Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1994 Nov;6(11):1665–1679. doi: 10.1105/tpc.6.11.1665

Sugar sensing in higher plants.

J C Jang 1, J Sheen 1
PMCID: PMC160552  PMID: 7827498

Abstract

Sugar repression of photosynthetic genes is likely a central control mechanism mediating energy homeostasis in a wide range of algae and higher plants. It overrides light activation and is coupled to developmental and environmental regulations. How sugar signals are sensed and transduced to the nucleus remains unclear. To elucidate sugar-sensing mechanisms, we monitored the effects of a variety of sugars, glucose analogs, and metabolic intermediates on photosynthetic fusion genes in a sensitive and versatile maize protoplast transient expression system. The results show that sugars that are the substrates of hexokinase (HK) cause repression at a low concentration (1 to 10 mM), indicating a low degree of specificity and the irrelevance of osmotic change. Studies with various glucose analogs suggest that glucose transport across the plasma membrane is necessary but not sufficient to trigger repression, whereas subsequent phosphorylation by HK may be required. The effectiveness of 2-deoxyglucose, a nonmetabolizable glucose analog, and the ineffectiveness of various metabolic intermediates in eliciting repression eliminate the involvement of glycolysis and other metabolic pathways. Replenishing intracellular phosphate and ATP diminished by hexoses does not overcome repression. Because mannoheptulose, a specific HK inhibitor, blocks the severe repression triggered by 2-deoxyglucose and yet the phosphorylated products per se do not act as repression signals, we propose that HK may have dual functions and may act as a key sensor and signal transmitter of sugar repression in higher plants.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Azcón-Bieto J. Inhibition of photosynthesis by carbohydrates in wheat leaves. Plant Physiol. 1983 Nov;73(3):681–686. doi: 10.1104/pp.73.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bessell E. M., Thomas P. The deoxyfluoro-D-glucopyranose 6-phosphates and their effect on yeast glucose phosphate isomerase. Biochem J. 1973 Jan;131(1):77–82. doi: 10.1042/bj1310077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bessell E. M., Thomas P. The effect of substitution at C-2 of D-glucose 6-phosphate on the rate of dehydrogenation by glucose 6-phosphate dehydrogenase (from yeast and from rat liver). Biochem J. 1973 Jan;131(1):83–89. doi: 10.1042/bj1310083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brun T., Roche E., Kim K. H., Prentki M. Glucose regulates acetyl-CoA carboxylase gene expression in a pancreatic beta-cell line (INS-1). J Biol Chem. 1993 Sep 5;268(25):18905–18911. [PubMed] [Google Scholar]
  5. Carlson M. Regulation of sugar utilization in Saccharomyces species. J Bacteriol. 1987 Nov;169(11):4873–4877. doi: 10.1128/jb.169.11.4873-4877.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carlson S. G., Fawcett T. W., Bartlett J. D., Bernier M., Holbrook N. J. Regulation of the C/EBP-related gene gadd153 by glucose deprivation. Mol Cell Biol. 1993 Aug;13(8):4736–4744. doi: 10.1128/mcb.13.8.4736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cheng C. L., Acedo G. N., Cristinsin M., Conkling M. A. Sucrose mimics the light induction of Arabidopsis nitrate reductase gene transcription. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1861–1864. doi: 10.1073/pnas.89.5.1861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cherry J. R., Johnson T. R., Dollard C., Shuster J. R., Denis C. L. Cyclic AMP-dependent protein kinase phosphorylates and inactivates the yeast transcriptional activator ADR1. Cell. 1989 Feb 10;56(3):409–419. doi: 10.1016/0092-8674(89)90244-4. [DOI] [PubMed] [Google Scholar]
  9. Dickinson C. D., Altabella T., Chrispeels M. J. Slow-growth phenotype of transgenic tomato expressing apoplastic invertase. Plant Physiol. 1991 Feb;95(2):420–425. doi: 10.1104/pp.95.2.420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Entian K. D., Barnett J. A. Regulation of sugar utilization by Saccharomyces cerevisiae. Trends Biochem Sci. 1992 Dec;17(12):506–510. doi: 10.1016/0968-0004(92)90341-6. [DOI] [PubMed] [Google Scholar]
  11. Entian K. D., Fröhlich K. U. Saccharomyces cerevisiae mutants provide evidence of hexokinase PII as a bifunctional enzyme with catalytic and regulatory domains for triggering carbon catabolite repression. J Bacteriol. 1984 Apr;158(1):29–35. doi: 10.1128/jb.158.1.29-35.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Entian K. D. Genetic and biochemical evidence for hexokinase PII as a key enzyme involved in carbon catabolite repression in yeast. Mol Gen Genet. 1980;178(3):633–637. doi: 10.1007/BF00337871. [DOI] [PubMed] [Google Scholar]
  13. Entian K. D., Hilberg F., Opitz H., Mecke D. Cloning of hexokinase structural genes from Saccharomyces cerevisiae mutants with regulatory mutations responsible for glucose repression. Mol Cell Biol. 1985 Nov;5(11):3035–3040. doi: 10.1128/mcb.5.11.3035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gancedo J. M. Carbon catabolite repression in yeast. Eur J Biochem. 1992 Jun 1;206(2):297–313. doi: 10.1111/j.1432-1033.1992.tb16928.x. [DOI] [PubMed] [Google Scholar]
  15. Gerhardt R., Stitt M., Heldt H. W. Subcellular Metabolite Levels in Spinach Leaves : Regulation of Sucrose Synthesis during Diurnal Alterations in Photosynthetic Partitioning. Plant Physiol. 1987 Feb;83(2):399–407. doi: 10.1104/pp.83.2.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. German M. S. Glucose sensing in pancreatic islet beta cells: the key role of glucokinase and the glycolytic intermediates. Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1781–1785. doi: 10.1073/pnas.90.5.1781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. German M. S., Moss L. G., Rutter W. J. Regulation of insulin gene expression by glucose and calcium in transfected primary islet cultures. J Biol Chem. 1990 Dec 25;265(36):22063–22066. [PubMed] [Google Scholar]
  18. Goldschmidt E. E., Huber S. C. Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiol. 1992 Aug;99(4):1443–1448. doi: 10.1104/pp.99.4.1443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Graham I. A., Denby K. J., Leaver C. J. Carbon Catabolite Repression Regulates Glyoxylate Cycle Gene Expression in Cucumber. Plant Cell. 1994 May;6(5):761–772. doi: 10.1105/tpc.6.5.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Graham I. A., Leaver C. J., Smith S. M. Induction of Malate Synthase Gene Expression in Senescent and Detached Organs of Cucumber. Plant Cell. 1992 Mar;4(3):349–357. doi: 10.1105/tpc.4.3.349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hammonds P., Schofield P. N., Ashcroft S. J. Glucose regulates preproinsulin messenger RNA levels in a clonal cell line of simian virus 40-transformed B cells. FEBS Lett. 1987 Mar 9;213(1):149–154. doi: 10.1016/0014-5793(87)81481-3. [DOI] [PubMed] [Google Scholar]
  22. Hoffman C. S., Winston F. Glucose repression of transcription of the Schizosaccharomyces pombe fbp1 gene occurs by a cAMP signaling pathway. Genes Dev. 1991 Apr;5(4):561–571. doi: 10.1101/gad.5.4.561. [DOI] [PubMed] [Google Scholar]
  23. Kim S. R., Costa M. A., An G. H. Sugar response element enhances wound response of potato proteinase inhibitor II promoter in transgenic tobacco. Plant Mol Biol. 1991 Nov;17(5):973–983. doi: 10.1007/BF00037137. [DOI] [PubMed] [Google Scholar]
  24. Komor E., Schobert C., Cho B. H. Sugar specificity and sugar-proton interaction for the hexose-proton-symport system of Chlorella. Eur J Biochem. 1985 Feb 1;146(3):649–656. doi: 10.1111/j.1432-1033.1985.tb08700.x. [DOI] [PubMed] [Google Scholar]
  25. Lin W. Potassium and Phosphate Uptake in Corn Roots: Further Evidence for an Electrogenic H/K Exchanger and an OH/Pi Antiporter. Plant Physiol. 1979 May;63(5):952–955. doi: 10.1104/pp.63.5.952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lin W., Schmitt M. R., Hitz W. D., Giaquinta R. T. Sugar transport into protoplasts isolated from developing soybean cotyledons : I. Protoplast isolation and general characteristics of sugar transport. Plant Physiol. 1984 Aug;75(4):936–940. doi: 10.1104/pp.75.4.936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Loza-Tavera H., Martínez-Barajas E., Sánchez-de-Jiménez E. Regulation of ribulose-1,5-bisphosphate carboxylase expression in second leaves of maize seedlings from low and high yield populations. Plant Physiol. 1990 Jun;93(2):541–548. doi: 10.1104/pp.93.2.541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ma H., Bloom L. M., Walsh C. T., Botstein D. The residual enzymatic phosphorylation activity of hexokinase II mutants is correlated with glucose repression in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Dec;9(12):5643–5649. doi: 10.1128/mcb.9.12.5643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ma H., Botstein D. Effects of null mutations in the hexokinase genes of Saccharomyces cerevisiae on catabolite repression. Mol Cell Biol. 1986 Nov;6(11):4046–4052. doi: 10.1128/mcb.6.11.4046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Marie S., Diaz-Guerra M. J., Miquerol L., Kahn A., Iynedjian P. B. The pyruvate kinase gene as a model for studies of glucose-dependent regulation of gene expression in the endocrine pancreatic beta-cell type. J Biol Chem. 1993 Nov 15;268(32):23881–23890. [PubMed] [Google Scholar]
  31. Miernyk J. A., Dennis D. T. Mitochondrial, plastid, and cytosolic isozymes of hexokinase from developing endosperm of Ricinus communis. Arch Biochem Biophys. 1983 Oct 15;226(2):458–468. doi: 10.1016/0003-9861(83)90315-6. [DOI] [PubMed] [Google Scholar]
  32. Nelson T., Harpster M. H., Mayfield S. P., Taylor W. C. Light-regulated gene expression during maize leaf development. J Cell Biol. 1984 Feb;98(2):558–564. doi: 10.1083/jcb.98.2.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Newgard C. B. Cellular engineering for the treatment of metabolic disorders: prospects for therapy in diabetes. Biotechnology (N Y) 1992 Oct;10(10):1112–1120. doi: 10.1038/nbt1092-1112. [DOI] [PubMed] [Google Scholar]
  34. Pelham H. R. Control of protein exit from the endoplasmic reticulum. Annu Rev Cell Biol. 1989;5:1–23. doi: 10.1146/annurev.cb.05.110189.000245. [DOI] [PubMed] [Google Scholar]
  35. Plaut Z., Mayoral M. L., Reinhold L. Effect of altered sink: source ratio on photosynthetic metabolism of source leaves. Plant Physiol. 1987 Nov;85(3):786–791. doi: 10.1104/pp.85.3.786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rose M., Albig W., Entian K. D. Glucose repression in Saccharomyces cerevisiae is directly associated with hexose phosphorylation by hexokinases PI and PII. Eur J Biochem. 1991 Aug 1;199(3):511–518. doi: 10.1111/j.1432-1033.1991.tb16149.x. [DOI] [PubMed] [Google Scholar]
  37. SALAS J., SALAS M., VINUELA E., SOLS A. GLUCOKINASE OF RABBIT LIVER. J Biol Chem. 1965 Mar;240:1014–1018. [PubMed] [Google Scholar]
  38. Saier M. H., Jr A multiplicity of potential carbon catabolite repression mechanisms in prokaryotic and eukaryotic microorganisms. New Biol. 1991 Dec;3(12):1137–1147. [PubMed] [Google Scholar]
  39. Schäffner A. R., Sheen J. Maize rbcS promoter activity depends on sequence elements not found in dicot rbcS promoters. Plant Cell. 1991 Sep;3(9):997–1012. doi: 10.1105/tpc.3.9.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sheen J. Metabolic repression of transcription in higher plants. Plant Cell. 1990 Oct;2(10):1027–1038. doi: 10.1105/tpc.2.10.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sheen J. Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell. 1991 Mar;3(3):225–245. doi: 10.1105/tpc.3.3.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sheen J. Protein phosphatase activity is required for light-inducible gene expression in maize. EMBO J. 1993 Sep;12(9):3497–3505. doi: 10.1002/j.1460-2075.1993.tb06024.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sonnewald U., Brauer M., von Schaewen A., Stitt M., Willmitzer L. Transgenic tobacco plants expressing yeast-derived invertase in either the cytosol, vacuole or apoplast: a powerful tool for studying sucrose metabolism and sink/source interactions. Plant J. 1991 Jul;1(1):95–106. doi: 10.1111/j.1365-313x.1991.00095.x. [DOI] [PubMed] [Google Scholar]
  44. Stock J. Protein phosphorylation: phosphoprotein talk. Curr Biol. 1993 May 1;3(5):303–305. doi: 10.1016/0960-9822(93)90186-r. [DOI] [PubMed] [Google Scholar]
  45. Sturm A., Chrispeels M. J. cDNA cloning of carrot extracellular beta-fructosidase and its expression in response to wounding and bacterial infection. Plant Cell. 1990 Nov;2(11):1107–1119. doi: 10.1105/tpc.2.11.1107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Tal M., Wu Y. J., Leiser M., Surana M., Lodish H., Fleischer N., Weir G., Efrat S. [Val12] HRAS downregulates GLUT2 in beta cells of transgenic mice without affecting glucose homeostasis. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5744–5748. doi: 10.1073/pnas.89.13.5744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Thevelein J. M. Fermentable sugars and intracellular acidification as specific activators of the RAS-adenylate cyclase signalling pathway in yeast: the relationship to nutrient-induced cell cycle control. Mol Microbiol. 1991 Jun;5(6):1301–1307. doi: 10.1111/j.1365-2958.1991.tb00776.x. [DOI] [PubMed] [Google Scholar]
  48. Thevelein J. M. The RAS-adenylate cyclase pathway and cell cycle control in Saccharomyces cerevisiae. Antonie Van Leeuwenhoek. 1992 Aug;62(1-2):109–130. doi: 10.1007/BF00584466. [DOI] [PubMed] [Google Scholar]
  49. Thorens B., Weir G. C., Leahy J. L., Lodish H. F., Bonner-Weir S. Reduced expression of the liver/beta-cell glucose transporter isoform in glucose-insensitive pancreatic beta cells of diabetic rats. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6492–6496. doi: 10.1073/pnas.87.17.6492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Tubbe A., Buckhout T. J. In Vitro Analysis of the H-Hexose Symporter on the Plasma Membrane of Sugarbeets (Beta vulgaris L.). Plant Physiol. 1992 Jul;99(3):945–951. doi: 10.1104/pp.99.3.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Weiner H., McMichael R. W., Huber S. C. Identification of factors regulating the phosphorylation status of sucrose-phosphate synthase in vivo. Plant Physiol. 1992 Aug;99(4):1435–1442. doi: 10.1104/pp.99.4.1435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Welsh M., Nielsen D. A., MacKrell A. J., Steiner D. F. Control of insulin gene expression in pancreatic beta-cells and in an insulin-producing cell line, RIN-5F cells. II. Regulation of insulin mRNA stability. J Biol Chem. 1985 Nov 5;260(25):13590–13594. [PubMed] [Google Scholar]
  53. Zimmermann F. K., Scheel I. Mutants of Saccharomyces cerevisiae resistant to carbon catabolite repression. Mol Gen Genet. 1977 Jul 7;154(1):75–82. doi: 10.1007/BF00265579. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES