Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1999 Dec 1;344(Pt 2):503–509.

Sugar/osmoticum levels modulate differential abscisic acid-independent expression of two stress-responsive sucrose synthase genes in Arabidopsis.

A Déjardin 1, L N Sokolov 1, L A Kleczkowski 1
PMCID: PMC1220669  PMID: 10567234

Abstract

Sucrose synthase (Sus) is a key enzyme of sucrose metabolism. Two Sus-encoding genes (Sus1 and Sus2) from Arabidopsis thaliana were found to be profoundly and differentially regulated in leaves exposed to environmental stresses (cold stress, drought or O(2) deficiency). Transcript levels of Sus1 increased on exposure to cold and drought, whereas Sus2 mRNA was induced specifically by O(2) deficiency. Both cold and drought exposures induced the accumulation of soluble sugars and caused a decrease in leaf osmotic potential, whereas O(2) deficiency was characterized by a nearly complete depletion in sugars. Feeding abscisic acid (ABA) to detached leaves or subjecting Arabidopsis ABA-deficient mutants to cold stress conditions had no effect on the expression profiles of Sus1 or Sus2, whereas feeding metabolizable sugars (sucrose or glucose) or non-metabolizable osmotica [poly(ethylene glycol), sorbitol or mannitol] mimicked the effects of osmotic stress on Sus1 expression in detached leaves. By using various sucrose/mannitol solutions, we demonstrated that Sus1 was up-regulated by a decrease in leaf osmotic potential rather than an increase in sucrose concentration itself. We suggest that Sus1 expression is regulated via an ABA-independent signal transduction pathway that is related to the perception of a decrease in leaf osmotic potential during stresses. In contrast, the expression of Sus2 was independent of sugar/osmoticum effects, suggesting the involvement of a signal transduction mechanism distinct from that regulating Sus1 expression. The differential stress-responsive regulation of Sus genes in leaves might represent part of a general cellular response to the allocation of carbohydrates during acclimation processes.

Full Text

The Full Text of this article is available as a PDF (272.4 KB).

Selected References

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

  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. Chopra S., Del-favero J., Dolferus R., Jacobs M. Sucrose synthase of Arabidopsis: genomic cloning and sequence characterization. Plant Mol Biol. 1992 Jan;18(1):131–134. doi: 10.1007/BF00018465. [DOI] [PubMed] [Google Scholar]
  3. Drew Malcolm C. OXYGEN DEFICIENCY AND ROOT METABOLISM: Injury and Acclimation Under Hypoxia and Anoxia. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):223–250. doi: 10.1146/annurev.arplant.48.1.223. [DOI] [PubMed] [Google Scholar]
  4. Déjardin A., Rochat C., Maugenest S., Boutin J. P. Purification, characterization and physiological role of sucrose synthase in the pea seed coat (Pisum sativum L.). Planta. 1997;201(2):128–137. doi: 10.1007/BF01007697. [DOI] [PubMed] [Google Scholar]
  5. Fu H., Kim S. Y., Park W. D. A potato Sus3 sucrose synthase gene contains a context-dependent 3' element and a leader intron with both positive and negative tissue-specific effects. Plant Cell. 1995 Sep;7(9):1395–1403. doi: 10.1105/tpc.7.9.1395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fu H., Kim S. Y., Park W. D. High-level tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene require 5' and 3' flanking sequences and the leader intron. Plant Cell. 1995 Sep;7(9):1387–1394. doi: 10.1105/tpc.7.9.1387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fu H., Park W. D. Sink- and vascular-associated sucrose synthase functions are encoded by different gene classes in potato. Plant Cell. 1995 Sep;7(9):1369–1385. doi: 10.1105/tpc.7.9.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Gustin M. C., Albertyn J., Alexander M., Davenport K. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1998 Dec;62(4):1264–1300. doi: 10.1128/mmbr.62.4.1264-1300.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Heim U., Weber H., Bäumlein H., Wobus U. A sucrose-synthase gene of Vicia faba L.: expression pattern in developing seeds in relation to starch synthesis and metabolic regulation. Planta. 1993;191(3):394–401. doi: 10.1007/BF00195698. [DOI] [PubMed] [Google Scholar]
  11. Hesse H., Willmitzer L. Expression analysis of a sucrose synthase gene from sugar beet (Beta vulgaris L.). Plant Mol Biol. 1996 Mar;30(5):863–872. doi: 10.1007/BF00020799. [DOI] [PubMed] [Google Scholar]
  12. Karrer E. E., Rodriguez R. L. Metabolic regulation of rice alpha-amylase and sucrose synthase genes in planta. Plant J. 1992 Jul;2(4):517–523. [PubMed] [Google Scholar]
  13. Kleczkowski L. A. A phosphoglycerate to inorganic phosphate ratio is the major factor in controlling starch levels in chloroplasts via ADP-glucose pyrophosphorylase regulation. FEBS Lett. 1999 Apr 1;448(1):153–156. doi: 10.1016/s0014-5793(99)00346-4. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Koch K. E., Nolte K. D., Duke E. R., McCarty D. R., Avigne W. T. Sugar Levels Modulate Differential Expression of Maize Sucrose Synthase Genes. Plant Cell. 1992 Jan;4(1):59–69. doi: 10.1105/tpc.4.1.59. [DOI] [PMC free article] [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. Madhani H. D., Fink G. R. The riddle of MAP kinase signaling specificity. Trends Genet. 1998 Apr;14(4):151–155. doi: 10.1016/s0168-9525(98)01425-5. [DOI] [PubMed] [Google Scholar]
  19. Martin T., Frommer W. B., Salanoubat M., Willmitzer L. Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs. Plant J. 1993 Aug;4(2):367–377. doi: 10.1046/j.1365-313x.1993.04020367.x. [DOI] [PubMed] [Google Scholar]
  20. Miyata S., Urao T., Yamaguchi-Shinozaki K., Shinozaki K. Characterization of genes for two-component phosphorelay mediators with a single HPt domain in Arabidopsis thaliana. FEBS Lett. 1998 Oct 16;437(1-2):11–14. doi: 10.1016/s0014-5793(98)01188-0. [DOI] [PubMed] [Google Scholar]
  21. Nolte K. D., Koch K. E. Companion-Cell Specific Localization of Sucrose Synthase in Zones of Phloem Loading and Unloading. Plant Physiol. 1993 Mar;101(3):899–905. doi: 10.1104/pp.101.3.899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Ricard B., Rivoal J., Spiteri A., Pradet A. Anaerobic stress induces the transcription and translation of sucrose synthase in rice. Plant Physiol. 1991 Mar;95(3):669–674. doi: 10.1104/pp.95.3.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ricard B, Toai TV, Chourey P, Saglio P. Evidence for the critical role of sucrose synthase for anoxic tolerance of maize roots using a double mutant . Plant Physiol. 1998 Apr;116(4):1323–1331. doi: 10.1104/pp.116.4.1323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Salanoubat M., Belliard G. The steady-state level of potato sucrose synthase mRNA is dependent on wounding, anaerobiosis and sucrose concentration. Gene. 1989 Dec 7;84(1):181–185. doi: 10.1016/0378-1119(89)90153-4. [DOI] [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. Villand P., Olsen O. A., Kleczkowski L. A. Molecular characterization of multiple cDNA clones for ADP-glucose pyrophosphorylase from Arabidopsis thaliana. Plant Mol Biol. 1993 Dec;23(6):1279–1284. doi: 10.1007/BF00042361. [DOI] [PubMed] [Google Scholar]
  30. Xue Z. T., Larsen K., Jochimsen B. U. Oxygen regulation of uricase and sucrose synthase synthesis in soybean callus tissue is exerted at the mRNA level. Plant Mol Biol. 1991 May;16(5):899–906. doi: 10.1007/BF00015081. [DOI] [PubMed] [Google Scholar]
  31. Yu S. M., Lee Y. C., Fang S. C., Chan M. T., Hwa S. F., Liu L. F. Sugars act as signal molecules and osmotica to regulate the expression of alpha-amylase genes and metabolic activities in germinating cereal grains. Plant Mol Biol. 1996 Mar;30(6):1277–1289. doi: 10.1007/BF00019558. [DOI] [PubMed] [Google Scholar]
  32. Zeng Y, Wu Y, Avigne WT, Koch KE. Differential regulation of sugar-sensitive sucrose synthases by hypoxia and anoxia indicate complementary transcriptional and posttranscriptional responses . Plant Physiol. 1998 Apr;116(4):1573–1583. doi: 10.1104/pp.116.4.1573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. van Ghelue M., Ribeiro A., Solheim B., Akkermans A. D., Bisseling T., Pawlowski K. Sucrose synthase and enolase expression in actinorhizal nodules of Alnus glutinosa: comparison with legume nodules. Mol Gen Genet. 1996 Mar 7;250(4):437–446. doi: 10.1007/BF02174032. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES