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. 2001 Feb 15;354(Pt 1):67–72. doi: 10.1042/0264-6021:3540067

Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis.

I Ciereszko 1, H Johansson 1, L A Kleczkowski 1
PMCID: PMC1221629  PMID: 11171080

Abstract

UDP-glucose pyrophosphorylase (UGPase) is a key enzyme producing UDP-glucose, which is involved in an array of metabolic pathways concerned with, among other functions, the synthesis of sucrose and cellulose. An Arabidopsis thaliana UGPase-encoding gene, Ugp, was profoundly up-regulated by feeding sucrose to the excised leaves and by an exposure of plants to low temperature (5 degrees C). The UGPase activity and its protein content also increased under conditions of sucrose feeding and exposure to cold. The sucrose effect on Ugp was apparently specific and was mimicked by exposure of dark-adapted leaves to light. Drought and O2 deficiency had some down-regulating effects on expression of Ugp. The sugar-signalling pathway for Ugp regulation was independent of hexokinase, as was found by using transgenic plants with increased and decreased expression of the corresponding gene. Subjecting mutants deficient in abscisic acid (ABA) to cold stress conditions had no effect on Ugp expression profiles. Okadaic acid was a powerful inhibitor of Ugp expression, whereas it up-regulated the gene encoding sucrose synthase (Sus1), indicating distinct transduction pathways in transmitting the sugar signal for the two genes in A. thaliana. We suggest that Ugp gene expression is mediated via a hexokinase-independent and ABA-insensitive pathway that involves an okadaic acid-responsive protein phosphatase. The data point towards Ugp as a possible regulatory entity that is closely involved in the homoeostatic readjustment of plant responses to environmental signals.

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Selected References

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  1. Amor Y., Haigler C. H., Johnson S., Wainscott M., Delmer D. P. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9353–9357. doi: 10.1073/pnas.92.20.9353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bialojan C., Takai A. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem J. 1988 Nov 15;256(1):283–290. doi: 10.1042/bj2560283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chiou T. J., Bush D. R. Sucrose is a signal molecule in assimilate partitioning. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4784–4788. doi: 10.1073/pnas.95.8.4784. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dijkwel P. P., Huijser C., Weisbeek P. J., Chua N. H., Smeekens S. C. Sucrose control of phytochrome A signaling in Arabidopsis. Plant Cell. 1997 Apr;9(4):583–595. doi: 10.1105/tpc.9.4.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Déjardin A., Sokolov L. N., Kleczkowski L. A. Sugar/osmoticum levels modulate differential abscisic acid-independent expression of two stress-responsive sucrose synthase genes in Arabidopsis. Biochem J. 1999 Dec 1;344(Pt 2):503–509. [PMC free article] [PubMed] [Google Scholar]
  6. Ehness R., Ecker M., Godt D. E., Roitsch T. Glucose and Stress Independently Regulate Source and Sink Metabolism and Defense Mechanisms via Signal Transduction Pathways Involving Protein Phosphorylation. Plant Cell. 1997 Oct;9(10):1825–1841. doi: 10.1105/tpc.9.10.1825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eimert K., Villand P., Kilian A., Kleczkowski L. A. Cloning and characterization of several cDNAs for UDP-glucose pyrophosphorylase from barley (Hordeum vulgare) tissues. Gene. 1996 May 8;170(2):227–232. doi: 10.1016/0378-1119(95)00873-x. [DOI] [PubMed] [Google Scholar]
  8. Flores-Díaz M., Alape-Girón A., Persson B., Pollesello P., Moos M., von Eichel-Streiber C., Thelestam M., Florin I. Cellular UDP-glucose deficiency caused by a single point mutation in the UDP-glucose pyrophosphorylase gene. J Biol Chem. 1997 Sep 19;272(38):23784–23791. doi: 10.1074/jbc.272.38.23784. [DOI] [PubMed] [Google Scholar]
  9. Gosti F., Bertauche N., Vartanian N., Giraudat J. Abscisic acid-dependent and -independent regulation of gene expression by progressive drought in Arabidopsis thaliana. Mol Gen Genet. 1995 Jan 6;246(1):10–18. doi: 10.1007/BF00290128. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Halford NG, Purcell PC, Hardie DG. Is hexokinase really a sugar sensor in plants? Trends Plant Sci. 1999 Mar;4(3):117–120. doi: 10.1016/s1360-1385(99)01377-1. [DOI] [PubMed] [Google Scholar]
  12. Huber Steven C., Huber Joan L. ROLE AND REGULATION OF SUCROSE-PHOSPHATE SYNTHASE IN HIGHER PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):431–444. doi: 10.1146/annurev.arplant.47.1.431. [DOI] [PubMed] [Google Scholar]
  13. Jang J. C., León P., Zhou L., Sheen J. Hexokinase as a sugar sensor in higher plants. Plant Cell. 1997 Jan;9(1):5–19. doi: 10.1105/tpc.9.1.5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Katsube T., Kazuta Y., Mori H., Nakano K., Tanizawa K., Fukui T. UDP-glucose pyrophosphorylase from potato tuber: cDNA cloning and sequencing. J Biochem. 1990 Aug;108(2):321–326. doi: 10.1093/oxfordjournals.jbchem.a123200. [DOI] [PubMed] [Google Scholar]
  15. Koch K. E. CARBOHYDRATE-MODULATED GENE EXPRESSION IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1996 Jun;47(NaN):509–540. doi: 10.1146/annurev.arplant.47.1.509. [DOI] [PubMed] [Google Scholar]
  16. Lang V., Mantyla E., Welin B., Sundberg B., Palva E. T. Alterations in Water Status, Endogenous Abscisic Acid Content, and Expression of rab18 Gene during the Development of Freezing Tolerance in Arabidopsis thaliana. Plant Physiol. 1994 Apr;104(4):1341–1349. doi: 10.1104/pp.104.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Leung Jeffrey, Giraudat Jerome. ABSCISIC ACID SIGNAL TRANSDUCTION. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):199–222. doi: 10.1146/annurev.arplant.49.1.199. [DOI] [PubMed] [Google Scholar]
  18. Martin T., Hellmann H., Schmidt R., Willmitzer L., Frommer W. B. Identification of mutants in metabolically regulated gene expression. Plant J. 1997 Jan;11(1):53–62. doi: 10.1046/j.1365-313x.1997.11010053.x. [DOI] [PubMed] [Google Scholar]
  19. Miernyk J. A. Protein folding in the plant cell. Plant Physiol. 1999 Nov;121(3):695–703. doi: 10.1104/pp.121.3.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mita S., Murano N., Akaike M., Nakamura K. Mutants of Arabidopsis thaliana with pleiotropic effects on the expression of the gene for beta-amylase and on the accumulation of anthocyanin that are inducible by sugars. Plant J. 1997 Apr;11(4):841–851. doi: 10.1046/j.1365-313x.1997.11040841.x. [DOI] [PubMed] [Google Scholar]
  21. Nordin K., Heino P., Palva E. T. Separate signal pathways regulate the expression of a low-temperature-induced gene in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol. 1991 Jun;16(6):1061–1071. doi: 10.1007/BF00016077. [DOI] [PubMed] [Google Scholar]
  22. Pego J. V., Weisbeek P. J., Smeekens S. C. Mannose inhibits Arabidopsis germination via a hexokinase-mediated step. Plant Physiol. 1999 Mar;119(3):1017–1023. doi: 10.1104/pp.119.3.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Prata RTN., Williamson J. D., Conkling M. A., Pharr D. M. Sugar Repression of Mannitol Dehydrogenase Activity in Celery Cells. Plant Physiol. 1997 May;114(1):307–314. doi: 10.1104/pp.114.1.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Roitsch T. Source-sink regulation by sugar and stress. Curr Opin Plant Biol. 1999 Jun;2(3):198–206. doi: 10.1016/S1369-5266(99)80036-3. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Shinozaki K., Yamaguchi-Shinozaki K. Gene Expression and Signal Transduction in Water-Stress Response. Plant Physiol. 1997 Oct;115(2):327–334. doi: 10.1104/pp.115.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sokolov L. N., Déjardin A., Kleczkowski L. A. Sugars and light/dark exposure trigger differential regulation of ADP-glucose pyrophosphorylase genes in Arabidopsis thaliana (thale cress). Biochem J. 1998 Dec 15;336(Pt 3):681–687. doi: 10.1042/bj3360681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Strand A., Hurry V., Gustafsson P., Gardeström P. Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J. 1997 Sep;12(3):605–614. doi: 10.1046/j.1365-313x.1997.00605.x. [DOI] [PubMed] [Google Scholar]
  29. Takeda S., Mano S., Ohto Ma., Nakamura K. Inhibitors of Protein Phosphatases 1 and 2A Block the Sugar-Inducible Gene Expression in Plants. Plant Physiol. 1994 Oct;106(2):567–574. doi: 10.1104/pp.106.2.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zrenner R., Willmitzer L., Sonnewald U. Analysis of the expression of potato uridinediphosphate-glucose pyrophosphorylase and its inhibition by antisense RNA. Planta. 1993;190(2):247–252. doi: 10.1007/BF00196618. [DOI] [PubMed] [Google Scholar]

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