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

Volumn 23, Issue 1, 2000, Pages 43-53

  Tauberger, Eva ^a   Fernie, Alisdair R ^a   Emmermann, Michael ^a,b   Renz, Andreas ^a,c   Kossmann, Jens ^a   Willmitzer, Lothar ^a   Trethewey, Richard N ^a,d  

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

^b PlantTec Biotechnologie GmbH   (Germany)

^c BASF SE   (Germany)

^d Metanomics GmbH   (Germany)

Author keywords

Amylop last; Glucose 6 phosphate; Phosphoglucomutase; Potato; Starch; Tuber

Indexed keywords

AMYLOPLAST; ANTISENSE TECHNOLOGY; BIOCHEMICAL PATHWAY; CARBON TRANSPORT; CYTOSOL; ENZYME ACTIVITY; ENZYME INHIBITION; GLUCOSE 6 PHOSPHATE; GLUCOSE METABOLISM; PHOSPHOGLUCOMUTASE; PLASTID; POTATO; STPPGM GENE; TRANSGENIC PLANT; TUBER;

ANTISENSE ELEMENTS (GENETICS); BASE SEQUENCE; BIOLOGICAL TRANSPORT; CARBON; CYTOSOL; DNA PRIMERS; DNA, COMPLEMENTARY; GLUCOSE-6-PHOSPHATE; GLYCOLYSIS; ORGANELLES; PHENOTYPE; PHOSPHOGLUCOMUTASE; PLANTS, GENETICALLY MODIFIED; PLASTIDS; SOLANUM TUBEROSUM;

SOLANUM TUBEROSUM;

EID: 0033902395     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2000.00783.x     Document Type: Article

References (52)

1. Arnon, M.I. (1949) Copper enzymes in isolated chloroplasts. Phenoloxidase in Beta vulgaris. Plant Physiol. 24, 1-15.
2. Batz, O., Scheibe, R. and Neuhaus, H.E. (1993) Identification of the putative hexose-phosphate translocator of amyloplasts from cauliflower buds. Biochem. J. 294, 15-17.
3. Batz, O., Maass, U., Henrichs, G. and Scheibe, R. and Neuhaus, H.E. (1994) Glucose-and ADPGIc-dependent starch synthesis in isolated cauliflower-bud amyloplasts. Analysis of the interaction of various potential precursors. Biochim. Biophys. Acta, 1200, 148-154.
4. Boles, E., Liebetrau, W., Hofmann, M. and Zimmermann, F.K. (1994) A family of hexosephosphate mutases in Saccharomyces cerevisiae. Eur. J.Biochem. 220, 83-96.
5. Burrell, M.M., Mooney, P.J., Blundy, M., Carter, D., Wilson, F., Green, J., Blundy, K.S. and ap Rees, T. (1994) Genetic manipulation of 6-phosphofructokinase in potato tubers. Planta, 194, 95-101.
6. Caspar, T., Huber, S.C. and Somerville, C. (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol. 79, 11-17.
7. Dietze, J., Blau, A. and Willmitzer, L. (1995) Agrobacterium-mediated transformation of potato (Solarium tuberosum). In Gene Transfer to Plants XXII (Potrykus, I. and Spangenberg, G., eds). Berlin: Springer Verlag, pp. 24-29.
8. Emanuelsson, O., Mielsen, H. and von Heijne, G. (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8, 978-984.
9. Entwistle, G. and ap Rees, T. (1990) Lack of fructose-1,6-bisphosphatase in a range of higher plants that store starch. Biochem. J. 271, 467-472.
10. Gavel, Y. and von Heijne, G. (1990) A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett. 261, 455-458.
11. Geigenberger, P., Müller-Röber, B. and Stitt, M. (1999) Contribution of adenosine 5′-diphosphoglucose pyrophosphorylase in response to short-term water deficit. Planta, 209, 502-528.
12. Haake, V., Zrenner, R., Sonnewald, U. and 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 J. 14, 147-157.
13. Hanson, K.R. and McHale, N.A. (1988) A starchless mutant of Nicotiana silvestris containing a modified plastid phosphoglucomutase. Plant Physiol. 88, 838-844.
14. Harrison, C.J., Hedley, C.L. and Wang, T.L. (1998) Evidence that the rug3 locus of pea (Pisum sativum L.) encodes plastidial phosphoglucomutase confirms that the imported substrate for starch synthesis in pea amyloplasts is glucose-6-phosphate. Plant J. 13, 753-762.
15. Hatzfeld, W.-D. and 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, 198-204.
16. Hill, L.M. and 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.
17. Jelitto, T., Sonnewald, U., Willmitzer, L., Hajirezaei, M. and Stitt, M. (1992) Inorganic pyrophosphate content and metabolites in leaves and tubers of potato and tobacco plants expressing E. coli pyrophosphatase in their cytosol: biochemical evidence that sucrose metabolism has been manipulated. Planta, 188, 238-244.
18. Kammerer, B., Fischer, K., Hilpert, B., Schubert, S., Gutensohn, M., Weber, A. and and. Flugge, U.-I. (1998) Molecular characterisation of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell, 10, 105-117.
19. Keegstra, K. and Olsen, L.J. (1989) Chloroplast precursors and their transport across the envelope membranes. Annu. Rev. Klösgen, R.B., Saedler, H. and Weil, J.-H. (1989) The amyloplast-targeting transit peptide of the waxy protein of maize also mediates protein transport in vitro into chloroplasts. Mol. Gen. Genet. 217, 155-161.
20. Keegstra, K. and Olsen, L.J. (1989) Chloroplast precursors and their transport across the envelope membranes. Annu. Rev. Klösgen, R.B., Saedler, H. and Weil, J.-H. (1989) The amyloplast-targeting transit peptide of the waxy protein of maize also mediates protein transport in vitro into chloroplasts. Mol. Gen. Genet. 217, 155-161.
21. Kosegarten, H. and Mengel, K. (1994) Evidence for a glucose-1-phosphate translocator in storage tissue amyloplasts of potato (Solanum tuberosum) suspension-cultured cells. Physiol. Plant. 91, 111-120.
22. Kossmann, J., Visser, R.G.F., Müller-Röber, B., Willmitzer, L. and Sonnewald, U. (1991) Cloning and expression analysis of a potato cDNA that encodes branching enzyme: evidence for coexpression of starch biosynthetic genes. Mol. Gen. Genet. 230, 39-44.
23. Kossmann, J., Müller-Röber, B., Dyer, T.A., Raines, C.A., Sonnewald, U. and and. Willmitzer, L. (1992) Cloning and expression analysis of the plastidic fructose-1,6-bisphosphatase coding sequences: circumstantial evidence for the transport of hexoses into chloroplasts. Planta, 188, 7-12.
24. Kruger, N.J. (1997) Carbohydrate synthesis and degradation. In Plant Metabolism (Dennis, D.T., Turpin, D.H., Lefebvre, D.D., Layzell, D.B., eds). Harlow: Longman, pp. 83-104.
25. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-692.
26. Liu, X.J., Prat, S., Willmitzer, L. and Frommer, W.B. (1990) Cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I patatin promoter-GUS-gene fusion. Mol. Gen. Genet. 223, 401-406.
27. Logemann, J., Schell, J. and Willmitzer, L. (1987) Improved method for the isolation of RNA from plant tissues. Ann. Biochem. 163, 16-20.
28. Lu, M. and Kleckner, N. (1994) Molecular cloning and characterisation of the pgm gene encoding phosphoglucomutase of Escherichia coli. J. Bacteriol. 176, 5847-5851.
29. McMichael, R.W., 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.
30. Manjunath, S., Kenneth, L.C.H., Winkle, P.V. and Bailey-Serres, J: (1998) Molecular and biochemical characrterisation of cytosolic phosphoglucomutase in maize. Expression during development and in response to oxygen deprivation. Plant Physiol. 117, 997-1006.
31. Martin, C. and Smith, A.M. (1995) Starch biosynthesis. Plant Cell, 7, 971-985.
32. Murashige, T. and Skoog, F. (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15, 473-497.
33. Müller-Röber, B., Sonnewald, U. and Willmitzer, L. (1992) Antisense inhibition of the ADPglucose pyrophosphorylase in transgenic potato leads to sugar-storing tubers and influences tuber formation and expression of tuber storage protein genes. EMBO J. 11, 1229-1238.
34. Naeem, M., Tetlow, I.J. and Emes, M.J. (1997) Starch synthesis in amyloplasts purified from developing potato tubers. Plant J. 11, 1095-1103.
35. Penger, A., Pelzer-Reith, B. and Schnarrenberger, C. (1994) cDNA sequence for the plastidic phosphoglucomutase from Spinacea oleracea (L). Plant Physiol. 105, 1439-1440.
36. Pozueta-Romero, J., Perata, P. and Akazawa, T. (1999) Sucrose-starch conversion in heterotrophic tissues. Crit Rev. Plant Sci. 18, 489-525.
37. ap Rees, T. and Morrell, S. (1990) Carbohydrate metabolism in developing potatoes. Am. Potato J. 67, 835-847.
38. 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.
39. Rocha-Sosa, M., Sonnewald, U., Frommer, W., Stratmann, M., Schell, J. and Willmitzer, L. (1989) Both developmental and metabolic signals activate the promoter of the class I patatin gene. EMBO J. 8, 23-29.
40. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
41. Schott, K., Borchert, S., Müller-Röber, B. and Heldt, H.W. (1995) Transport of inorganic phosphate and C3-and C6-sugar phosphates across the envelope membranes of potato tuber amyloplasts. Planta, 196, 647-652.
42. Sweetlove, L.J., Burrell, M.M. and ap Rees, T. (1996) Characterisation of transgenic potato (Solanum tuberosum) tubers with increased ADPglucose pyrophosphorylase. Biochem. J. 320, 487-492.
43. Sweetlove, L.J., Müller-Röber, B., Willmitzer, L. and Hill, S.A. (1999) The contribution of adencsine 5′-diphosphoglucose pyrophosphorylase to the control of starch synthesis in potato tubers. Planta, 209, 330-337.
44. Takamiya, S. and Fukui, T. (1978) Purification and multiple forms of phosphoglucomutase from potato tubers. Plant Cell Physiol. 19, 759-768.
45. Trethewey, R.N. and Smith, A.M. (2000) Transitory starch degradation. In Photosynthesis: Physiology and Metabolism (Leegood, R.C., Sharkey, T.D. and von Caemmerer, S., eds). Dordrecht: Kluwer Academic Publishers (in press).
46. Trethewey, R.N. and Willmitzer, L. (1998) The application of transgenic technology to the stucy of sink metabolism in potato. In Regulation of Primary Metabolic Pathways in Plants (Kruger, N.J., Hill, S.A. and Ratcliffe, R.G., eds). Dordrecht: Kluwer Academic Publishers, pp. 239-256.
47. Trethewey, R.N., Geigenberger, P., Riedel, K., Hajirezaei, M.R., Sonnewald, U., Stitt, M., Riesmeier, J.W. and 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 J. 15, 109-118.
48. Trethewey, R.N., Geigenberger, P., Sonnewald, U., Hennig, A., 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.
49. Veramendi, J., Roessner, U., Renz, A., Willmitzer, L. and Trethewey, R.N. (1999) Antisense repression of hexokinase 1 leads to an overaccumulation of starch in leaves of transgenic potato plants but not significant changes in tuber metabolism. Plant Physiol. 121, 1-11.
50. Viola, R., Davies, H.V. and 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 carbon-13 spectroscopy. Planta, 183, 202-208.
51. Waegemann, K. and Soil, J. (1991) Characterisation of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant J. 1, 149-158.
52. Wischmann, B., Nielsen, T.H. and Möller, B.L. (1999) In vitro biosynthesis of phosphorylated starch in intact potato amyloplasts. Plant Physiol. 119, 455-462.