Abstract
The mechanisms by which higher plants recognize and respond to sugars are largely unknown. Here, we present evidence that the first enzyme in the hexose assimilation pathway, hexokinase (HXK), acts as a sensor for plant sugar responses. Transgenic Arabidopsis plants expressing antisense hexokinase (AtHXK) genes are sugar hyposensitive, whereas plants overexpressing AtHXK are sugar hypersensitive. The transgenic plants exhibited a wide spectrum of altered sugar responses in seedling development and in gene activation and repression. Furthermore, overexpressing the yeast sugar sensor YHXK2 caused a dominant negative effect by elevating HXK catalytic activity but reducing sugar sensitivity in transgenic plants. The result suggests that HXK is a dual-function enzyme with a distinct regulatory function not interchangeable between plants and yeast.
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- Bork P., Sander C., Valencia A. Convergent evolution of similar enzymatic function on different protein folds: the hexokinase, ribokinase, and galactokinase families of sugar kinases. Protein Sci. 1993 Jan;2(1):31–40. doi: 10.1002/pro.5560020104. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Brusslan J. A., Tobin E. M. Light-independent developmental regulation of cab gene expression in Arabidopsis thaliana seedlings. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7791–7795. doi: 10.1073/pnas.89.16.7791. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen M. H., Liu L. F., Chen Y. R., Wu H. K., Yu S. M. Expression of alpha-amylases, carbohydrate metabolism, and autophagy in cultured rice cells is coordinately regulated by sugar nutrient. Plant J. 1994 Nov;6(5):625–636. doi: 10.1046/j.1365-313x.1994.6050625.x. [DOI] [PubMed] [Google Scholar]
- 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]
- Chevalier C., Bourgeois E., Pradet A., Raymond P. Molecular cloning and characterization of six cDNAs expressed during glucose starvation in excised maize (Zea mays L.) root tips. Plant Mol Biol. 1995 Jun;28(3):473–485. doi: 10.1007/BF00020395. [DOI] [PubMed] [Google Scholar]
- Chory J. Out of darkness: mutants reveal pathways controlling light-regulated development in plants. Trends Genet. 1993 May;9(5):167–172. doi: 10.1016/0168-9525(93)90163-c. [DOI] [PubMed] [Google Scholar]
- Czakó M., Jang J. C., Herr J. M., Jr, Márton L. Differential manifestation of seed mortality induced by seed-specific expression of the gene for diphtheria toxin A chain in Arabidopsis and tobacco. Mol Gen Genet. 1992 Oct;235(1):33–40. doi: 10.1007/BF00286178. [DOI] [PubMed] [Google Scholar]
- Dai N., Schaffer A. A., Petreikov M., Granot D. Arabidopsis thaliana hexokinase cDNA isolated by complementation of yeast cells. Plant Physiol. 1995 Jun;108(2):879–880. doi: 10.1104/pp.108.2.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dangl J. L., Preuss D., Schroeder J. I. Talking through walls: signaling in plant development. Cell. 1995 Dec 29;83(7):1071–1077. doi: 10.1016/0092-8674(95)90134-5. [DOI] [PubMed] [Google Scholar]
- DeWald D. B., Sadka A., Mullet J. E. Sucrose Modulation of Soybean Vsp Gene Expression Is Inhibited by Auxin. Plant Physiol. 1994 Feb;104(2):439–444. doi: 10.1104/pp.104.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deng X. W. Fresh view of light signal transduction in plants. Cell. 1994 Feb 11;76(3):423–426. doi: 10.1016/0092-8674(94)90107-4. [DOI] [PubMed] [Google Scholar]
- 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]
- Efrat S., Tal M., Lodish H. F. The pancreatic beta-cell glucose sensor. Trends Biochem Sci. 1994 Dec;19(12):535–538. doi: 10.1016/0968-0004(94)90056-6. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- 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]
- Flavell R. B. Inactivation of gene expression in plants as a consequence of specific sequence duplication. Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3490–3496. doi: 10.1073/pnas.91.9.3490. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Gietz D., St Jean A., Woods R. A., Schiestl R. H. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 1992 Mar 25;20(6):1425–1425. doi: 10.1093/nar/20.6.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Granner D., Pilkis S. The genes of hepatic glucose metabolism. J Biol Chem. 1990 Jun 25;265(18):10173–10176. [PubMed] [Google Scholar]
- Grupe A., Hultgren B., Ryan A., Ma Y. H., Bauer M., Stewart T. A. Transgenic knockouts reveal a critical requirement for pancreatic beta cell glucokinase in maintaining glucose homeostasis. Cell. 1995 Oct 6;83(1):69–78. doi: 10.1016/0092-8674(95)90235-x. [DOI] [PubMed] [Google Scholar]
- Huber S. C., Hanson K. R. Carbon Partitioning and Growth of a Starchless Mutant of Nicotiana sylvestris. Plant Physiol. 1992 Aug;99(4):1449–1454. doi: 10.1104/pp.99.4.1449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jang J. C., Sheen J. Sugar sensing in higher plants. Plant Cell. 1994 Nov;6(11):1665–1679. doi: 10.1105/tpc.6.11.1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kim S. Y., May G. D., Park W. D. Nuclear protein factors binding to a class I patatin promoter region are tuber-specific and sucrose-inducible. Plant Mol Biol. 1994 Oct;26(2):603–615. doi: 10.1007/BF00013747. [DOI] [PubMed] [Google Scholar]
- Knight J. S., Gray J. C. Expression of genes encoding the tobacco chloroplast phosphate translocator is not light-regulated and is repressed by sucrose. Mol Gen Genet. 1994 Mar;242(5):586–594. doi: 10.1007/BF00285282. [DOI] [PubMed] [Google Scholar]
- Lam H. M., Peng S. S., Coruzzi G. M. Metabolic regulation of the gene encoding glutamine-dependent asparagine synthetase in Arabidopsis thaliana. Plant Physiol. 1994 Dec;106(4):1347–1357. doi: 10.1104/pp.106.4.1347. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu X. J., Prat S., Willmitzer L., Frommer W. B. cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I patatin promoter/GUS-gene fusion. Mol Gen Genet. 1990 Sep;223(3):401–406. doi: 10.1007/BF00264446. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Maas C., Schaal S., Werr W. A feedback control element near the transcription start site of the maize Shrunken gene determines promoter activity. EMBO J. 1990 Nov;9(11):3447–3452. doi: 10.1002/j.1460-2075.1990.tb07552.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Magnuson M. A., Andreone T. L., Printz R. L., Koch S., Granner D. K. Rat glucokinase gene: structure and regulation by insulin. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4838–4842. doi: 10.1073/pnas.86.13.4838. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matschinsky F., Liang Y., Kesavan P., Wang L., Froguel P., Velho G., Cohen D., Permutt M. A., Tanizawa Y., Jetton T. L. Glucokinase as pancreatic beta cell glucose sensor and diabetes gene. J Clin Invest. 1993 Nov;92(5):2092–2098. doi: 10.1172/JCI116809. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Minet M., Dufour M. E., Lacroute F. Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 1992 May;2(3):417–422. doi: 10.1111/j.1365-313x.1992.00417.x. [DOI] [PubMed] [Google Scholar]
- Mita S., Suzuki-Fujii K., Nakamura K. Sugar-inducible expression of a gene for beta-amylase in Arabidopsis thaliana. Plant Physiol. 1995 Mar;107(3):895–904. doi: 10.1104/pp.107.3.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mol J. N., van der Krol A. R., van Tunen A. J., van Blokland R., de Lange P., Stuitje A. R. Regulation of plant gene expression by antisense RNA. FEBS Lett. 1990 Aug 1;268(2):427–430. doi: 10.1016/0014-5793(90)81298-3. [DOI] [PubMed] [Google Scholar]
- Mueckler M. Glucokinase, glucose sensing, and diabetes. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):784–785. doi: 10.1073/pnas.90.3.784. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakamura K., Ohto M. A., Yoshida N., Nakamura K. Sucrose-Induced Accumulation of beta-Amylase Occurs Concomitant with the Accumulation of Starch and Sporamin in Leaf-Petiole Cuttings of Sweet Potato. Plant Physiol. 1991 Jul;96(3):902–909. doi: 10.1104/pp.96.3.902. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nam H. G., Giraudat J., Den Boer B., Moonan F., Loos WDB., Hauge B. M., Goodman H. M. Restriction Fragment Length Polymorphism Linkage Map of Arabidopsis thaliana. Plant Cell. 1989 Jul;1(7):699–705. doi: 10.1105/tpc.1.7.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nishi S., Stoffel M., Xiang K., Shows T. B., Bell G. I., Takeda J. Human pancreatic beta-cell glucokinase: cDNA sequence and localization of the polymorphic gene to chromosome 7, band p 13. Diabetologia. 1992 Aug;35(8):743–747. doi: 10.1007/BF00429094. [DOI] [PubMed] [Google Scholar]
- Prior C., Mamessier P., Fukuhara H., Chen X. J., Wesolowski-Louvel M. The hexokinase gene is required for transcriptional regulation of the glucose transporter gene RAG1 in Kluyveromyces lactis. Mol Cell Biol. 1993 Jul;13(7):3882–3889. doi: 10.1128/mcb.13.7.3882. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reynolds S. J., Smith S. M. Regulation of expression of the cucumber isocitrate lyase gene in cotyledons upon seed germination and by sucrose. Plant Mol Biol. 1995 Dec;29(5):885–896. doi: 10.1007/BF00014963. [DOI] [PubMed] [Google Scholar]
- Rodermel S. R., Abbott M. S., Bogorad L. Nuclear-organelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell. 1988 Nov 18;55(4):673–681. doi: 10.1016/0092-8674(88)90226-7. [DOI] [PubMed] [Google Scholar]
- Sadka A., DeWald D. B., May G. D., Park W. D., Mullet J. E. Phosphate Modulates Transcription of Soybean VspB and Other Sugar-Inducible Genes. Plant Cell. 1994 May;6(5):737–749. doi: 10.1105/tpc.6.5.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saier M. H., Jr, Chauvaux S., Deutscher J., Reizer J., Ye J. J. Protein phosphorylation and regulation of carbon metabolism in gram-negative versus gram-positive bacteria. Trends Biochem Sci. 1995 Jul;20(7):267–271. doi: 10.1016/s0968-0004(00)89041-6. [DOI] [PubMed] [Google Scholar]
- Saier M. H., Jr, Wu L. F., Reizer J. Regulation of bacterial physiological processes by three types of protein phosphorylating systems. Trends Biochem Sci. 1990 Oct;15(10):391–395. doi: 10.1016/0968-0004(90)90238-7. [DOI] [PubMed] [Google Scholar]
- Schmidt R., West J., Love K., Lenehan Z., Lister C., Thompson H., Bouchez D., Dean C. Physical map and organization of Arabidopsis thaliana chromosome 4. Science. 1995 Oct 20;270(5235):480–483. doi: 10.1126/science.270.5235.480. [DOI] [PubMed] [Google Scholar]
- 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]
- Smith S. B., Taylor M. A., Burch L. R., Davies H. V. Primary structure and characterization of a cDNA clone of fructokinase from potato (Solanum tuberosum L. cv record). Plant Physiol. 1993 Jul;102(3):1043–1043. doi: 10.1104/pp.102.3.1043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stachelek C., Stachelek J., Swan J., Botstein D., Konigsberg W. Identification, cloning and sequence determination of the genes specifying hexokinase A and B from yeast. Nucleic Acids Res. 1986 Jan 24;14(2):945–963. doi: 10.1093/nar/14.2.945. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Szekeres M., Németh K., Koncz-Kálmán Z., Mathur J., Kauschmann A., Altmann T., Rédei G. P., Nagy F., Schell J., Koncz C. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell. 1996 Apr 19;85(2):171–182. doi: 10.1016/s0092-8674(00)81094-6. [DOI] [PubMed] [Google Scholar]
- Thomas B. R., Rodriguez R. L. Metabolite Signals Regulate Gene Expression and Source/Sink Relations in Cereal Seedlings. Plant Physiol. 1994 Dec;106(4):1235–1239. doi: 10.1104/pp.106.4.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Trumbly R. J. Glucose repression in the yeast Saccharomyces cerevisiae. Mol Microbiol. 1992 Jan;6(1):15–21. doi: 10.1111/j.1365-2958.1992.tb00832.x. [DOI] [PubMed] [Google Scholar]
- Tsukaya H., Ohshima T., Naito S., Chino M., Komeda Y. Sugar-Dependent Expression of the CHS-A Gene for Chalcone Synthase from Petunia in Transgenic Arabidopsis. Plant Physiol. 1991 Dec;97(4):1414–1421. doi: 10.1104/pp.97.4.1414. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weigel D., Nilsson O. A developmental switch sufficient for flower initiation in diverse plants. Nature. 1995 Oct 12;377(6549):495–500. doi: 10.1038/377495a0. [DOI] [PubMed] [Google Scholar]
- Zachgo E. A., Wang M. L., Dewdney J., Bouchez D., Camilleri C., Belmonte S., Huang L., Dolan M., Goodman H. M. A physical map of chromosome 2 of Arabidopsis thaliana. Genome Res. 1996 Jan;6(1):19–25. doi: 10.1101/gr.6.1.19. [DOI] [PubMed] [Google Scholar]
- van der Krol A. R., Mol J. N., Stuitje A. R. Antisense genes in plants: an overview. Gene. 1988 Dec 10;72(1-2):45–50. doi: 10.1016/0378-1119(88)90126-6. [DOI] [PubMed] [Google Scholar]
- von Schaewen A., Stitt M., Schmidt R., Sonnewald U., Willmitzer L. Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J. 1990 Oct;9(10):3033–3044. doi: 10.1002/j.1460-2075.1990.tb07499.x. [DOI] [PMC free article] [PubMed] [Google Scholar]