An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished

Plant Journal

Volumn 32, Issue 5, 2002, Pages 685-699

  Schneider, Anja ^a   Häusler, Rainer E ^a   Kolukisaoglu, Üner ^b,d   Kunze, Reinhard ^a   Van der Graaff, Eric ^a   Schwacke, Rainer ^a   Catoni, Elisabetta ^c   Desimone, Marcelo ^b   Flügge, Ulf Ingo ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b MAX PLANCK INSTITUTE FOR THE STUDY OF SOCIETIES   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

^d UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

6 bisphosphate; Adg1; Carbohydrate metabolism; Fructose 2; Photosynthesis; Reverse genetics; Sex1

Indexed keywords

BIOSYNTHESIS; MOLECULAR WEIGHT; MUTAGENESIS; PHOTOSYNTHESIS; STARCH; SUGAR (SUCROSE);

PHOSPHATE TRANSLOCATORS;

PLANTS (BOTANY);

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; CARBON DIOXIDE; CHLOROPLASTS; FRUCTOSEDIPHOSPHATES; GENE DELETION; GENE EXPRESSION REGULATION, PLANT; LIGHT; MEMBRANE TRANSPORT PROTEINS; PERIODICITY; PHENOTYPE; PHOTOSYNTHESIS; PLANT PROTEINS; STARCH;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; INSERTION SEQUENCES;

EID: 0347264778     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2002.01460.x     Document Type: Article

References (48)

1. Bergmeyer, H. (1974) Methoden der Enzymatischen Analyse, 3rd Edn. Weinheim, Germany: Verlag Chemie.
2. Caspar, T., Lin, T.-P., Kakefuda, G., Benbow, L., Preiss, J. and Somerville, C. (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol. 95, 1181-1188.
3. Corbesier, L., Lejeune, P. and Bernier, G. (1998) The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: Comparison between the wild type and a starchless mutant. Planta, 206, 131-137.
4. Draborg, H., Villadsen, D. and Nielsen, T.H. (2001) Transgenic Arabidopsis plants with decreased activity of fructose-6-phosphate, 2-kinase/fructose-2,6-bisphosphatase have altered carbon partitioning. Plant Physiol. 126, 750-758.
5. Eicks, M., Maurino, V., Knappe, S., Flügge, U.I. and Fischer, K. (2002) The plastidic pentose phosphate translocator represents a link between the cytosolic and the plastidic pentose phosphate pathways in plants. Plant Physiol. 128, 512-522.
6. Feldmann, K.A. (1991) T-DNA insertion mutagenesis in Arabidopsis-mutational spectrum. Plant J. 1, 71-82.
7. Fischer, K., Kammerer, B., Gutensohn, M., Arbinger, B., Weber, A., Häusler, R.E. and Flügge, U.I. (1997) A new class of plastidic phosphate translocators: A putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell 9, 453-462.
8. Fliege, R., Flügge, U.I., Werdan, K. and Heldt, H.W. (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.
9. Flügge, U.I. (1999) Phosphate translocators in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 27-45.
10. Flügge, U.I., Fischer, K., Gross, A., Sebald, W., Lottspeich, F. and Eckerskorn, C. (1989) The triose phosphate-3-phosphoglyceratephosphate translocator from spinach chloroplasts: Nucleotide sequence of a full-length cDNA clone and import of the in vitro synthesized precursor protein into chloroplasts. EMBO J. 8, 39-46.
11. Flügge, U.I. and Weber, A. (1994) A rapid method for measuring organelle-specific substrate transport in homogenates from plant tissues. Planta, 194, 181-185.
12. Forsthoefel, N.R., Wu, Y., Schulz, B., Bennett, M.J. and Feldmann, K.A. (1992) T-DNA insertion mutagenesis in Arabidopsis: Prospects and perspectives. Aust. J. Plant Physiol. 19, 353-366.
13. Genty, B., Briantais, J.M. and Baker, N.R. (1989) The relationship between the quantum yield of photosynthetic transport and quenching of chlorophyll fluorescence. Biochim. Biophys. Acta 990, 87-92.
14. Hattenbach, A., Müller-Röber, B., Nast, G. and Heineke, D. (1997) Antisense repression of both ADP-glucose pyrophosphorylase and triose phosphate translocator modifies carbohydrate partitioning in potato leaves. Plant Physiol. 115, 471-475.
15. Häusler, R.E., Fischer, K.L. and Flügge, U.I. (2000a) Determination of low abundant metabolites in plant extracts by NAD(P)H fluorescence with a microtiter plate reader. Anal. Biochem. 281, 1-8.
16. Häusler, R.E., Schlieben, N.H. and Flügge, U.I. (2000b) Control of carbon partitioning and photosynthesis by the triose phosphate/phosphate translocator in transgenic tobacco plants (Nicotiana tabacum). Part II. Assessment control, coefficients triose phosphate/phosphate translocator. Planta, 210, 383-390.
17. Häusler, R.E., Schlieben, N.H., Nicolay, P., Fischer, K., Fischer, K.L. and Flügge, U.I. (2000c) Control of carbon partitioning and photosynthesis by the triose phosphate/phosphate translocator in transgenic tobacco plants (Nicotiana tabacum L). Part I. Comparative physiological analysis of tobacco plants with antisense repression and overexpression of the triose phosphate/phosphate translocator. Planta, 210, 371-382.
18. Häusler, R.E., Schlieben, N.H., Schulz, B. and Flügge, U.I. (1998) Compensation of decreased triose phosphate/phosphate translocator activity by accelerated starch turnover and glucose transport in transgenic tobacco. Planta, 204, 366-376.
19. Heineke, D., Kruse, A., Flügge, U.I., Frommer, W.B., Riesmeier, J.W., Willmitzer, L. and Heldt, H.W. (1994) Effect of antisense repression of the chloroplast triose-phosphate translocator on photosynthetic metabolism in transgenic potato plants. Planta, 193, 174-180.
20. Kammerer, B., Fischer, K., Hilpert, B., Schubert, S., Gutensohn, M., Weber, A. and Flügge, 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.
21. Larondelle, Y., Mertens, E., Van Schaftingen, E. and Hers, H.G. (1986) Purification and properties of spinach leaf phosphofructokinase 2/fructose 2,6-bisphosphatase. Eur. J. Biochem. 161, 351-357.
22. Lin, T.-P., Caspar, T., Somerville, C. and Preiss, J. (1988a) Isolation and characterization of a starchless mutant of Arabidopsis thaliana (L.) lacking ADP-glucose pyrophosphorylase activity. Plant Physiol. 86, 1131-1135.
23. Lin, T.-P., Caspar, T., Somerville, C. and Preiss, J. (1988b) A starch deficient mutant of Arabidopsis thaliana with low ADP-glucose pyrophosphorylase activity lacks one of the two subunits of the enzyme. Plant Physiol. 88, 1175-1181.
24. Lin, T.-P., Spilatro, S.R. and Preiss, J. (1988c) Subcellular localization and characterization of amylases in Arabidopsis leaf. Plant Physiol. 86, 251-259.
25. Liu, Y.G., Mitsukawa, N., Oosumi, T. and Whittier, R.F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457-463.
26. Logemann, J., Schell, J. and Willmitzer, L. (1987) Improved method for the isolation of RNA from plant tissues. Anal. Biochem. 163, 16-20.
27. Lorberth, R., Ritte, G., Willmitzer, L. and Kossmann, J. (1998) Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nature Biotechn. 16, 473-477.
28. Poolman, M.G., Fell, D.A. and Thomas, S. (2000) Modelling photosynthesis and its control. J. Exp. Bot. 51, 319-328.
29. Quick, P., Siegl, G., Neuhaus, E., Feil, R. and Stitt, M. (1989) Short-term water stress leads to a stimulation of sucrose synthesis by activating sucrose-phosphate synthase. Planta, 117, 535-546.
30. Riesmeier, J.W., Flügge, U.I., Schulz, B., Heineke, D., Heldt, H.W., Willmitzer, L. and Frommer, W.B. (1993) Antisense repression of the chloroplast triose phosphate translocator affects carbon partitioning in transgenic potato plants. Proc. Natl. Acad. Sci. USA 90, 6160-6164.
31. Ritte, G., Lloyd, J., Eckermann, N., Rottmann, A., Kossmann, J. and Steup, M. (2002) The starch related R1 protein is an α-glucan,water dikinase. Proc. Natl. Acad. Sci. USA99, 7166-7171.
32. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A. Laboratory Manual, 2nd Edn. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
33. Schreiber, U., Schliwa, U. and Bilger, B. (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth. Res. 10, 51-62.
34. Shirokane, Y., Ichikawa, K. and Suzuki, M. (2000) A novel enzymic determination of maltose. Carbohydr. Res. 329, 699-702.
35. Stitt, M. (1990) Fructose-2,6-bisphosphate as a regulatory molecule in plants. Annu. Rev. Plant Physiol. Plant. Mol. Biol. 41, 153-185.
36. Stitt, M., Cseke, C. and Buchanan, B.B. (1984) Regulation of fructose 2,6-bisphosphate concentration in spinach leaves. Eur. J. Biochem. 143, 89-93.
37. Stitt, M., Gerhardt, R., Kurzel, B. and Heldt, H.W. (1983) A role of fructose 2,6-bisphosphate in the regulation of sucrose synthesis in spinach leaves. Plant Physiol. 72, 1139-1141.
38. Stitt, M., Iilley, R.M.C., Gerhardt, R. and Heldt, H.W. (1989) Determination of metabolite levels in specific cells and subcellular compartments of plant leaves. Meth Enzymol. 174, 518-522.
39. Strand, A., Zrenner, R., Trevanion, S., Stitt, M., Gustafsson, P. and Gardestrom, P. (2000) Decreased expression of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose-1,6-bisphosphatase and sucrose phosphate synthase, has remarkably different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J. 23, 759-770.
40. Streatfield, S.J., Weber, A., Kinsman, E.A., Häusler, R.E., Li, J., Post-Beittenmiller, D., Kaiser, W.M., Pyke, K.A., Flügge, U.I. and Chory, J. (1999) The phosphoenolpyruvate/phosphate translocator is required for phenolic metabolism, palisade cell development, and plastid-dependent nuclear gene expression. Plant Cell 11, 1609-1622.
41. Van Schaftingen, E. (1984) D-fructose 2,6-bisphosphate. In Methods of Enzymatic Analysis (H.Bergmeyer, ed.). Weinheim, Germany: Verlag Chemie, pp. 335-341.
42. Von Caemmerer, S. and Farquhar, G.D. (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta, 153, 376-387.
43. Weber, A., Servaites, J.C., Geiger, D.R., Kofler, H., Hille, D., Gröner, F., Hebbeker, U. and Flügge, U.I. (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12, 787-802.
44. Wiese, A., Gröner, F., Sonnewald, U., Deppner, H., Lerchl, J., Hebbeker, U., Flügge, U.I. and Weber, A. (1999) Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Lett. 461, 13-18.
45. Yang, Y. and Steup, M. (1990) Polysaccharide fraction from higher plants which strongly interacts with the cytosolic phosphorylase isozyme. Plant Physiol. 94, 960-969.
46. Yu, T.S., Kofler, H., Häusler, R.E. et al. (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13, 1907-1918.
47. Zeeman, S.C., Northrop, F., Smith, A.M. and Ap Rees, T. (1998a) A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J. 15, 357-365.
48. Zeeman, S.C., Umemoto, T., Lue, W.-L., Au-Yeung, P., Martin, C., Smith, A.M. and Chen, J. (1998b) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10, 1699-1711.