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Free cyclitol unloading from seed coats on stem–leaf–pod explants of low-raffinose, low-stachyose, low-phytin soybean

Published online by Cambridge University Press:  24 September 2010

Suzanne M. Kosina ,
Steven R. Schnebly  and
Ralph L. Obendorf
Suzanne M. Kosina
Affiliation:
Seed Biology, Department of Crop and Soil Sciences, Cornell University, Ithaca, NY14853, USA
Steven R. Schnebly
Affiliation:
Pioneer Hi-Bred, A DuPont Business, 810 Sugar Grove Ave., Hwy44, Dallas Center, IA50063, USA
Ralph L. Obendorf*
Affiliation:
Seed Biology, Department of Crop and Soil Sciences, Cornell University, Ithaca, NY14853, USA
*
*Correspondence Fax: +1-607-255-2644 Email: [email protected]
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Abstract

Raffinose, stachyose and phytin are undesirable compounds for soybean food and animal feed products. In seeds, raffinose and stachyose are believed to contribute to desiccation and cold stress tolerance. Thus, removal of these compounds from soybean by genetic mutation has resulted in a more commercially desirable composition, but potentially less physiologically viable seeds. In an effort to develop a method to improve viability and seed storability in soybean, stem–leaf–pod explants of three low raffinose, low stachyose lines, two of which were also low in phytin, and a check line were fed solutions containing d-chiro-inositol, myo-inositol or d-pinitol, free cyclitols which unload through the seed coat to the developing embryo where they accumulate as fagopyritols, galactinol and galactopinitols, respectively, during seed maturation. Increased galactopinitol and fagopyritol accumulation may substitute for the roles of raffinose and stachyose in low raffinose, stachyose and phytin seeds. Explants of all lines unloaded d-chiro-inositol, myo-inositol and d-pinitol. Fed d-chiro-inositol accumulated in leaf tissues demonstrating uptake into explants. Fed d-chiro-inositol and myo-inositol accumulated in pod wall and seed coat tissues of one or more lines. The results indicate that d-chiro-inositol was unloaded from the seed coat to the embryo in increased amounts after feeding. The potential use of increased maternal d-chiro-inositol for synthesis of fagopyritols in embryos to improve seed performance in low-stachyose and low-phytin soybean seeds is supported. The seed coat cup unloading of fed free cyclitols may provide a model system to test effective unloading of upregulated maternally synthesized cyclitols.

Keywords

Glycine max (L.) Merrilld-chiro-inositolmyo-inositold-pinitolseed coat cup unloadingsoybean stem-leaf-pod explantsucrose
Type
Research Article
Information
Seed Science Research , Volume 20 , Issue 4 , December 2010 , pp. 223 - 236
Copyright
Copyright © Cambridge University Press 2010

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References

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
Buitink, J., Thomas, M., Gissot, L. and Leprince, O. (2004) Starvation, osmotic stress and desiccation tolerance lead to expression of different genes of the regulatory beta and gamma subunits of the SnRK1 complex in germinating seeds of Medicago truncatula. Plant Cell and Environment 27, 55–67.CrossRefGoogle Scholar
Caffrey, M., Fonseca, V. and Leopold, A.C. (1988) Lipid–sugar interactions: relevance to anhydrous biology. Plant Physiology 86, 754–758.CrossRefGoogle ScholarPubMed
Chappell, A.S., Scaboo, A.M., Wu, X., Nguyen, H., Pantalone, V.R. and Bilyeu, K.D. (2006) Characterization of the MIPS gene family in Glycine max. Plant Breeding 125, 493–500.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
Chiera, J.M. and Grabau, E.A. (2007) Localization of myo-inositol phosphate synthase (GmMIPS-1) during the early stages of soybean seed development. Journal of Experimental Botany 58, 2261–2268.CrossRefGoogle ScholarPubMed
Chiera, J.M., Streeter, J.G. and Finer, J.J. (2006) Ononitol and pinitol production in transgenic soybean containing the inositol methyl transferase gene from Mesembryanthemum crystallinum. Plant Science 171, 647–654.CrossRefGoogle Scholar
Dittrich, P. and Brandl, A. (1987) Revision of the pathway of d-pinitol formation in Leguminosae. Phytochemistry 26, 1925–1926.CrossRefGoogle Scholar
Ellis, E.C. and Spanswick, R.M. (1987) Sugar efflux from attached seed coats of Glycine max (L.) Merr. Journal of Experimental Botany 38, 1470–1483.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
Heaney, R.P., Weaver, C.M. and Fitzsimmons, M.L. (1991) Soybean phytate content – effect on calcium absorption. American Journal of Clinical Nutrition 53, 745–747.CrossRefGoogle ScholarPubMed
Hegeman, C.E., Good, L.L. and Grabau, E.A. (2001) Expression of d-myo-inositol-3-phosphate synthase in soybean. Implications for phytic acid biosynthesis. Plant Physiology 125, 1941–1948.CrossRefGoogle ScholarPubMed
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
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., 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 ScholarPubMed
Htoo, J.K., Sauer, W.C., Zhang, Y., Cervantes, M., Liao, S.F., Araiza, B.A., Morales, A. and Torrentera, N. (2007) The effect of feeding low-phytate barley–soybean meal diets differing in protein content to growing pigs on the excretion of phosphorus and nitrogen. Journal of Animal Science 85, 700–705.CrossRefGoogle ScholarPubMed
Kosina, S.M., Castillo, A., Schnebly, S.R. and Obendorf, R.L. (2009) Soybean seed coat cup unloading on plants with low-raffinose, low-stachyose seeds. Seed Science Research 19, 145–153.CrossRefGoogle Scholar
Koster, K.L. and Leopold, A.C. (1988) Sugars and desiccation tolerance in seeds. Plant Physiology 88, 829–832.CrossRefGoogle ScholarPubMed
Lahuta, L.B., Górecki, R.J. and Horbowicz, M. (2005) High concentrations of d-pinitol or d-chiro-inositol inhibit the biosynthesis of raffinose family oligosaccharides in maturing smooth tare (Vicia tetrasperma [L.] Schreb.) seeds. Acta Physiologiae Plantarum 27, 505–513.CrossRefGoogle Scholar
Loewus, F.A. and Murthy, P.P.N. (2000) myo-Inositol metabolism in plants. Plant Science 150, 1–19.CrossRefGoogle Scholar
Lynch, S.R., Dassenko, S.A., Cook, J.D., Juillerat, M.A. and Hurrell, R.F. (1994) Inhibitory effect of a soybean-protein related moiety on iron-absorption in humans. American Journal of Clinical Nutrition 60, 567–572.CrossRefGoogle ScholarPubMed
Ma, J.M., Horbowicz, M. and Obendorf, R.L. (2005) Cyclitol galactosides in embryos of buckwheat stem–leaf–seed explants fed d-chiro-inositol, myo-inositol, or d-pinitol. Seed Science Research 15, 329–338.CrossRefGoogle Scholar
Meis, S.J., Fehr, W.R. and Schnebly, S.R. (2003) Seed source effect on field emergence of soybean lines with reduced phytate and raffinose saccharides. Crop Science 43, 1336–1339.CrossRefGoogle Scholar
Mitsuhashi, N., Kondo, M., Nakaune, S., Ohnishi, M., Hayashi, M., Hara-Nishimura, I., Richardson, A., Fukaki, H., Nishimura, M. and Mimura, T. (2008) Localization of myo-inositol-1-phosphate synthase to the endosperm in developing seeds of Arabidopsis. Journal of Experimental Botany 59, 3069–3076.CrossRefGoogle Scholar
Neus, J.D., Fehr, W.R. and Schnebly, S.R. (2005) Agronomic and seed characteristics of soybean with reduced raffinose and stachyose. Crop Science 45, 589–592.CrossRefGoogle Scholar
Nunes, A.C.S., Vianna, G.R., Cuneo, F., Amaya-Farfán, J., de Capdeville, G., Rech, E.L. and Aragão, F.J.L. (2006) RNAi-mediated silencing of the myo-inositol-1-phosphate synthase gene (GmMIPS1) in transgenic soybean inhibited seed development and reduced phytate content. Planta 224, 125–132.CrossRefGoogle ScholarPubMed
Obendorf, R.L. (1997) Oligosaccharides and galactosyl cyclitols in seed desiccation tolerance (Review Update). Seed Science Research 7, 63–74.CrossRefGoogle 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., 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
Obendorf, R.L., Sensenig, E.M., Wu, J., Ohashi, M., O'Sullivan, T.E., Kosina, S.M. and Schnebly, S.R. (2008 a) Soluble carbohydrates in mature soybean seed after feeding d-chiro-inositol, myo-inositol, or d-pinitol to stem-leaf-pod explants of low-raffinose, low-stachyose lines. Plant Science 175, 650–655.CrossRefGoogle Scholar
Obendorf, R.L., Zimmerman, A.D., Ortiz, P.A., Taylor, A.G. and Schnebly, S.R. (2008 b) Imbibitional chilling sensitivity and soluble carbohydrate composition of low raffinose, low stachyose soybean seed. Crop Science 48, 2396–2403.CrossRefGoogle Scholar
Obendorf, R.L., Zimmerman, A.D., Zhang, Q., Castillo, A., Kosina, S.M., Bryant, E.G., Sensenig, E.M., Wu, J. and Schnebly, S.R. (2009) Accumulation of soluble carbohydrates during seed development and maturation of low-raffinose, low-stachyose soybean. Crop Science 49, 329–341.CrossRefGoogle Scholar
Rosnoblet, C., Aubry, C., Leprince, O., Vu, B.L., Rogniaux, H. and Buitink, J. (2007) The regulatory gamma subunit SNF4b of the sucrose non-fermenting-related kinase complex is involved in longevity and stachyose accumulation during maturation of Medicago truncatula seeds. Plant Journal 51, 47–59.CrossRefGoogle ScholarPubMed
Sebastian, S.A., Kerr, P.S., Pearlstein, R.W. and Hitz, W.D. (2000) Soybean germplasm with novel genes for improved digestibility. pp. 56–73in Drackley, J.K. (Ed.) Soy in animal nutrition. Savoy, Illinois, Federation of Animal Science Societies.Google Scholar
Sharpley, A.N., Daniel, T., Sims, T., Lemunyon, J., Stevens, R. and Perry, R. (2003) Agricultural phosphorus and eutrophication (2nd edition). Agricultural Research Service, ARS 149. Washington, DC, United States Department of Agriculture.Google Scholar
Streeter, J.G. (2001) Simple partial purification of d-pinitol from soybean leaves. Crop Science 41, 1985–1987.CrossRefGoogle Scholar
Streeter, J.G., Lohnes, D.G. and Fioritto, R.J. (2001) Patterns of pinitol accumulation in soybean plants and relationships to drought tolerance. Plant Cell and Environment 24, 429–438.CrossRefGoogle Scholar
Suarez, F.L., Springfield, J., Furne, J.K., Lohrmann, T.T., Kerr, P.S. and Levitt, M.D. (1999) Gas production in humans ingesting a soybean flour derived from beans naturally low in oligosaccharides. American Journal of Clinical Nutrition 69, 135–139.CrossRefGoogle ScholarPubMed
Thorne, J.H. (1980) Kinetics of 14C-photosynthate uptake by developing soybean fruit. Plant Physiology 65, 975–979.CrossRefGoogle Scholar
Thorne, J.H. (1981) Morphology and ultrastructure of maternal seed tissues of soybean in relation to the import of photosynthate. Plant Physiology 67, 1016–1025.CrossRefGoogle Scholar
Thorne, J.H. and Rainbird, R.M. (1983) An in vivo technique for the study of phloem unloading in seed coats of developing soybean seeds. Plant Physiology 72, 268–271.CrossRefGoogle Scholar