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Biochemistry and physiology of raffinose family oligosaccharides and galactosyl cyclitols in seeds

Published online by Cambridge University Press:  22 February 2007

Thomas Peterbauer  and
Andreas Richter
Thomas Peterbauer
Affiliation:
Chemical Physiology of Plants, Institute of Ecology, University of Vienna, A-1091 Vienna, Austria
Andreas Richter*
Affiliation:
Chemical Physiology of Plants, Institute of Ecology, University of Vienna, A-1091 Vienna, Austria
*
*Correspondence Fax: +43-1-4277-9542 Email: Andreas.Richter@univie.ac.at
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Abstract

Raffinose family oligosaccharides (RFOs) are of almost ubiquitous occurrence in plant seeds. They accumulate during seed development and disappear rapidly during germination. The biosynthesis of raffinose, the first member of the series, proceeds by addition of a galactosyl unit to sucrose. Galactinol, a galactosyl derivative of myo-inositol, acts as a galactosyl donor. It is synthesized from UDP-D-GALACTOSE AND MYO-INOSITOL. STACHYOSE, VERBASCOSE AND AJUGOSE, THE NEXT HIGHER RFOS, ARE EITHER SYNTHESIZED BY GALACTINOL-DEPENDENT GALACTOSYLTRANSFERASES OR BY TRANSFER OF GALACTOSYL UNITS BETWEEN TWO RFO MOLECULES. IN SEEDS, THE METABOLISM OF METHYLATED INOSITOLS, SUCH AS D-ononitol and D-pinitol, is linked with the RFO pathway. In contrast to myo-inositol, these cyclitols are galactosylated by transfer of galactosyl residues from galactinol and not from UDP-D-galactose. However, the resulting galactosyl cyclitols can replace galactinol as galactosyl donors for the biosynthesis of stachyose. These recently discovered branches of the RFO pathway are active in seeds of a range of crop species, especially in legumes. We focus here on the biochemistry and molecular biology of the enzymes of RFO and galactosyl cyclitol biosynthesis. The metabolic control and hormonal regulation of the pathway during seed development and germination is discussed. The controversial role of α-galactosidases, which are believed to hydrolyse RFOs during germination, is reviewed critically.

Keywords

cyclitolsdevelopmentα-galactosidasegerminationraffinoseseedsstachyose
Type
Invited Review
Information
Seed Science Research , Volume 11 , Issue 3 , September 2001 , pp. 185 - 197
Copyright
Copyright © Cambridge University Press 2001

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References

Allan, S.M. and Hitz, W.D. (2000) Plant raffinose synthase homologs. International Patent Publication WO 00/24915, PCT/US99/24923.Google Scholar
Avigad, G. and Dey, P.M. (1997) Carbohydrate metabolism: Storage carbohydrates. pp. 143–204in Dey, P.M.; Harbourne, J. (Eds) Plant biochemistry. San Diego, Academic Press.CrossRefGoogle Scholar
Bachmann, M. and Keller, F. (1995) Metabolism of the raffinose family oligosaccharides in leaves of Ajuga reptans L. Inter- and intracellular compartmentation. Plant Physiology 109, 991–998.CrossRefGoogle ScholarPubMed
Bachmann, M., Matile, P. and Keller, F. (1994) Metabolism of the raffinose family oligosaccharides in leaves of Ajuga reptans L. Cold acclimation, translocation, and sink to source transition: Discovery of a chain elongation enzyme. Plant Physiology 105, 1335–1345.CrossRefGoogle ScholarPubMed
Baucells, F., Perez, J.F., Morales, J. and Gasa, J. (2000) Effect of α-galactosidase supplementation of cereal-soya-bean-pea diets on the productive performances, digestibility and lower gut fermentation in growing and finishing pigs. Animal Science 71, 157–164.CrossRefGoogle Scholar
Bentsink, L., Alonso-Blanco, C., Vreugdenhil, D., Tesnier, K., Groot, S.P.C. and Koornneef, M. (2000) Genetic analysis of seed-soluble oligosaccharides in relation to seed storability of Arabidopsis. Plant Physiology 124, 1595–1604.CrossRefGoogle ScholarPubMed
Bethke, P.C., Swanson, S.J., Hillmer, S. and Jones, R.L. (1998) From storage compartment to lytic organelle: The metamorphosis of the aleurone protein storage vacuole. Annals of Botany 82, 399–412.CrossRefGoogle Scholar
Black, M., Corbineau, F., Gee, H. and Côme, D. (1999) Water content, raffinose, and dehydrins in the induction of desiccation tolerance in immature wheat embryos. Plant Physiology 120, 463–471.CrossRefGoogle ScholarPubMed
Blackman, S.A., Obendorf, R.L. and Leopold, A.C. (1992) Maturation proteins and sugars in desiccation tolerance of developing soybean seeds. Plant Physiology 100, 225–230.CrossRefGoogle ScholarPubMed
Bradford, K.J., Chen, F., Cooley, M.B., Dahal, P., Downie, B., Fukunaga, K.K., Gee, O.H., Gurusinghe, S., Mella, R.A., Nonogaki, H., Wu, C.-T., Yang, H. and Yim, K.-O. (2000) Gene expression prior to radicle emergence in imbibed tomato seeds. pp. 231–251in Black, M.; Bradford, K.J.; Vázquez-Ramos, J. (Eds) Seed biology. Advances and applications. Wallingford, UK, CAB International.Google Scholar
Braun, R. and Keller, F. (2000) Vacuolar chain elongation of raffinose oligosaccharides in Ajuga reptans. Australian Journal of Plant Physiology 27, 743–746.Google Scholar
Brenac, P., Smith, M.E. and Obendorf, R.L. (1997a) Raffinose accumulation in maize embryos in the absence of a fully functional Vp1 gene product. Planta 103, 222–228.CrossRefGoogle Scholar
Brenac, P., Horbowicz, M., Downer, S.M., Dickerman, A.M., Smith, M.E. and Obendorf, R.L. (1997b) Raffinose accumulation related to desiccation tolerance during maize (Zea mays L.) seed development and maturation. Journal of Plant Physiology 150, 481–488.CrossRefGoogle Scholar
Buckeridge, M.S. and Dietrich, S.M.C. (1996) Mobilisation of the raffinose family oligosaccharides and galactomannan in germinating seeds of Sesbania marginata Bent. (Leguminosae-Faboideae). Plant Science 117, 33–43.CrossRefGoogle Scholar
Buitink, J., Hemminga, M.A. and Hoekstra, F.A. (2000a) Is there a role for oligosaccharides in seed longevity? An assessment of intracellular glass stability. Plant Physiology 122, 1217–1224.CrossRefGoogle Scholar
Buitink, J., van den Dries, I.J., Hoekstra, F.A., Alberda, M. and Hemminga, M.A. (2000b) High critical temperature above T-g may contribute to the stability of biological systems. Biophysical Journal 79, 1119–1128.CrossRefGoogle Scholar
Castillo, E.M., de Lumen, B.O., Reyes, P.S. and de Lumen, H.Z. (1990) Raffinose synthase and galactinol synthase in developing seeds and leaves of legumes. Journal of Agricultural and Food Chemistry 38, 351–355.CrossRefGoogle Scholar
Castonguay, Y. and Nadeau, P. (1998) Enzymatic control of soluble carbohydrate accumulation in cold-acclimated crowns of alfalfa. Crop Science 38, 1183–1189.CrossRefGoogle Scholar
Chien, C.T., Lin, T.P., Juo, C.G. and Her, G.R. (1996) Occurrence of a novel galactopinitol and its changes with other non-reducing sugars during development of Leucaena leucocephala seeds. Plant and Cell Physiology 37, 539–544.CrossRefGoogle Scholar
Chrost, B. and Schmitz, K. (2000) Purification and characterization of multiple forms of α-galactosidase in Cucumis melo plants. Journal of Plant Physiology 156, 483–491.CrossRefGoogle Scholar
Corbineau, F., Picard, M.A., Fougereux, J.A., Ladonne, F. and Côme, D. (2000) Effects of dehydration conditions on desiccation tolerance of developing pea seeds as related to oligosaccharide content and cell membrane properties. Seed Science Research 10, 329–339.CrossRefGoogle Scholar
Crowe, J.H., Hoekstra, F.A., Nguyen, K.H. and Crowe, L.M. (1996) Is vitrification involved in depression of the phase transition temperature in dry phospholipids? Biochimica et Biophysica Acta 1280, 187–196.CrossRefGoogle ScholarPubMed
Davis, M.O., Hata, D.J., Johnson, S.A., Walker, J.C. and Smith, D.S. (1996) Cloning, expression and characterization of a blood group B active recombinant α-D-galactosidase from soybean (Glycine max). Biochemistry and Molecular Biology International 39, 471–485.Google ScholarPubMed
Davis, M.O., Hata, D.J., Johnson, S.A., Jones, D.E., Harmata, M.A., Evans, M.L., Walker, J.C. and Smith, D.S. (1997) Cloning, sequence, and expression of a blood group B active recombinant α-D-galactosidase from pinto bean (Phaseolus vulgaris). Biochemistry and Molecular Biology International 42, 453–467.Google ScholarPubMed
Del Campillo, E., Shannon, L.M. and Hankins, C.N. (1981) Molecular properties of the enzymic phytohemagglutinin of mung bean. Journal of Biological Chemistry 256, 7177–7180.CrossRefGoogle ScholarPubMed
Dey, P.M. (1981) α-Galactosidase from sweet chestnut seeds. Phytochemistry 20, 1493–1496.CrossRefGoogle Scholar
Dey, P.M. (1983) Galactokinase of Vicia faba seeds. European Journal of Biochemistry 136, 155–159.CrossRefGoogle ScholarPubMed
Dey, P.M. (1985) D-Galactose-containing oligosaccharides. pp. 53–129in Dey, P.M.; Dixon, R. (Eds) Biochemistry of storage carbohydrates in green plants. New York, Academic Press.Google Scholar
Dey, P.M., Pridham, J.B. and Sumar, N. (1982a) Multiple forms of Vicia faba α-galactosidases and their relationships. Phytochemistry 21, 2195–2199.CrossRefGoogle Scholar
Dey, P.M., Hustler, M.J., Pridham, J.B. and Sumar, N. (1982b) Factors affecting the extraction and relative proportions of multiple forms of plant α-galactosidases. Phytochemistry 21, 1557–1562.CrossRefGoogle Scholar
Dey, P.M., Del Campillo, E.M. and Lezica, R.P. (1983) Characterization of a glycoprotein α-galactosidase from lentil seeds (Lens culinaris). Journal of Biological Chemistry 258, 923–929.CrossRefGoogle ScholarPubMed
Dittrich, P. and Brandl, A. (1987) Revision of the pathway of D-pinitol formation in Leguminosae. Phytochemistry 26, 1925–1926.CrossRefGoogle Scholar
Downie, B. and Bewley, J.D. (2000) Soluble sugar content of white spruce (Picea glauca) seeds during and after germination. Physiologia Plantarum 110, 1–12.CrossRefGoogle Scholar
Foley, M.E., Nichols, M.B. and Myers, S.P. (1993) Carbohydrate concentrations and interactions in afterripening-responsive dormant Avena fatua caryopses induced to germinate by gibberellic acid. Seed Science Research 3, 271–278.CrossRefGoogle Scholar
Frias, J., Vidal-Valverde, C., Bakhsh, A., Arthur, A.E. and Hedley, C. (1994) An assessment of variation for nutritional and non-nutritional carbohydrates in lentil seeds (Lens culinaris). Plant Breeding 113, 170–173.CrossRefGoogle Scholar
Frias, J., Bakhsh, A., Jones, D.A., Arthur, A.E., Vidal- Valverde, C., Rhodes, M.J.C. and Hedley, C.L. (1999) Genetic analysis of the raffinose oligosaccharide pathway in lentil seeds. Journal of Experimental Botany 50, 469–476.CrossRefGoogle Scholar
Gao, Z.F. and Schaffer, A.A. (1999) A novel alkaline α- galactosidase from melon fruit with a substrate preference for raffinose. Plant Physiology 119, 979–987.CrossRefGoogle ScholarPubMed
Górecki, R.J., Brenac, P., Clapham, W.M., Willcott, J.B. and Obendorf, R.L. (1996) Soluble carbohydrates in white lupin (Lupinus albus L. cv. Ultra) seeds matured at 13° and 28°C. Crop Science 36, 1277–1282.CrossRefGoogle Scholar
Górecki, R.J., Piotrowicz-Cieslak, A.I., Lahuta, L.B. and Obendorf, R.L. (1997) Soluble carbohydrates in desiccation tolerance of yellow lupin seeds during maturation and germination. Seed Science Research 7, 107–115.CrossRefGoogle Scholar
Greutert, H. and Keller, F. (1993) Further evidence for stachyose and sucrose/H+ antiporters on the tonoplast of Japanese artichoke (Stachys sieboldii) tubers. Plant Physiology 101, 1317–1322.CrossRefGoogle ScholarPubMed
Groot, S.P.C., Van der Geest, A.H.M., Tesnier, K., Alonso- Blanco, C., Bentsink, L., Donkers, H., Koornneef, M., Vreugdenhil, D. and Bino, R.J. (2000) Molecular genetic analysis of Arabidopsis seed quality. pp. 123–132in Black, M.; Bradford, K.J.; Vázquez-Ramos, J. (Eds) Seed biology. Advances and applications. Wallingford, UK, CAB International.Google Scholar
Handley, L.W., Pharr, D.M. and McFeeters, R.F. (1983) Relationship between galactinol synthase activity and sugar composition of leaves and seeds of several crop species. Journal of the American Society for Horticultural Science 108, 600–605.CrossRefGoogle Scholar
Hankins, C.N. and Shannon, L.M. (1978) The physical and enzymatic properties of a phytohemagglutinin from mung beans. Journal of Biological Chemistry 253, 7791–7797.CrossRefGoogle ScholarPubMed
Hankins, C.N., Kindinger, J.I. and Shannon, L.M. (1980) Legume α-galactosidase forms devoid of hemagglutinin activity. Plant Physiology 66, 375–378.CrossRefGoogle ScholarPubMed
Haritatos, E., Keller, F. and Turgeon, R. (1996) Raffinose oligosaccharide concentrations measured in individual cell and tissue types in Cucumis melo L. leaves: Implications for phloem loading. Planta 198, 614–622.CrossRefGoogle ScholarPubMed
Haritatos, E., Ayre, B.G. and Turgeon, R. (2000) Identification of phloem involved in assimilate loading in leaves by the activity of the galactinol synthase promoter. Plant Physiology 123, 929–937.CrossRefGoogle ScholarPubMed
Hendrix, D.L. (1990) Carbohydrates and carbohydrate enzymes in developing cotton ovules. Physiologia Plantarum 78, 85–92.CrossRefGoogle Scholar
Herman, E.M. and Larkins, B.A. (1999) Protein storage bodies and vacuoles. The Plant Cell 11, 601–603.CrossRefGoogle ScholarPubMed
Herman, E.M. and Shannon, L.M. (1985) Accumulation and subcellular localization of α-galactosidasehemagglutinin in developing soybean cotyledons. Plant Physiology 77, 886–890.CrossRefGoogle ScholarPubMed
Hitz, W.D. and Sebastian, S.A. (1998) Soybean plant producing seeds with reduced levels of raffinose saccharides and phytic acid. International Patent Application WO98/45448, PCT/US98/06822.Google Scholar
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
Holthaus, U. and Schmitz, K. (1991) Distribution and immunolocalization of stachyose synthase in Cucumis melo L. Planta 185, 479–486.CrossRefGoogle ScholarPubMed
Horbowicz, M. and Obendorf, R.L. (1994) Seed desiccation tolerance and storability: Dependance on flatulenceproducing oligosaccharides and cyclitols – review and survey. Seed Science Research 4, 385–405.CrossRefGoogle Scholar
Horbowicz, M., Obendorf, R.L., McKersie, B.D. and Viands, D.R. (1995) Soluble saccharides and cyclitols in alfalfa (Medicago sativa L.) somatic embryos, leaflets, and mature seeds. Plant Science 109, 191–198.CrossRefGoogle Scholar
Horbowicz, M., Brenac, P. and Obendorf, R.L. (1998) Fagopyritol B1, O-α-D-galactopyranosyl-(1–2)-D-chiroinositol, a galactosyl cyclitol in maturing buckwheat seeds associated with desiccation tolerance. Planta 205, 1–11.CrossRefGoogle Scholar
Jauh, G.Y., Phillips, T.E. and Rogers, J.C. (1999) Tonoplast intrinsic protein isoforms as markers for vacuolar functions. The Plant Cell 11, 1867–1882.CrossRefGoogle ScholarPubMed
Joersbo, M., Pedersen, S.G., Nielsen, J.E., Marcussen, J. and Brunstedt, J. (1999) Isolation and expression of two cDNA clones encoding UDP-galactose epimerase expressed in developing seeds of the endospermous legume guar. Plant Science 142, 147–154.CrossRefGoogle Scholar
Kandler, O. and Hopf, H. (1980) Occurence, metabolism, and function of oligosaccharides. pp. 221–270in Preiss, J. (Ed.) The biochemistry of plants, vol. 3. Carbohydrates: structure and function. New York, Academic Press.CrossRefGoogle Scholar
Kandler, O. and Hopf, H. (1982) Oligosaccharides based on sucrose (sucrosyl oligosaccharides). Encyclopedia of Plant Physiology (New Series) 13A, 348–383.Google Scholar
Kaplan, C.P., Tugal, H.B. and Baker, A. (1997) Isolation of a cDNA encoding an Arabidopsis galactokinase by functional expression in yeast. Plant Molecular Biology 34, 497–506.CrossRefGoogle ScholarPubMed
Keller, F. (1992a) Galactinol synthase is an extravacuolar enzyme in tubers of Japanese artichoke (Stachys sieboldii). Plant Physiology 99, 1251–1253.CrossRefGoogle ScholarPubMed
Keller, F. (1992b) Transport of stachyose and sucrose by vacuoles of Japanese artichoke (Stachys sieboldii) tubers. Plant Physiology 98, 442–445.CrossRefGoogle ScholarPubMed
Keller, F. and Matile, P. (1985) The role of the vacuole in storage and mobilisation of stachyose in tubers of Stachys sieboldii. Journal of Plant Physiology 119, 369–380.CrossRefGoogle Scholar
Keller, F. and Pharr, D.M. (1996) Metabolism of carbohydrates in sinks and sources: galactosyl-sucrose oligosaccharides. pp. 115–184in Zamski, E.; Schaffer, A.A. (Eds) Photoassimilate distribution in plants and crops. New York, Marcel Dekker.Google Scholar
Keller, R., Brearley, C.A., Trethewey, R.N. and Muller- Rober, B. (1998) Reduced inositol content and altered morphology in transgenic potato plants inhibited for 1D-myo-inositol 3-phosphate synthase. The Plant Journal 16, 403–410.CrossRefGoogle Scholar
Kerr, P.S. and Sebastian, S.A. (1998) Soybean products with improved carbohydrate composition and soybean plants. International Patent Publication WO 93/07742, PCT/US92/08958.Google Scholar
Kerr, P.S., Pearlstein, R.W., Schweiger, B.J., Becker- Manley, M.F. and Pierce, J.W. (1993) Nucleotide sequences of galactinol synthase from zucchini and soybean. International Patent Publication WO 93/02196, PCT/US92/06057.Google Scholar
Koster, K.L. and Leopold, A.C. (1988) Sugars and desiccation tolerance in seeds. Plant Physiology 88, 829–832.CrossRefGoogle ScholarPubMed
Kuo, T.M., VanMiddlesworth, J.F. and Wolf, W.J. (1988) Content of raffinose oligosaccharides and sucrose in various plant seeds. Journal of Agricultural and Food Chemistry 36, 32–36.CrossRefGoogle Scholar
Kuo, T.M., Lowell, C.A. and Smith, P.T. (1997) Changes in soluble carbohydrates and enzymic activities in maturing soybean seed tissues. Plant Science 125, 1–11.Google Scholar
Lahuta, L.B., Login, A., Rejowski, A., Socha, A. and Zalewski, K. (2000) Influence of water deficit on the accumulation of sugars in developing field bean (Vicia faba var. minor) seeds. Seed Science and Technology 28, 93–100.Google Scholar
Lehle, L. and Tanner, W. (1973) The function of myo-inositol in the biosynthesis of raffinose. Purification and characterization of galactinol:sucrose 6-galactosyltransferase from Vicia faba seeds. European Journal of Biochemistry 38, 103–110.CrossRefGoogle ScholarPubMed
Leopold, A.C., Sun, W.Q. and Bernal-Lugo, I. (1994) The glassy state in seeds: analysis and function. Seed Science Research 4, 267–274.CrossRefGoogle Scholar
Lin, T.P. and Huang, N.H. (1994) The relationship between carbohydrate composition of some tree seeds and their longevity. Journal of Experimental Botany 45, 1289–1294.CrossRefGoogle Scholar
Lin, T.-P., Yen, W.-L. and Chien, C.-T. (1998) Disappearance of desiccation tolerance of imbibed crop seeds is not associated with the decline of oligosaccharides. Journal of Experimental Botany 49, 1203–1212.CrossRefGoogle Scholar
Liu, J.J.J., Odegard, W. and de Lumen, B.O. (1995) Galactinol synthase from kidney bean cotyledon and zucchini leaf. Plant Physiology 109, 505–511.CrossRefGoogle ScholarPubMed
Liu, J.J.J., Krenz, D.C., Galvez, A.F. and de Lumen, B.O. (1998) Galactinol synthase (GS): increased enzyme activity and levels of mRNA due to cold and desiccation. Plant Science 134, 11–20.CrossRefGoogle Scholar
Loewus, F.A. and Murthy, P.P.N. (2000) myo-Inositol metabolism in plants. Plant Science 150, 1–19.CrossRefGoogle Scholar
Madore, M. (1995) Catabolism of raffinose family oligosaccharides as translocates in higher plants. pp. 204–214in Madore, M.; Lucas, W.J. (Eds) Current topics in plant physiology, vol. 13. Carbon partitioning and source-sink interactions in plants. Rockville, Maryland, American Society of Plant Physiologists.Google Scholar
Main, E.L., Pharr, D.M., Huber, S.C. and Moreland, D.E. (1983) Control of galactosyl-sugar metabolism in relation to rate of germination. Physiologia Plantarum 59, 387–392.CrossRefGoogle Scholar
McCleary, B.V. and Matheson, N.K. (1974) α-DGalactosidase activity and galactomannan and galactosylsucrose oligosaccharide depletion in germinating legume seeds. Phytochemistry 13, 1747–1757.CrossRefGoogle Scholar
Modi, A.T., McDonald, M.B. and Streeter, J.G. (2000) Soluble carbohydrates in soybean seeds during development and imbibition. Seed Science and Technology 28, 115–127.Google Scholar
Muller, L.L. and Jacks, T.J. (1983) Intracellular distribution of free sugars in quiescent cottonseed. Plant Physiology 71, 703–704.CrossRefGoogle ScholarPubMed
Muzquiz, M., Burbano, C., Pedrosa, M.M., Folkman, W. and Gulewicz, K. (1999) Lupins as a potential source of raffinose family oligosaccharides – Preparative method for their isolation and purification. Industrial Crops and Products 9, 183–188.CrossRefGoogle Scholar
Nichols, M.B., Bancal, M.-O., Foley, M.E. and Volenec, J.J. (1993) Nonstructural carbohydrates in dormant and afterriped wild oat caryopses. Physiologia Plantarum 88, 221–228.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., Dickerman, A.M., Brenac, P. and Smith, M.E. (1998a) Soluble oligosaccharides and galactosyl cyclitols in maturing soybean seeds in planta and in vitro. Crop Science 38, 78–84.CrossRefGoogle Scholar
Obendorf, R.L., Dickerman, A.M., Pflum, T.M., Kacalanos, M.A. and Smith, M.E. (1998b) Drying rate alters soluble carbohydrates, desiccation tolerance, and subsequent seedling growth of soybean (Glycine max L. Merrill) zygotic embryos during in vitro maturation. Plant Science 132, 1–12.CrossRefGoogle Scholar
Ooms, J.J.J., Léon-Kloosterziel, K.M., Bartels, D., Koornneef, M. and Karssen, C.M. (1993) Acquisition of desiccation tolerance and longevity in seeds of Arabidopsis thaliana. A comparative study using abscisic acid-insensitive abi3 mutants. Plant Physiology 102, 1185–1191.CrossRefGoogle ScholarPubMed
Ooms, J.J.J., Wilmer, J.A. and Karssen, C.M. (1994) Carbohydrates are not the sole factor determining desiccation tolerance in seeds of Arabidopsis thaliana. Physiologia Plantarum 90, 431–436.CrossRefGoogle Scholar
Oosumi, C., Nozaki, J. and Kida, T. (1998) Raffinose synthetase gene, process for producing raffinose, and transformed plant. International Patent Publication WO98/49273, PCT/JP97/03879.Google Scholar
Overbeeke, N., Fellinger, A.J., Toonen, M.Y., van Wassenaar, D. and Verrips, C.T. (1989) Cloning and nucleotide sequence of the α-galactosidase cDNA from Cyamopsis tetragonoloba (guar). Plant Molecular Biology 13, 541–550.CrossRefGoogle ScholarPubMed
Paris, N., Stanley, C.M., Jones, R.L. and Rogers, J.C. (1996) Plant cells contain two functionally distinct vacuolar compartments. Cell 85, 563–572.CrossRefGoogle ScholarPubMed
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. (2000) Galactinolindependent synthesis of verbascose in seeds of Pisum sativum. Plant Physiology and Biochemistry 38 (Suppl.), 127.Google Scholar
Peterbauer, T., Puschenreiter, M. and Richter, A. (1998) Metabolism of galactosylononitol in seeds of Vigna umbellata. Plant and Cell Physiology 39, 334–341.CrossRefGoogle Scholar
Peterbauer, T., Mucha, J., Mayer, U., Popp, M., Glössl, J. and Richter, A. (1999) Stachyose synthesis in seeds of adzuki bean (Vigna angularis): Molecular cloning and functional expression of stachyose synthase. The Plant Journal 20, 509–518.CrossRefGoogle ScholarPubMed
Plant, A.R. and Moore, K.G. (1983) The protein, lipid and carbohydrate composition of protein bodies from Lupinus angustifolius seeds. Phytochemistry 22, 2359–2363.CrossRefGoogle Scholar
Porter, J.E., Herrmann, K.M. and Ladisch, M.R. (1990) Integral kinetics of α-galactosidase purified from Glycine max for simultaneous hydrolysis of stachyose and raffinose. Biotechnology and Bioengineering 35, 15–22.CrossRefGoogle ScholarPubMed
Reid, J.S.G. and Meier, H. (1973) Enzymic activities and galactomannan mobilisation in germinating seeds of fenugreek (Trigonella foenum-graecum L. Leguminosae). Secretion of α-galactosidase and α-mannosidase by the aleurone layer. Planta 112, 301–308.CrossRefGoogle Scholar
Richter, A., Peterbauer, T. and Brereton, I. (1997) Structure of galactosylononitol. Journal of Natural Products 60, 749–751.CrossRefGoogle Scholar
Richter, A., Hoch, G., Puschenreiter, M., Mayer, U. and Peterbauer, T. (2000) The role of stachyose synthase in the oligosaccharide metabolism of legume seeds. pp. 75–84in Black, M.; Bradford, K.J.; Vásquez-Ramos, J. (Eds) Seed biology. Advances and applications. Wallingford, UK, CAB International.Google Scholar
Saravitz, D.M., Pharr, D.M. and Carter, T.E. (1987) Galactinol synthase activity and soluble sugars in developing seeds of four soybean genotypes. Plant Physiology 83, 185–189.CrossRefGoogle ScholarPubMed
Seiler, A. (1977) Galaktomannanabbau in keimenden Johannisbrotsamen (Ceratonia siliqua L.). Planta 134, 209–221.CrossRefGoogle ScholarPubMed
Sekhar, K.N.C. and DeMason, D.A. (1990) Identification and immunocytochemical localization of α- galactosidase in resting and germinated date palm (Phoenix dactylifera L.) seeds. Planta 181, 53–61.CrossRefGoogle ScholarPubMed
Sinniah, U.R., Ellis, R.H. and John, P. (1998) Irrigation and seed quality development in rapid-cycling brassica: Soluble carbohydrates and heat-stable proteins. Annals of Botany 82, 647–655.CrossRefGoogle Scholar
Sprenger, N. and Keller, F. (2000) Allocation of raffinose family oligosaccharides to transport and storage pools in Ajuga reptans: the roles of two distinct galactinol synthases. The Plant Journal 21, 249–258.CrossRefGoogle ScholarPubMed
Swanson, S.J., Bethke, P.C. and Jones, R.L. (1998) Barley aleurone cells contain two types of vacuoles: characterization of lytic organelles by use of fluorescent probes. The Plant Cell 10, 685–698.CrossRefGoogle ScholarPubMed
Tanner, W. and Kandler, O. (1966) Biosynthesis of stachyose in Phaseolus vulgaris. Plant Physiology 41, 1540–1542.CrossRefGoogle ScholarPubMed
Tanner, W. and Kandler, O. (1968) myo-Inositol, a cofactor in the biosynthesis of stachyose. European Journal of Biochemistry 4, 233–239.CrossRefGoogle ScholarPubMed
Tanner, W., Lehle, L. and Kandler, O. (1967) myo-Inositol, a cofactor in the biosynthesis of verbascose. Biochemical and Biophysical Research Communications 29, 166–171.CrossRefGoogle ScholarPubMed
Tanner, W., Seifarth, H. and Kandler, O. (1968) Der Umsatz der Oligosaccharide in reifenden und keimenden Samen von Phaseolus vulgaris. Zeitschrift für Pflanzenphysiologie 58, 369–377.Google Scholar
Tortuero, F., Fernandez, E., Ruperez, P. and Moreno, M. (1997) Raffinose and lactic acid bacteria influence caecal fermentation and serum cholesterol in rats. Nutrition Research 17, 41–49.CrossRefGoogle Scholar
Voragen, A.G.J. (1998) Technological aspects of functional food-related carbohydrates. Trends in Food Science and Technology 9, 328–335.CrossRefGoogle Scholar
Watanabe, E. and Oeda, K. (1998) Raffinose synthetase genes and use thereof. European Patent Application EP0849359, 97122417.5.Google Scholar
Widders, I.E. and Kwantes, M. (1995) Environmental effects on seed dry weight and carbohydrate composition as related to expansive growth of cucumber (Cucumis sativus L.) fruit. Scientia Horticulturae 64, 21–31.CrossRefGoogle Scholar
Zhu, A. and Goldstein, J. (1994) Cloning and functional expression of a cDNA encoding coffee bean α- galactosidase. Gene 140, 227–231.CrossRefGoogle ScholarPubMed
Zhu, A. and Wang, Z.K. (1996) Expression and characterization of recombinant α-galactosidase in baculovirus-infected insect cells. European Journal of Biochemistry 235, 332–337.CrossRefGoogle ScholarPubMed