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An alkaline α-galactosidase transcript is present in maize seeds and cultured embryo cells, and accumulates during stress

Published online by Cambridge University Press:  22 February 2007

Tian-Yong Zhao ,
J. Willis Corum III ,
Jeffrey Mullen ,
Robert B. Meeley ,
Timothy Helentjaris ,
David Martin  and
Bruce Downie
Tian-Yong Zhao
Affiliation:
Department of Anatomy and Neurobiology, Medical Center, University of Kentucky, Lexington, KY 40536-0298, USA Department of Horticulture, Plant Science Building, University of Kentucky, Lexington, KY, 40546-0312, USA University of Kentucky Seed Biology Program, University of Kentucky, Lexington, Kentucky, USA
J. Willis Corum III
Affiliation:
College of Medicine, Dean's Office, University of Kentucky, Lexington, KY, 40546-0293, USA Department of Horticulture, Plant Science Building, University of Kentucky, Lexington, KY, 40546-0312, USA University of Kentucky Seed Biology Program, University of Kentucky, Lexington, Kentucky, USA
Jeffrey Mullen
Affiliation:
Pioneer Hi-Bred International, Inc., 7300 NW 62nd Ave Box 1004, Johnston, IA, 50131, USA
Robert B. Meeley
Affiliation:
Pioneer Hi-Bred International, Inc., 7300 NW 62nd Ave Box 1004, Johnston, IA, 50131, USA
Timothy Helentjaris
Affiliation:
Pioneer Hi-Bred International, Inc., 7300 NW 62nd Ave Box 1004, Johnston, IA, 50131, USA
David Martin
Affiliation:
Department of Horticulture, Plant Science Building, University of Kentucky, Lexington, KY, 40546-0312, USA University of Kentucky Seed Biology Program, University of Kentucky, Lexington, Kentucky, USA
Bruce Downie*
Affiliation:
Department of Horticulture, Plant Science Building, University of Kentucky, Lexington, KY, 40546-0312, USA University of Kentucky Seed Biology Program, University of Kentucky, Lexington, Kentucky, USA
*
*Correspondence: Fax: +1 859 257 7874 Email: adownie@uky.edu
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Abstract

Raffinose family oligosaccharides (RFO) accumulate in many developing seeds and are degraded during seed germination. However, acidic α-galactosidase (AGAL) activity and subcellular location do not correlate with raffinose depletion; alkaline α-galactosidases (AGA) may be responsible for RFO hydrolysis in germinating seeds. Three cDNA clones for AGA/SEED IMBIBITION PROTEIN were obtained from the Pioneer Hi-Bred maize expressed sequence database. Two of the clones were expressed in Escherichia coli, and the recombinant proteins, when incubated with naturally occurring galactosides or p-nitrophenyl α-d-galactose, exhibited AGA activity with maximum catalysis at pH 7.5 (ZmAGA1) or pH 8.5 (ZmAGA3). No raffinose biosynthetic capacity was observed with either enzyme. Maximal α-galactosidase activity in mature dehydrated, germinating and germinated maize (Zea mays) seeds occurred at pH 7.5. ZmAGA1 was the sole family member detected in seeds and maize Hi-II, embryo-derived, callus cells. Its transcript accumulated when seed germination was interrupted by heat, cold or dehydration stress, but not in response to NaCl. Tissue prints localized transcripts to the scutellum or the embryo axis, depending on the stress applied. In maize Hi-II callus cells, transcripts accumulated when callus was subjected to heat stress (42 °C), during which ZmAGA1 transcript accumulation was further induced by sucrose. Galactosides in a variety of forms, including raffinose, partially repressed the sucrose-induced accumulation of transcript in heat-stressed callus.

Keywords

alkaline α-galactosidasegerminationmaizeraffnose family oligosaccharidesseed imbibition protein (SIP)
Type
Research Article
Information
Seed Science Research , Volume 16 , Issue 2 , June 2006 , pp. 107 - 121
Copyright
Copyright © Cambridge University Press 2006

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References

Armstrong, C.L. and Green, C.E. (1985) Establishment and maintenance of friable, embryogenic maize callus and the involvement of L-proline. Planta 164, 207–214.CrossRefGoogle ScholarPubMed
Bailly, C., Audigier, C., Ladonne, F., Wagner, M.H., Coste, F., Corbineau, F., Côme, D. (2001) Changes in oligosaccharide content and antioxidant enzyme activities in developing bean seeds as related to acquisition of drying tolerance and seed quality. Journal of Experimental Botany 52, 701–708.CrossRefGoogle ScholarPubMed
Bassel, G.W., Mullen, R.T. and Bewley, J.D. (2001) α-Galactosidase is synthesized in tomato seeds during development and is localized in the protein storage vacuoles. Canadian Journal of Botany 79, 1417–1424.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.Google Scholar
Bernal-Lugo, I. and Leopold, A.C. (1998) The dynamics of seed mortality. Journal of Experimental Botany 49, 1455–1461.Google Scholar
Black, M., Corbineau, F., Grzensik, M., Guy, P., Côme, D. (1996) Carbohydrate metabolism in the developing and maturing wheat embryo in relation to its desiccation tolerance. Journal of Experimental Botany 47, 161–169.Google Scholar
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.Google Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
Buckeridge, M.S. and Dietrich, S.M.C (1996) Mobilisation of the raffinose family oligosaccharides and galactomannan in germinating seeds of Sesbania marginata Benth. (Leguminosae-Faboideae). Plant Science 117, 33–43.CrossRefGoogle Scholar
Buitink, J., Claessens, M.M.A.E., Hemminga, M.A. and Hoekstra, F.A. (1998) Influence of water content and temperature on molecular mobility and intracellular glasses in seed and pollen. Plant Physiology 118, 531–541.Google Scholar
Buitink, J., Hemminga, M.A. and Hoekstra, F.A. (2000) Is there a role for oligosaccharides in seed longevity? An assessment of intracellular glass stability. Plant Physiology 122, 1217–1224.Google Scholar
Carmi, N., Zhang, G., Petreikov, M., Gao, Z., Eyal, Y., Granot, D. and Schaffer, A.A. (2003) Cloning and functional expression of alkaline α-galactosidase from melon fruit: Similarity to plant SIP proteins uncovers a novel family of plant glycosyl hydrolases. Plant Journal 33, 97–106.Google Scholar
Chiou, T.-J. and Bush, D.R. (1998) Sucrose is a signal molecule in assimilate partitioning. Proceedings of the National Academy of Sciences, USA 95, 4784–4788.CrossRefGoogle ScholarPubMed
Chu, C.C., Wang, C.C., Sun, C.S., Hsu, C., Yin, K.C., Chu, C.Y. and Bi, F.Y. (1975) Establishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources. Scientia Sinica 18, 659–668.Google Scholar
Corbineau, F., Picard, M.A., Fougereux, J.-A., Ladonne, F., 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.Google Scholar
Dellaporta, S.L., Wood, J. and Hicks, J.B. (1983) A plant DNA minipreparation: Version II. Plant Molecular Biology Reporter 1, 19–21.CrossRefGoogle Scholar
Denhardt, D.T. (1966) A membrane-filter technique for the detection of complementary DNA. Biochemical and Biophysical Research Communications 23, 641–646.CrossRefGoogle ScholarPubMed
Dirk, L.M.A., van der, Krol A.R., Vreugdenhil, D., Hilhorst, H.W.M. and Bewley, J.D. (1999) Galactomannan, soluble sugar, and starch mobilization following germination of Trigonella foenum-graecum L. seeds. Plant Physiology and Biochemistry 37, 41–50.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
Farrar, J., Pollock, C. and Gallagher, J. (2000) Sucrose and the integration of metabolism in vascular plants. Plant Science 154, 1–11.Google Scholar
Feinberg, A.P. and Vogelstein, B. (1983) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Analytical Biochemistry 132, 6–13.CrossRefGoogle ScholarPubMed
Feurtado, J.A., Banik, M. and Bewley, J.D. (2001) The cloning and characterization of α-galactosidase present during and following germination of tomato (Lycopersicon esculentum Mill.) seeds. Journal of Experimental Botany 52, 1239–1249.Google Scholar
Fujiki, Y., Ito, M., Nishida, I. and Watanabe, A. (2000) Multiple signaling pathways in gene expression during sugar starvation. Pharmacological analysis of din gene expression in suspension-cultured cells of Arabidopsis. Plant Physiology 124, 1139–1147.Google Scholar
Fujiki, Y., Yoshikawa, Y., Sato, T., Inada, N., Ito, M., Nishida, I. and Watanabe, A. (2001) Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiologia Plantarum 111, 345–352.CrossRefGoogle ScholarPubMed
Gao, Z. and Schaffer, A.A. (1999) A novel alkaline α-galactosidase from melon fruit with a substrate preference for raffinose. Plant Physiology 119, 979–987.Google Scholar
Golovina, E.A., Tikhonov, A.N. and Hoekstra, F.A. (1997) An electron paramagnetic resonance spin-probe study of membrane-permeability changes with seed aging. Plant Physiology 114, 383–389.CrossRefGoogle ScholarPubMed
Gurusinghe, S. and Bradford, K.J. (2001) Galactosyl-sucrose oligosaccharides and potential longevity of primed seeds. Seed Science Research 11, 121–133.Google Scholar
Haer, F.C. (1969) An introduction to chromatography on impregnated glass fiber. Ann Arbor, Michigan, Ann Arbor Science Publishers.Google Scholar
Heck, G.R, Dorsett, C., Ho, T.-H.D. (1991). Cloning and characterization of a gene, Sip1, associated with seed imbibition in barley. Accession M77475. GenBank Direct submission.Google Scholar
Henrissat, B. and Bairoch, A. (1993) New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochemical Journal 293, 781–788.Google Scholar
Herman, E.M. and Shannon, L.M. (1985) Accumulation and subcellular localization of α-galactosidase-hemagglutinin in developing soybean cotyledons. Plant Physiology 77, 886–890.CrossRefGoogle ScholarPubMed
Hoekstra, F.A., Haigh, A.M., Tetteroo, F.A.A., Van Roekel, T. (1994) Changes in soluble sugars in relation to desiccation tolerance in cauliflower seeds. Seed Science Research 4, 143–147.CrossRefGoogle Scholar
Irving, D.E., Shingleton, G.J., Hurst, P.L., Seelye, J.F. and Sinclair, B.K. (2000) Inhibition of hexokinase and expression of asparagine synthetase and α-galactosidase genes during sugar feeding and starvation of asparagus (Asparagus officinalis) callus cultures. New Zealand Journal of Crop and Horticultural Science 28, 81–88.CrossRefGoogle Scholar
Koster, K.L. (1991) Glass formation and desiccation tolerance in seeds. Plant Physiology 96, 302–304.Google Scholar
Koster, K.L. and Leopold, A.C. (1988) Sugars and desiccation tolerance in seeds. Plant Physiology 88, 829–832.Google Scholar
Kuo, T.M., Van Middlesworth, 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
Lee, R.-H., Lin, M.-C., Chen, S.-C.G. (2004) A novel alkaline α-galactosidase gene is involved in rice leaf senescence. Plant Molecular Biology 55, 281–295.CrossRefGoogle ScholarPubMed
Liu, J.J., Krenz, D.C., Galvez, A.F., 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
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
Nichols, M.B., Bancal, M.-O., Foley, M.E. and Volenec, J.J. (1993) Non-structural carbohydrates in dormant and afterripened wild oat caryopses. Physiologia Plantarum 88, 221–228.CrossRefGoogle Scholar
Ohshima, T., Hayashi, H. and Chino, M. (1990) Collection and chemical composition of pure phloem sap from Zea mays L. Plant and Cell Physiology 31, 735–737.Google Scholar
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.Google Scholar
Peterbauer, T. and Richter, A. (2001) Biochemistry and physiology of raffinose family oligosaccharides and galactosyl cyclitols in seeds. Seed Science Research 11, 185–197.Google Scholar
Peterbauer, T., Mach, L., Mucha, J. and Richter, A. (2002) Functional expression of a cDNA encoding pea (Pisum sativum L.) raffinose synthase, partial purification of the enzyme from maturing seeds, and steady-state kinetic analysis of raffinose synthesis. Planta 215, 839–846.Google Scholar
Peterbauer, T., Karner, U., Mucha, J., Mach, L., Jones, D.A., Hedley, C.L. and Richter, A. (2003) Enzymatic control of the accumulation of verbascose in pea seeds. Plant, Cell and Environment 26, 1385–1391.CrossRefGoogle Scholar
Reed, K.C. and Mann, D.A. (1985) Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Research 13, 7207–7221.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning. A laboratory manual (2nd edition). Cold Spring Harbor, New York, Cold Spring Harbor Laboratory Press.Google Scholar
Statistical Analysis Systems (SAS)(1999) Statistical analysis systems Version 8. Cary, North Carolina, SAS Institute Inc.Google Scholar
Sun, W.Q. and Leopold, A.C. (1993) The glassy state and accelerated aging of soybeans. Physiologia Plantarum 89, 767–774.Google Scholar
Sun, W.Q., Irving, T.C. and Leopold, A.C. (1994) The role of sugar, vitrification and membrane phase transition in seed desiccation tolerance. Physiologia Plantarum 90, 621–628.Google Scholar
Swofford, D.L. (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sunderland, Massachusetts, Sinauer Associates.Google Scholar
Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., Yamaguchi-Shinozaki, K. and Shinozaki, K. (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant Journal 29, 417–426.CrossRefGoogle ScholarPubMed
Thompson, J.D., Higgins, D.G. and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
Wan, C.-Y. and Wilkins, T.A. (1994) A modified hot borate method significantly enhances the yield of high quality RNA from cotton (Gossypium hirsutum L.). Analytical Biochemistry 223, 7–12.Google Scholar
Weiner, H., Blechschmidt-Schneider, S., Mohme, H., Eschrich, W. and Heldt, H.W. (1991) Phloem transport of amino acids. Comparison of amino acid contents of maize leaves and of the sieve tube exudate. Plant Physiology and Biochemistry 29, 19–23.Google Scholar
Xu, Q., Belcastro, M.P., Villa, S.T., Dinkins, R.D., Clarke, S.G. and Downie, A.B. (2004) A second protein L-isoaspartyl methyltransferase gene in Arabidopsis produces two transcripts whose products are sequestered in the nucleus. Plant Physiology 136, 2652–2664.Google Scholar
Zhao, T.-Y., Thacker, R., Corum, J.W., Snyder, J.C., Meeley, R.B., Obendorf, R.L. and Downie, B. (2004a) Expression of the maize GALACTINOL SYNTHASE gene family: (I) Expression of two different genes during seed development and germination. Physiologia Plantarum 121, 634–646.CrossRefGoogle Scholar
Zhao, T.-Y., Martin, D., Meeley, R.B. and Downie, B. (2004b) Expression of the maize GALACTINOL SYNTHASE gene family: (II) Kernel abscission, environmental stress and myo-inositol influences accumulation of transcript in developing seeds and callus cells. Physiologia Plantarum 121, 647–655.Google Scholar