Abstract
In green leaves and a number of algae, photosynthetically derived carbon is ultimately converted into two carbohydrate end-products, sucrose and starch. Drainage of carbon from the Calvin cycle proceeds via triose phosphate, fructose 6-phosphate and glycollate. Gluconeogenesis in photosynthetic cells is controlled by light, inorganic phosphate and phosphorylated sugars. Light stimulates the production of dihydroxyacetone phosphate, the initial substrate for sucrose and starch synthesis, and inhibits the degradative pathways in the chloroplast. Phosphate inactivates reactions of synthesis and activates reactions of degradation. Among the phosphorylated sugars a special role is allocated to fructose 2,6-bisphosphate, which is present in the cytoplasm at very low concentrations and inhibits sucrose synthesis directly by inactivating pyrophosphatedependent phosphofructokinase. The synthesis of sucrose plays a central role in the partitioning of photosynthetic carbon. The cytoplasmic enzymes, fructose bisphosphate phosphatase and sucrose phosphate synthase are likely key points of regulation. The regulation is carried out by several effector metabolites. Fructose 2,6-bisphosphate is likely to be the main coordinator of the rate of sucrose synthesis, hence of photosynthetic carbon partitioning between sucrose and starch.
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References
Amir J and Preiss J (1982) Kinetic characterization of spinach leaf sucrose-phosphate synthase. Plant Physiol 69: 1027–1030
Anderson LE, Hansen MJ and Anderson JB (1979) Light-dark modulation of phosphoglucomutase activity in pea leaf chloroplasts. Plant physiol 63 (Suppl): 2
Avigad G (1982) Sucrose and other disaccharides. In Loewus A and Tanner W (ed) Plant carbohydrates I Intracellular carbohydrates. Encyclopedia of Plant Physiol new series, Springer Verlag Berlin Heidelberg New York, Vol 13A pp 217–347
Balogh A, Wong JH, Wötzel C, Soll J, Cséke C and Buchanan BB (1984) Metabolitemediated catalyst conversion of PFK and PFP: a mechanism of enzyme regulation in green plants. FEBS Lett 169: 287–292
Bassham JA, Benson AA, Kay LD, Harris AZ, Wilson AT and Calvin M (1954) The path of carbon in photosynthesis. XXI. J Amer Chem Soc 76: 1760–1770
Bird IF, Cornelius MJ, Keys MT and Whittingham CP (1974) Intracellular site of sucrose synthesis in leaves. Phytochemistry 13: 59–64
Bourdu R, Champigny ML, Lefort M, Maslow M and Moyse A (1965) Structure et activités de l'appareil photosynthétique des feuilles de Bryophyllum diagremontianum Berger, en fonction de leur croissance, de la carence et de la nutrition azotées. Physiol Vég 3: 355–392
Buchanan L, Lynch VH, Benson AA, Braney DF and Calvin M (1953) The path of carbon in photosynthesis. XVIII. The identification of nucleotide coenzymes. J Biol Chem 203: 935–945
Champigny ML (1976) La Régulation du cycle de Calvin. Physiol Vég 14: 607–628
Champigny ML, Bismuth E and Sarda C (1982) Analyse des relations géniques entre formes spontanées et cultivées chez le mil à chandelle. IV.—Croissance, accumulation d'amidon chez les parents et chez les hybrides réciproques de première génération entre un écotype de Pennisetum mollissimum Hochst (forme spontanée) et une forme cultivée Pennisetum americanum (L.) Leeke. Agronomie 2: 365–372
Champigny ML and Moyse A (1979) Photosynthatic carbon metabolism in wild, primitive and cultivated forms of wheat at three levels of ploidy: role of the glycolate pathway. Physiol Vég 20: 1167–1168
Chatterton NJ and Silvius JE (1980) Photosynthate partitioning into leaf starch as affected by daily photosynthetic period duration in six species. Physiol Plant 49: 141–144
Cséke C and Buchanan BB (1983) An enzyme synthesizing fructose 2,6-bisphosphate occurs in leaves and is regulated by metabolite effectors. FEBS Lett 155: 139–142
Cséke C, Weeden NF, Buchanan BB and Uyeda K (1982) A special fructose bisphosphate functions as a cytoplasmic regulatory metabolite in green leaves. Proc Natl Acad Sci USA 79: 4322–4326
Doehlert DG and Huber SC (1983) Spinach leaf sucrose phosphate synthase: activation by glucose-6-phosphate and interaction with inorganic phosphate. FEBS Lett 153: 293–297
Fisher DB and Outlaw WH (1979) Sucrose compartmentation in the palidase parenchyma of Vicia faba L. Plant Physiol 64: 481–483
Fliege R, Flügge UI, Werdan K and Heldt HW (1978) Specific transport of inorganic phosphate, 3-phosphoglycerate and triosephosphates across the inner membrane of the envelope in spinach chloroplasts. Biochim Biophys Acta 502: 232–247
Flügge UI, Freisl M and Heldt HW (1980) Balance between metabolite accumulation and transport in relation to photosynthesis by isolated spinach chloroplasts. Plant Physiol 65: 574–577
Foyer C, Rowell J and Walker D (1983) The effect of sucrose on the rate of de novo sucrose biosynthesis in leaf protoplasts from spinach wheat and barley. Arch Biochem Biophys 220: 232–238
Ghosh HP and Preiss J (1965) The biosynthesis of starch in spinach chloroplasts. J Biol Chem 240: 960–961
Ghosh HP and Preiss J (1966) Adenosine diphosphate glucose pyrophosphorylase. A regulatory enzyme in the biosynthesis of starch in spinach leaf chloroplasts. J Biol Chem 241: 4491–4505
Harbron S, Foyer C and Walker D (1981) The purification and properties of sucrose-phosphate synthetase from spinach leaves: the involvement of this enzyme and sucrose bisphosphatase in the regulation of sucrose biosynthesis. Arch Biochem Biophys 212: 237–246
Hawker JS (1967) The activity of uridine diphosphate glucose-D-fructose 6-phosphate 2-glucosyltransferase in leaves. Biochem J 105: 943–949
Hawker JS, Marschner H and Downton WJS (1974) Effects of sodium and potassium on starch synthesis in leaves. Aust J Plant Physiol 1: 491–501
Hawker JS, Ozbun JL, Ozaki H, Greenburg E and Preiss J (1974) Interaction of spinach leaf adenosine diphosphate glucose α-4-glucan α-4-glucosyl transferase and α-1,4-glucan, α-1,4-glucan-6-glycosyl transferase in synthesis of branched α-glucan. Arch Biochem Biophys 160: 530–551
Heldt HW, Gardemann A, Gerhardt R, Herzog B, Stitt M and Wirtz W (1984) The regulation of CO2 fixation and of sucrose synthesis in plants. In Sybesma C (ed) Advances in photosynthesis research. Martinus Nijhoff/Dr W Junk Publishers, The Hague, Boston, Lancaster Vol II pp 617–624
Herold A (1980) Regulation of photosynthesis by sink activity — the missing link. New Phytol 86: 134–144
Hers HG and Van Schaftingen E (1982) Fructose 2,6-bisphosphate 2 years after its discovery. Biochem J 206: 1–12
Huber SC (1981) Inter-aand intra-specific variation in photosynthetic formation of starch and sucrose. Z Pflanzenphysiol 101: 49–54
Huber SC (1981) Interspecific variation in activity and regulation of leaf sucrose phosphate synthetase. Z Pflanzenphysiol 102: 443–450
Huber SC (1983) Role of sucrose-phosphate synthase in partitioning of carbon in leaves. Plant Physiol 71: 818–821
Huber SC and Bickett DM (1984) Evidence for control of carbon partitioning by fructose 2,6-bisphosphate in spinach leaves. Plant Physiol 74: 445–447
Huber SC and Israel DW (1982) Biochemical basis for partitioning of photosynthetically fixed carbon between starch and sucrose in soybean (Glycine max Merr.) leaves. Plant Physiol 69: 691–696
Huber SC, Rufty TWJr, Kerr PS and Doehlert D (1983) Different mechanisms for the regulation of sucrose phosphate synthase. A key enzyme in photosynthetic sucrose formation. In Randall DD, Blevine DG, Larson RL, Rapp BJ eds, Current Topics in Plant Biochemistry and Physiology, University of Missouri Columbia, Missouri USA, Vol. 2, pp 20–32
Kachru RB and Anderson LE (1975) Inactivation of pea leaf phosphofructokinase by light and dithiothreitol. Plant Physiol 55: 199–202
Kaiser G, Martinoia E and Wiemken A (1982) Rapid appearance of photosynthetic products in the vacuoles isolated from barley mesophyll protoplasts by a new fast method. Z Fflanzenphysiol 107: 103–113
Mendicino J (1960) Sucrose phosphate synthesis in wheat germ and green leaves. J Biol Chem 235: 3347–3352
Moyse A (1967) Les Chloroplastes: Activités photosynthétiques et métabolisme des glucides. Biochemistry of chloroplasts, in Goodwin TW (ed). Academic Press, London, New York, pp 91–129
Okita TW, Greenberg E, Kuhn D and Preiss DN (1979) Subcellular localization of the starch degradative and biosynthetic enzymes of spinach leaves. Plant Physiol 64: 187–192
Pollock CJ (1976) Changes in the activity of sucrose-synthesizing enzymes in developing leaves of Lolium temulentum. Plant Sci Lett 7: 27–31
Preiss J (1982) Regulation of the biosynthesis and degradation of starch. Annu Rev Plant Physiol 33: 431–454
Preiss J and Levi C (1980) Starch biosynthesis and degradation. In Preiss J (ed) The Biochemistry of Plants, Academic Press London New York, Vol 3, pp 371–423
Rufty TWJr and Huber SC (1983) Changes in starch formation and activities of sucrose phosphate synthase and cytoplasmic fructose-1,6-bisphosphatase in response to source-sink alteration. Plant Physiol 72: 474–480
Sachs J (1887) In Lectures of the physiology of plants (translated by HM Ward), Oxford Univ Press (Clarendon), London and New York, pp 304–325
Salerno GL and Pontis HG (1978) Studies on sucrose phosphate phosphatase. The inhibitory action of sucrose. FEBS Lett 86: 263–267
Steup M, Peavey DG and Gibbs M (1976) The regulation of starch metabolism by inorganic phosphate. Biochem Biophys Res Commun 72: 1554–1561
Stitt M, Gerhardt R, Kürzel B and Heldt HW (1983) A role for fructose 2,6-bisphosphate in the regulation of sucrose synthesis in spinach leaves. Plant Physiol 72: 1139–1141
Stitt M and Heldt HW (1981) Simultaneous synthesis and degradation of starch in spinach chloroplasts in the light. Biochim Biophys Acta 638: 1–11
Stitt M and Heldt HW (1981) Physiological rates of starch breakdown in isolated intact spinach chloroplasts. Plant Physiol 68: 755–761
Stitt M, Herzog B and Heldt HW (1984) Control of photosynthetic sucrose synthesis by fructose 2,6-bisphosphate. I. Coordination of CO2 fixation and sucrose synthesis. Plant Physiol 75: 548–553
Stitt M, Kurzel B and Heldt HW (1984) Control of photosynthetic sucrose 2,6-bisphosphate. II. Partitioning between sucrose and starch. Plant Physiol 75: 554–560
Stitt M, Mieskes G, Soling H-D and Heldt HW (1982) On a possible role of fructose 2,6-bisphosphate in regulating photosynthetic metabolism in leaves. FEBS Lett 145: 217–221
Stitt M, Wirtz W and Heldt HW (1983) Regulation of sucrose synthesis by cytoplasmic fructose bisphosphatase and sucrose phosphate synthase during photosynthesis in varying light and carbon dioxide. Plant Physiol 72: 767–774
Van Schaftingen E, Hue L and Hers HG (1980) Fructose 2,6-bisphosphate, the probable structure of the glucose and glucagon-sensitive stimulator of phosphofructokinase. Biochem J 192: 897–901
Wardlaw IF (1968) The control and pattern of movement of carbohydrates in plants. Bot Rev 34: 79–105
Whittingham CP, Keys AJ and Bird IF (1979) The enzymology of sucrose synthesis in leaves. In Gibbs M, Latzko A (ed) Photosynthesis II Photosynthetic carbon metabolism and related processes. Encyclopedia of Plant Physiol, new series, Springer-Verlag, Berlin, Heidelberg, New York, Vol 6, pp 313–326
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Champigny, M.L. Regulation of photosynthetic carbon assimilation at the cellular level: a review. Photosynth Res 6, 273–286 (1985). https://doi.org/10.1007/BF00049283
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DOI: https://doi.org/10.1007/BF00049283