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. 1997 May;114(1):307–314. doi: 10.1104/pp.114.1.307

Sugar Repression of Mannitol Dehydrogenase Activity in Celery Cells.

RTN Prata 1, J D Williamson 1, M A Conkling 1, D M Pharr 1
PMCID: PMC158306  PMID: 12223706

Abstract

We present evidence that the activity of the mannitol-catabolizing enzyme mannitol dehydrogenase (MTD) is repressed by sugars in cultured celery (Apium graveolens L.) cells. Furthermore, this sugar repression appears to be mediated by hexokinases (HKs) in a manner comparable to the reported sugar repression of photosynthetic genes. Glucose (Glc)-grown cell cultures expressed little MTD activity during active growth, but underwent a marked increase in MTD activity, protein, and RNA upon Glc starvation. Replenishment of Glc in the medium resulted in decreased MTD activity, protein, and RNA within 12 h. Addition of mannoheptulose, a competitive inhibitor of HK, derepressed MTD activity in Glc-grown cultures. In contrast, the addition of the sugar analog 2-deoxyglucose, which is phosphorylated by HK but not further metabolized, repressed MTD activity in mannitol-grown cultures. Collectively, these data suggest that HK and sugar phosphorylation are involved in signaling MTD repression. In vivo repression of MTD activity by galactose (Gal), which is not a substrate of HK, appeared to be an exception to this hypothesis. Further analyses, however, showed that the products of Gal catabolism, Glc and fructose, rather than Gal itself, were correlated with MTD repression.

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Selected References

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  1. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  2. Fernández R., Herrero P., Fernández M. T., Moreno F. Mechanism of inactivation of hexokinase PII of Saccharomyces cerevisiae by D-xylose. J Gen Microbiol. 1986 Dec;132(12):3467–3472. doi: 10.1099/00221287-132-12-3467. [DOI] [PubMed] [Google Scholar]
  3. Herbers K., Meuwly P., Frommer W. B., Metraux J. P., Sonnewald U. Systemic Acquired Resistance Mediated by the Ectopic Expression of Invertase: Possible Hexose Sensing in the Secretory Pathway. Plant Cell. 1996 May;8(5):793–803. doi: 10.1105/tpc.8.5.793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Herrero P., Fernández R., Moreno F. The hexokinase isoenzyme PII of Saccharomyces cerevisiae ia a protein kinase. J Gen Microbiol. 1989 May;135(5):1209–1216. doi: 10.1099/00221287-135-5-1209. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. 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]
  8. 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]
  9. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. SALAS J., SALAS M., VINUELA E., SOLS A. GLUCOKINASE OF RABBIT LIVER. J Biol Chem. 1965 Mar;240:1014–1018. [PubMed] [Google Scholar]
  13. 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]
  14. Stoop J. M., Williamson J. D., Conkling M. A., Pharr D. M. Purification of NAD-dependent mannitol dehydrogenase from celery suspension cultures. Plant Physiol. 1995 Jul;108(3):1219–1225. doi: 10.1104/pp.108.3.1219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Stoop JMH., Pharr D. M. Effect of Different Carbon Sources on Relative Growth Rate, Internal Carbohydrates, and Mannitol 1-Oxidoreductase Activity in Celery Suspension Cultures. Plant Physiol. 1993 Nov;103(3):1001–1008. doi: 10.1104/pp.103.3.1001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Vojtek A. B., Fraenkel D. G. Phosphorylation of yeast hexokinases. Eur J Biochem. 1990 Jun 20;190(2):371–375. doi: 10.1111/j.1432-1033.1990.tb15585.x. [DOI] [PubMed] [Google Scholar]
  18. Walsh M. C., Scholte M., Valkier J., Smits H. P., van Dam K. Glucose sensing and signalling properties in Saccharomyces cerevisiae require the presence of at least two members of the glucose transporter family. J Bacteriol. 1996 May;178(9):2593–2597. doi: 10.1128/jb.178.9.2593-2597.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Williamson J. D., Hirsch-Wyncott M. E., Larkins B. A., Gelvin S. B. Differential Accumulation of a Transcript Driven by the CaMV 35S Promoter in Transgenic Tobacco. Plant Physiol. 1989 Aug;90(4):1570–1576. doi: 10.1104/pp.90.4.1570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Williamson J. D., Stoop J. M., Massel M. O., Conkling M. A., Pharr D. M. Sequence analysis of a mannitol dehydrogenase cDNA from plants reveals a function for the pathogenesis-related protein ELI3. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7148–7152. doi: 10.1073/pnas.92.16.7148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Zamski E., Yamamoto Y. T., Williamson J. D., Conkling M. A., Pharr D. M. Immunolocalization of mannitol dehydrogenase in celery plants and cells. Plant Physiol. 1996 Nov;112(3):931–938. doi: 10.1104/pp.112.3.931. [DOI] [PMC free article] [PubMed] [Google Scholar]

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