Heterologous expression of a ketohexokinase in potato plants leads to inhibited rates of photosynthesis, severe growth retardation and abnormal leaf development

Planta

Volumn 218, Issue 4, 2004, Pages 569-578

  Geigenberger, Peter ^a   Regierer, Babette ^a,b   Lytovchenko, Anna ^a   Leisse, Andrea ^a   Schauer, Nicolas ^a   Springer, Fransiska ^a   Kossmann, Jens ^a,c   Fernie, Alisdair R ^a  

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

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Fructose 1 phosphate; Hypoxia; Ketohexokinase; Photosynthesis; Solanum

Indexed keywords

BIOSYNTHESIS; ENZYMES; FRUCTOSE; METABOLISM; OXIDATION; PHOSPHATES; PHOTOSYNTHESIS; STARCH;

GROWTH RETARDATION; HETEROLOGOUS EXPRESSION;

PLANTS (BOTANY);

CARBON DIOXIDE; CHLOROPHYLL; FRUCTOKINASE; HEXOKINASE; KETOHEXOKINASE;

ANIMAL; ARTICLE; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; METABOLISM; PHYSIOLOGY; PLANT LEAF; POTATO; RAT; TRANSGENIC PLANT;

ANIMALS; CARBON DIOXIDE; CHLOROPHYLL; FRUCTOKINASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; HEXOKINASE; LIVER; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; RATS; SOLANUM TUBEROSUM; TRANSCRIPTION, GENETIC;

ANIMALIA; SOLANUM; SOLANUM TUBEROSUM;

EID: 1442290974     PISSN: 00320935     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00425-003-1152-y     Document Type: Article

References (56)

1. Cole CV, Ross C (1966) Extraction, separation and quantitative estimation of soluble nucleotides and sugar phosphates in plant tissues. Anal Biochem 17:526-530
2. Dietze J, Blau A, Willmitzer L (1995) Agrobacterium mediated transformation of potato (Solanum tuberosum). In: Potrykus I, Spangenberg G (eds) Gene transfer to plants xxii. Springer, Berlin Heidelberg New York, pp 24-29
3. Doehlert DC (1989) Separation and characterisation of 4 hexose kinases from developing maize kernels. Plant Physiol 89:1042-1048
4. Donaldson IA, Doyle TC, Matas N (1993) Expression of rat liver ketohexokinase in yeast results in fructose intolerance. Biochem J 291:179-186
5. Fernie AR, Riesmeier JW, Martiny A, Ramalingam S, Willmitzer L, Trethewey RN (2000) Consequences of the expression of a bacterial glucokinase, both in combination with, and independently of a yeast-derived invertase, in potato tubers. Aust J Plant Physiol 26:827-833
6. Fernie AR, Roscher A, Ratcliffe RG, Kruger NJ (2001a) Fructose 2,6-bisphosphate activates pyrophosphate: fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta 212:250-263
7. Fernie AR, Roessner U, Geigenberger P (2001b) The sucrose analog palatinose leads to a stimulation of sucrose degradation and starch synthesis when supplied to discs of growing potato tubers (Solanum tuberosum). Plant Physiol 125:1967-1977
8. Galina A, Reis M, Albequerque MC, Puyou AG, Puyou MTG, de Meis L (1995) Different properties of the mitochondrial and cytosolic hexokinases in maize roots. Biochem J 309:105-112
9. Geiger DR (1976) Effects of translocation and assimilate demands on photosynthesis. Can J Bot 54:2337-2345
10. Geigenberger P (2003) The response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6:247-256
11. Geigenberger P, Lerchl J, Stitt M, Sonnewald U (1996) Phloem-specific expression of pyrophosphatase inhibits long distance transport of carbon and amino acids in tobacco plants. Plant Cell Environ 19:43-55
12. Geigenberger P, Reimholz R, Geiger M, Merlo L, Canale V, Stitt M (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta 201:502-518
13. Geigenberger P, Hajirezaei M, Geiger M, Deiting U, Sonnewald U, Stitt M (1998) Overexpression of pyrophosphatase leads to increased sucrose degradation and starch synthesis, increased activities of enzymes for sucrose-starch interconversion, and increased levels of nucleotides in growing potato tubers. Planta 205:428-437
14. Geigenberger P, Fernie AR, Gibon Y, Christ M, Stitt M (2000) Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biol Chem 381:723-740
15. Graham D, ap Rees T (1965) Occurrence of fructose 1-phosphate in tissues of higher plants. Nature 208:88-89
16. Hatzfeld WD, Dancer J, Stitt M (1990) Fructose 2,6-bisphosphate, metabolites and coarse control of pyrophosphate-fructose 6-phosphate phosphotransferase during triose phosphate cycling in heterotrophic cell suspension cultures of Chenopodium rubrum. Planta 180:205-211
17. Haüsler RE, Schlieben NH, Flügge UI (2000) Control of carbon partitioning and photosynthesis by the triose phosphate/phosphate translocator in transgenic tobacco plants (Nicotiana tabacum). II. Assessment of control coefficients of the triose phosphate/phosphate translocator. Planta 210:383-390
18. Heineke D, Kruse A, Flugge UI, Frommer WB, Riesmeier JW, Willmitzer L, Heldt HW (1994) Effect of antisense repression of the chloroplast triose-phosphate translocator on photosynthetic metabolism in transgenic potato plants. Planta 155:174-180
19. Heinze F (1973) Fructose metabolism In: MacDonald I (ed) Progress in biochemical pharmacology. Karger, Basel, pp 1-42
20. Hodgson RJ, Plaxton WC (1998) Purification and characterization of cytosolic fructose 1,6-bisphosphate aldolase from endosperm of germinating castor oil seeds. Arch Biochem Biophys 355:189-196
21. Jang JC, Leon P, Zhou L, Sheen J (1997) Hexokinase as a sugar sensor in higher plants. Plant Cell 9:5-19
22. Kossmann J, Sonnewald U, Willmitzer L (1994) Reduction of the chloroplastic fructose 1,6-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. Plant J 6:637-650
23. Krapp A, Quick WP, Stitt M (1991) Ribulose 1,5-bisphosphate carboxylase oxygenase, other Calvin cycle enzymes and chlorophyll decrease when glucose is supplied to mature spinach leaves via the transpiration stream. Planta 186:58-69
24. Kruger NJ (1997) Carbohydrate synthesis and degradation. In: Dennis DT, Turpin DH, Lefebvre DD, Layzell DB (eds) Plant metabolism. Longmann, Harlow, pp 83-104
25. Leegood RC, Furbank RT (1986) Stimulation of photosynthesis by 2% oxygen at low temperatures is restored by phosphate. Planta 176:117-126
26. Lerchl J, Geigenberger P, Stitt M, Sonnewald U (1995) Impaired photosynthetic partitioning caused by phloem specific removal of pyrophosphate can be complemented by a phloem specific cytosolic yeast invertase in transgenic plants. Plant Cell 7:259-270
27. Lichtenthaler HK (1987) Chlorophylls and carotenoids - pigments of photosynthetic biomembranes. Methods Enzymol 148:350-382
28. Liu XJ, Prat S, Willmitzer L, Frommer WB (1990) Cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I palatin promoter-GUS-gene fusion. Mol Gen Genet 223:401-406
29. Logemann J, Schell J, Willmitzer (1987) Improved method for the isolation of RNA from plant tissues. Ann Biochem 163:16-20
30. Lytovchenko A, Bieberich K, Willmitzer L, Fernie AR (2002) Carbon assimilation and metabolism in leaves deficient in plastidial phosphoglucomutase. Planta 215:802-811
31. Martinez-Barajas E, Randall DD (1998) Purification and characterization of a glucokinase from young tomato (Lycopersicon esculentum L. Mill) fruit. Planta 205:567-573
32. Morgan LJ, Pridham JB (1986) Fructose 1-phosphate formation in Jerusalem artichoke (Helianthus tuberosus) tubers. Phytochemistry 25:19-22
33. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473-497
34. Niculescu L, Veiga da Cunha M, van Schaftingen E (1996) Enzymatic assays of fructose 1-phosphate and fructose 1,6-bis-phosphate in the picomole range. Anal Biochem 235:243-244
35. Pego JV, Smeekens SCM (2000) Plant fructokinases: a sweet family get-together. Trends Plant Sci 5:531-536
36. Riesmeier JW, Flugge UI, Schulz B, Heineke D, Heldt HW, Willmitzer L, Frommer WB (1993) Antisense repression of the chloroplast triose phosphate translocator affects carbon partitioning in transgenic potato plants. Proc Natl Acad Sci USA 90:6160-6164
37. Riesmeier JW, Willmitzer L, Frommer WB (1994) Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J 13:1-7
38. Rocha-Sosa M, Sonnewald U, Frommer W, Stratmann M, Shell J, Willmitzer L (1989) Both developmental and metabolic signals activate the promoter of the class I palatin gene. EMBO J 8:23-29
39. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13:11-29
40. Roessner-Tunali U, Hegemann B, Lytovchenko A, Carrari F, Bruedigam C, Granot D, Fernie AR (2003) Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol 133:84-99
41. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
42. Schnarrenberger C, Kruger I (1986) Distinction between cytosol and chloroplast fructose bisphosphate aldolases from pea, wheat and corn leaves. Plant Physiol 80:301-304
43. Schneider A, Häusler RE, Kolukisaoglu U, Kunze R, van der Graff E, Schwacke R, Catoni E, Desimone M, Flügge UI (2002) 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 J 32:685-699
44. Schwimmer S, Bevenue A, Weston WJ (1956) Separation of hexose phosphates by paper electrophoresis in borate buffers. Arch Biochem Biophys 60:279-183
45. Sharkey TD, Vanderveer PJ (1989) Stromal phosphate concentration is low during feedback limited photosynthesis. Plant Physiol 91:679-684
46. cat and carbamylation of rubisco. Photosynth Res 28:41-48
47. Sindelar L, Sindelarova M, Burketova L (1998) Hexokinase of tobacco leaves: influence of plant age on particulate and soluble isozyme composition. Biol Plant 40:469-474
48. Stokes DM, Walker DA (1972) Photosynthesis by isolated chloroplasts. Inhibition by DL-glyceraldehyde of carbon dioxide assimilation. Biochem J 128:1147-1157
49. Taylor MA, Ross HA, Gardener A, Davies HV (1995) Characterisation of a cDNA encoding fructokinase from potato (Solanum tuberosum L). J Plant Physiol 145:253-256
50. Theodorou ME, Kruger NJ (2001) Physiological relevance of fructose 2,6-bisphosphate in the regulation of spinach leaf pyrophosphate: fructose 6-phosphate 1-phosphotransferase. Planta 213:147-157
51. Van Dongen JT, Schurr U, Pfister M, Geigenberger P (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol 131:1529-1543
52. Veiga da Cunha M, Houyoux A, van Schaftingen E (2000) Overexpression and purification of fructose 1-phosphate kinase from Escherichia coli: application to the assay of fructose 1-phosphate. Protein Express Purif 19:48-52
53. Veramendi J, Roessner U, Renz A, Willmitzer L, Trethewey RN (1999) Antisense repression of hexokinase 1 leads to an over-accumulation of starch in leaves of transgenic potato plants but not significant changes in tuber metabolism. Plant Physiol 121:1-11
54. Veramendi J, Fernie AR, Leisse A, Willmitzer L, Trethewey RN (2002) Potato hexokinase 2 complements transgenic Arabidopsis plants deficient in hexokinase 1 but does not play a key role in tuber carbohydrate metabolism. Plant Mol Biol 49:491-501
55. Von Schaewen A, Stitt M, Schmidt R, Sonnewald U, Willmitzer L (1990) Expression of a yeast invertase in the cell wall of tobacco and Arabidopsis plants leads to the accumulation of carbohydrates and inhibition of photosynthesis and strongly influences plant growth and phenotype of transgenic tobacco plants. EMBO J 9:3033-3044
56. Weisse A, Gröner F, Sonnewald U, Deppner H, Lerchl J, Hebbeker U, Flügge UI, Weber A (1999) Spinach hexokinase is located on the outer envelope membranes of plastids. FEBS Lett 461:13-18