Transforming wheat vacuolar invertase into a high affinity sucrose:sucrose 1-fructosyltransferase

New Phytologist

Volumn 180, Issue 4, 2008, Pages 822-831

  Schroeven, Lindsey ^a   Lammens, Willem ^a   Van Laere, André ^a   Van Den Ende, Wim ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

1 SST (sucrose:sucrose 1 fructosyltransferase); Fructan; Hydrolase; Invertase; Transferase

Indexed keywords

BETA FRUCTOFURANOSIDASE; FRUCTAN; GLYCOSYLTRANSFERASE; HYDROGEN; INULOSUCRASE;

ENZYME ACTIVITY; KINETICS; MUTATION; SUCROSE; WHEAT;

AMINO ACID SEQUENCE; ARTICLE; BIOSYNTHESIS; CELL VACUOLE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MUTATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; WHEAT;

AMINO ACID SEQUENCE; BETA-FRUCTOFURANOSIDASE; EVOLUTION, MOLECULAR; FRUCTANS; HEXOSYLTRANSFERASES; HYDROGEN; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TRITICUM; VACUOLES;

TRITICUM AESTIVUM;

EID: 55649093367     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2008.02603.x     Document Type: Article

References (61)

1. Alberto F, Bignon C, Sulzenbacher G, Henrissat B, Czjzek M. 2004. The three-dimensional structure of invertase (beta-fructosidase) from Thermotoga maritima reveals a bimodular arrangement and an evolutionary relationship between retaining and inverting glycosidases. Journal of Biological Chemistry 279 : 18 903 18 910.
2. Amiard V, Morvan-Bertrand A, Billard JP, Huault C, Keller F, Prud'homme MP. 2003. Fructans, but not the sucrosyl-galactosides, raffinose and loliose, are affected by drought stress in perennial ryegrass. Plant Physiology 132 : 2218 2229.
3. Chalmers J, Lidgett A, Cummings N, Cao YY, Forster J, Spangenberg G. 2005. Molecular genetics of fructan metabolism in perennial ryegrass. Plant Biotechnology Journal 3 : 459 474.
4. Chambert R, Petit-Glatron MF. 1991. Polymerase and hydrolase activities of Bacillus subtilis levansucrase can be separately modulated by site-directed mutagenesis. Biochemical Journal 279 : 35 41.
5. De Coninck B, Van den Ende W, Le Roy K. 2007. Fructan ExoHydrolases (FEHs) in plants: properties, occurrence and 3-D structure. In : Shiomi N, Benkeblia N, Onodera S, eds. Recent advances in fructooligosaccharides research. Kerala, India : Research Signpost, 157 179.
6. DeLano WL. 2002. The PyMOL molecular graphics system. San Carlos, CA, USA : DeLano Scientific.
7. Duchateau N, Bortlik K, Simmen U, Wiemken A, Bancal P. 1995. Sucrose-fructan 6-fructosyltransferase, a key enzyme for diverting carbon from sucrose to fructan in barley leaves. Plant Physiology 107 : 1249 1255.
8. Fujita K, Takegawa K. 2002. Tryptophan-216 is essential for the transglycosylation activity of endo-β-N-acetylglucosaminidase A. Biochemical and Biophysical Research Communications 283 : 680 686.
9. Gallagher JA, Cairns AJ, Pollock CJ. 2004. Cloning and characterization of a putative fructosyltransferase and two putative invertase genes from the temperate grass Lolium temulentum L. Journal of Experimental Botany 55 : 557 569.
10. Gallagher JA, Cairns AJ, Turner LB 2007. Fructan in temperate forage grasses; agronomy, physiology. In : Shiomi N, Benkeblia N, Onodera S, eds. Recent advances in fructooligosaccharides research. Kerala, India : Research Signpost, 15 46.
11. Gebbing T. 2003. The enclosed and exposed part of the peduncle of wheat (Triticum aestivum) - spatial separation of fructan storage. New Phytologist 159 : 245 252.
12. Hendry GAF. 1993. Evolutionary origins and natural functions of fructans - A climatological, biogeographic and mechanistic appraisal. New Phytologist 123 : 3 14.
13. Henrissat B. 1991. A classification of glycosyl hydrolases based on amino-acid-sequence similarities. Biochemical Journal 280 : 309 316.
14. Hincha DK, Livingston DP, Premakumar R, Zuther E, Obel N, Cacela C, Heyer AG. 2007. Fructans from oat and rye: composition and effects on membrane stability during drying. Biochimica et Biophysica Acta-Biomembranes 1768 : 1611 1619.
15. Hisano H, Kanazawa A, Kawakami A, Yoshida M, Shimamoto Y, Yamada T. 2004. Transgenic perennial ryegrass plants expressing wheat fructosyltransferase genes accumulate increased amounts of fructan and acquire increased tolerance on a cellular level to freezing. Plant Science 167 : 861 868.
16. Hisano H, Kanazawa A, Yoshida M, Humphreys MO, Iizuka M, Kitamura K, Yamada T. 2008. Coordinated expression of functionally diverse fructosyltransferase genes is associated with fructan accumulation in response to low temperature in perennial ryegrass. New Phytologist 178 : 766 780.
17. Housley TL, Gibeaut DM, Carpita NC, Sims I, Pollock CJ. 1991. Fructosyl transfer from sucrose and oligosaccharides during fructan synthesis in excised leaves of Lolium temulentum L. New Phytologist 119 : 491 497.
18. Huang LF, Bocock PN, Davis JM, Koch KE. 2007. Regulation of invertase: a suite of transcriptional and post-transcriptional mechanisms. Functional Plant Biology 34 : 499 507.
19. Ji XM, Van den Ende W, Schroeven L, Clerens S, Geuten K, Cheng SH, Bennett J. 2007. The rice genome encodes two vacuolar invertases with fructan exohydrolase activity but lacks the related fructan biosynthesis genes of the Pooideae. New Phytologist 173 : 50 62.
20. Kawakami A, Sato Y, Yoshida M. 2008. Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. Journal of Experimental Botany 59 : 793 802.
21. Kawakami A, Yoshida M. 2002. Molecular characterization of sucrose:sucrose 1-fructosyltransferase and sucrose:fructan 6- fructosyltransferase associated with fructan accumulation in winter wheat during cold hardening. Bioscience Biotechnology and Biochemistry 66 : 2297 2305.
22. Kawakami A, Yoshida M. 2005. Fructan: fructan 1-fructosyltransferase, a key enzyme for biosynthesis of graminan oligomers in hardened wheat. Planta 223 : 90 104.
23. Kawakami A, Yoshida M, Van den Ende W. 2005. Molecular cloning and functional analysis of a novel 6&1-FEH from wheat (Triticum aestivum L.) preferentially degrading small graminans like bifurcose. Gene 358 : 93 101.
24. Kelly R, Leemhuis H, Dijkhuizen L. 2007. Conversion of a cyclodextrin glucanotransferase into an R-amylase: assessment of directed evolution strategies. Biochemistry 46 : 11216 11222.
25. Lammens W, Le Roy K, Van Laere A, Rabijns A, Van den Ende W. 2008. Crystal structures of Arabidopsis thaliana cell-wall invertase mutants in complex with sucrose. Journal of Molecular Biology 377 : 378 385.
26. Lasseur B, Lothier J, Djoumad A, De Coninck B, Smeekens S, Van Laere A, Morvan-Bertrand A, Van den Ende W, Prud'homme MP. 2006. Molecular and functional characterization of a cDNA encoding fructan:fructan 6G-fructosyltransferase (6G-FFT)/fructan:fructan 1-fructosyltransferase (1-FFT) from perennial ryegrass (Lolium perenne L.). Journal of Experimental Botany 57 : 2719 2734.
27. Le Roy K, Lammens W, Van Laere A, Van den Ende W. 2008. Influencing the binding configuration of sucrose in the active sites of chicory fructan 1-exohydrolase and sugar beet fructan 6-exohydrolase. New Phytologist 178 : 572 580.
28. Le Roy K, Lammens W, Verhaest M, De Coninck B, Rabijns A, Van Laere A, Van den Ende W. 2007. Unraveling the difference between invertases and fructan exohydrolases: a single amino acid (Asp239) substitution transforms Arabidopsis cell-wall invertase 1 into a fructan 1-exohydrolase. Plant Physiology 145 : 616 625.
29. Lewis DH. 1993. Nomenclature and diagrammatic representation of oligomeric fructans - a paper for discussion. New Phytologist 124 : 583 594.
30. Li HJ, Yang AF, Zhang XC, Gao F, Zhang JR. 2007. Improving freezing tolerance of transgenic tobacco expressing sucrose:sucrose 1- fructosyltransferase gene from Lactuca sativa. Plant Cell, Tissue and Organ Culture 89 : 37 48.
31. Lothier J, Lasseur B, Le Roy K, Van Laere A, Prud'homme MP, Barre P, Van den Ende W, Morvan-Bertrand A. 2007. Cloning, gene mapping, and functional analysis of a fructan 1-exohydrolase (1-FEH) from Lolium perenne implicated in fructan synthesis rather than in fructan mobilization. Journal of Experimental Botany 58 : 1969 1983.
32. Maleux K, Van den Ende W. 2007. Levans in excised leaves of Dactylis glomerata: effects of temperature, light, sugars and senescence. Journal of Plant Biology 50 : 671 680.
33. Morvan-Bertrand A, Boucaud J, Le Saos J, Prud'homme MP. 2001. Roles of the fructans from leaf sheaths and from the elongating leaf bases in the regrowth following defoliation of Lolium perenne L. Planta 213 : 109 120.
34. Nagaraj VJ, Altenbach D, Galati V, Luscher M, Meyer AD, Boller T, Wiemken A. 2004. Distinct regulation of sucrose:sucrose-1-fructosyltransferase (1-SST) and sucrose:fructan-6-fructosyltransferase (6-SFT), the key enzymes of fructan synthesis in barley leaves: 1-SST as the pacemaker. New Phytologist 161 : 735 748.
35. Nagaraj VJ, Galati V, Luscher M, Boller T, Wiemken A. 2005. Cloning and functional characterization of a cDNA encoding barley soluble acid invertase (HvINV1). Plant Science 168 : 249 258.
36. Pollock CJ, Cairns AJ. 1991. Fructan metabolism in grasses and cereals. Annual Review of Plant Physiology and Plant Molecular Biology 42 : 77 101.
37. Prud'homme MP, Morvan-Bertrand A, Lasseur B, Lothier J, Meuriot F, Decau ML, Noiraud-Romy N. 2007. Lolium perenne, backbone of sustainable development, source of fructans for grazing animals and potential source of novel enzymes. In : Shiomi N, Benkeblia N, Onodera S, eds. Recent advances in fructooligosaccharides research. Kerala, India : Research Signpost, 231 258.
38. Reddy A, Maley F. 1996. Studies on identifying the catalytic role of Glu-204 in the active site of yeast invertase. Journal of Biological Chemistry 271 : 13953 13958.
39. Ritsema T, Hernandez L, Verhaar A, Altenbach D, Boller T, Wiemken A, Smeekens S. 2006. Developing fructan-synthesizing capability in a plant invertase via mutations in the sucrose-binding box. Plant Journal 48 : 228 237.
40. Ritsema T, Verhaar A, Vijn I, Smeekens S. 2005. Using natural variation to investigate the function of individual amino acids in the sucrose-binding box of fructan: fructan 6G-fructosyltransferase (6G-FFT) in product formation. Plant Molecular Biology 58 : 597 607.
41. Roberfroid MB. 2007. Prebiotics: the concept revisited. Journal of Nutrition 137 : 830S 837S.
42. Roitsch T, Gonzalez MC. 2004. Function and regulation of plant invertases: sweet sensations. Trends in Plant Science 9 : 606 613.
43. Schnyder H, Gillenberg C, Hinz J. 1993. Fructan contents and dry-matter deposition in different tissues of the wheat-grain during development. Plant, Cell & Environment 16 : 179 187.
44. Sedmak JJ, Grossberg SE. 1977. A rapid, sensitive, and versatile assay for protein using Coomassie Brilliant Blue G250. Analytical Biochemistry 79 : 544 552.
45. Sprenger N, Bortlik K, Brandt A, Boller T, Wiemken A. 1995. Purification, cloning, and functional expression of sucrose: fructan 6-fructosyltransferase, a key enzyme of fructan synthesis in barley. Proceedings of the National Academy of Sciences, USA 92 : 11652 11656.
46. Sturm A. 1999. Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiology 121 : 1 7.
47. Tang S, Yang S, Cha H, Woo E, Park C, Park K. 2006. Contribution of W229 to the transglycosylation activity of 4-alpha-glucanotransferase from Pyrococcus furiosus. Biochimica et Biophysica Acta-Proteins and Proteomics 1764 : 1633 1638.
48. Van den Ende W, Clerens S, Vergauwen R, Van Riet L, Van Laere A, Yoshida M, Kawakami A. 2003. Fructan 1-exohydrolases β(2,1)-trimmers during graminan biosynthesis in stems of wheat - Purification, characterization, mass mapping, and cloning of two fructan 1-exohydrolase isoforms. Plant Physiology 131 : 621 631.
49. Van den Ende W, Van Laere A. 1996. Fructan synthesizing and degrading activities in chicory roots (Cichorium intybus L.) during field-growth, storage and forcing. Journal of Plant Physiology 149 : 43 50.
50. Van den Ende W, Van Laere A. 2007. Fructans in dicotyledonous plants: occurrence and metabolism. In : Shiomi N, Benkeblia N, Onodera S, eds. Recent advances in fructooligosaccharides research. Kerala, India : Research Signpost, 1 14.
51. Van den Ende W, Van Wonterghem D, Dewil E, Verhaert P, De Loof A, Van Laere A. 1996. Purification and characterization of 1-SST, the key enzyme initiating fructan biosynthesis in young chicory roots (Cichorium intybus). Physiologia Plantarum 98 : 455 466.
52. Van den Ende W, Yoshida M, Clerens S, Vergauwen R, Kawakami A. 2005. Cloning, characterization and functional analysis of novel 6-kestose exohydrolases (6-KEHs) from wheat (Triticum aestivum). New Phytologist 166 : 917 932.
53. Van Laere A, Van den Ende W. 2002. Inulin metabolism in dicots: chicory as a model system. Plant, Cell & Environment 25 : 803 813.
54. Van Riet L, Nagaraj V, Van den Ende W, Clerens S, Wiemken A, Van Laere A. 2006. Purification, cloning and functional characterization of a fructan 6-exohydrolase from wheat (Triticum aestivum L.). Journal of Experimental Botany 57 : 213 223.
55. Verhaest M, Lammens W, Le Roy K, De Coninck B, De Ranter CJ, Van Laere A, Van den Ende W, Rabijns A. 2006. X-ray diffraction structure of a cell-wall invertase from Arabidopsis thaliana. Acta Crystallographica Section D-Biological Crystallography 62 : 1555 1563.
56. Vijn I, van Dijken A, Luscher M, Bos A, Smeets E, Weisbeek P, Wiemken A, Smeekens S. 1998. Cloning of sucrose:sucrose 1-fructosyltransferase from onion and synthesis of structurally defined fructan molecules from sucrose. Plant Physiology 117 : 1507 1513.
57. Vijn I, Smeekens S. 1999. Fructan: more than a reserve carbohydrate? Plant Physiology 120 : 351 359.
58. Wei JZ, Chatterton NJ. 2001. Fructan biosynthesis and fructosyltransferase evolution: expression of the 6-SFT (sucrose:fructan 6-fructosyltransferase) gene in crested wheatgrass (Agropyron cristatum). Journal of Plant Physiology 158 : 1203 1213.
59. Xue GP, McIntyre CL, Jenkins CLD, Glassop D, van Herwaarden AF, Shorter R. 2008. Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiology 146 : 441 454.
60. Yoshida M, Kawakami A, Van den Ende W. 2007. Graminan metabolism in cereals: wheat as a model system. In : Shiomi N, Benkeblia N, Onodera S, eds. Recent advances in fructooligosaccharides research. Kerala, India : Research Signpost, 201 212.
61. Zuccaro A, Götze S, Kneip S, Dersch P, Seibel J. 2008. Tailor-made fructooligosaccharides by a combination of substrate and genetic engineering. ChemBioChem 9 : 143 149.