Regulation of sucrose metabolism in higher plants: Localization and regulation of activity of key enzymes

Critical Reviews in Biochemistry and Molecular Biology

Volumn 35, Issue 4, 2000, Pages 253-289

  Winter, H ^a   Huber, S C ^b  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

14 3 3 proteins; Actin cytoskeleton; CDPK; Invertase; Regulatory protein phosphorylation; SNF1 protein kinase; Sucrose synthase; Sucrose phosphate synthase; Sucrose sensing; Translocation

Indexed keywords

BETA FRUCTOFURANOSIDASE; SUCROSE;

CARBOHYDRATE METABOLISM; CELL WALL; CYTOSKELETON; CYTOSOL; GENE EXPRESSION REGULATION; HYDROLYSIS; NONHUMAN; PHOTOSYNTHESIS; PLANT; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW;

EMBRYOPHYTA;

EID: 0033829914     PISSN: 10409238     EISSN: None     Source Type: Journal    
DOI: 10.1080/10409230008984165     Document Type: Review

References (216)

1. Amor, Y., Haigler, C. H., Johnson, S., Wainscott, M., and Delmer, D. P. 1995. 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. 92:9353-9357.
2. Anderson, L. E., Goldhaber, I. M., Li, D., Tang, X., Xiang, M., and Prakash, N. 1995. Enzyme-enzyme interaction in the chloroplast. Glyceraldehyde-3-P dehydrogenase, triose phosphate isomerase and aldolase. Planta 196:245-255.
3. Athwal, G. S., Huber, J. L., and Huber, S. C. 1998. Phosphorylated nitrate reductase and 14-3-3 proteins. Site of interaction, effects of ions, and evidence for an AMP-binding site on 14-3-3 proteins. Plant Physiol. 118:1041-1048.
4. Bachmann, M., Matile, P., and Keller, F. 1994. Metabolism of the raffinose family oligosaccharides in leaves of Ajuga reptans L. Cold acclimation, translocation, and sink to source transition: discovery of chain elongation enzyme. Plant Physiol. 105:1335-1345.
5. Bachmann, M., Shiraishi, N., Campbell, W. H., Yoo, B.-C., Harmon, A. C., and Huber, S. C. 1996. Identification of Ser-543 as the major regulatory phosphorylation site in spinach leaf nitrate reductase. Plant Cell 8:505-517.
6. Beebe, D. U. and Turgeon, R. 1992. Localization of galactinol, raffinose, and stachyose synthesis in Cucurbita pepo leaves. Planta 188:354-361.
7. Bell, R. M. and Burns, D. J. 1991. Lipid activation of protein kinase C. J. Biol. Chem. 266:4661-4664.
8. Braselmann, S. and McCormick, F. 1995. BCR and RAF form a complex in vivo via 14-3-3 proteins. EMBO J. 14:4839-4848.
9. + antiport. Plant Physiol. 78:871-875.
10. Bush, D. R. 1993. Proton-coupled sugar and amino acid transporters in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44:513-542.
11. Carlson, S. J. and Chourey, P. S. 1996. Evidence for plasma membrane-associated forms of sucrose synthase in maize. Mol. Gen. Genet. 252:303-310.
12. Castrillo, M. 1992. Sucrose metabolism in bean plants under water deficit. J. Exp. Botany 43:1557-1561.
13. Chen, J. Q. and Black, C. C. 1992. Biochemical and immunological properties of alkaline invertase isolated from sprouting soybean hypocotyls. Arch. Biochem. Biophys. 295:61-69.
14. Chen, Y. C. and Chourey, P. S. 1989. Spatial and temporal expression of the two sucrose synthase genes in maize: immunohistological evidence. Theor. Appl. Genet. 78:5553-559.
15. Chiou, T.-J. and Bush, D. R. 1998. Sucrose is a signal molecule in assimilate partitioning. Proc. Natl. Acad. Sci. U.S.A. 95:4784-4788.
16. Chopra, S., Del-Favero, J., Dolferus, R. and Jacobs, M. 1992. Sucrose synthase of arabidopsis: genomic cloning and sequence characterization. Plant Mol. Biol. 18:131-134.
17. Chourey, P. S. and Taliercio, E. W. 1994. Epistatic interaction and functional compensation between the two tissue and cell-specific sucrose synthase genes in maize. Proc. Natl. Acad. Sci. U.S.A. 91:7917-7921.
18. Chourey, P. S., Taliercio, E. W., Carlson, S. J., and Ruan, Y.-L. 1998. Genetic evidence that the two isoenzymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Mol. Gen. Genet. 259:88-96.
19. Clegg, J. S. 1992. Cellular infrastructure and metabolic organization. Cell Regul. 33:3-14.
20. Datcheva, M., Buster, D., Vulliet, R., and Delmer, D. 1998. Membrane-associated sucrose synthase: mechanism of membrane association and role in glucan synthesis. Plant Polysaccharide Symposium, Davis, CA.
21. Déjardin, A., Rochat, C., Wuillèm, S., and Boulin, J.-P. 1997. Contribution of sucrose synthase, ADP-glucose pyrophosphorylase and starch synthase to starch synthesis in developing pea seeds. Plant Cell Environ. 20:1421-1430.
22. Doehlert, D. C. and Huber, S. C. 1983. Regulation of spinach leaf sucrose phosphate synthase by glucose-6-phosphate, inorganic phosphate and pH. Plant Physiol. 73:989-994.
23. Doehlert, D. C. and Huber, S. C. 1983. Spinach leaf sucrose phosphate synthase. Activation by glucose 6-phosphate and interaction with inorganic phosphate. FEBS Lett. 153:293-297.
24. Doehlert, D. C. and Huber, S. C. 1985. The role of sulfhydryl groups in the regulation of spinach leaf sucrose-phosphate synthase. Biochim. Biophys. Acta 830:267-273.
25. Douglas, P., Pigaglio, E., Ferrer, A., Halford, N. G., and MacKintosh, C. 1996. Three spinach leaf nitrate reductase/3-hydroxy-3-methylglutaryl-CoA reductase kinases that are regulated by reversible phosphorylation and/or calcium ions. Biochem. J. 325:101-109.
26. Duchateau, N., Bortlik, K., Simmen, U., Wiemken, A., and Bancal, P. 1995. Sucrose: fructan 6-fructosyltransferase, a key enzyme for diverting carbon from sucrose to fructan in barley leaves. Plant Physiol. 107:1249-1255.
27. Echeverria, E., Salvucci, M. E., Gonzalez, P., Paris, G., and Salerno, G. 1997. Physical and kinetic evidence for an association between sucrose-phosphate synthase and sucrose-phosphate phosphatase. Plant Physiol. 115:223-227.
28. Edelman, J. and Jefford, T. G. 1968. The mechanism of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus L. New Phytol. 67:517-531.
29. Ernes, M. J. and Neuhaus, H. E. 1997. Metabolism and transport in non-photosynthetic plastids. J. Exp. Bot. 48:1995-2005.
30. Escherich, W. 1980. Free space invertase, its possible role in phloem unloading. Ber. Deut. Bot. Ges. 93:363-378.
31. Fu, H., Kim, S. Y., and Park, W. D. 1995. High-level tuber expression and sucrose inducibility of a potato sus4 sucrose synthase gene requires 5′ and 3′ flanking sequences and the leader intron. Plant Cell 7:1387-1394.
32. Fu, H., Kim, S. Y., and Park, W. D. 1995. 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 7:1395-1403.
33. Fu, H. and Park, W. D. 1995. Sink- and vascular-associated sucrose synthase functions are encoded by different gene clases in potato. Plant Cell 7:1369-1385.
34. Gaertner, F. H. 1978. Unique catalytic properties of enzyme clusters. Trends Biochem. Sci. 3:63-65.
35. Gallagher, J. A. and Pollock, C. J. 1998. Isolation and characterization of a cDNA clone from Lolium temulentum L. encoding for a sucrose hydrolytic enzyme which shows alkaline/neutral invertase activity. J. Exp. Botany 49:789-795.
36. Galtier, N., Foyer, C. H., Huber, J., Voelker, T. A. and Huber, S. C. 1993. Effects of elevated sucrose phosphate synthase activity on photosynthesis, assimilate partitioning and growth in tomato (Lycopersicon esculentum var. UC82B). Plant Physiol. 101:535-543.
37. Galtier, N., Foyer, C. H., Murkie, E., Alred, R., Quick, P., Voelker, T. A., Thepenier, C., Lasceve, G., and Betsche, T. 1995. Effects of light and atmospheric carbon dioxide enrichment on photosynthesis and carbon partitioning in the leaves of tomato (Lycopersicon esculentum L.) plants overexpressing sucrose phosphate synthase. J. Exp. Botany 46:1335-1344.
38. Geigenberger, P., Krause, K.-P., Hill, L. M., Reimholz, R., MacRae, E., Quick, P., Sonnewald, U., and Stitt, M., Eds. (1995). The regulation of sucrose synthesis in leaves and tubers of potato plants. Sucrose Metabolism, Biochemistry, Physiology and Molecular Biology. Rockville, MD, American Society of Plant Physiologists.
39. Geigenberger, P., Reimholz, R., Geiger, M., Merlo, L., Canale, V., and Stitt, M. 1997. Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta 201:502-518.
40. Gerhardt, R., Stitt, M., and Heldt, H. W. 1987. Subcellular metabolite levels in spinach leaves. Plant Physiol. 83:399-403.
41. Getz, H.-P. 1991. Sucrose transport in tonoplast vesicles of red beet roots is linked to ATP hydrolysis. Planta 185:261-268.
42. Giegenberger, P., Geiger, M., and Stitt, M. 1998. High-temperature perturbation of starch synthesis is attributable to inhibition of ADP-glucose pyrophosphorylase by decreased levels of glycerate-3-phosphate in growing potato tubers. Plant Physiol. 117:1307-1316.
43. Gierson, C., Du, J.-S., de Torres Zabala, M., Beggs, K., Smith, C., Haldsworth, M., and Bevan, M. 1994. Separate cis sequences and trans factors direct metabolic and developmental regulation of a potato tuber storage protein gene. Plant J. 5:815-826.
44. Greiner, S., Krausgrill, S. and Rausch, T. 1998. Cloning of a tobacco apoplasmic invertase inhibitor. Proof of function of the recombinant protein and expression analysis during plant development. Plant Physiol. 116:733-742.
45. Guglielminetti, L., Alpi, A., and Perata, P. 1996. Shrunken-1-encoded sucrose synthase is not required for the sucrose-ethanol transition in maize under anaerobic conditions. Plant Sci. 119:1-10.
46. Guglielminetti, L., Perata, P., and Alpi, A. 1995. Effect of anoxia on carbohydrate metabolism in rice seedlings. Plant Physiol. 108:735-741.
47. Guy, C. L., Huber, J. L., and Huber, S. C. 1992. Sucrose phosphate synthase and sucrose accumulation at low temperature. Plant Physiol. 100:502-508.
48. 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.
49. Haouazine-Takvorian, N., Tymowska-Lalanne, Z., Takvorian, A., Tregear, J., Lejeune, B., Lecharny, A., and Kreis, M. 1997. Characterization of two members of the Arabidopsis thaliana gene family, Atβfruct3 and Atβfruct4, coding for vacuolar invertases. Gene 197:239-251.
50. Hare, P. D., Cress, W. A., and Van Staden, J. 1998. Dissecting the roles of osmolyte accumulation during stress. Plant, Cell, Environ. 21:535-553.
51. Haritatos, E. and Turgeon, R. 1995. Symplastic phloem loading by polymer trapping. In: Sucrose Metabolism, Biochemistry, Physiology and Molecular Biology, Pontis, H. G., Salerno, G. L., and Echeverria, E. J., Eds., American Society of Plant Physiologists, Rockville, 216-224.
52. +-ATPase genes from potato. Plant Mol. Biol. 26:979-988.
53. Heineke, D., Sonnewald, U., Büssis, D., Günter, G., Leidreiter, K., Wilke, I., Raschke, K., Willmitzer, L., and Heldt, H. W. 1992. Apoplastic expression of yeast-derived invertase in potato: effect on photosynthesis, leaf solute composition, water relations, and tuber composition. Plant Physiol. 100:301-308.
54. Heinlein, M. and Starlinger, P. 1989. Tissue-and cell-specific expression of the two sucrose synthase isoenzymes in developing maize kernels. Mol. Gen. Genet. 215:441-446.
55. Heldt, H. W. and Sauer, R. 1971. The inner membrane of the chloroplast envelope as the site of specific metabolite transport. Biochim. Biophys. Acta 234:83-91.
56. Hendrix, D. L. and Huber, S. C. 1986. Diurnal fluctuations in cotton leaf carbon export, carbohydrate content, and sucrose synthesizing enzymes. Plant Physiol. 81:584-586.
57. Herbers, K., Meuwly, P., Frommer, W. B., Metrauc, J. P., and Sonnewald, U. 1996. Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793-803.
58. Hill, L. M., Reimholz, R., Schröder, R., Nielsen, T. H., and Stitt, M. 1996. The onset of sucrose accumulation in cold-stored potato tubers is caused by an increased rate of sucrose synthesis and coincides with low levels of hexose-phosphates, an activation of sucrose phosphate synthase and the appearance of a new form of amylase. Plant, Cell, Environ. 19:1223-1237.
59. Holaday, A. S., Martindale, W., Alred, R., Brooks, A., and Leegood, R. C. 1992. Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low temperature. Plant Physiol. 98:1105-1114.
60. Hole, D. J., Cobb, B. G., Hole, P. S., and Drew, M. C. 1992. Enhancement of anerobic respiration in root tips of Zea mays following low-oxygen (hypoxic) acclimation. Plant Physiol. 99:213-218.
61. Holtaus, U. and Schmitz, K. 1991. Distribution and immunolocalization of stachyose synthase in Cucurbita melo L. Planta 185:479-486.
62. Houweling, M., Jamil, H., Hatch, G. M., and Vance, D. E. 1994. Dephosphorylation of CTP-phosphocholine cytidyltransferase is not required for binding to membranes. J. Biol. Chem. 269:7544-7551.
63. Huang, J. W., Chen, J. T., Yu, W. P., Shyur, L. G., Wang, A. Y., Sung, H. Y., Lee, P. D., and Su, J. C. 1996. Complete structures of three rice sucrose synthase isogenes and differential regulation of their expressions. Biosci. Biotechnol. Biochem. 60:233-239.
64. Huber, J. L. A. and Huber, S. C. 1992. Site-specific serine phosphorylation of spinach leaf sucrose-phosphate synthase. Biochem. J. 283:877-882.
65. Huber, S. C. 1989. Biochemical mechanism for regulation of sucrose accumulation in leaves during photosynthesis. Plant Physiol. 91:656-662.
66. Huber, S. C. and Huber, J. L. 1991. In vitro phosphorylation and inactivation of spinach leaf sucrose-phosphate synthase by an endogenous protein kinase. Biochim. Biophys. Acta 1091:393-400.
67. Huber, S. C. and Huber, J. L. 1991. Regulation of maize leaf sucrose-phosphate synthase by protein phosphorylation. Plant Cell Physiol. 32:319-326.
68. Huber, S. C. and Huber, J. L. 1996. Role and regulation of sucrose-phosphate synthase in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:431-444.
69. Huber, S. C., Huber, J. L., Liao, P.-C., Gage, D. A., McMichael, R. W., Chourey, P. S., Hannah, L. C., and Koch, K. 1996. Phosphorylation of Ser-15 of maize leaf sucrose synthase: occurrence in vivo and possible regulatory significance. Plant Physiol. 112:793-802.
70. Huber, S. C., Huber, J. L., and Pharr, D. M. 1993. Assimilate partitioning and utilization in source and sink tissues. In: International Crop Science I, 789-797. Buxton, D. R., Shibles, R., Forsberg, R. A., et al., Eds., Crop Science Society of America, Inc. Madison, WI.
71. Huber, S. C., Huber, J. L. A., and McMichael, R. W., Jr. 1992. The regulation of sucrose synthesis in leaves. In: Carbon Partitioning within and between Organisms. Pollock, C. J., Farrar, J. F., and A. J. Gordon Eds., BIOS Scientific Publishers Ltd., Oxford, 1-25.
72. Huber, S. C. and Kaiser, W. M. 1996. 5-Aminoimidazole-4-carboxamide riboside activates nitrate reductase in darkened spinach and pea leaves. Physiol. Plant. 98:833-837.
73. Huber, S. C., Kaiser, W. M., Toroser, D., Athwal, G. S., Winter, H., and Huber, J. L. 1999. Regulation of sucrose metabolism by protein phosphorylation. Stimulation of sucrose synthesis by osmotic stress and 5-aminoimidazole-4-carboxamide riboside. In: Carbohydrate Metabolism in Plants, Bryant, J., Burrell, M., and Kruger, N., Eds., BIOS Scientific Publishers Ltd., Oxford, 61-68.
74. Huber, S. C., Kerr, P. S., and Kalt-Torres, W. 1985. Regulation of sucrose formation and movement. In: Regulation of Carbohydrate Partitioning in Photosynthetic Tissue, Preiss, J. and Heath, R., Eds., Waverly Press, Baltimore, MD, 199-214.
75. Huber, S. C., McMichael, R. W., Jr., Bachmann, M., Huber, J. L., Shannon, J. C., Kang, K.-K., and Paul, M. 1996. Regulation of leaf sucrose-phosphate synthase and nitrate reductase by reversible protein phosphorylation. In: Protein Phosphorylation in Plants, Shewry, P. R., Halford, N. G., and Hooley, R., Eds., Clarendon Press, Oxford, 19-34.
76. 2+]. In: Carbon Partitioning and Source-Sink Interactions in Plants, Madore, M. A. and Lucas, W. J., Eds., American Society of Plant Physiologists Rockville, 35-44.
77. Huber, S. C., Nielsen, T. H., Huber, J. L. A., and Pharr, D. M. 1989. Variation among species in light activation of sucrose-phosphate synthase. Plant Cell Physiol. 30:277-285.
78. Huber, S. C., Toroser, D., Winter, H., Athwal, G. S., and Huber, J. L. 1998. Regulation of plant metabolism by protein phosphorylation. Possible regulation of sucrose-phosphate synthase by 14-3-3 proteins. XIth International Photosynthesis Congress, Budapest, Hungary, Kluwer Academic Publishers.
79. Ishiguro, S. and Nakamura, K. 1992. The nuclear factor SP8BF binds to the 5′-upstream regions of three different genes coding for major proteins of sweet potato tuberous roots. Plant Mol. Biol. 18:97-108.
80. Iyer, S. and Caplan, A. 1998. Products of proline catabolism can induce osmotically regulated genes in rice. Plant Physiol. 116:203-211.
81. Jang, J.-C., Leon, P., Zhou, L., and Sheen, J. 1997. Hexokinase as a sugar sensor in higher plants. The Plant Cell 9:5-19.
82. Jeong, B.-R. and Housley, T. L. 1990. Fructan metabolism in wheat in alternating warm and cold environments. Plant Physiol. 93:902-906.
83. Jones, D. H., Ley, S., and Aitken, A. 1995. Isoforms of 14-3-3 protein can form homo- and heterodimers in vivo and in vitro: implications for function as adapter proteins. FEBS Lett. 368:55-58.
84. Jones, T. L. and Ort, D. R. 1997. Circadian regulation of sucrose phosphate synthase activity in tomato by protein phosphorylation activity. Plant Physiol. 113:1167-1175.
85. Jones, T. L., Tucker, D. E., and Ort, D. R. 1998. Chilling delays circadian pattern of sucrose phosphate synthase and nitrate reductase activity in tomato. Plant Physiol. 118:149-158.
86. Kaiser, G. and Heber, U. 1984. Sucrose transport into vacuoles isolated from barley mesophyll protoplasts. Planta 91:656-662.
87. Kaiser, W. M. and Huber, S. C. 1997. Correlation between apparent phosphorylation state of nitrate reductase (NR), NR hysteresis and degradation of NR protein. J. Exp. Botany 48:1367-1374.
88. Kallarackal, J., Orlich, G., Schobert, C., and Komor, E. 1989. Sucrose transport into the phloem of Ricinus communis L. seedlings as measured by the analysis of sieve tube sap. Planta 177:327-335.
89. Kaurin, A., Junttila, O., and Hansen, J. 1981. Seasonal changes in frost hardiness in cloudberry (Rubus chamaemorus) in relation to carbohydrate content with special reference to sucrose. Plant Physiol. 52:310-314.
90. Keller, F. 1992. Transport of stachyose and sucrose by vacuoles of Japanese artichoke (Stachys sieboldii) tubers. Plant Physiol. 98:442-445.
91. Kennelly, P. J. and Krebs, E. G. 1991. Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266:15555-15558.
92. Kerr, P. S. and Huber, S. C. 1987. Coordinate control of sucrose formation in soybean leaves by sucrose-phosphate synthase and fructose-2,6-bisphosphate. Planta 170:197-204.
93. Kerr, P. S., Pearlstein, R. W., Schweiger, B. J., Becker-Manley, M. F., and Pierce, J. W. 1993. Nucleotide sequences of galactinol synthase from zucchini and soybean.
94. Kerr, P. S., Rufty, T. W., Jr., and Huber, S. C. 1985. Endogenous rhythms in photosynthesis, sucrose phosphate synthase activity, and stomatal resistance in leaves of soybean (Glycine max [L.] Merr.). Plant Physiol. 77:275-280.
95. Kim, S. Y., May, G. D., and Park, W. D. 1994. Nuclear factors binding to a class-I patatin promoter region are tuber specific and sucrose inducible. Plant Mol. Biol. 26:603-615.
96. Klann, E. M., Hall, B., and Bennett, A. B. 1996. Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit. Plant Physiol 112:1321-1330.
97. Klein, R. R., Crafts-Brandner, S. J., and Salvucci, M. E. 1993. Cloning and developmental expression of the sucrose-phosphate-synthae gene from spinach. Planta 190:498-510.
98. Koch, K. E. 1996. Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:509-540.
99. Koch, K. E., Nolte, K. D., Duke, E. R., McCarty, D. R., and Avigne, W. T. 1992. Sugar levels modulate differential expression of maize sucrose synthase genes. Plant Cell 4:59-69.
100. Koch, K. E., Xu, J., Duke, E. R., McCarty, D. R., Yuan, C.-X., Tan, B.-C., and Avigne, W. T. 1995. Sucrose provides a long distance signal for coarse control of genes affecting its metabolism. In: Sucrose Metabolism, Biochemistry, Physiology and Molecular Biology, Pontis, H. G., Salerno, H. G., and Echeverria, E., Eds., American Soc. Plant Physiol., Rockville, MD, 266-277.
101. Krause, K.-P. 1994. Zur Regulation von Saccharose-phosphatsynthase. Bayreuth, Universitat Bayreuth.
102. Krause, K.-P., Hill, L., Reimholz, R., Nielsen, T. H., Sonnewald, U., and Stitt, M. 1998. Sucrose metabolism in cold-stored potato tubers with decreased expression of sucrose phosphate synthase. Plant, Cell, Environ. 21:285-299.
103. Krausegrill, S., Greiner, S., Kröger, U., Vogel, R., and Rausch, T. 1998. In transformed tobacco cells the apoplasmic invertase inhibitor operates as a regulatory switch of cell wall invertase. The Plant J. 13:275-280.
104. Kühn, C., Franceschi, V. R., Schulz, A., Lemoine, R., and Frommer, W. B. 1997. Localization and turnover of sucrose transporters in enucleate sieve elements indicate macromolecular trafficking. Science 275:1298-1300.
105. Kühn, C., Quick, W. P., Schulz, A., Lemoine, R., and Frommer, W. B. 1996. Companion cell-specific inhibition of the potato sucrose transporter SUT1. Plant Cell Environ. 19:1115-1123.
106. Lalonde, S., Boles, E., Hellmann, H., Barker, L., Patrick, J. W., Frommer, W. B., and Ward, J. M. 1999. The dual function of sugar carriers: transport and sugar sensing. Plant Cell 11:707-726.
107. Lauriere, C., Lauriere, M., Sturm, A., Faye, L., and Chrispeels, M. 1988. Characterization of β-fructosidase, an extracellular glycoprotein of carrot cells. Biochimie 70:1483-1491.
108. Lee, H. and Sturm, A. 1996. Purification and characterization of neutral and alkaline invertase from carrot. Plant Physiol. 112:1513-1522.
109. Lindblom, S., Ek, P., Muszynska, G., Ek, B., Szczegielniak, J., and Engström, L. 1997. Phosphorylation of sucrose synthase from maize seedlings. Acta Biochim. Polonica 44:809-818.
110. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, Y., and Shinozaki, K. 1998. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391-1406.
111. Lohaus, G., Winter, H., Riens, B., and Heldt, H. W. 1996. Further studies of the phloem loading process in leaves of barley and spinach. Bot. Acta 108:270-275.
112. Lucas, W. J., Bouché-Pillon, S., Jackson, D. P., Nguyen, L., Baker, L., Ding, B., and Hake, S. 1995. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:1980-1983.
113. Lucas, W. J., Olesinski, A., Hull, R. J., Haudenshield, J. S., Deom, C. M., Beachy, R. N., and Wolf, S. 1993. Influence of the tobacco mosaic virus 30-kDa movement protein on carbon metabolism and photosynthate partitioning in transgenic tobacco plants. Planta 190:88-96.
114. Lue, M.-Y. and Lee, H. 1994. Protein phosphatase inhibitors enhance the expression of an alpha-amylase gene, alpha Amy 3, in cultured rice cells. Biochem. Biophys. Res. Commun. 205:807-816.
115. 4 plants. Planta 202:249-256.
116. Maas, C., Schaal, S., and Werr, W. 1990. A feedback control element near the transcription start site of the maize Shrunken gene determines promoter activity. EMBO J. 9:3447-3452.
117. Macioszek, J. and Anderson, L. E. 1987. Changing kinetic properties of the two enzymes phosphoglycerate kinase/NADP-linked glyceraldehyde-3-phosphate dehydrogenase couple from pea chloroplasts during photosynthetic induction. Biochem. Biophys. Acta 892:185-190.
118. Martin, T., Frommer, W. B., Salanoubat, M., and Willmitzer, L. 1993. Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolism of sucrose both during phloem loading and in sink organs. Plant J. 4:367-377.
119. McCarty, D. R., Shaw, J. R., and Hannah, L. C. 1986. The cloning, genetic mapping, and expression of the constitutive sucrose synthase locus of maize. Proc. Natl. Acad. Sci. U.S.A. 83:9099-9103.
120. McElfresh, K. C. and Chourey, P. S. 1988. Anaerobiosis induces transcription but not translation of sucrose synthase in maize. Plant Physiol. 87:542-546.
121. McMichael, R. W., Jr., Bachmann, M., and Huber, S. C. 1995. Spinach leaf sucrose-phosphate synthase and nitrate reductase are phosphorylated/ inactivated by multiple protein kinases in vitro. Plant Physiol. 108:1077-1082.
122. McMichael, R. W., Jr., Klein, R. R., Salvucci, M. E., and Huber, S. C. 1993. Identification of the major regulatory phosphorylation site in sucrose-phosphate synthase. Arch. Biochem. Biophys. 307:248-252.
123. McMichael, R. W., Jr., Kochansky, J., Klein, R. R., and Huber, S. C. 1995. Characterization of the substrate specificity of sucrose-phosphate synthase protein kinase. Arch. Biochein. Biophys. 321:71-75.
124. Micallef, B. J., Haskins, K. A., Vanderveer, P. J., Roh, K.-S., Shewmaker, C. K., and Sharkey, T. D. 1995. Altered photosynthesis, flowering, and fruiting in transgenic tomato plants that have an increased capacity for sucrose synthesis. Planta 196:327-334.
125. Muslin, A. J., Tanner, J. W., Allen, P. M., and Shaw, A. S. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84:889-897.
126. 11. Plant Cell Physiol. 39:1337-1341.
127. Nakai, T., Tonnouchi, N., Tsuchida, T., Mori, H., Sakai, F., and Hayashi, T. 1997. Synthesis of asymmetrically labeled sucrose by a recombinant sucrose synthase. Biosci. Biotechnol. Biochem. 61:1955-1956.
128. Nakai, T., Tonouchi, N., Konishi, T., Tsuchida, T., Yoshinaga, F., Sakai, F., and Hayashi, T. 1999. Enhancement of cellulose production by expression of sucrose synthase in Acetobacter xylinum. Proc. Natl. Acad. Sci. U.S.A. 96:14-18.
129. Newton, A. C. 1993. Interaction of proteins with lipid headgroups: lessons from protein kinase C. Annu. Rev. Biophys. Biomol. Struct. 22:1-25.
130. Nguyen-Quoc, B., Krivitzky, M., Huber, S. C., and Lecharny, A. 1990. Sucrose synthase in developing maize leaves. Regulation of activity by protein level during the import to export transition. Plant Physiol. 94:516-523.
131. 4 species. Plant Physiol. 84: 1096-1101.
132. 2+ signaling in the sugar-inducible expression of genes coding for sporamin and β-amylase of sweet potato. Plant J. 7:297-305.
133. Ohyama, A., Ito, H., Sato, T., Nishimura, S., Imai, T., and Hirai, M. 1995. Suppression of acid invertase activity by antisense RNA modifies the sugar composition of tomato fruit. Plant Cell Physiol. 36:369-376.
134. O'Reilly, G. and Clarke, F. 1993. Identification of an actin binding region in aldolase. FEBS Lett. 321:69-72.
135. Overall, R. L. and Blackmann, L. M. 1996. A model for the macromolecular structure of plasmodesmata. Trends Plant Sci. 1:207-211.
136. Overvoorde, P. J., Frommer, W. B., and Grimes, H. D. 1996. A soybean sucrose binding protein independently mediates nonsaturable sucrose uptake in yeast. Plant Cell 8:271-280.
137. Pilon-Smits, E. A. H., Ebskamp, M. J. M., Paul, M. J., Jeuken, M. J. W., Weisbeek, P. J., and Smeekens, S. C. M. 1995. Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiol 107:125-130.
138. Plaxton, W. C. 1996. The organization and regulation of plant glycolysis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:185-214.
139. Pollock, C. J. and Caims, A. J. 1991. Fructan metabolism in grasses and cereals. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42:77-101.
140. Pontis, H. G., Babio, J. R., and Salerno, G. 1981. Reversible unidirectional inhibition of sucrose synthase activity by disulfides. Proc. Natl. Acad. Sci. U.S.A. 78:6667-6669.
141. Preller, A. and Wilson, J. E. 1992. Localization of the type III isozyme of hexokinase at the nuclear periphery. Arch. Biochem. Biophys. 294:482-492.
142. Purcell, P. C., Smith, A. M., and Halford, N. G. 1998. Antisense expression of a sucrose nonfermenting-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.
143. Quick, P., Siegl, G., Neuhaus, H. E., Feil, R., and Stitt, M. 1989. Short-term water stress leads to a stimulation of sucrose synthesis by activating sucrose-phosphate synthase. Planta 177:536-546.
144. Quick, W. P. 1996. Sucrose metabolism in sources and sinks. In: Photoassimilate Distribution in Plants, Zamski, E. and Schaffer, A. A. Eds., Marcel Dekker, New York, 115-156.
145. Reimholz, R., Geigenberger, P., and 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.
146. Reimholz, R., Geiger, M., Haake, V., Deiting, U., Krause, K.-P., Sonnewald, U., and Stitt, M. 1997. Potato plants contain multiple forms of sucrose-phosphate synthase, which differ in their tissue distributions, their levels during development, and their responses to low temperature. Plant, Cell, Environ. 20:291-305.
147. Ricard, B., Rivoal, J., Spiteri, A., and Pradet, A. 1991. Anaerobic stress induces the transcription and translation of sucrose synthase in rice. Plant Physiol 95:669-674.
148. Ricard, B., Van Taoi, T., Chourey, P., and Saglio, P. 1998. Evidence for the critical role of sucrose synthase for anoxic tolerance of maize roots using a double mutant. Plant Physiol. 116:1323-1331.
149. Richardo, C. P. P. and ap Rees, T. 1970. Invertase activity during the development of carrot roots. Phytochemistry 9:239-247.
150. Riesmeier, J. W., Willmitzer, L., and Frommer, W. B. 1992. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO J. 11:4705-4713.
151. Roblin, G., Sakr, S., Bonmort, J., and Delrot, S. 1998. Regulation of a plant plasma membrane sucrose transporter by phosphorylation. FEBS Lett. 424:165-168.
152. Roitsch, T., Bittner, M., and Godt, D. E. 1995. Induction of apoplastic invertase of Chenopodhim rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol. 108:285-294.
153. Ross, H. A., McRae, D., and Davis, H. V. 1996. Sucrolytic enzyme activities in cotyledons of the Faba Bean. Developmental changes and purification of alkaline invertase. Plant Physiol. 11:329-338.
154. Ruan, Y.-L., Chourey, P. S., Delmer, D. P., and Perez-Grau, L. 1997. The differential expression of sucrose synthase in relation to diverse patterns of carbon partitioning in developing cotton seeds. Plant Physiol. 115:325-385.
155. Rufty, T. W., Jr., Kerr, P. S., and Huber, S. C. 1983. Characterization of diurnal changes in activities of enzymes involved in sucrose biosynthesis. Plant Physiol. 73:428-433.
156. Salerno, G. L., Echeverria, E., and Pontis, H. G. 1996. Activation of sucrose-phosphate synthase by a protein factor/sucrose-phosphate phosphatase. Cell. Mol. Biol. 42:665-672.
157. Salvucci, M. E., van de Loo, F. J., and Klein, R. R. 1995. The structure of sucrose-phosphate synthase. In: Sucrose Metabolism, Biochemistry, Physiology and Molecular Biology, Pontis, H. G., Salerno, G. L., and Echeverria, E., Eds., American Society of Plant Physiologists, Rockville, 1-10.
158. Sander, A., Krausgrill, S., Greiner, S., Weil, M., and Rausch, T. 1996. Sucrose protects cell wall invertase but not vacuolar invertase against proteinaceous inhibitors. FEBS Lett. 385:171-175.
159. Sauer, N. and Stolz, J. 1994. SUC1 and SUC2: two sucrose transporters from Arabidopsis thaliana. Expression and characterization in baker's yeast and identification of the histidine tagged protein. Plant J. 6:67-77.
160. Scheibe, R. 1991. Redox-modulation of chloroplast enzymes. A common principle for individual control. Plant Physiol. 96:1-3.
161. Schleucher, J., Vanderveer, P. J., and Sharkey, T. D. 1998. Export of carbon from chloroplasts at night. Plant Physiol. 118:1439-1445.
162. Scholes, J., Bundock, N., Wilde, R., and Rolfe, S. 1996. The impact of reduced vacuolar invertase activity on the photosynthetic and carbohydrate metabolism of tomato. Planta 200:265-272.
163. Schulz, A., Kühn, C., Riesmeier, J. W., and Frommer, W. B. 1998. Ultrastructural effects in potato leaves due to antisense-inhibition of the
164. Shaw, J. R., Ferl, R. J., Baier, J., St. Clair, D., Carson, C., McCarty, D. R., and Hannah, L. C. 1994. Structural features of the maize Sus1 gene and protein. Plant Physiol. 106:1659-1665.
165. Siegl, G., MacKintosh, C., and Stitt, M. 1990. Sucrose-phosphate synthase is dephosphorylated by protein phosphatase 2A in spinach leaves. FEBS Lett. 270:198-202.
166. Smeekens, S. 1998. Sugar regulation of gene expression in plants. Curr. Opin. Plant Biol. 1: 230-234.
167. Sprenger, N., Bortlik, K., Brandt, A., Boller, T., and Wiemken, A. 1995. Purification, cloning and functional expression of sucrose:fructan 6-fructosyltransferase, a key enzyme of fructan synthesis in barley. Proc. Natl. Acad. Sci. U.S.A. 92:11652-11656.
168. Srere, P. A. 1987. Complexes of sequential metabolic enzymes. Annu. Rev. Biochem. 56:89-124.
169. Stadler, P. and Sauer, N. 1996. The Arabidopsis thaliana AtSUC2 gene is specifically expressed in companion cells. Bot. Acta 109:299-308.
170. Stadler, R., Brandner, J., Schulz, A., Gahrtz, M., and Sauer, N. 1995. Phloem loading by the PmSUC2 sucrose carrier from Plantago major occurs into companion cells. Plant Cell 7:1545-1554.
171. Steponkus, P. L. and Lanphear, F. O. 1968. The relationship of carbohydrates to cold acclimation of Hedera helix L. cv. Thorndale. Physiol. Plantarum 22:777-791.
172. Stitt, M., Huber, S. C., and Kerr, P. S. 1987. Control of photosynthetic sucrose formation. In: The Biochemistry of Plants, Hatch, M. D. and Boardman, N. K. Eds., Academic Press, New York, 327-409.
173. Stitt, M., Wilke, I., Feil, R., and Heldt, H. W. 1988. Coarse control of sucrose-phosphate synthase in leaves: Alterations of the kinetic properties in response to the rate of photosynthesis and the accumulation of sucrose. Planta 174:217-230.
174. Sturm, A. and Chrispeels, M. J. 1990. cDNA cloning of carrot extracellular β-fructosidase and its expression in response to wounding and bacterial infection. The Plant Cell 2:1107-1119.
175. Sturm, A., Sebkova, V., Lorenz, K., Hardegger, M., Lienhard, S., and Unger, C. 1995. Development- and organ-specific expression of the genes for sucrose synthase and three isoenzymes of acid β-fructosidase in carrot. Planta 195:601-610.
176. Sullivan, J. E., Brocklehurst, K. J., Marley, A. E., Carey, F., Carling, D., and Beri, R. K. 1994. Inhibition of lipolysis and lipogenesis in isolated rat adipocytes with AICAR, a cell-permeable activator of AMP-activated protein kinase. FEBS Lett. 353:33-36.
177. Sun, J., Loboda, T., Sung, S.-J. S., and Black, C. C. J. 1992. Sucrose synthase in wild tomato, Lycopersicon chmielewskii, and tomato fruit sink strength. Plant Physiol. 98:1163-1169.
178. Takeda, S., Mano, S., Ohto, M., and Nakamura, K. 1994. Inhibitors of protein phosphatases 1 and 2A block the sugar-inducible gene expression in plants. Plant Physiol. 106:567-574.
179. Taliercio, E. W. and Chourey, P. S. 1989. Posttranscriptional control of sucrose synthase expression in anaerobic seedlings of maize. Plant Physiol. 90:1359-1364.
180. Thummler, F. and Verma, D. P. 1987. Nodulin-100 of soybean is the subunit of sucrose synthase regulated by the availability of free heme in nodules. J. Biol. Chem. 262:14730-14736.
181. Tognetti, J. A., Salerno, G. L., Crespi, M. D., and Pontis, H. G. 1990. Sucrose and fructan metabolism of different wheat cultivars at chilling temperatures. Physiol. Plantarum 78:554-559.
182. Toroser, D., Athwal, G. S., and Huber, S. C. 1998. Site-specific regulatory interaction between spinach leaf sucrose-phosphate synthase and 14-3-3 proteins. FEBS Lett. 435:110-114.
183. Toroser, D. and Huber, S. C. 1997. Protein phosphorylation as a mechanism for osmotic-stress activation of sucrose-phosphate synthase. Plant Physiol. 114:947-955.
184. 2+ dependence and substrate specificities. Arch. Biochem. Biophys. 355:291-300.
185. Toroser, D., McMichael, R. W., Jr., Krause, K.-P., Kurreck, J., Sonnewald, U., Stitt, M., and Huber, S. C. 1999. Site-directed mutagenesis of serine 158 demonstrates its role in spinach leaf sucrose-phosphate synthase modulation. Plant J. 17:407-413.
186. Toyoda, Y., Miwa, I., Kamiya, M., Ogiso, S., Nonogaki, T., Aoki, S., and Okusa, J. 1994. Evidence of glucokinase translocation by glucose in rat hepatocytes. Biochem. Biophys. Res. Commun. 204:252-256.
187. Trethewey, R. N., Geigenberger, P., Hennig, A., Fleischer-Notter, H., Müller-Röber, B., and Willmitzer, L. 1999. Induction of the activity of glycolytic enzymes correlates with enhanced hydrolysis of sucrose in the cytosol of transgenic potato tubers. Plant Cell Environ. 22:71-79.
188. + symporter gene directs expression of β-glucuronidase to the phloem: phloem loading and unloading by SUC2. Planta 196:564-570.
189. Tymowska-Lalanne, Z. and Kreis, M. 1998. Expression of the Arabidopsis thaliana invertase gene family. Planta 207:259-265.
190. Umemura, T.-A., Perata, P., Futsuhara, Y., and Yamaguchi, J. 1998. Sugar-sensing and α-amylase gene repression in rice embryos. Planta 204:420-428.
191. 2+-dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Mol. Gen. Genet. 244:331-340.
192. van Bel, A. 1993. Strategies of phloem loading. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 253-281.
193. Van den Ende, W. and Van Laere, A. 1995. Purification and properties of a neutral invertase from the roots of Cichorium intybits. Physiol. Plantarum 93:241-248.
194. Vassey, T. L. and Sharkey, T. D. 1989. Mild water stress of Phaseolus vulgaris plants leads to reduced starch synthesis and extractable sucrose phosphate synthase activity. Plant Physiol. 89: 1066-1070.
195. Vincent, M. F., Bontemps, F., and Van den Berghe, G. 1992. Inhibition of glycolysis by 5-amino-4-imidazolecarboxamide riboside in isolated rat hepatocytes. Biochem. J. 281:267-272.
196. von Schaewen, A., Stitt, M., Schmidt, R., Sonnewald, U., and Willmitzer, L. 1990. Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J. 9:3033-3044.
197. Wagner, W., Keller, F., and Wiemken, A. 1983. Fructan metabolism in cerals: induction in leaves and compartmentation in protoplasts and vacuoles. Zeitschrift fuer Pflanzenphysiologie 112: 359-372.
198. Walker, J. L. and Huber, S. C. 1989. Regulation of sucrose-phosphate synthase activity in spinach leaves by protein level and covalent modification. Planta 177:116-120.
199. Walker, R. P., Winters, A. L., and Pollock, C. J. 1997. Purification and characterisation of invertases from leaves of Lolium temulentum L. New Phytol. 135:259-266.
200. Weber, H., Borisjuk, L., Heim, U., Sauer, N., and Wobus, U. 1997. A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seeds. Plant Cell 9:895-908.
201. Weiner, H., McMichael, R. W., Jr., and Huber, S. C. 1992. Identification of factors regulating the phosphorylation status of sucrose-phosphate synthase in vivo. Plant Physiol. 99:1435-1442.
202. Weiner, H., Weiner, H., and Stitt, M. 1993. Sucrose-phosphate synthase phosphatase, a type 2 A protein phosphatase, changes its sensitivity toward inhibition by inorganic phosphate in spinach leaves. FEBS Lett. 333:159-164.
203. Winter, H., Huber, J. L., and Huber, S. C. 1997. Membrane association of sucrose synthase: changes during the graviresponse and possible control by protein phosphorylation. FEBS Lett. 420:151-155.
204. Winter, H., Huber, J. L., and Huber, S. C. 1998. Identification of sucrose synthase as an actin binding protein. FEBS Lett. 430:205-208.
205. Winter, H., Robinson, D. G., and Heldt, H. W. 1994. Subcellular volumes and metabolite concentrations in barley leaves. Planta 193:532-555.
206. Winzer, T., Lohaus, G., and Heldt, H. W. 1996. Influence of phloem transport, N-fertilization and ion accumulation on sucrose storage in the taproots of fodder beet and sugar beet. J. Exp. Bot. 47:863-870.
207. Wolosiuk, R. A. and Pontis, H. G. 1974. The role of sucrose and sucrose synthetase in plant carbohydrate metabolism. Mol. Cell. Biochem. 4:115-123.
208. Xoconostle-Cázares, B., Xiang, Y., Ruiz-Medrano, R., Wang, H.-L., Monzer, J., Yoo, B.-C., McFarland, K. C., Franceschi, V. R., and Lucas, W. J. 1999. Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283:94-98.
209. Xu, J., Avigne, W. T., McCarty, D. R., and Koch, K. E. 1996. A similar dichotomy of sugar modulation and developmental expression affects both paths of sucrose metabolism: evidence from a maize invertase gene family. Plant Cell 8: 1209-1220.
210. Yang, N.-S. and Russel, D. 1990. Maize sucrose synthase-1 promoter directs phloem cell-specific expression of Gus gene in transgenic tobacco plants. Proc. Natl. Acad. Sci. U.S.A. 87:4144-4148.
211. Yu, W. P., Wang, A. Y., Juang, R. H., Sung, H. Y., and Su, J. C. 1992. Isolation of rice sucrose synthase cDNA and genomic DNA. Plant Mol. Biol. 18:139-142.
212. 2+-dependent protein kinase. FEBS Lett. 410:126-130.
213. Zhang, X.-Q., Lund, A. A., Sarath, G., Cerny, R. L., Roberts, D. M., and Chollet, R. 199X. Soybean nodule sucrose synthase (nodulin-100): analysis of its phosphorylation using recombinant and authentic nodule enzymes. Arch. Biochem. Biophys. 371:70-87.
214. Zrenner, R., Salanoubat, M., Willmitzer, L., and Sonnewald, U. 1995. Evidence of the crucial role of sucrose synthase for sink strength using transgenic potato plants (Solanum tuberosum L.). Plant J. 7:97-107.
215. Zrenner, R., Schuler, K., and Sonnewald, U. 1996. Soluble acid invertase determines the hexose-to-sucrose ratio in cold-stored potato tubers. Planta 198:246-252.
216. Zrenner, R. and Stitt, M. 1991. Comparison of the effect of rapidly and gradually developing water-stress on carbohydrate metabolism in spinach leaves. Plant Cell Environ. 14:939-946.