Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating post-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers

Plant Journal

Volumn 35, Issue 4, 2003, Pages 490-500

  Tiessen, Axel ^a   Prescha, Katrin ^a   Branscheid, Anja ^a   Palacios, Natalia ^a   McKibbin, Rowan ^b   Halford, Nigel G ^b   Geigenberger, Peter ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Carbohydrates; Plant carbon metabolism; Signal perception and transduction; Sink source interactions; Solanum tuberosum cv. Desire ; Starch biosynthesis

Indexed keywords

REDOX REACTIONS; STARCH; SUGAR (SUCROSE); SYNTHESIS (CHEMICAL);

STARCH SYNTHESIS;

PLANTS (BOTANY);

ENZYME ACTIVATION; GLUCOSE; GLUCOSE-1-PHOSPHATE ADENYLYLTRANSFERASE; HEXOKINASE; NUCLEOTIDYLTRANSFERASES; OXIDATION-REDUCTION; PLANTS, GENETICALLY MODIFIED; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; SOLANUM TUBEROSUM; SUCROSE;

BACTERIA (MICROORGANISMS); EMBRYOPHYTA; SOLANUM; SOLANUM TUBEROSUM;

EID: 0042352390     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2003.01823.x     Document Type: Article

References (54)

1. Ballicora, M.A., Frueauf, J.B., Fu, Y.B., Schurmann, P. and Preiss, J. (2000) Activation of the potato tuber ADP-glucose pyrophosphorylase by thioredoxin. J. Biol. Chem. 275, 1315-1320.
2. Barker, L., Kuhn, C., Weise, A., Schulz, A., Gebhardt, C., Hirner, B., Hellmann, H., Schulze, W., Ward, J.M. and Frommer, W.B. (2000) SUT2, a putative sucrose sensor in sieve elements. Plant Cell, 12, 1153-1164.
3. Bouly, J.P., Gissot, L., Lessard, P., Kreis, M. and Thomas, M. (1999) Arabidopsis thaliana proteins related to the yeast SIP and SNF4 interact with AKIN alpha 1, an SNF1-like protein kinase. Plant J. 18, 541-550.
4. Buessis, D., Heineke, D., Sonnewald, U., Willmitzer, L., Raschke, K. and Heldt, H.W. (1997) Solute accumulation and decreased photosynthesis in leaves of potato plants expressing yeast-derived invertase either in the apoplast, vacuole or cytosol. Planta, 202, 126-136.
5. Chiou, T.J. and Bush, D.R. (1998) Sucrose is a signal molecule in assimilate partitioning. Proc. Natl. Acad. Sci. USA, 95, 4784-4788.
6. Ciereszko, I., Johansson, H. and Kleczkowski, L.A. (2001) Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis. Biochem. J. 354, 67-72.
7. Coruzzi, G.M. and Zhou, L. (2001) Carbon and nitrogen sensing and signaling in plants: emerging 'matrix effects'. Curr. Opin. Plant Biol. 4, 247-253.
8. Farras, R., Ferrando, A., Jasik, J., Kleinow, T., Okresz, L., Tiburcio, A., Salchert, K., del Pozo, C., Schell, J. and Koncz, C. (2001) SKP1-SnRK protein kinase interactions mediate proteasomal binding of a plant SCF ubiquitin ligase. EMBO J. 20, 2742-2756.
9. Fernie, A.R., Riesmeire, J.W., Martiny, A., Ramalingam, S., Willmitzer, L. and Trethewey, R.N. (2000) Consequences of the expression of a bacterial glucokinase in potato tubers, both in combination with and independently of a yeast-derived invertase. Aust. J. Plant. Physiol. 27, 827-833.
10. Fernie, A.R., Roessner, U. and Geigenberger, P. (2001) The sucrose analog palatinose leads to a stimulation of sucrose degradation and starch synthesis when supplied to discs of growing potato tubers. Plant Physiol. 125, 1967-1977.
11. Fu, Y.B., Ballicora, M.A., Leykam, J.F. and Preiss, J. (1998) Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. J. Biol. Chem. 273, 25045-25052.
12. Geigenberger, P. (2003) Regulation of sucrose to starch conversion in growing potato tubers. J. Exp. Bot. 54, 457-465.
13. Geigenberger, P., Hajirezaei, M., Geiger, M., Deiting, U., Sonnewald, U. and Stitt, M. (1998) Overexpression of pyrophosphatase leads to increased sucrose degradation and starch synthesis, increased activities of enzymes for sucrose-starch interconversions, and increased levels of nucleotides in growing potato tubers. Planta, 205, 428-437.
14. Geiger, M., Stitt, M. and Geigenberger, P. (1998) Metabolism in slices from growing potato tubers responds differently to addition of sucrose and glucose. Planta, 206, 234-244.
15. Hajirezaei, M.R., Takahata, Y., Trethewey, R.N., Willmitzer, L. and Sonnewald, U. (2000) Impact of elevated cytosolic and apoplastic invertase activity on carbon metabolism during potato tuber development. J. Exp. Bot. 51, 439-445.
16. Halford, N.G. and Hardie, D.G. (1998) SNF1-related protein kinases: global regulators of carbon metabolism in plants? Plant. Mol. Biol. 37, 735-748.
17. Halford, N.G., Purcell, P.C. and Hardie, D.G. (1999) Is hexokinase really a sugar sensor in plants? Trends Plant Sci. 4, 117-120.
18. Hanson, J., Johannesson, H. and Engstrom, P. (2001) Sugar-dependent alterations in cotyledon and leaf development in transgenic plants expressing the HDZhdip gene ATHB13. Plant. Mol. Biol. 45, 247-262.
19. Hardie, D.G. and Carling, D. (1997) The AMP-activated protein kinase - fuel gauge of the mammalian cell. Eur. J. Biochem. 246, 259-273.
20. Hardie, D.G., Carling, D. and Carlson, M. (1998) The AMP-activated/SNF1 protein kinase subfamily - metabolic sensors of the eukaryotic cell. Annu. Rev. Biochem. 67, 821-855.
21. Ho, S.L., Chao, Y.C., Tong, W.F. and Yu, S.M. (2001) Sugar coordinately and differentially regulates growth- and stress-related gene expression via a complex signal transduction network and multiple control mechanisms. Plant Physiol. 125, 877-890.
22. Jang, J.C. and Sheen, J. (1994) Sugar sensing in higher plants. Plant Cell, 6, 1665-1679.
23. Jang, J.C. and Sheen, J. (1997) Sugar sensing in higher plants. Trends Plant Sci. 2, 208-214.
24. Jang, J.C., Leon, P., Zhou, L. and Sheen, J. (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell, 9, 5-19.
25. Jelitto, T., Sonnewald, U., Willmitzer, L., Hajirezeai, M. and Stitt, M. (1992) Inorganic pyrophosphate content and metabolites in potato and tobacco plants expressing Escherichia coli pyrophosphatase in their cytosol. Planta, 188, 238-244.
26. Johnston, M. (1999) Feasting, fasting and fermenting - glucose sensing in yeast and other cells. Trends Genet, 15, 29-33.
27. Kleinow, T., Bhalerao, R., Breuer, F., Umeda, M., Salchert, K. and Koncz, C. (2000) Functional identification of an Arabidopsis Snf4 ortholog by screening for heterologous multicopy suppressors of snf4 deficiency in yeast. Plant J. 23, 115-122.
28. Koch, K.E. (1996) Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 509-540.
29. Loef, I., Stitt, M. and Geigenberger, P. (2001) Increased levels of adenine nucleotides modify the interaction between starch synthesis and respiration when adenine is supplied to discs from growing potato tubers. Planta, 212, 782-791.
30. Loreti, E., Alpi, A. and Perata, P. (2000) Glucose and disaccharide-sensing mechanisms modulate the expression of alpha-amylase in barley embryos. Plant Physiol. 123, 939-948.
31. Loreti, E., De Bellis, L., Alpi, A. and Perata, P. (2001) Why and how do plant cells sense sugars? Ann. Bot.-Lond. 88, 803-812.
32. Martin, T., Hellmann, H., Schmidt, R., Willmitzer, L. and Frommer, W.B. (1997) Identification of mutants in metabolically regulated gene expression. Plant J. 11, 53-62.
33. Martin, C. and Smith, A.M. (1995) Starch biosynthesis. Plant Cell, 7, 971-985.
34. Pego, J.V., Weisbeek, P.J. and Smeekens, S.C.M. (1999) Mannose inhibits Arabidopsis germination via a hexokinase-mediated step. Plant Physiol. 119, 1017-1023.
35. Preiss, J. (1988) Biosynthesis of starch and its regulation. In The Biochemistry of Plants (Preiss, J., ed.). San Diego, California: Academic Press, pp. 181-254.
36. Purcell, P.C., Smith, A.M. and Halford, N.G. (1998) Antisense expression of a sucrose non-fermenting-1-related protein kinase sequence in potato results in decreased expression of sucrose synthase in tubers and loss of sucrose-inducibility of sucrose synthase transcripts in leaves. Plant J. 14, 195-202.
37. Renz, A. and Stitt, M. (1993) Substrate specificity and product inhibition of different forms of fructokinases and hexokinases in developing potato tubers. Planta, 190, 166-175.
38. Roessner, U., Willmitzer, L. and Fernie, A.R. (2001) High-resolution metabolic phenotyping of genetically and environmentally diverse potato tuber systems. Identification of phenocopies. Plant Physiol. 127, 749-764.
39. Roitsch, T., Bittner, M. and Godt, D.E. (1995) Induction of apoplastic invertase of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol. 108, 285-294.
40. Rolland, F., Moore, B. and Sheen, J. (2002) Sugar sensing and signaling in plants. Plant Cell, 14, S185-S205.
41. Rook, F., Gerrits, N., Kortstee, A., van Kampen, M., Borrias, M., Weisbeek, P. and Smeekens, S. (1998) Sucrose-specific signalling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene. Plant J. 15, 253-263.
42. Rook, F., Corke, F., Card, R., Munz, G., Smith, C. and Bevan, M.W. (2001) Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling. Plant J. 26, 421-433.
43. Schnarrenberger, C. (1990) Characterization and compartmentation in green leaves of hexokinases with different specificities for glucose, fructose and mannose and for nucleoside triphosphates. Planta, 181, 249-255.
44. Sheen, J., Zhou, L. and Jang, J.C. (1999) Sugars as signaling molecules. Curr. Opin. Plant Biol. 2, 410-418.
45. Smeekens, S. (2000) Sugar-induced signal transduction in plants. Annu. Rev. Plant Physiol. 51, 49-81.
46. Sonnewald, U., Hajirezaei, M.R., Kossmann, J., Heyer, A., Trethewey, R.N. and Willmitzer, L. (1997) Increased potato tuber size resulting from apoplastic expression of a yeast invertase. Nat. Biotechnol. 15, 794-797.
47. Tauberger, E., Hoffmann-Benning, S., Fleischer-Notter, H., Willmitzer, L. and Fisahn, J. (1999) Impact of invertase overexpression on cell size, starch granule formation and cell wall properties during tuber development in potatoes with modified carbon allocation patterns. J. Exp. Bot. 50, 477-486.
48. Tiessen, A., Hendriks, J.H.M., Stitt, M., Branscheid, A., Gibon, Y., Farre, E.M. and Geigenberger, P. (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell, 14, 2191-2213.
49. Toroser, D., Plaut, Z. and Huber, S.C. (2000) Regulation of a plant SNF1-related protein kinase by glucose-6-phosphate. Plant Physiol. 123, 403-411.
50. Trethewey, R.N., Geigenberger, P., Riedel, K., Hajirezaei, M.R., Sonnewald, U., Stitt, M., Riesmeier, J.W. and Willmitzer, L. (1998) Combined expression of glucokinase and invertase in potato tubers leads to a dramatic reduction in starch accumulation and a stimulation of glycolysis. Plant J. 15, 109-118.
51. Trethewey, R.N., Riesmeier, J.W., Willmitzer, L., Stitt, M. and Geigenberger, P. (1999) Tuber-specific expression of a yeast invertase and a bacterial glucokinase in potato leads to an activation of sucrose phosphate synthase and the creation of a sucrose futile cycle. Planta, 208, 227-238.
52. Veramendi, J., Roessner, U., Renz, A., Willmitzer, L. and Trethewey, R.N. (1999) Antisense repression of hexokinase 1 leads to an overaccumulation of starch in leaves of transgenic potato plants but not to significant changes in tuber carbohydrate metabolism. Plant Physiol. 121, 123-133.
53. Veramendi, J., Fernie, A.R., Leisse, A., Willmitzer, L. and Trethewey, R.N. (2002) Potato hexokinase 2 complements transgenic Arabidopsis plants deficient in hexokinase 1 but does not play a key role in tuber carbohydrate metabolism. Plant. Mol. Biol. 49, 491-501.
54. Weiner, H., Heldt, H.W. and Stitt, M. (1987) Subcellular compartmentation of pyrophosphate and pyrophosphatase in leaves. Biochim. Biophys. Acta, 893, 13-21.