Skip to main content
Log in

Gene expression studies on developing kernels of maize sucrose synthase (SuSy) mutants show evidence for a third SuSy gene

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Previous studies have identified two tissue- and cell-specific, yet functionally redundant, sucrose synthase (SuSy) genes, Sh1 and Sus1, which encode biochemically similar isozymes, SH1 and SUS1 (previously referred to as SS1 and SS2, respectively). Here we report evidence for a third SuSy gene in maize, Sus3, which is more similar to dicot than to monocot SuSys. RNA and/or protein blot analyses on developing kernels and other tissues show evidence of expression of Sus3, although at the lowest steady-state levels of the three SuSy gene products and without a unique pattern of tissue specificity. Immunoblots of sh1sus1-1 embryos that are either lacking or deficient for the embryo-specific SUS1 protein have shown a protein band which we attribute to the Sus3 gene, and may contribute to the residual enzyme activity seen in embryos of the double mutant. We also studied developing seeds of the double mutant sh1sus1-1, which is missing 99.5% of SuSy enzyme activity, for evidence of co-regulation of several genes of sugar metabolism. We found a significant reduction in the steady-state levels of Miniature-1 encoded cell wall invertase2, and Sucrose transporter (Sut) mRNAs in the double mutant, relative to the lineage-related sh1Sus1 and sh1Sus1 kernels. Down-regulation of the Mn1 gene was also reflected in significant reductions in cell wall invertase activity. Co-regulatory changes were not seen in the expression of Sucrose phosphate synthase, UDP-glucose pyrophosphorylase, and ADP-glucose pyrophosphorylase.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Altschul, S.F., Madden, T.L., Schäffer, A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389-3402.

    Google Scholar 

  • Amor, Y., Haigler, C.H., Johnson, S., Wainscott, M. and Delmer, D.P. 1995. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc. Natl. Acad. Sci. USA 92: 9353-9357.

    Google Scholar 

  • Aoki, N., Hirose, T., Takahashi, S., Ono, K., Ishimaru, K. and Ohsugi, R. 1999. Molecular cloning and expression analysis of a gene for a sucrose transporter in maize (Zea mays L.). Plant Cell Physiol. 40: 1072-1078.

    Google Scholar 

  • Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. and Struhl, K. 1993. Current Protocols in Molecular Biology. John Wiley, New York.

    Google Scholar 

  • Buczynski, S.R., Thom, M., Chourey, P.S. and Maretzki, A. 1993. Tissue distribution and characterization of sucrose synthase isozymes in sugarcane. J. Plant Physiol. 142: 641-646.

    Google Scholar 

  • Carlson, S.J. and Chourey, P.S. 1996. Evidence of plasma membrane-associated forms of sucrose synthase in maize. Mol. Gen. Genet. 252: 303-310.

    Google Scholar 

  • Carlson, S.J. and Chourey, P.S. 1999. A re-evaluation of the relative roles of two invertases, Incw2 and IVR1, in developing maize kernels and other tissues. Plant Physiol. 121: 1025-1035.

    Google Scholar 

  • Carlson, S.J., Shanker, S. and Chourey, P.S. 2000. A point mutation at the Miniature1 seed locus reduces levels of the encoded protein, but not its mRNA, in maize. Mol. Gen. Genet. 263: 367-373.

    Google Scholar 

  • Cheng, W.-H. and Chourey, P.S. 1999. Genetic evidence that invertase mediated release of hexoses is critical for appropriate carbon partitioning and normal seed development in maize. Theor. Appl. Genet. 98: 485-495.

    Google Scholar 

  • Cheng, W.-H., Taliercio, E.W. and Chourey, P.S. 1996. The Miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel. Plant Cell 8: 971-983.

    Google Scholar 

  • Chengappa, S., Guilleroux, M., Phillips, W. and Shields, R. 1999. Transgenic tomato plants with decreased sucrose synthase are unaltered in starch and sugar accumulation in the fruit. Plant Mol. Biol. 40: 213-221.

    Google Scholar 

  • Chourey, P.S. 1981. Genetic control of sucrose synthetase in maize endosperm. Mol. Gen. Genet. 184: 372-376.

    Google Scholar 

  • Chourey, P.S. and Nelson, O.E. 1976. The enzymatic deficiency conditioned by the shrunken-1 mutations in maize. Biochem. Genet. 14: 1041-1054.

    Google Scholar 

  • Chourey, P.S. and Nelson, O.E. 1979. Interallelic complementation at the sh locus in maize at the enzyme level. Genetics 91: 317-325.

    Google Scholar 

  • Chourey, P.S. and Taliercio, E.W. 1994. Epistatic interaction and functional compensation between the two tissue-and cell-specific sucrose synthase genes in maize. Proc. Natl. Acad. Sci. USA 91: 7917-7921.

    Google Scholar 

  • Chourey, P.S., DeRobertis, G.A. and Still, P.E. 1988. Altered tissue specificity of the revertant shrunken allele upon DS excision is associated with loss of expression and molecular rearrangement at the corresponding non-allelic isozyme locus in maize. Mol. Gen. Genet. 214: 300-306.

    Google Scholar 

  • Chourey, P.S., Chen, Y.-C. and Miller, M.E. 1991a. Early cell degeneration in developing endosperm is unique to the shrunken mutation in maize. Maydica 36: 141-146.

    Google Scholar 

  • Chourey, P.S., Taliercio, E.W. and Kane, E.J. 1991b. Tissue specific expression and anaerobically induced posttranscriptional modulation of sucrose synthase genes in Sorghum bicolor M. Plant Physiol. 96: 485-490.

    Google Scholar 

  • Chourey, P.S., Taliercio, E.W., Carlson, S.J. and Ruan, Y.-L. 1998. Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Mol. Gen. Genet. 259: 88-96.

    Google Scholar 

  • D'Aoust, M.-A., Yelle, S. and Nguyen-Quoc, B. 1999. Antisense inhibition of tomato fruit sucrose synthase decreases fruit setting and the sucrose unloading capacity of young fruit. Plant Cell 11: 2407-2418.

    Google Scholar 

  • Doehlert, D.C. and Kuo, T.M. 1990. Sugar metabolism in developing kernels of starch-deficient endosperm mutants of maize. Plant Physiol. 92: 990-994.

    Google Scholar 

  • Fu, H. and Park, W.D. 1995. Sink-and vascular-associated sucrose synthase functions are encoded by different gene classes in potato. Plant Cell 7: 1369-1385.

    Google Scholar 

  • Gai, X., Lal, S., Xing, L., Brendel, V. and Walbot, V. 2000. Gene discovery using the maize genome database ZmDB. Nucl. Acids Res. 28: 94-96.

    Google Scholar 

  • Giroux, M.J. and Hannah, L.C. 1994. ADP-glucopyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Mol. Gen. Genet. 243: 400-408.

    Google Scholar 

  • Guerin, J. and Carbonero, P. 1997. The spatial distribution of sucrose synthase isozymes in barley. Plant Physiol. 114: 55-62.

    Google Scholar 

  • Gupta, M., Chourey, P.S., Burr, B. and Still, P.E. 1988. cDNAs of two non-allelic sucrose synthase genes in maize: cloning, expression, characterization and molecular mapping of sucrose synthase-2 gene. Plant Mol. Biol. 10: 215-224.

    Google Scholar 

  • Heim, U., Weber, H., Baumlein, H. and Wobus, U. 1993. A sucrose synthase gene of Vicia faba L.; expression pattern in developing seeds in relation to starch synthesis and metabolic regulation. Planta 191: 394-401.

    Google Scholar 

  • Hesse, H. and Willmitzer, L. 1996. Expression analysis of a sucrose synthase gene from sugar beet (Beta vulgaris L.). Plant Mol. Biol. 30: 863-872.

    Google Scholar 

  • Hofmann, K. and Stoffel, W. 1993. Tmbase: a database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 347: 166.

    Google Scholar 

  • Huber, S.C., Huber, J.L., Liao, P.-C., Gage, D.A., McMichael, R.J. Jr., Chourey, P.S., Hannah, L.C. and Koch, K. 1996. Phosphorylation of serine-15 of maize leaf sucrose synthase: occurrence in vivo and possible regulatory significance. Plant Physiol 112: 793-802.

    Google Scholar 

  • Im, K.H. 1996. Regulation of sucrose phosphate synthase expression in maize. Ph.D. thesis, University of Florida, Gainesville.

    Google Scholar 

  • Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680.

    Google Scholar 

  • Marana, C., Gracia-Olmedo, F. and Carbonero, P. 1988. Linked sucrose synthase genes in group-7 chromosomes in hexaploid wheat (Triticum aestivum L.). Gene 63: 253-260.

    Google Scholar 

  • Martin, T., Frommer, W.B., Salanonbat, M. and Willmitzer, L. 1993. Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs. Plant J 4: 367-377.

    Google Scholar 

  • McCarty D.R., Shaw J.R. and Hannah L.C. 1986. The cloning, genetic mapping, and expression of the constitutive sucrose synthase locus of maize. Proc. Natl. Acad. Sci. USA 83: 9099-9103.

    Google Scholar 

  • McElfresh, K.C. and Chourey, P.S. 1988. Anaerobiosis induces transcription but not translation of sucrose synthase in maize. Plant Physiol 87: 542-546.

    Google Scholar 

  • Miller M.E. and Chourey, P.S. 1992. The maize invertase-deficient minature-1 seed mutation is associated with aberrant pedicel and endosperm development. Plant Cell 4: 297-305.

    Google Scholar 

  • Page, R.D.M. 1996. TreeView for Macintosh, version 1.3. Published electronically on the Internet, available at http://taxonomy.zoology.gla.ac.uk/rod/treeview.html

  • Ruan, Y.-L. and Chourey, P.S. 1998. A fiberless seed mutation in cotton is associated with lack of fiber cell initiation in ovule epidermis and alterations in sucrose synthase expression and carbon partitioning in developing seeds. Plant Physiol 118: 399-406.

    Google Scholar 

  • Scott, P. and Chourey, P.S. 2000. Metabolic analyses of a double mutant of sucrose synthase (SuSy) genes in developing endosperm. Maize Genetics Conference Abstracts, Coeur d'Alene, Idaho.

  • Sebkova, V., Unger, C., Hardegger, M. and Sturm, A. 1995. Biochemical, physiological and molecular characterization of sucrose synthase from Daucus carota. Plant Physiol. 108: 75-83.

    Google Scholar 

  • Shaw, J.R., Ferl, R.J., Baier, J., St. Clair, D., Carson, C., McCarty, D.R. and Hannah, L.C. 1994. Structural features of the maize sus1 gene and protein. Plant Physiol. 106: 1659-1663.

    Google Scholar 

  • Sowokinos, J.R., Thomas, C. and Burrell, M.M. 1997. Pyrophosphorylases in potato. V. Allelic polymorphism of UGP-glucose pyrophosphorylase in potato cultivars and its association with tuber resistance to sweetening in the cold. Plant Physiol 113: 511-517.

    Google Scholar 

  • Springer, B., Werr, W., Starlinger, P., Bennett, D.C., Zokolica, M. and Freeling, M. 1986. The shrunken gene on chromosome 9 of Zea mays L. is expressed in various plant tissues and encodes an anaerobic protein. Mol. Gen. Genet. 205: 461-468.

    Google Scholar 

  • Tang, Q.-Q. and Sturm, A. 1999. Antisense repression of sucrose synthase in carrot (Daucus carota L.) affects growth rather than sucrose partitioning. Plant Mol. Biol. 41: 465-479.

    Google Scholar 

  • Thompson, J.D., Higgins, D.G. and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673-4680.

    Google Scholar 

  • Tsai, C.Y., Salamini, F. and Nelson, O.E. 1970. Enzymes of carbohydrate metabolism in the developing endosperm of maize. Plant Physiol. 46: 299-306.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Prem S. Chourey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carlson, S.J., Chourey, P.S., Helentjaris, T. et al. Gene expression studies on developing kernels of maize sucrose synthase (SuSy) mutants show evidence for a third SuSy gene. Plant Mol Biol 49, 15–29 (2002). https://doi.org/10.1023/A:1014457901992

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1014457901992

Navigation