Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-29T19:16:18.088Z Has data issue: false hasContentIssue false
  • English
  • Français

Cyclitol galactosides in embryos of buckwheat stem–leaf–seed explants fed D-chiro-inositol, myo-inositol or D-pinitol

Published online by Cambridge University Press:  22 February 2007

Janet M. Ma ,
Marcin Horbowicz  and
Ralph L. Obendorf
Janet M. Ma
Affiliation:
Seed Biology, Department of Crop and Soil Sciences, 617 Bradfield Hall, Cornell University Agricultural Experiment Station, Cornell University, Ithaca, NY 14853-1901, USA
Marcin Horbowicz
Affiliation:
Seed Biology, Department of Crop and Soil Sciences, 617 Bradfield Hall, Cornell University Agricultural Experiment Station, Cornell University, Ithaca, NY 14853-1901, USA Research Institute for Vegetable Crops, Skierniewice, Poland
Ralph L. Obendorf*
Affiliation:
Seed Biology, Department of Crop and Soil Sciences, 617 Bradfield Hall, Cornell University Agricultural Experiment Station, Cornell University, Ithaca, NY 14853-1901, USA
*
*Correspondence: Fax: +1 607 255 2644 Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Crop seeds accumulate soluble carbohydrates as part of their maturation process. In legume seeds, the major soluble carbohydrates are sucrose and its galactosides raffinose, stachyose and verbascose. In buckwheat (Fagopyrum esculentum Moench) seeds, the major soluble carbohydrates are sucrose and galactosides of d-chiro-inositol, named fagopyritols. This study was conducted to determine changes in soluble carbohydrate accumulation in embryos of buckwheat seeds after feeding solutions containing the free cyclitols D-chiro-inositol, myo-inositol and d-pinitol to stem–leaf–seed explants. Feeding D-chiro-inositol to explants resulted in a fourfold to fivefold increase in the accumulation of free d-chiro-inositol, fagopyritol A1 and fagopyritol B1 in embryos of mature seeds, but resulted in 30% less embryo dry weight compared to the control treatment without cyclitols. Feeding myo-inositol to buckwheat explants increased d-chiro-inositol in leaves and increased accumulation of fagopyritol A1 and fagopyritol B1 fivefold in embryos, fagopyritol A2 and fagopyritol B2 fourfold; fagopyritol A3 and fagopyritol B3 were also detected, with no reduction in accumulated embryo dry weight. Feeding d-pinitol to buckwheat explants resulted in accumulation of free d-pinitol in mature embryos, but not galactopinitols. D-Pinitol, galactopinitol A and galactopinitol B were not detected in embryos from explants fed solutions without d-pinitol. Feeding d-pinitol also resulted in reduced D-chiro-inositol accumulation by buckwheat seeds. The results indicate that myo-inositol may be the precursor to d-chiro-inositol synthesis, and fagopyritols accumulated in response to d-chiro-inositol availability in the embryo. We suggest that increasing myo-inositol in buckwheat maternal tissues may be an effective means to enhance the accumulation of D-chiro-inositol and fagopyritols in seeds, compounds that may be beneficial for the treatment of non-insulin-dependent diabetes mellitus.

Keywords

Fagopyrum esculentumPolygonaceaefagopyritolD-chiro-inositolbuckwheat seedcyclitol transport
Type
Research Article
Information
Seed Science Research , Volume 15 , Issue 4 , December 2005 , pp. 329 - 338
Copyright
Copyright © Cambridge University Press 2005

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Berlin, W.K., Wang, S.N. and Shen, T.Y. (1990) Glycosyl inositol derivatives. II. Synthesis of 2-amino-2-deoxy- d -galactosyl-α-(1→3)-D-chiro -inositol. Tetrahedron Letters 31, 1109–1112.CrossRefGoogle Scholar
Dittrich, P. and Brandl, A. (1987) Revision of the pathway of d -pinitol formation in Leguminosae. Phytochemistry 26, 1925–1926.CrossRefGoogle Scholar
Elpidina, E.N., Dunaevsky, Y.E. and Belozersky, M.A. (1990) Protein bodies from buckwheat seed cotyledons: isolation and characteristics. Journal of Experimental Botany 41, 969–977.CrossRefGoogle Scholar
Gomes, C.I., Obendorf, R.L. and Horbowicz, M. (2005) myo -Inositol, D-chiro-inositol, and D-pinitol synthesis, transport, and galactoside formation in soybean explants. Crop Science 45, 1312–1319.CrossRefGoogle Scholar
Hitz, W.D., Carlson, T.J., Kerr, P.S. and Sebastian, S.A. (2002) Biochemical and molecular characterization of a mutation that confers a decreased raffinosaccharide and phytic acid phenotype on soybean seeds. Plant Physiology 128, 650–660.CrossRefGoogle ScholarPubMed
Hoch, G., Peterbauer, T. and Richter, A. (1999) Purification and characterization of stachyose synthase from lentil (Lens culinaris) seeds: galactopinitol and stachyose synthesis. Archives of Biochemistry and Biophysics 366, 75–81.CrossRefGoogle ScholarPubMed
Horbowicz, M. and Obendorf, R.L. (1992) Changes in sterols and fatty acids of buckwheat endosperm and embryo during seed development. Journal of Agricultural and Food Chemistry 40, 745–750.CrossRefGoogle Scholar
Horbowicz, M. and Obendorf, R.L. (1994) Seed desiccation tolerance and storability: Dependence on flatulence-producing oligosaccharides and cyclitols – review and survey. Seed Science Research 4, 385–405.CrossRefGoogle Scholar
Horbowicz, M. and Obendorf, R.L. (2005) Fagopyritol accumulation and germination of buckwheat seeds matured at 15, 22, and 30°C. Crop Science 45, 1264–1270.CrossRefGoogle Scholar
Horbowicz, M., Brenac, P. and Obendorf, R.L. (1998) Fagopyritol B1, O -α- d -galactopyranosyl-(1→2)- D-chiro-inositol, a galactosyl cyclitol in maturing buckwheat seeds associated with desiccation tolerance. Planta 205, 1–11.CrossRefGoogle Scholar
Johnson, M.D. and Wang, X. (1996) Differentially expressed forms of 1l -myo-inositol-1-phosphate synthase (EC 5.5.1.4) in Phaseolus vulgaris. Journal of Biological Chemistry 271, 17215–17218.CrossRefGoogle Scholar
Kawa, J.M., Taylor, C.G. and Przybylski, R. (2003) Buckwheat concentrate reduces serum glucose in streptozotocin-diabetic rats. Journal of Agricultural and Food Chemistry 51, 7287–7291.CrossRefGoogle ScholarPubMed
Keller, R., Brearley, C.A., Trethewey, R., Müller-Röber, B. (1998) Reduced inositol content and altered morphology in transgenic potato plants inhibited for 1D-myo-inositol 3-phosphate synthase. Plant Journal 16, 403–410.CrossRefGoogle Scholar
Larner, J. (2001) D-chiro-Inositol in insulin action and insulin resistance – old-fashioned biochemistry still at work. IUBMB Life 51, 139–148.CrossRefGoogle ScholarPubMed
Larner, J. and Huang, L.C. (1999) Identification of a novel inositol glycan signaling pathway with significant therapeutic relevance to insulin resistance: an insulin signaling model using both tyrosine kinase and G-proteins. Diabetes Reviews 7, 217–231.Google Scholar
Larner, J., Huang, L.C., Schwartz, C.F.W., Oswald, A.S., Shen, T.Y., Kinter, M., Tang, G. and Zeller, K. (1988) Rat liver insulin mediator which stimulates pyruvate dehydrogenase phosphatase contains galactosamine and D-chiro-inositol. Biochemical and Biophysical Research Communications 151, 1416–1426.CrossRefGoogle Scholar
Larner, J., Price, J.D., Heimark, D., Smith, L., Rule, G., Piccariello, T., Fonteles, M.C., Pontes, C., Vale, D. and Huang, L. (2003) Isolation, structure, synthesis, and bioactivity of a novel putative insulin mediator. A galactosamine chiro-inositol pseudo-disaccharide Mn 2+ chelate with insulin-like activity. Journal of Medicinal Chemistry 46, 3283–3291.CrossRefGoogle ScholarPubMed
Loewus, F.A., Murthy, P.P.N. (2000) myo -Inositol metabolism in plants. Plant Science 150, 1–19.CrossRefGoogle Scholar
Lu, C., Xu, J.Zho, P., Ma, H., Tong, H., Jin, Y. and Li, S. (1992) Clinical application and therapeutic effect of composite tartary buckwheat flour on hyperglycemia and hyperlipidemia. pp. 458–464. in Lin, R.;, Zhou, M.;, Tao, Y.;, Li, J.;, Zhang, Z. (Eds) Proceedings of the 5th international symposium on buckwheat, 20–26. August 1992, Taiyuan, China. Beijing Agriculture Publishing House.Google Scholar
Ma, J.M. (2003) Transport of the free cyclitols D-chiro -inositol, myo -inositol, or D-pinitol fed to buckwheat explants and analysis of galactosyl cyclitols in seeds. Plant Science Research Honours Thesis, College of Agriculture and Life Sciences, Cornell University, Ithaca, New York.Google Scholar
Morris, M.R. (1952) Cytogenetic studies on buckwheat. Genetic and cytological studies of compatibility in relation to heterostyly in common buckwheat, Fagopyrum sagittatum. Journal of Heredity 42, 85–89.CrossRefGoogle Scholar
Obendorf, R.L. (1997) Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance. Seed Science Research 7, 63–74.CrossRefGoogle Scholar
Obendorf, R.L., Horbowicz, M. and Taylor, D.P. (1993) Structure and chemical composition of developing buckwheat seed. pp. 244–251. Janick, J.;, Simon, J.E. (Eds) New crops. New York, John Wiley & Sons.Google Scholar
Obendorf, R.L., Horbowicz, M., Dickerman, A.M., Brenac, P. and Smith, M.E. (1998) Soluble oligosaccharides and galactosyl cyclitols in maturing soybean seeds in planta and in vitro. Crop Science 38, 78–84.CrossRefGoogle Scholar
Obendorf, R.L., Steadman, K.J., Fuller, D.J., Horbowicz, M. and Lewis, B.A. (2000) Molecular structure of fagopyritol A1 (O-α-D-galactopyranosyl-(1→3)-D-chiro-inositol) by NMR. Carbohydrate Research 328, 623–627.CrossRefGoogle Scholar
Obendorf, R.L., Odorcic, S., Ueda, T., Coseo, M.P. and Vassallo, E. (2004) Soybean galactinol synthase forms fagopyritol B1 but not galactopinitols: substrate feeding of isolated embryos and heterologous expression. Seed Science Research 14, 321–333.CrossRefGoogle Scholar
Odorcic, S. and Obendorf, R.L. (2003) Galactosyl cyclitol accumulation enhanced by substrate feeding of soybean embryos. pp. 51–60. in Nicolás, G.;, Bradford, K.J.;, Côme, D.;, Pritchard, H.The biology of seeds: Recent research advances. Wallingford, CABI Publishing.Google Scholar
Peterbauer, T. and Richter, A. (1998) Galactosylononitol and stachyose synthesis in seeds of adzuki bean: Purification and characterization of stachyose synthase. Plant Physiology 117, 165–172.CrossRefGoogle ScholarPubMed
Peterbauer, T. and Richter, A. (2001) Biochemistry and physiology of raffinose family oligosaccharides and galactosyl cyclitols in seeds. Seed Science Research 11, 185–198.Google Scholar
Peterbauer, T., Mucha, J., Mach, L. and Richter, A. (2002) Chain-elongation of raffinose in pea seeds: Isolation, characterization and molecular cloning of a multifunctional enzyme catalyzing the synthesis of stachyose and verbascose. Journal of Biological Chemistry 277, 194–200.CrossRefGoogle ScholarPubMed
Peterbauer, T., Brereton, I. and Richter, A. (2003) Identification of a digalactosyl ononitol from seeds of adzuki bean (Vigna angularis). Carbohydrate Research 338, 2017–2019.CrossRefGoogle ScholarPubMed
Quemener, B. and Brillouet, J.M. (1983) Ciceritol, a pinitol digalactoside from seeds of chickpea, lentil and white lupin. Phytochemistry 22, 1745–1751.CrossRefGoogle Scholar
Richter, A., Peterbauer, T. and Brereton, I. (1997) The structure of galactosyl ononitol. Journal of Natural Products 60, 749–751.CrossRefGoogle Scholar
Schweizer, T.F. and Horman, I. (1981) Purification and structure determination of three α- d -galactopyranosylcyclitols from soya beans. Carbohydrate Research 95, 61–71.CrossRefGoogle Scholar
Slawinska, J. and Obendorf, R.L. (2001) Buckwheat seed set in planta and during in vitro inflorescence culture: Evaluation of temperature and water deficit stress. Seed Science Research 11, 223–233.Google Scholar
Steadman, K.J., Burgoon, M.S., Schuster, R.L., Lewis, B.A., Edwardson, S.E. and Obendorf, R.L. (2000) Fagopyritols, D-chiro-inositol, and other soluble carbohydrates in buckwheat seed milling fractions. Journal of Agricultural and Food Chemistry 48, 2843–2847.CrossRefGoogle ScholarPubMed
Steadman, K.J., Burgoon, M.S., Lewis, B.A., Edwardson, S.E. and Obendorf, R.L. (2001a) Buckwheat seed milling fractions: Description, macronutrient composition, and dietary fiber. Journal of Cereal Science 33, 271–278.CrossRefGoogle Scholar
Steadman, K.J., Fuller, D.J. and Obendorf, R.L. (2001b) Purification and molecular structure of two diagalactosyl D-chiro-inositols and two triagalactosyl D-chiro-inositols from buckwheat seeds. Carbohydrate Research 331, 19–25.CrossRefGoogle Scholar
Szczecinski, P., Gryff-Keller, A., Horbowicz, M. and Lahuta, L.B. (2000) Galactosylpinitols isolated from vetch (Vicia villosa Roth.) seeds. Journal of Agricultural and Food Chemistry 48, 2717–2720.CrossRefGoogle ScholarPubMed
Taylor, D.P. and Obendorf, R.L. (2001) Quantitative assessment of some factors limiting seed set in buckwheat. Crop Science 41, 1792–1799.CrossRefGoogle Scholar
Ueda, T., Coseo, M.P., Harrell, T.J. and Obendorf, R.L. (2005) A multifunctional galactinol synthase catalyzes the synthesis of fagopyritol A1 and fagopyritol B1 in buckwheat seed. Plant Science 168, 681–690.CrossRefGoogle Scholar
Wang, J., Liu, Z., Fu, X., Run, M. (1992) A clinical observation on the hypoglycemic effect of Xinjiang buckwheat. pp. 465–467. in Lin, R.;, Zhou, M.;, Tao, Y.;, Li, J.;, Zhang, Z.Proceedings of the 5th international symposium on buckwheat, 20–26. August 1992, Taiyuan China. Beijing Agricultural Publishing House.Google Scholar
Whistler, R.L. and Durso, D.F. (1950) Chromatographic separation of sugars on charcoal. Journal of the American Chemical Society 72, 677–679.CrossRefGoogle Scholar