Unexpected presence of graminan- and levan-type fructans in the evergreen frost-hardy eudicot pachysandra terminalis (buxaceae): Purification, cloning, and functional analysis of a 6-SST/6-SFT Enzyme

Plant Physiology

Volumn 155, Issue 1, 2011, Pages 603-614

  van den Ende, Wim ^a   Coopman, Marlies ^a   Clerens, Stefan ^b   Vergauwen, Rudy ^a   le Roy, Katrien ^a   Lammens, Willem ^a   van Laere, André ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b AGRESEARCH LTD   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ASTERACEAE; BUXACEAE; HORDEUM; HORDEUM VULGARE; MAGNOLIOPHYTA; PACHYSANDRA TERMINALIS; PICHIA PASTORIS; TRITICUM AESTIVUM;

EID: 78650973089     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.162222     Document Type: Article

References (75)

1. Altenbach D, Nüesch E, Meyer AD, Boller T, Wiemken A (2004) The large subunit determines catalytic specificity of barley sucrose:fructan 6-fructosyltransferase and fescue sucrose:sucrose 1-fructosyltransferase. FEBS Lett 567: 214-218
2. Altenbach D, Ritsema T (2007) Structure-function relations and evolution of fructosyltransferases. In N Shiomi, N Benkeblia, S Onodera, eds, Recent Advances in Fructooligosaccharides Research. Research Signpost, Kerala, India, pp 135-156
3. Altenbach D, Rudiño-Pinera E, Olvera C, Boller T, Wiemken A, Ritsema T (2009) An acceptor-substrate binding site determining glycosyl transfer emerges from mutant analysis of a plant vacuolar invertase and a fructosyltransferase. Plant Mol Biol 69: 47-56
4. Anderson CL, Bremer K, Friis EM (2005) Dating phylogenetically basal eudicots using rbcL sequences andmultiple fossil reference points. Am J Bot 92: 1737-1748
5. Bancal P, Gibeaut DM, Carpita NC (1993) Analytical methods for the determination of fructan structure and biosynthesis. In M Suzuki, NJ Chatterton, eds, Science and Technology of Fructans. CRC Press, Boca Raton, FL, pp 83-118
6. Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J 277: 2022-2037
7. Curtis PD, Rowland ED, Good GL (2002) Developing a plant-based vole repellent: screening of ten candidate species. Crop Prot 21: 299-306
8. De Coninck B, Le Roy K, Francis I, Clerens S, Vergauwen R, Halliday A, Smith SM, Van Laere A, Van den EndeW (2005) Arabidopsis AtcwINV3 and 6 are not invertases but are fructan exohydrolases (FEHs) with different substrate specificities. Plant Cell Environ 28: 432-443
9. del Viso F, Casabuono AC, Couto AS, Hopp HE, Puebla AF, Heinz RA, Heinz RA (2010) Functional characterization of a sucrose:fructan 6-fructosyltransferase of the cold-resistant grass Bromus pictus by heterelogous expression in Pichia pastoris and Nicotiana tabacum and its involvement in freezing tolerance. J Plant Physiol (in press)
10. del Viso F, Puebla AF, Fusari CM, Casabuono AC, Couto AS, Pontis HG, Hopp HE, Heinz RA (2009) Molecular characterization of a putative sucrose:fructan 6-fructosyltransferase (6-SFT) of the cold-resistant Patagonian grass Bromus pictus associated with fructan accumulation under low temperatures. Plant Cell Physiol 50: 489-503
11. Devkota KP, Lenta BN, Fokou PA, Sewald N (2008) Terpenoid alkaloids of the Buxaceae family with potential biological importance. Nat Prod Rep 25: 612-630
12. Dionne J, Rochefort S, Huff DR, Desjardins Y, Bertrand A, Castonguay Y (2009) Variability for freezing tolerance among 42 Ecotypes of greentype annual bluegrass. Crop Sci 50: 321-336
13. Edelman J, Jefford T (1968) The mechanism of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus. New Phytol 67: 517-531
14. Hendry G (1993) Evolutionary origins and natural functions of fructans. A climatological, biogeographic and mechanistic appraisal. New Phytol 123: 3-14
15. Hincha DK, Zuther E, Hellwege EM, Heyer AG (2002) Specific effects of fructo- and gluco-oligosaccharides in the preservation of liposomes during drying. Glycobiology 12: 103-110
16. Hincha DK, Zuther E, Heyer AG (2003) The preservation of liposomes by raffinose family oligosaccharides during drying is mediated by effects on fusion and lipid phase transitions. Biochim Biophys Acta 1612: 172-177
17. 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 Sci 167: 861-868
18. 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 Phytol 178: 766-780
19. Hoot SB, Magallon S, Crane PR (1999) Phylogeny of basal eudicots based on three molecular data sets: atpB, rbcL, and 18S nuclear ribosomal DNA sequences. Ann Mo Bot Gard 86: 1-32
20. Ji X, Shiran B, Wan J, Lewis DC, Jenkins CL, Condon AG, Richards RA, Dolferus R (2010) Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell Environ 33: 926-942
21. Ji X, Van den Ende W, Schroeven L, Clerens S, Geuten K, Cheng S, 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 Phytol 173: 50-62
22. Jiao Z, Li J (2009) Phylogenetics and biogeography of eastern Asian-North American disjunct genus Pachysandra (Buxaceae) inferred from nucleotide sequences. J Syst Evol 47: 191-201
23. Kawakami A, Sato Y, Yoshida M (2008) Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. J Exp Bot 59: 803-814
24. Kinghorn AD, Su BN, Jang DS, Chang LC, Lee D, Gu JQ, Carcache-Blanco EJ, Pawlus AD, Lee SK, Park EJ, et al (2004) Natural inhibitors of carcinogenesis. Planta Med 70: 691-705
25. Koops AJ, Jonker HH (1994) Purification and characterization of the enzymes of fructan biosynthesis in tubers of Helianthus tuberosus Colombia 1. Fructan-fructan fructosyl transferase. J Exp Bot 45: 1623-1631
26. Koops AJ, Jonker HH (1996) Purification and characterisation of the enzymes of fructan biosynthesis in tubers of Helianthus tuberosus Colombia 2. Purification of sucrose:sucrose 1-fructosyltransferase and reconstitution of fructan synthesis in vitro with purified sucrose:sucrose 1-fructosyltransferase and fructan:fructan 1-fructosyltransferase. Plant Physiol 110: 1167-1175
27. Lammens W, Le Roy K, Schroeven L, Van Laere A, Rabijns A, Van den Ende W (2009) Structural insights into GH32 and GH68 enzymes: functional implications. J Exp Bot 60: 727-740
28. 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.). J Exp Bot 57: 2719-2734
29. Lasseur B, Schroeven L, Lammens W, Le Roy K, Spangenberg G, Manduzio H, Vergauwen R, Lothier J, Prud'homme MP, Van den Ende W (2009) Transforming a fructan:fructan 6G-fructosyltransferase from perennial ryegrass into a sucrose:sucrose 1-fructosyltransferase. Plant Physiol 149: 327-339
30. Le Roy K, Lammens W, Verhaest M, De Coninck B, Rabijns A, Van Laere A, Van den EndeW (2007) Unraveling the difference between invertases and fructan exohydrolases: A single amino acid (Asp-239) substitution transforms Arabidopsis cell wall invertase1 into a fructan 1-exohydrolase. Plant Physiol 145: 616-625
31. 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 Organ Cult 89: 37-48
32. Livingston DP III, Henson CA (1998) Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: responses to second-phase cold hardening. Plant Physiol 116: 403-408
33. Livingston DP III, Hincha DK, Heyer AG (2009) Fructan and its relationship to abiotic stress tolerance in plants. Cell Mol Life Sci 66: 2007-2023
34. 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. J Exp Bot 58: 1969-1983
35. Maleux K, Van den Ende W (2007) Levans in excised leaves of Dactylis glomerata: effects of light, sugars, temperature and senescence. J Plant Biol 50: 671-675
36. Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147: 1251-1263
37. Parvanova D, Ivanov S, Konstantinova T, Karanov E, Atanassov A, Tsvetkov T, Alexieva V, Djilianov D (2004) Transgenic tobacco plants accumulating osmolytes show reduced oxidative damage under freezing stress. Plant Physiol Biochem 42: 57-63
38. 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 N Shiomi, N Benkeblia, S Onodera, eds, Recent Advances in Fructooligosaccharides Research. Research Signpost, Kerala, India, pp 231-258
39. Ritsema T, Hernández 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 J 48: 228-237
40. Roberfroid MB (2007) Prebiotics: the concept revisited. J Nutr 137(3, Suppl 2) 830S-837S
41. Roberfroid MB, Delzenne NM (1998) Dietary fructans. Annu Rev Nutr 18: 117-143
42. Sandve SR, Fjellheim S (2010) Did gene family expansions during the Eocene-Oligocene boundary climate cooling play a role in Pooideae adaptation to cool climates? Mol Ecol 19: 2075-2088
43. Schroeven L, Lammens W, Kawakami A, Yoshida M, Van Laere A, Van den Ende W (2009) Creating S-type characteristics in the F-type enzyme fructan:fructan 1-fructosyltransferase of Triticum aestivum L. J Exp Bot 60: 3687-3696
44. Schroeven L, Lammens W, Van Laere A, Van den Ende W (2008) Transforming wheat vacuolar invertase into a high affinity sucrose:sucrose 1-fructosyltransferase. New Phytol 180: 822-831
45. Simmen U, Obenland D, Boller T, Wiemken A (1993) Fructan synthesis in excised barley leaves (Identification of two sucrose:sucrose fructosyltransferases induced by light and their separation from constitutive invertases). Plant Physiol 101: 459-468
46. 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. Proc Natl Acad Sci USA 92: 11652-11656
47. Stoyanova S, Geuns J, Hideg E, Van den EndeW (2010) The food additives inulin and stevioside counteract oxidative stress. Int J Food Sci Nutr (in press)
48. Tamura K, Kawakami A, Sanada Y, Tase K, Komatsu T, Yoshida M (2009) Cloning and functional analysis of a fructosyltransferase cDNA for synthesis of highly polymerized levans in timothy (Phleum pratense L.). J Exp Bot 60: 893-905
49. Valluru R, Lammens W, Claupein W, Van den Ende W (2008) Freezing tolerance by vesicle-mediated fructan transport. Trends Plant Sci 13: 409-414
50. Valluru R, Van den Ende W (2008) Plant fructans in stress environments: emerging concepts and future prospects. J Exp Bot 59: 2905-2916
51. Van den Ende W, Clerens S, Vergauwen R, Boogaerts D, Le Roy K, Arckens L, Van Laere A (2006) Cloning and functional analysis of a high DP 1-FFT from Echinops ritro. Comparison of the native and recombinant enzymes. J Exp Bot 57: 775-789
52. Van den Ende W, Clerens S, Vergauwen R, Van Riet L, Van Laere A, Yoshida M, Kawakami A (2003b) Fructan 1-exohydrolases. b (2,1) trimmers during graminan biosynthesis in stems of wheat (Triticum aestivum L.)? Purification, characterization, mass mapping and cloning of two fructan 1-exohydrolase isoforms. Plant Physiol 131: 621-631
53. Van den Ende W, De Coninck B, Clerens S, Vergauwen R, Van Laere A (2003a) Unexpected presence of fructan 6-exohydrolases (6-FEHs) in non-fructan plants: characterization, cloning, mass mapping and functional analysis of a novel "cell-wall invertase-like" specific 6-FEH from sugar beet (Beta vulgaris L.). Plant J 36: 697-710
54. Van den Ende W, Lammens W, Van Laere A, Schroeven L, Le Roy K (2009) Donor and acceptor substrate selectivity among plant glycoside hydrolase family 32 enzymes. FEBS J 276: 5788-5798
55. Van den Ende W, Michiels A, Le Roy K, Van Laere A (2002) Cloning of a vacuolar invertase from Belgian endive leaves (Cichorium intybus). Physiol Plant 115: 504-512
56. Van den Ende W, Michiels A, Van Wonterghem D, Clerens SP, De Roover J, Van Laere AJ (2001) Defoliation induces fructan 1-exohydrolase II in Witloof chicory roots. Cloning and purification of two isoforms, fructan 1-exohydrolase IIa and fructan 1-exohydrolase IIb. Mass fingerprint of the fructan 1-exohydrolase II enzymes. Plant Physiol 126: 1186-1195
57. Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: scavenging and salvaging? J Exp Bot 60: 9-18
58. Van den Ende W, Van Laere A (2007) Fructans in dicotyledonous plants: Occurrence and metabolism. In N Shiomi, N Benkeblia, S Onodera, eds, Recent Advances in Fructooligosaccharides Research. Research Signpost, Kerala, India, pp 1-14
59. Van den Ende W, Van Wonterghem D, Dewil E, Verhaert P, De Loof A, Van Laere A (1996a) Purification and characterization of 1-SST, the key enzyme initiating fructan biosynthesis in young chicory roots (Cichorium intybus L.). Physiol Plant 98: 455-466
60. Van den Ende W, Van Wonterghem D, Verhaert P, Dewil E, Van Laere A (1996b) Purification and characterization of fructan:fructan fructosyl transferase from chicory (Cichorium intybus L) roots. Planta 199: 493-502
61. 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 Phytol 166: 917-932
62. Vanhaecke M, Van den Ende W, Van Laere A, Herdewijn P, Lescrinier E (2006) Complete NMR characterization of lychnose from Stellaria media (L.) Vill. Carbohydr Res 341: 2744-2750
63. 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.). J Exp Bot 57: 213-223
64. Van Waes C, Baert J, Carlier L, Van Bockstaele E (1998) A rapid determination of the total sugar content and the average inulin chain length in roots of chicory (Cichorium intybus L). J Sci Food Agric 76: 107-110
65. Vereyken IJ, Chupin V, Demel RA, Smeekens SCM, De Kruijff B (2001) Fructans insert between the headgroups of phospholipids. Biochim Biophys Acta 1510: 307-320
66. Vergauwen R, Van den Ende W, Van Laere A (2000) The role of fructan in flowering of Campanula rapunculoides. J Exp Bot 51: 1261-1266
67. Vijn I, Smeekens S (1999) Fructan: more than a reserve carbohydrate? Plant Physiol 120: 351-360
68. Volaire F, Thomas H, Lelièvre F (1998) Survival and recovery of perennial forage grasses under prolonged Mediterranean drought. I. Growth, death, water relations and solute content in herbage and stubble. New Phytol 140: 439-449
69. von Balthazar M, Endress PK, Qiu YL (2000) Phylogenetic relationships in Buxaceae based on nuclear internal transcribed spacers and plastid ndhF sequences. Int J Plant Sci 161: 785-792
70. 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). J Plant Physiol 158: 1203-1213
71. Wiemken A, Frehner M, Keller F, Wagner W (1986) Fructan metabolism, enzymology and compartmentation. Curr Top Plant Biochem Physiol 5: 17-37
72. Yamada K, Kojima T, Bantog N, Shimoda T, Mori H, Shiratake K, Yamaki S (2007) Cloning of two isoforms of soluble acid invertase of Japanese pear and their expression during fruit development. J Plant Physiol 164: 746-755
73. Yoshida M, Kawakami A, Van den Ende W (2007) Graminan metabolism in cereals: wheat as a model system. In N Shiomi, N Benkeblia, S Onodera, eds, Recent Advances in Fructooligosaccharides Research. Research Signpost, Kerala, India, pp 201-212
74. Zhou SP, Sauve RJ, Mmbaga MT (2005) Adaptation of Pachysandra terminalis Sieb. & Zucc. to freezing temperatures by the accumulation of mRNA and cold-induced proteins. HortScience 40: 346-347
75. Zhu JJ, Beck E (1991) Water relations of Pachysandra leaves during freezing and thawing. Plant Physiol 97: 1146-1153