian carcinoma tumorigenesis. Clin Cancer Res 12:7159–7164

    Article  CAS  Google Scholar 

  • Scherz H, Huck CW, Bonn GK (2005) Electrophoresis carbohydrates. encyclopedia of analytical. Science 28:433–445

    Google Scholar 

  • Schürks N, Wingender J, Flemming HC, Mayer C (2002) Monomer composition and sequence of alginates from Pseudomonas aeruginosa. Int J Biol Macromol 30:105–111

    Article  Google Scholar 

  • Stintzi A, Weber H, Reymond P, Browse J, Farmer EE (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc Natl Acad Sci USA 98:12837–12842

    Article  CAS  Google Scholar 

  • Stössel P (1984) Regulation by sulfhydryl groups of glyceollin accumulation in soybean hypocotyls. Planta 160:314–319

    Article  Google Scholar 

  • Wood CE, Boue SM, Collins-Burow BM, Rhodes LV, Register TC, Cline JM, Dewi FN, Burow ME (2012) Glyceollin-elicited soy protein consumption induces distinct transcriptional effects as compared to standard soy protein. J Agric Food Chem 60:81–86

    Article  CAS  Google Scholar 

  • Yoon EK, Jeong YT, Li X, Song-Cui PD, Kim YH, Yong DK, Chang HW, Lee SH, Hwang SL (2013) Glyceollin improves endoplasmic reticulum stress-induced insulin resistance through CaMKK-AMPK pathway in L6 myotubes. J Nutr Biochem 24:1053–1061

    Article  CAS  Google Scholar 

  • Yoshikawa M, Yoshikawa M (1978) Divers mode of action of biotic and abiotic phytoalexin elicitors. Nature 275:546–547

    Article  CAS  Google Scholar 

  • Zhang Z, Yu G, Guan H, Zhao X, Du Y, Jiang X (2004) Preparation and structure elucidation of alginate oligosaccharides degraded by alginate lyase from Vibro sp. 510. Carbohydr Res 339:1475–1481

    Article  CAS  Google Scholar 

  • Zhang Z, Yu G, Zhao X, Liu H, Guan H, Lawson AM, Chai W (2006) Sequence analysis of alginate-derived oligosaccharides by negative-ion electrospray tandem mass spectrometry. J Am Soc Mass Spectrom 17:621–630

    Article  Google Scholar 

  • Zhang Y, Liu H, Yin H, Wang W, Zhao X, Du Y (2013) Nitric oxide mediates alginate oligosaccharides-induced root development in wheat (Triticum aestivum L.). Plant Physiol Biochem 71:49–56

    Article  CAS  Google Scholar 

  • Zhang S, Tang W, Jiang L, Hou Y, Yang F, Chen W, Li X (2015) Elicitor activity of algino-oligosaccharide and its potential application in protection of rice plant (Oryza saliva L.) against Magnaporthe grisea. Biotechnol Biotechnol Equip 29:1–7

    Article  Google Scholar 

  • Zheng LY, Zhu JF (2003) Study on antimicrobial activity of chitosan with different molecular weights. Carbohyd Polym 54:527–530

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the moral and financial support received from the National Natural Science Foundation of China (No. 31171628).

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Authors and Affiliations

  1. Key Laboratory for Feed Biotechnology of the Ministry of Agriculture, Feed Research Institute, Chinese Academy of Agricultural Sciences, No. 12 Zhongguancun South Street, Beijing, 100081, People’s Republic of China

    Qing Peng, Long Gao, Ojokoh Eromosele, Yu Qiao & Bo Shi

  2. Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, 1-1-1, Yayoi, Bunkyo-ku, Tokyo, 113-8657, Japan

    Mimin Zhang

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  1. Qing Peng
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Correspondence to Bo Shi.

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Supplemental Fig. 1

1H NMR (500 MHz) spectra of (a) F1, (b) F3, (c) F5 and (d) F7. The experimental temperature was 25 °C. The water peak was 4.70 (EPS 804 kb)

Supplemental Fig. 2

13C NMR (125 MHz) spectra of (a) F1, (b) F3, (c) F5 and (d) F7. The experimental temperature was 25 °C (EPS 704 kb)

Supplemental Fig. 3

2D NMR spectra of F1 (△G) obtained at 500 MHz at 25 °C. (a) COSY, (b) HSQC, and (c) HMBC (EPS 2867 kb)

Supplemental Fig. 4

2D NMR spectra of F3 (△MG) obtained at 500 MHz at 25 °C. (a) COSY, (b) HSQC, and (c) HMBC (EPS 1645 kb)

Supplemental Fig. 5

2D NMR spectra of F5 (△GMG) obtained at 500 MHz at 25 °C. (a) COSY, (b) HSQC, and (c) HMBC (EPS 2008 kb)

Supplemental Fig. 6

2D NMR spectra of F7 (△MGGG) obtained at 500 MHz at 25 °C. (a) COSY, (b) HSQC, and (c) HMBC (EPS 3585 kb)

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Peng, Q., Zhang, M., Gao, L. et al. Effects of alginate oligosaccharides with different molecular weights and guluronic to mannuronic acid ratios on glyceollin induction and accumulation in soybeans. J Food Sci Technol 55, 1850–1858 (2018). https://doi.org/10.1007/s13197-018-3101-6

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  • DOI: https://doi.org/10.1007/s13197-018-3101-6

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