Reduction of the cytosolic fructose-1,6-bisphosphatase in transgenic potato plants limits photosynthetic sucrose biosynthesis with no impact on plant growth and tuber yield

Plant Journal

Volumn 9, Issue 5, 1996, Pages 671-681

  Zrenner, Rita ^a,b   Krause, Klaus Peter ^a   Apel, Peter ^a   Sonnewald, Uwe ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYOPHYTA; SOLANUM TUBEROSUM;

ANTISENSE OLIGONUCLEOTIDE; FRUCTOSE BISPHOSPHATASE; HYBRID PROTEIN; SUCROSE;

ARTICLE; BIOSYNTHESIS; COMPARATIVE STUDY; CYTOSOL; DARKNESS; ENZYMOLOGY; ESCHERICHIA COLI; GENE LIBRARY; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; OPEN READING FRAME; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT ROOT; POTATO; RESTRICTION MAPPING; RHIZOBIUM RADIOBACTER; SEQUENCE HOMOLOGY; TRANSGENIC PLANT;

CLONING, MOLECULAR; CYTOSOL; DARKNESS; ESCHERICHIA COLI; FRUCTOSE-BISPHOSPHATASE; GENE LIBRARY; LIGHT; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES, ANTISENSE; OPEN READING FRAMES; PHOTOSYNTHESIS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; RECOMBINANT FUSION PROTEINS; RESTRICTION MAPPING; RHIZOBIUM RADIOBACTER; SEQUENCE HOMOLOGY, NUCLEIC ACID; SOLANUM TUBEROSUM; SUCROSE;

EID: 0030139567     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.1996.9050671.x     Document Type: Article

References (55)

1. Amasino, R.M. (1986) Acceleration of nucleic acid hybridisation rate by polyethylene glycol. Anal. Biochem. 152, 304-307.
2. Apel, P., Hillmer, S., Pfeffer, M. and Mühle, K. (1996) Study on the carbon metabolism type of Diplotaxis tenuifolia (L.) DC. (Brassicaceae). Photosynthetica, 32, 237-243.
3. Bevan, M. (1984) Binary Agrobacterium vectors for plant transformation. Nucl. Acids Res. 12, 8711-8721.
4. Bullock, W.O., Fernandez, J.M. and Short, J.M. (1987) XL1-blue: a high efficiency plasmid transforming recA Escherichia coli strain with β-glucuronidase selection. BioTechniques 5, 376-378.
5. von Caemmerer, S. and Farquhar, G.D. (1981) Some relationship between the biochemistry of photosynthesis and the gas exchange of leaves. Planta, 153, 376-387.
6. Daie, J. (1993) Cytosolic fructose-1,6-bisphosphatase: A key enzyme in the sucrose biosynthetic pathway. Photosyn. Res. 38, 5-14.
7. Deblaere, R., Bytebier, B., de Greve, H., Debroek, F., Schell, J., van Montagu, M. and Leemans, J. (1985) Efficient octopine Ti plasmid-derived vectors of Agrobacterium mediated gene transfer to plants. Nucl. Acids Res. 13, 4777-4788.
8. Doehlert, D.C. and Huber, S.C. (1983) Regulation of spinach leaf sucrose-phosphate synthase by Glc6P, inorganic phosphate and pH. Plant Physiol. 73, 989-994.
9. El-Maghrabi, M.R., Pilkis, J., Marker, A., Colosia, A., D'Angelo, A., Fraser, B. and Pilkis, S. (1988) cDNA sequence of rat liver fructose-1,6-bisphosphatase and evidence for down-regulation of its mRNA by insulin. Proc. Natl Acad. Sci. USA, 85, 8430-8434.
10. Franck, A., Guilley, H., Jonard, G., Richards, K. and Hirth, L. (1980) Nucleotide sequence of Cauliflower Mosaic Virus DNA. Cell, 21, 285-294.
11. Frisch, D.A., Harris-Haller, L.W., Yokubaitis, N.T., Thomas, T.L., Hardin, S.H. and Hall, T.C. (1995) Complete sequence of the binary vector Bin 19. Plant Mol. Biol. 27, 405-409.
12. Frommer, W.B. and Sonnewald, U. (1995) Molecular analysis of carbon partitioning in solanaceous species. J. Exp. Bot. 46, 587-607.
13. Gerhardt, R. and Heldt, H.W. (1984) Measurements of subcellular metabolite levels by fractionation of freeze-stopped material in nonaqueous media. Plant Physiol. 75, 542-547.
14. Gielen, J., de Beuckeleer, M., Seurinck, J., Debroeck, H., de Greve, H., Lemmers, M., van Montagu, M. and Schell, J. (1984) The complete nucleotide sequence of the TL-DNA of the Agrobacterium tumefaciens plasmid pTiAch5. EMBO J. 3, 835-846.
15. Hajirezaei, M., Sonnewald, U., Viola, R., Carlisle, S., Dennis, D. and Stitt, M. (1994) Transgenic potato plants with strongly reduced expression of pyrophosphate:fructose-6-phosphate phosphotransferase show no visible phenotype and only minor changes in metabolic fluxes in their tubers. Planta, 92, 16-30.
16. Harn C. and Daie, J. (1992a) Cloning and nucleotide sequence of a cDNA encoding the cytosolic fructose-1,6-bisphosphatase of sugar beet (Beta vulgaris L). Plant Physiol. 98, 790-791.
17. Harn C. and Daie, J. (1992b) Regulation of the cytosolic fructose-1,6-bisphosphatase by post-translational modification and protein level in drought-stressed leaves of sugarbeet. Plant Cell Physiol. 33, 763-770.
18. Heineke, D., Kruse, A., Flügge, U.I., Frommer, W.B., Riesmeier, J.W. 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.
19. Höfgen, R. and Willmitzer, L (1988) Storage of competent cells for Agrobacterium transformation. Nucl. Acids Res. 16, 9877.
20. Höfgen, R. and Willmitzer, L. (1990) Biochemical and genetic analysis of different patatin isoforms expressed in various organs of potato (Solanum tuberosum L). Plant Sci. 66, 221-230.
21. Horsnell, P.R. and Raines, C.A. (1991) Nucleotide sequence of a cDNA clone encoding chloroplast fructose-1,6-bisphosphatase from Arabidopsis thaliana. Plant Mol. Biol. 17, 185-186.
22. Huber, S.C., Kerr, P.S. and Torres, W.K. (1985) Regulation of sucrose synthesis and movement. In Regulation of Carbon Partitioning in Photosynthetic Tissue (R.L. Heath, J. Preiss, eds). Baltimore, MD: Williams and Wilkins, pp. 199-214.
23. Huber, J.L.A., Huber, S.C. and Nielsen, T.H. (1989) Protein phosphorylation as a mechanism for regulation of spinach leaf sucrose-phosphate synthase activity. Arch. Biochem. Biophys. 270, 681-690.
24. Hur, Y., Unger, E.A. and Vasconcelos, A.C. (1992) Isolation and characterization of a cDNA encoding cytosolic fructose-1,6-bisphosphatase from spinach. Plant Mol. Biol. 18, 788-802.
25. Jelitto, T., Sonnewald, U., Willmitzer, L., Hajirezeai, M. and Stitt, M. (1992) Inorganic pyrophosphate content and metabolites in potato and tobacco plants expressing E. coli pyrophosphatase in their cytosol. Planta, 188, 238-244.
26. Kelly, G.J., Zimmermann, G. and Latzko, E. (1982) Fructose-bisphosphatase from spinach leaf chloroplast and cytoplasm. Methods Enzymol. 90, 371-378.
27. Khayat, E., Harn, C. and Daie, J. (1993) Purification and light-dependent molecular modulation of the cytosolic fructose-1,6-bisphosphatase in sugarbeet leaves. Plant Physiol. 101, 57-64.
28. Koßmann, J., Müller-Röber, B., Dyer, T.A., Raines, C.A., Sonnewald, U. and Willmitzer, L (1992) Cloning and expression analysis of the plastidic fructose-1,6-bisphosphatase coding sequence from potato: circumstantial evidence for the import of hexoses into chloroplasts. Planta, 188, 7-12.
29. Kruckeberg, A.L., Neuhaus, H.E., Feil, R., Gottlieb, L.D. and Stitt, M. (1989) Decreased activity mutants of phosphoglucose isomerase in the cytosol and chloroplast of Clarkia xantiana. Biochem. J. 261, 457-467.
30. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
31. Laroche, A., Frick, M.M., Kazala, C., Weselake, R.J. and Thomas, J.E. (1995) Isolation and characterization of an oilseed rape fructose-1,6-bisphosphatase cDNA. Plant Physiol. 108, 1335-1336.
32. Lerchl, J., Geigenberger, P., Stitt, M. and Sonnewald, U. (1995) Inhibition of long-distance sucrose transport by inorganic pyrophosphatase can be complemented by phloem-specific expression of cytosolic yeast-derived invertase in transgenic plants. Plant Cell 7, 259-270.
33. Marcus, F. and Harrsch, P.B. (1990) Amino acid sequence of spinach chloroplast fructose-1,6-bisphosphatase. Arch. Biochim. Biophys. 279, 151-157.
34. Marcus, F., Moberly, L. and Latshaw, S. (1988) Comparative amino acid sequence of fructose-1,6-bisphosphatase: identification of a region unique to the light-regulated chloroplast enzyme. Proc. Natl Acad. Sci. USA, 85, 5379-5383.
35. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
36. Paul, M., Sonnewald, U., Hajirezaei, M., Dennis, D. and Stitt, M. (1995) Transgenic tobacco plants with strongly decreased expression of pyrophosphate: fructose-6-phosphate 1-phosphotransferase do not differ significantly from wild-type in photosynthate partitioning, plant growth or their ability to cope with limiting phosphate, limiting nitrogen and suboptimal temperatures. Planta, 196, 277-283.
37. Preiss, J. (1982) Biosynthesis of starch and its regulation. In Encyclopedia of Plant Physiology, New Series, Volume 13A (Loewus, F.A., Tanner, W., eds). Berlin: Springer, pp. 397-417.
38. Quick, W.P., Siegl, G., Neuhaus, H.E. and Stitt, M. (1989) Shortterm water stress leads to a stimulation of sucrose synthesis by activating sucrose phosphate synthase. Planta, 177, 535-546.
39. Raines, C.A., Lloyd, J.C., Longstaff, M., Bradley, D. and Dyer, T. (1988) Chloroplast fructose-1,6-bisphosphatase: the product of a mosaic gene. Nucl. Acids Res. 16, 7931-7942.
40. 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.
41. Riesmeier, J., 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
42. Rocha-Sosa, M., Sonnewald, U., Frommer, W., Stratmann, M., Schell, J. and Willmitzer, L. (1989) Both developmental and metabolic signals activate the promoter of a class I patatin gene. EMBO J. 8, 23-29.
43. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
44. Sanger, F., Nicklein, S. and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 74, 5463-5467.
45. Schäfer, G. and Heber, U. (1977) Glucose transport into spinach chloroplasts. Plant Physiol. 60, 286-289.
46. 2 sensitivity in a Flaveria linearis mutant. Plant Physiol. 86, 667-671.
47. Sharkey, T.D., Savitch, L. V., Vanderveer, P.J. and Micallef, B.J. (1992) Carbon partitioning in a Flaveria linearis mutant with reduced cytosolic fructose bisphosphatase. Plant Pysiol. 100, 210-215.
48. Sonnewald, U. (1992) Expression of E. coli. inorganic pyrophosphatase in transgenic plants alters photoassimilate partitioning. Plant J. 2, 571-581.
49. Stitt, M. (1990) Fructose-2,6-bisphosphate as a regulatory molecule in plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 41, 153-185.
50. Stitt, M. and Quick, W.P. (1989) Photosynthetic carbon partitioning: its regulation and possibilities for manipulation. Physiol. Plant. 77, 633-641
51. Stitt, M. and Sonnewald, U. (1995) Regulation of metabolism in transgenic plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 46, 341-368.
52. Stitt, M., Lilley, R.M.C., Gerhardt, R. and Heldt, H.W. (1989) Determination of metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol. 174, 518-552.
53. Trethewey, R.N. and ap Rees, T. (1994) A mutant of Arabidopsis lacking the ability to transport glucose across the chloroplast envelope. Biochem. J. 301, 449-454.
54. Vervliet, G., Holsters, M., Teuchy, H., van Montagu, M. and Schell, J. (1975) Characterisation of different plaque-forming and defective temperate phages in Agrobacterium strains. J. Gen. Virol. 26, 33-48.
55. Walker, J.L.A. and Huber, S.C. (1989) Regulation of sucrosephosphate synthase activity in spinach leaves by protein level and covalent modification. Planta, 117,116-120.