Metabolic control analysis and regulation of the conversion of sucrose to starch in growing potato tubers

Plant, Cell and Environment

Volumn 27, Issue 6, 2004, Pages 655-673

  Geigenberger, P ^a   Stitt, M ^a   Fernie, A R ^a  

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

Author keywords

Adenylate supply; Metabolic control analysis; Metabolic regulation; Solanum tuberosum (potato); Starch

Indexed keywords

STARCH;

SOLANUM; SOLANUM TUBEROSUM;

EID: 2642563865     PISSN: 01407791     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2004.01183.x     Document Type: Review

References (121)

1. Baba T., Noro M., Hiroto M. & Arai Y. (1990) Properties of primer-dependent starch synthesis catalysed by starch synthase from potato tubers. Phytochemistry 29, 719-723.
2. Ballicora M.A., Frueauf J.B., Fu Y.B., Schurmann P. & Preiss J. (2000) Activation of the potato tuber ADP-glucose pyrophosphorylase by thioredoxin. Journal of Biological Chemistry 275, 1315-1320.
3. Beckles D.M., Smith A.M. & ap Rees T. (2001) A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiology 125, 818-827.
4. Blenow A. & Johansson G. (1991) Isolation of a Q-enzyme with Mr 103 000 from potato tubers. Phytochemistry 30, 437-444.
5. Bologa K.L., Fernie A.R., Leisse A., Loureiro M.E. & Geigenberger P. (2003) A bypass of sucrose synthase leads to low internal oxygen and impaired metabolic performance in growing potato tubers. Plant Physiology 132, 2058-2072.
6. Burton W.G. (1989) The Potato. Longmann, New York, USA.
7. Cotelle V., Meek S.E.M., Provan F., Milne F.C., Morrice N. & MacKintosh C. (2000) 14-3-3s regulate global cleavage of their diverse binding partners in sugar-starved Arabidopsis cells. EMBO Journal 19, 2869-2876.
8. Crabtree B. & Newsholme E.A. (1987) A systemic approach to describing and analysing metabolic control systems. Trends in Biochemical Sciences 12, 4-12.
9. Dancer J., Neuhaus H.E. & Stitt M. (1990) Cytosolic cycles regulate the turnover of sucrose in heterotrophic cell suspension cultures of Chenopodium rubrum L. Planta 182, 223-231.
10. Denyer K., Dunlap F., Thorbjornsen T., Keeling P. & Smith A.M. (1996) The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiology 112, 779-785.
11. Denyer K., Foster J. & Smith A.M. (1995) The contributions of adenosine 5′-diphosphoglucose pyrophosphorylase and starch-branching enzyme to the control of starch synthesis in developing pea embryos. Planta 197, 57-62.
12. Doehlert D.C. (1987) Substrate inhibition of maize endosperm sucrose synthase by fructose and its interaction with glucose inhibition. Plant Science 52, 153-157.
13. Doehlert D.C. & Huber S.C. (1983) Regulation of spinach leaf sucrose phosphate synthase by glucose 6-phosphate, inorganic phosphate and pH. Plant Physiology 73, 989-994.
14. Edwards A., Borthakur A., Bornemann S., Venail J., Denyer K., Waite D., Fulton D., Smith A. & Martin C. (1999) Specificity of starch synthase isoforms from potato. European Journal of Biochemistry 266, 724-736.
15. Farre E.M., Tiessen A., Roessner U., Geigenberger P., Trethewey R.N. & Willmitzer L. (2001) Analysis of the compartmentation of glycolytic intermediates, nucleotides, sugars, organic acids, amino acids, and sugar alcohols in potato tubers using a nonaqueous fractionation method. Plant Physiology 127, 685-700.
16. Fernie A.R., Roessner U. & 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 Physiology 125, 1967-1977.
17. Fernie A.R., Roessner U., Trethewey R.N. & Willmitzer L. (2001a) The contribution of plastidial phosphoglucomutase to the control of starch synthesis within the potato tuber. Planta 213, 418-426.
18. Fernie A.R., Roscher A., Ratcliffe R.G. & Kruger N.J. (2001b) Fructose 2,6-bisphosphate activates pyrophosphate: fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta 212, 250-263.
19. Fernie A.R., Tauberger E., Lytovchenko A., Roessner U., Willmitzer L. & Trethewey R.N. (2002a) Antisense repression of cytosolic phosphoglucomutase in potato (Solanum tuberosum) results in severe growth retardation, reduction in tuber number and altered carbon metabolism. Planta 214, 510-520.
20. Fernie A.R., Tiessen A., Stitt M., Willmitzer L. & Geigenberger P. (2002b) Altered metabolic fluxes result from shifts in metabolite levels in sucrose phosphorylase-expressing potato tubers. Plant, Cell and Environment 25, 1219-1232.
21. Fernie A.R., Willmitzer L. & Trethewey R.N. (2002) Sucrose to starch: a transition in molecular plant physiology. Trends in Plant Science 7, 35-41.
22. Fox S.R., Rawsthorne S. & Hills M.J. (2001) Fatty acid synthesis in pea root plastids is inhibited by the action of long-chain acylcoenzyme as on metabolite transporters. Plant Physiology 126, 1250-1256.
23. Fu Y.B., Ballicora M.A., Leykam J.F. & Preiss J. (1998) Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. Journal of Biological Chemistry 39, 25045-25052.
24. Geigenberger P. (2003a) Regulation of sucrose to starch conversion in growing potato tubers. Journal of Experimental Botany 54, 457-465.
25. Geigenberger P. (2003b) Response of plant metabolism to too little oxygen. Current Opinions in Plant Biology 6, 247-256.
26. Geigenberger P. & Stitt M. (1993) Sucrose synthase catalyszes a readily reversible reaction in vivo in developing potato tubers and other plant tissues. Planta 189, 329-339.
27. Geigenberger P. & Stitt M. (2000) Diurnal changes in sucrose, nucleotides, starch synthesis and AGPS transcript in growing potato tubers that are suppressed by decreased expression of sucrose phosphate synthase. Plant Journal 23, 795-806.
28. Geigenberger P., Fernie A.R., Gibon Y., Christ M. & Stitt M. (2000) Metabolic activity decreases as an adaptive response to low oxygen in growing potato tubers. Biological Chemistry 381, 723-740.
29. Geigenberger P., Geiger M. & Stitt M. (1998) High-temperature perturbation of starch synthesis is attributable to inhiition of ADPglucose pyrophosphorylase by decreased levels of glycerate 3-phosphate in growing potato tubers. Plant Physiology 117, 1307-1316.
30. Geigenberger P., Langenberger S., Wilke I., Heineke D., Heldt H.W. & Stitt M. (1993) Sucrose is metabolised by sucrose synthesis and glycolysis within the phloem complex of Ricinus communis seedlings. Planta 190, 446-453.
31. Geigenberger P., Merlo L., Reimholz R. & Stitt M. (1994) When rapidly growing potato tubers are detached from their mother plant there is a rapid inhibition of starch synthesis, involving inhibition of ADPglucose pyrophosphorylase. Planta 193, 486-493.
32. Geigenberger P., Müller-Röber B. & Stitt M. (1999) Contribution of adenosine 5′-diphosphoglucose pyrophosphorylase to the control of starch synthesis is decreased by water stress in growing potato tubers. Planta 209, 338-345.
33. Geigenberger P., Reimholz R., Deiting U., Sonnewald U. & Stitt M. (1999) Decreased expression of sucrose phosphate synthase strongly inhibits the water stress-induced synthesis of sucrose in growing potato tubers. Plant Journal 19, 119-129.
34. Geigenberger P., Reimholz R., Geiger M., Merlo L., Canale V. & Stitt M. (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short term water deficit. Planta 201, 502-518.
35. Geigenberger P., Stamme C., Tjaden J., Schulz A., Quick P.W., Betsche T., Kersting H.J. & Neuhaus H.E. (2001) Tuber physiology and properties of starch from tubers of transgenic potato plants with altered plastidic adenylate transporter activity. Plant Physiology 125, 1667-1678.
36. Geiger M., Stitt M. & Geigenberger P. (1998) Metabolism in potato tuber slices responds differently after addition of sucrose and glucose. Planta 206, 245-252.
37. Haake V., Geiger M., Walch-Liu P., Engels C., Zrenner R. & Stitt M. (1999) Changes in aldolase activity in wild-type potato plants are important for acclimation to growth irradiance and carbon dioxide concentration, because plastid aldolase exerts control over the ambient rate of photosynthesis across a range of growth conditions. Plant Journal 17, 479-489.
38. Haake V., Zrenner R., Sonnewald U. & Stitt M. (1998) A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. Plant Journal 14, 147-157.
39. Hajirezaei M., Sonnewald U., Viola R., Carlise S., Dennis D. & Stitt M. (1994) Transgenic potato plants with strongly decreased expression of pyrophosphate: fructose 6-phosphate phosphotransferase show no visible phenotype and only minor changes in metabolic fluxes in their tubers. Planta 180, 205-211.
40. Hardin S.C., Tang G.Q., Scholz A., Holtgraewe D., Winter H. & Huber S.C. (2003) Phosphorylation of sucrose synthase at serine 170: occurrence and possible role as a signal for proteolysis. Plant Journal 35, 588-603.
41. Hatzfeld W.D. & Stitt M. (1990) A study of the rate of recycling of triose phosphates in heterotrophic Chenopodium rubrum cells, potato tubers and maize endosperm. Planta 180, 205-211.
42. Heinrich R. & Rapoport T.A. (1974) A linear steady-state treatment of enzymatic chains. General properties, control and effector strength. European Journal of Biochemistry 42, 89-95.
43. Hendriks J.H.M., Kolbe A., Gibon Y., Stitt M. & Geigenberger P. (2003) ADP-glucose pyrophosphorylase is activated by post-translational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiology 133, 838-849.
44. Henkes S., Sonnewald U., Badur R., Flachmann R. & Stitt M. (2001) A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell 13, 535-551.
45. Hill L.M. & Smith A.M. (1991) Evidence that glucose 6-phosphate is imported as the substrate for starch synthesis by the plastids of developing pea embryos. Planta 185, 91-96.
46. Huber S.C., Huber J., 1 Chourey P.S., Hannah C. & 1. & Koch K. (1995) Sucrose synthase is phosphorylated in-vivo in maize leaves. Plant Physiology 108, 142-143.
47. James M.G., Denyer K. & Myers A.M. (2003) Starch synthesis in the cereal endosperm. Current Opinions in Plant Biology 6, 215-222.
48. 14C]sucrose in isolated wheat grains is dependent upon the activity of soluble starch synthase. Australian Journal of Plant Physiology 20, 329-335.
49. Jenner H.L., Winning B.M., Millar A.H., Tomlinson K.L., Leaver C.J. & Hill S.A. (2001) NAD malic enzyme and the control of carbohydrate metabolism in potato tubers. Plant Physiology 126, 1139-1149.
50. Kacser H. (1987) Control of metabolism. In The Biochemistry of Plants, Vol. 11 (ed. D. Davies), pp. 39-67. Academic Press, New York, USA.
51. Kacser H. & Burns J.A. (1973) The control of flux. Symposia of the Society of for Experimental Biology 28, 65-104.
52. Kalt-Torres W., Kerr P.S. & Huber S.C. (1987) Isolation and characterisation of multiple forms of maize leaf sucrose phosphate synthase. Plant Physiology 70, 653-658.
53. Kammerer B., Fischer K., Hilpert B., Schubert S., Gutensohn M., Weber A. & Flugge U.I. (1998) Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate phosphate antiporter. Plant Cell 10, 105-117.
54. Keeling P.L., Bacon P.J. & Holt D.C. (1993) Elevated temperature reduces starch deposition in wheat endosperm by reducing the activity of soluble starch synthase. Planta 191, 342-348.
55. Keeling P.L., Wood J.R., Tyson R.W. & Bridges I.G. (1988) Starch biosynthesis in developing wheat grain. Plant Physiology 87, 311-319.
56. Koch K.E. (1996) Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 509-540.
57. Kossmann J. & Lloyd J. (2000) Understanding and influencing starch biochemistry. Critical Review of Plant Science 19, 171-226.
58. Loef I., Stitt M. & Geigenberger P. (1999) Orotate leads to a specific increase in uridine nucleotide levels and a stimulation of sucrose degradation and starch synthesis in discs from growing potato tubers. Planta 209, 782-791.
59. Loef I., Stitt M. & 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.
60. Marshall J., Sidebottom C., Debet M., Martin C., Smith A.M. & Edwards A. (1996) Identification of the major starch synthase in the soluble fraction of potato tubers. Plant Cell 8, 1121-1135.
61. Martin C. & Smith A.M. (1995) Starch biosynthesis. Plant Cell 7, 971-985.
62. Merlo L., Geigenberger P., Hajirezaei M. & Stitt M. (1993) Changes of carbohydrates, metabolites and enzyme activities in potato tubers during development, and within a single tuber along a stolon apex gradient. Journal of Plant Physiology 144, 392-402.
63. Müller-Röber B., Kossmann J., Hannah L.C., Willmitzer L. & Sonnewald U. (1990) One of 2 different ADP-glucose pyrophosphorylase genes from potato responds strongly to elevated levels of sucrose. Molecular and General Genetics 224, 136-146.
64. Müller-Röber B., Sonnewald U. & Willmitzer L. (1992) Antisense inhibition of the ADPglucose pyrophosphorylase in transgenic potato leads to starch storing tubers and influences tuber formation and expression of tuber storage protein genes. EMBO Journal 11, 1229-1238.
65. Murata T. (1972) Sucrose synthase of rice grains and potato tubers. Agricultural and Biological Chemistry 36, 1815-1818.
66. Neuhaus H.E., Kruckleberg A.L., Feil R. & Stitt M. (1989) Reduced activity of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana 2. Study of the mechanisms which regulate photosynthate partitioning. Planta 178, 110-122.
67. Neuhaus H.E. & Stitt M. (1990) Control analysis of photosynthate partitioning- Impact of reduced activity of ADPglucose pyrophosphorylase or plastid phosphoglucomutase on the fluxes to starch and sucrose in Arabidposis thaliana (L) Heynh. Planta 182, 445-454.
68. Nielsen T.H., Krapp A., Roper-Schwarz U. & Stitt M. (1998) The sugar-mediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP glucose pyrophosphorylase is modified by phosphate and nitrogen. Plant, Cell and Environment 21, 443-454.
69. Okita T.W., Nakata P.A., Anderson J.M., Sowokinos S.J., Morell M. & Preiss J. (1990) The subunit structure of potato tuber ADPglucose pyrophosphorylase. Plant Physiology 93, 785-790.
70. Poolman M.G., Fell D.A. & Thomas S. (2000) Modelling photosynthesis and its control. Journal of Experimental Botany 51, 319-328.
71. Preiss J. (1988) Biosynthesis of starch and its regulation. In: The Biochemistry of Plants Vol. 14 (ed. J. Preiss), pp. 181-254. Academic Press, New York, USA.
72. Purcell P.C., Smith A.M. & 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 Journal 14, 195-202.
73. Quick P., Siegl G., Neuhaus E., Feil R. & Stitt M. (1989) Short-term water-stress leads to a stimulation of sucrose synthesis by activating sucrose phosphate synthase. Planta 177, 535-546.
74. ap Rees T. & Hill S.A. (1994) Metabolic control analysis of plant metabolism. Plant Cell and Environment 17, 587-599.
75. Regierer B., Fernie A.R., Springer F., Perez-Melis A., Leisse A., Koehl K., Willmitzer L., Geigenberger P. & Kossmann J. (2002) Starch content and yield increase as a result of altering adenylate pools in transgenic plants. Nature Biotechnology 20, 1256-1260.
76. Reimholz R., Geigenberger P. & Stitt M. (1994) Sucrose-phosphate synthase is regulated via metabolites and protein phosphorylation in potato tubers, in a manner analogous to the enzyme in leaves. Planta 192, 480-488.
77. Renz A., Merlo L. & Stitt M. (1993) Partial purification from potato tubers of three fructokinases and three hexokinases which show differing organ and developmental specificities. Planta 190, 156-165.
78. Renz A. & Stitt M. (1993) Substrate specificity and product inhibition of different forms of fructokinases and hexokinases in developing potato tubers. Planta 190, 156-165.
79. Rolleston F.S. (1972) A theoretical background to the use of measured intermediates in the study of the control of intermediary metabolism. Current Topics in Cell Regulation 5, 47-54.
80. Salanobat M. & Belliard G. (1989) The steady-state level of potato sucrose synthase messenger RNA is dependent on wounding, anaeobiosis and sucrose concentration. Gene 84, 181-185.
81. Savageau M.A. (1971) Parameter sensitivity as a criterion for evaluating and comparing the performance of biochemical systems. Nature 229, 542-544.
82. Scheible W.R., Gonzalez Fontes A., Lauerer M., MullerRober B., Caboche M. & Stitt M. (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9, 783-798.
83. Schomburg I., Chang A. & Schomburg D. (2002) BRENDA, enzyme data and metabolic information. Nucleic Acids Research 30, 47-49.
84. Schuster S., Fell D.A. & Dandekar T. (2000) A general definition of metabolic pathways useful for systematic organisation and analysis of complex metabolic networks. Nature Biotechnology 18, 326-361.
85. Siegl G., MacKintosch C. & Stitt M. (1990) Sucrose phosphate synthase is dephosphorylated by protein phosphatase 2A in spinach leaves - evidence form the effects of okadaic acid and microcystin. FEBS Letters 270, 198-202.
86. Smith A.M., Denyer K. & Martin C.R. (1995) What controls the amount and structure of starch in storage organs. Plant Physiology 107, 673-677.
87. Sokolov L.N., Dejardin A. & Kleczkowski L.A. (1998) Sugars and light/dark exposure trigger differential regulation of ADP-glucose pyrophosphorylase genes in Arabidopsis thaliana (thale cress). Biochemistry Journal 336, 681-687.
88. Sowokinos J.R. (1981) Pyrophosphorylases in Solanum tuberosum. II. Catalytic properties and regulation of ADPglucose pyrophosphorylase and UDPglucose pyrophosphorylase activities in potato tubers. Plant Physiology 68, 924-929.
89. Sowokinos J.R. & Preiss J. (1982) Phosphorylases in Solanum tuberosum. III. Purification, physical and catalytic properties of ADPglucose pyrophosphorylase in potatoes. Plant Physiology 69, 1459-1466.
90. Sowokinos J.R., Spychalla J.P. & Desborough S.L. (1993) Pyrophosphorylases in Solanum tuberosum. IV. Purification, tissue localisation, and physiochemical properties of UDPglucose pyrophosphorylase. Plant Physiology 101, 1073-1080.
91. Stark D.M., Timmerman K.P., Barry G.F., Preiss J. & Kishore G.M. (1992) Regulation of the amount of starch in plant tissues by ADPglucose pyrophosphorylase. Science 258, 287-292.
92. Stitt M. (1990) Application of control analysis to photosynthetic sucrose synthesis. In Control of Metabolic Processes (eds A. Cornish-Bowden & M.L. Cardenas). Plenum Press, New York, USA.
93. Stitt M. (1994) Flux control at the level of the pathway: studies with mutants and transgenic plants having a decreased activity of enzymes involved in photosynthesis partitioning. In Flux Control in Biological Systems, pp. 13-34. Academic Press Inc. New York, USA.
94. Stitt M. (1999) The first will be the last and the last will be first. non-regulated enzymes call the tune?. In Plant Carbohydrate Biochemistry (eds J.A. Bryant, M.M. Burrell & N.J.Kruger), pp. 1-16. Bios Scientific, Oxford, UK.
95. Stitt M., Lilley R.M., Gerhardt R. & Heldt H.W. (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods in Enzymology 174, 518-550.
96. Stitt M., Lilley R.M. & Heldt H.W. (1982) Adenine nucleotide levels in the cytosol, chloroplast and mitochondria of wheat leaf protoplasts. Plant Physiology 70, 971-977.
97. Stitt M. & Sonnewald U. (1995) Regulation of metabolism in transgenic plants. Annual Review of Plant Physiology 46, 341-368.
98. Sweetlove L.J.,Müller-Röber B., Willmitzer L. & Hill S.A. (1999) The contribution of adenosine 5′-diphosphoglucose pyrophosphorylase to the control of starch synthesis in potato tubers. Planta 209, 330-337.
99. Tauberger E., Fernie A.R., Emmermenn M., Renz A., Kossmann J., Willmitzer L. & Trethewey R.N. (2000) Antisense inhibition of plastidial phosphoglucomutase provides compelling evidence that potato tuber amyloplasts import carbon from the cytosol in the form of glucose 6-phosphate. Plant Journal 23, 43-53.
100. Thimm O., Bläsing O., Gibon Y., Nagel A., Meyer S., Krüger P., Selbig J., Müller L.A., Rhee S.Y. & Stitt M. (2004) MapMan: A user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant Journal XX, 00-00. (provisionally accepted).
101. Tiessen A., Hendriks J.H.M., Stitt M., Branscheid A., Gibon Y., Farre E.M. & 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.
102. Tiessen A., Prescha K., Branscheid A., Palacios N., McKibbin R., Halford N.G. & Geigenberger P. (2003) 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 35, 490-500.
103. Tjaden J., Möhlmann T., Kampfenkel K., Henrichs G. & Neuhaus H.E. (1998) Altered plastidic ATP/ADP transporter activity influences potato (Solanum tuberosum) tuber morphology, yield and composition of tuber starch. Plant Journal 16, 531-540.
104. Toroser D. & Huber S.C. (1997) Protein phosphorylation as a mechanism for osmotic-stress activation of sucrose-phosphate synthase in spinach leaves. Plant Physiology 114, 947-955.
105. Toroser D., Athwal G.S. & Huber S.C. (1998) Site-specific regulatory interaction between spinach leaf sucrose-phosphate synthase and 14-3-3 proteins. FEBS Letters 435, 110-114.
106. Toroser D., McMichael R., Krause K.P., Kurreck J., Sonnewald U., Stitt M. & Huber S.C. (1999) Site-directed mutagenesis of serine 158 demonstrates its role in spinach leaf sucrose-phosphate synthase modulation. Plant Journal 17, 407-413.
107. Trethewey R.N., Fernie A.R., Bachmann A., Fleischer-Notter H., Geigenberger P. & Willmitzer L. (2001) Glucose-independent induction of glycolysis in heterotrophic plant tissue. Plant, Cell and Environment 24, 357-365.
108. Trethewey R.N., Geigenberger P., Riedel K., Hajirzaei M.R., Sonnewald U., Stitt M., Riesmeier J.W. & 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 Journal 15, 109-118.
109. Trethewey R.N., Riesmeier J.W., Willmitzer L., Stitt M. & 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.
110. Veramendi J., Fernie A.R., Leisse A., Willmitzer L. & 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 Molecular Biology 49, 491-501.
111. Veramendi J., Roessner U., Renz A., Willmitzer L. & 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 Physiology 121, 1-11.
112. Viola R., Davies H.V. & Chudeck A.R. (1991) Pathways of starch and sucrose biosynthesis in developing tubers of potato (Solanum tuberosum L.) and seeds of faba bean (Vicia faba L.). Elucidation by 13C-nuclear-magnetic- resonance spectroscopy. Planta 183, 203-208.
113. Viola R., Roberts A.G., Haupt S., Gazzani S., Hancock R.D., Marmiroli N., Machray G.G. & Oparka K.J. (2001) Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13, 385-398.
114. Weiner H., McMichael R.W. & Huber S.C. (1992) Identification of factors regulating the phosphorylation status of sucrose phosphate synthase in vivo. Plant Physiology 99, 1435-1442.
115. Willmitzer L., Kossmann J., Müller-Röber B. & Sonnewald U. (1993) Starch synthesis in transgenic plants. In Plant Polymeric Carbohydrates (eds F. Meuser, D.J. Manners, & W. Seibel), pp. 33-39. Royal Society of Chemistry, Cambridge, UK.
116. Winter H. & Huber S.C. (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Critical Reviews in Molecular Biochemistry 35, 253-289.
117. Winter H., Huber J.L. & Huber S.C. (1997) Membrane association of sucrose synthase: changes during the graviresponse and possible control by protein phosphorylation. FEBS Letts 420, 151-155.
118. Zeng Y., Wu W., Avigne W.T. & Koch K.E. (1998) Differential regulation of sucrose-sensitive sucrose synthases by hypoxia and anoxia indicate complementary transcriptional and post-transcriptional reponses. Plant Physiology 116, 1573-1583.
119. Zeng Y., Wu Y., Avigne W.T. & Koch K.E. (1999) Rapid repression of maize invertases by low oxygen. Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Plant Physiology 121, 599-608.
120. Zrenner R., Salanoubat M., Willmitzer L. & Sonnewald U. (1995) Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants. Plant Journal 7, 97-107.
121. Zrenner R., Willmitzer L. & Sonnewald U. (1993) Analysis of the expression of potato uridinediphosphoglucose pyrophosphorylase and its inhibition by antisense RNA. Planta 190, 247-252.