Advertisement

Sugars as Antioxidants in Plants

  • Wim Van den EndeEmail author
  • Darin Peshev
Chapter

Abstract

Plants as sessile organisms are subjected to various forms of environmental stress. It is generally accepted that stress leads to excess concentrations of reactive oxygen species (ROS). Crop yield and quality are negatively affected by stress leading to oxidative damage. Here in this chapter, we will discuss the participation of carbohydrates in plant stress responses. Soluble carbohydrates (e.g., trehalose, sucrose, raffinose, etc.) are recognized compatible solutes. Sugars can replace water under drought stress. As such, they keep membrane surfaces “hydrated” and prevent membrane fusion by maintaining the space between phospholipid molecules. Small soluble sugars (glucose, fructose, sucrose) can also act as signals. They are now recognized as pivotal integrating regulatory molecules that control gene expression related to plant metabolism, stress resistance, growth and development. Finally, as a new concept, we propose that soluble vacuolar carbohydrates (e.g., fructans) may participate in vacuolar antioxidant processes, intimately linked to the well-known cytosolic antioxidant processes under stress. All these insights might contribute to the development of superior, stress tolerant crops.

Keywords

Antioxidants Carbohydrates Crops Disaccharides Fructans Osmoprotectants ROS stress Sugars 

References

  1. Albrecht G, Biemelt S, Baumgartner S (1997) Accumulation of fructans following oxygen deficiency stress in related plant species with different flooding tolerances. New Phytol 136:137–144Google Scholar
  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 Physiol 132:2218–2229PubMedCrossRefGoogle Scholar
  3. Amtmann A (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical componentsc of abiotic stress tolerances in plant. Mol Plant 2:3–12PubMedCrossRefGoogle Scholar
  4. Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942PubMedCrossRefGoogle Scholar
  5. Banguela A, Hernández L (2006) Fructans: From natural sources to transgenic plants. Biotecnología Aplicada 23:202–210Google Scholar
  6. Banguela A, Arrieta J, Rodriguez R, Trujillo L, Menendez C, Hernández L (2011) High levan accumulation in transgenic tobacco plants expressing the Gluconacetobacter diazotrophicus levansucrase gene. J Biotech 154:93–98CrossRefGoogle Scholar
  7. Bhaskar PB, Wu L, Busse JS et al (2010) Suppression of the vacuolar invertase gene prevents cold-induced sweetening in potato. Plant Physiol 154:939–948PubMedCrossRefGoogle Scholar
  8. Blochl A, Peterbauer T, Hofmann J, Richter A (2008) Enzymatic breakdown of raffinose oligosaccharides in pea seeds. Planta 228:99–110PubMedCrossRefGoogle Scholar
  9. 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 277:2022–2037PubMedCrossRefGoogle Scholar
  10. Bonfig KB, Gabler A, Simon UK et al (2010) Post-translational derepression of invertase activity in source leavess via down-regulation of invertase inhibitor expression is part of the plant defense response. Mol Plant 3:1037–48PubMedCrossRefGoogle Scholar
  11. Cairns AJ (2003) Fructan biosynthesis in transgenic plants. J Exp Bot 54:549–567PubMedCrossRefGoogle Scholar
  12. Carter C, Pan SQ, Jan ZH, Avila EL, Girke T, Raikhel NV (2004) The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted and unexpected proteins. Plant Cell 16:3285–3303PubMedCrossRefGoogle Scholar
  13. Cho YH, Yoo SD (2011) Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. Plos Genet 7:e1001263Google Scholar
  14. Davidson DJ, Chevalier PM (1992) Storage and remobilization of water-soluble carbohydrates in stems of spring wheat. Crop Sci 32:186–190CrossRefGoogle Scholar
  15. De Coninck B, Le Roy K, Francis I et al (2005) Arabidopsis AtcwINV 3 and 6 are not invertases but are fructan exohydrolases (FEHs) with different substrate specificities. Plant Cell Environ 28:432–443CrossRefGoogle Scholar
  16. De Gara L, de Pinto MC, Moliterni VMC, D’Egidio MG (2003) Redox regulation and storage processes during maturation in kernels of Triticum durum. J Exp Bot 54:249–258PubMedCrossRefGoogle Scholar
  17. De Roover J, Vandenbranden K, Van Laere A, Van den Ende W (2000) Drought induces fructan synthesis and 1-SST (sucrose: sucrose fructosyltransferase) in roots and leaves of chicory seedlings (Cichorium intybus L.). Planta 210:808–814PubMedCrossRefGoogle Scholar
  18. Debnam PM, Fernie AR, Leisse A et al (2004) Altered activity of the P2 isoform of plastidic glucose 6-phosphate dehydrogenase in tobacco (Nicotiana tabacum cv. Samsun) causes changes in carbohydrate metabolism and response to oxidative stress in leaves. Plant J 38:49–59PubMedCrossRefGoogle Scholar
  19. Djilianov D, Ivanov S, Moyankova D et al (2011) Sugar ratios, glutathione redox status and phenols in the resurrection species Haberlea rhodopensis and the closely related non-resurrection species Chirita eberhardtii. Plant Biology 13:767–776Google Scholar
  20. Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: A multifunctional molecule. Glycobiology 13:17R-27RPubMedCrossRefGoogle Scholar
  21. Espinoza C, Degenkolbe T, Caldana C et al (2010) Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. Plos One 5:19CrossRefGoogle Scholar
  22. Ferreres F, Figueiredo R, Bettencourt S et al (2011) Identification of phenolic compounds in isolated vacuoles of the medicinal plant Catharanthus roseus and their interaction with vacuolar class III peroxidase: An H2O2 affair?. J Exp Bot 62:2841–2854PubMedCrossRefGoogle Scholar
  23. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100PubMedCrossRefGoogle Scholar
  24. Frank G, Pressman E, Ophir R et al (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60:3891–3908PubMedCrossRefGoogle Scholar
  25. Gadegaard G, Didion T, Foiling M, Storgaard M, Andersen CH, Nielsen KK (2008) Improved fructan accumulation in perennial ryegrass transformed with the onion fructosyl transferase genes 1-SST and 6G-FFT. J Plant Physiol 165:1214–1225CrossRefGoogle Scholar
  26. Garg AK, Kim JK, Owens TG et al (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc  Natl Acad Sci U S Am 99:15898–15903CrossRefGoogle Scholar
  27. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol  Bioch 48:909–930CrossRefGoogle Scholar
  28. He XMM, Liu HW (2002) Formation of unusual sugars: Mechanistic studies and biosynthetic applications. Ann Rev Biochem 71:701–754PubMedCrossRefGoogle Scholar
  29. Hellwege EM, Czapla S, Jahnke A, Willmitzer L, Heyer AG (2000) Transgenic potato (Solanum tuberosum) tubers synthesize the full spectrum of inulin molecules naturally occurring in globe artichoke (Cynara scolymus) roots. Proc Natl Acad Sci US Am 97:8699–8704CrossRefGoogle Scholar
  30. Hendry GAF (1993) Evolutionary origins and natural functions of fructans—A climatological, biogeographic and mechanistiv appraisal. New Phytol 123:3–14CrossRefGoogle Scholar
  31. Hincha DK, Zuther E, Hellwege EM, Heyer AG (2002) Specific effects of fructo- and gluco-oligosaccharides in the preservation of liposomes during drying. Glycobiology 12:103–110PubMedCrossRefGoogle Scholar
  32. Hincha DK, Livingston DP, Premakumar R et al (2007) Fructans from oat and rye: Composition and effects on membrane stability during drying. Biochimica et Biophysica Acta-Biomembranes 1768:1611–1619CrossRefGoogle Scholar
  33. 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 167:861–868CrossRefGoogle Scholar
  34. Hodges DM, Andrews CJ, Johnson DA, Hamilton RI (1997) Antioxidant enzyme responses to chilling stress in differentially sensitive inbred maize lines. J  Exp Bot 48:1105–1113CrossRefGoogle Scholar
  35. Hothorn M, Van den Ende W, Lammens W, Rybin V, Scheffzek K (2010) Structural insights into the pH-controlled targeting of plant cell-wall invertase by a specific inhibitor protein. Proc Natl Acad Sci US Am 107:17427–17432CrossRefGoogle Scholar
  36. Hughes MA, Dunn MA (1996) The molecular biology of plant acclimation to low temperature. J Exp Bot 47:291–305Google Scholar
  37. Iftime D, Hannah MA, Peterbauer T, Heyer AG (2011) Stachyose in the cytosol does not influence freezing tolerance of transgenic Arabidopsis expressing stachyose synthase from adzuki bean. Plant Sci 180:24–30PubMedCrossRefGoogle Scholar
  38. Ji XM, Shiran B, Wan JL et al (2010) Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell Environ 33:926–942PubMedCrossRefGoogle Scholar
  39. Jin Y, Ni DA, Ruan YL (2009) Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell 21:2072–2089PubMedCrossRefGoogle Scholar
  40. Joudi M, Ahmadi A, Mohamadi V, Abbasi A, Vergauwen R, Mohamadi H, Van den Ende W (2011) Comparison of fructan dynamics in two wheat cultivars with different capacities of accumulation and remobilization under terminal drought stress. Physiol Plant 144:1–12Google Scholar
  41. 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 358:93–101PubMedCrossRefGoogle Scholar
  42. Kawakami A, Sato Y, Yoshida M (2008) Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. J Exp Bot 59:793–802PubMedCrossRefGoogle Scholar
  43. Klotke J, Kopka J, Gatzke N, Heyer AG (2004) Impact of soluble sugar concentrations on the acquisition of freezing tolerance in accessions of Arabidopsis thaliana with contrasting cold adaptation—evidence for a role of raffinose in cold acclimation. Plant Cell Environ 27:1395–1404CrossRefGoogle Scholar
  44. Koch K (2004) Sucrose metabolism: Regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246PubMedCrossRefGoogle Scholar
  45. Konstantinova T, Parvanova D, Atanassov A, Djilianov D (2002) Freezing tolerant tobacco, transformed to accumulate osmoprotectants. Plant Sci 163:157–164CrossRefGoogle Scholar
  46. Korn M, Gartner T, Erban A, Kopka J, Selbig J, Hincha DK (2010) Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol Plant 3:224–235PubMedCrossRefGoogle Scholar
  47. Lara MEB, Garcia MCG, Fatima T et al (2004) Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16:1276–1287CrossRefGoogle Scholar
  48. LeClere S, Schmelz EA, Chourey PS (2010) Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiol 153:306–318PubMedCrossRefGoogle Scholar
  49. Lenne T, Bryant G, Holcomb R, Koster KL (2007) How much solute is needed to inhibit the fluid to gel membrane phase transition at low hydration? Biochimica et Biophysica Acta-Biomembranes 1768:1019–1022CrossRefGoogle Scholar
  50. Levine H, Slade L (1991) Polymer physicochemical characterization of oligosaccharides. Acs Symposium Series 458:219–260Google Scholar
  51. Lewis DH (1984) Citation classic—sugar alcohols (polyols) in fungi and green plants. 1. Distribution, physiology and metabolism. Curr Contents Agr Biol Environ Sci 6:16Google Scholar
  52. 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 89:37–48CrossRefGoogle Scholar
  53. Li P, Wind JJ, Shi XL et al (2011) Fructose sensitivity is suppressed in Arabidopsis by the transcription factor ANAC089 lacking the membrane-bound domain. Proc Natl Acad Sci US Am 108:3436–3441CrossRefGoogle Scholar
  54. Linster CL, Adler LN, Webb K, Christensen KC, Brenner C, Clarke SG (2008) A second GDP-L-galactose phosphorylase in Arabidopsis en route to vitamin C—covalent intermediate and substrate requirements for the conserved reaction. J Biol Chem 283:18483–18492PubMedCrossRefGoogle Scholar
  55. Livingston DP, Tallury SP (2009) Freezing in non-acclimated oats. II: Thermal response and histology of recovery in gradual and rapidly frozen plants. Thermochimica Acta 481:20–27CrossRefGoogle Scholar
  56. Lothier J, Lasseur B, Prud’homme MP, Morvan-Bertrand A (2010) Hexokinase-dependent sugar signaling represses fructan exohydrolase activity in Lolium perenne. Funct Plant Biol 37:1151–1160CrossRefGoogle Scholar
  57. Lou Y, Gou JY, Xue HW (2007) PIP5K9, an Arabidopsis phosphatidylinositol monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar-mediated root growth. Plant Cell 19:163–181PubMedCrossRefGoogle Scholar
  58. Ma YY, Zhang YL, Lu J, Shao HB (2009) Roles of plant soluble sugars and their responses to plant cold stress. Afr J Biotechnol 8:2004–2010Google Scholar
  59. Michiels A, Van Laere A, Van den Ende W, Tucker M (2004) Expression analysis of a chicory fructan 1-exohydrolase gene reveals complex regulation by cold. J Exp Bot 55:1325–1333PubMedCrossRefGoogle Scholar
  60. Moore B, Zhou L, Rolland F et al (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Sci 300:332–336CrossRefGoogle Scholar
  61. Moore JP, Westall KL, Ravenscroft N, Farrant JM, Lindsey GG, Brandt WF (2005) The predominant polyphenol in the leaves of the resurrection plant Myrothamnus flabellifolius, 3,4,5 tri-O-galloylquinic acid, protects membranes against desiccation and free radical-induced oxidation. Biochem J 385:301–308PubMedCrossRefGoogle Scholar
  62. Muller B, Pantin F, Genard M et al (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729PubMedCrossRefGoogle Scholar
  63. Muller J, Boller T, Wiemken A (1995) Trehalose and trehalase in plants: Recent developments. Plant Sci 112:1–9CrossRefGoogle Scholar
  64. Mundree SG, Baker B, Mowla S et al (2002) Physiological and molecular insights into drought tolerance. Afr J Biotechnol 1:28–38Google Scholar
  65. Nagao M, Oku K, Minami A et al (2006) Accumulation of theanderose in association with development of freezing tolerance in the moss Physcomitrella patens. Phytochemistry 67:702–709PubMedCrossRefGoogle Scholar
  66. Nery DDM, da Silva CG, Mariani D et al (2008) The role of trehalose and its transporter in protection against reactive oxygen species. Biochimica et Biophysica Acta-General Subjects 1780:1408–1411CrossRefGoogle Scholar
  67. Nguyen GN, Hailstones DL, Wilkes M, Sutton BG (2010) Role of carbohydrate metabolism in drought-induced male sterility in rice anthers. J Agron Crop Sci 196:346–357CrossRefGoogle Scholar
  68. Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263PubMedCrossRefGoogle Scholar
  69. Ohnishi S, Miyoshi T, Shirai S (2010) Low temperature stress at different flower developmental stages affects pollen development, pollination, and pod set in soybean. Environ Exp Bot 69:56–62CrossRefGoogle Scholar
  70. Otto T, Zoitan T, Scott P (2009) Vegetative desiccation tolerance: Is it a goldmine for bioengineering crops? Plant Sci 176:187–199CrossRefGoogle Scholar
  71. Pan W, Sunayama Y, Nagata Y et al (2009) Cloning of a cDNA encoding the sucrose: sucrose 1-fructosyltransferase (1-SST) from yacon and its expression in transgenic rice. Biotechnol Equipment 23:1479–1484CrossRefGoogle Scholar
  72. Paradiso A, Cecchini C, De Gara L, D’Egidio MG (2006) Functional, antioxidant and rheological properties of meal from immature durum wheat. J Cereal Sci 43:216–222CrossRefGoogle Scholar
  73. Parvanova D, Popova A, Zaharieva I et al (2004) Low temperature tolerance of tobacco plants transformed to accumulate proline, fructans, or glycine betaine. Variable chlorophyll fluorescence evidence. Photosynthetica 42:179–185CrossRefGoogle Scholar
  74. Pennycooke JC, Jones ML, Stushnoff C (2003) Down-regulating alpha-galactosidase enhances freezing tolerance in transgenic petunia. Plant Physiol 133:901–909PubMedCrossRefGoogle Scholar
  75. Peters S, Keller F (2009) Frost tolerance in excised leaves of the common bugle (Ajuga reptans L.) correlates positively with the concentrations of raffinose family oligosaccharides (RFOs). Plant Cell Environ 32:1099–1107PubMedCrossRefGoogle Scholar
  76. Peters S, Mundree SG, Thomson JA, Farrant JM, Keller F (2007) Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): Both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit. J Exp Bot 58:1947–1956PubMedCrossRefGoogle Scholar
  77. Plaut Z, Butow BJ, Blumenthal CS, Wrigley CW (2004) Transport of dry matter into developing wheat kernels and its contribution to grain yield under post-anthesis water deficit and elevated temperature. Field Crops Res 86:185–198CrossRefGoogle Scholar
  78. Pollock CJ, Cairns AJ (1991) Fructan metabolism in grasses and cereals. Annu Rev Plant Physiol Plant Mol Biol 42:77–101CrossRefGoogle Scholar
  79. Pollock CJ, Cairns AJ, Gallagher J, Harrison J (1999) The integration of sucrose and fructan metabolism in temperate grasses and cereals. In: Kruger NJ, Hill SA, Ratcliffe RG (eds) Regulation of primary metabolic pathways in plants. pp. 195–226Google Scholar
  80. Proels RK, Roitsch T (2009) Extracellular invertase LIN6 of tomato: A pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm. J Exp Bot 60:1555–1567PubMedCrossRefGoogle Scholar
  81. Queval G, Jaillard D, Zechmann B, Noctor G (2011) Increased intracellular H2O2 availability preferentially drives glutathione accumulation in vacuoles and chloroplasts. Plant Cell Environ 34:21–32PubMedCrossRefGoogle Scholar
  82. Roberfroid MP (2007) The concept revisited. J Nutrition 137:830S-7SGoogle Scholar
  83. Roitsch T, Balibrea ME, Hofmann M, Proels R, Sinha AK (2003) Extracellular invertase: Key metabolic enzyme and PR protein. J Exp Bot 54:513–524PubMedCrossRefGoogle Scholar
  84. Roitsch T, Gonzalez MC (2004) Function and regulation of plant invertases: Sweet sensations. Trends Plant Sci 9:606–613PubMedCrossRefGoogle Scholar
  85. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: Conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709PubMedCrossRefGoogle Scholar
  86. Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: Roles in development, yield potential, and response to drought and heat. Mol Plant 3:942–955PubMedCrossRefGoogle Scholar
  87. Salerno GL, Curatti L (2003) Origin of sucrose metabolism in higher plants: When, how and why? Trends Plant Sci 8:63–69PubMedCrossRefGoogle Scholar
  88. Sauter JJ, Wisniewski M, Witt W (1996) Interrelationships between ultrastructure, sugar levels, and frost hardiness of ray parenchyma cells during frost acclimation and deacclimation in poplar (Populus x canadensis Moench ‘robusta’) wood. J Plant Physiol 149:451–461CrossRefGoogle Scholar
  89. Schneider T, Keller F (2009) Raffinose in chloroplasts is synthesized in the cytosol and transported across the chloroplast envelope. Plant Cell Physiol 50:2174–2182PubMedCrossRefGoogle Scholar
  90. Sevenier R, Hall RD, Van Der Meer IM, Hakkert HJC, van Tunen AJ, Koops AJ (1998) High level fructan accumulation in a transgenic sugar beet. Nat Biotechnol 16:843–846PubMedCrossRefGoogle Scholar
  91. Shen B, Jensen RG, Bohnert HJ (1997) Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiol 113:1177–1183PubMedCrossRefGoogle Scholar
  92. Sinkevich MS, Naraykina NV, Trunova TI (2010) Sugars participate in the antioxidant protection from oxidative stress induced by paraquat in the case of potato transformed with yeast invertase gene. Doklady Akademii Nauk 434:570–573Google Scholar
  93. Skirycz A, Vandenbroucke K, Clauw P et al (2011) Survival and growth of Arabidopsis plants given limited water are not equal. Nat Biotechnol 29:212–214PubMedCrossRefGoogle Scholar
  94. Smeekens S, Ma JK, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opinion Plant Biol 13:274–279CrossRefGoogle Scholar
  95. Stoop JM, Van Arkel J, Hakkert JC, Tyree C, Caimi PG, Koops AJ (2007) Developmental modulation of inulin accumulation in storage organs of transgenic maize and transgenic potato. Plant Sci 173:172–181CrossRefGoogle Scholar
  96. Stoyanova S, Geuns J, Hideg E, Van den Ende W (2011) The food additives inulin and stevioside counteract oxidative stress. Int J Food Sci Nutrition 62:207–214CrossRefGoogle Scholar
  97. Taji T, Ohsumi C, Iuchi S et al (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426PubMedCrossRefGoogle Scholar
  98. Tapernoux-Luthi EM, Bohm A, Keller F (2004) Cloning, functional expression, and characterization of the raffinose oligosaccharide chain elongation enzyme, galactan: galactan galactosyltransferase, from common bugle leaves. Plant Physiol 134:1377–1387PubMedCrossRefGoogle Scholar
  99. Tester M, Bacic A (2005) Abiotic stress tolerance in grasses. From model plants to crop plants. Plant Physiol 137:791–793PubMedCrossRefGoogle Scholar
  100. Uemura M, Steponkus PL (1999) Cold acclimation in plants: Relationship between the lipid composition and the cryostability of the plasma membrane. J Plant Res 112:245–254CrossRefGoogle Scholar
  101. Valluru R, Lammens W, Claupein W, Van den Ende W (2008) Freezing tolerance by vesicle-mediated fructan transport. Trends Plant Sci 13:409–414PubMedCrossRefGoogle Scholar
  102. Valluru R, Van den Ende W (2008) Plant fructans in stress environments: Emerging concepts and future prospects. J Exp Bot 59:2905–2916PubMedCrossRefGoogle Scholar
  103. 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 126:1186–1195PubMedCrossRefGoogle Scholar
  104. 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 Plantarum 115:504–512CrossRefGoogle Scholar
  105. Van den Ende W, Valluru R (2009) Sucrose, sucrosyl oligosaccharides, and oxidative stress: Scavenging and salvaging? J Exp Bot 60:9–18PubMedCrossRefGoogle Scholar
  106. Van den Ende W, Coopman M, Clerens S et al (2011) 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 Physiol 155:603–614PubMedCrossRefGoogle Scholar
  107. Van Laere A, Van den Ende W (2002) Inulin metabolism in dicots: Chicory as a model system. Plant Cell Environ 25:803–813CrossRefGoogle Scholar
  108. Vanhaecke M, Van den Ende W, Lescrinier E, Dyubankova N (2008) Isolation and characterization of a pentasaccharide from Stellaria media. J Nat Prod 71:1833–1836PubMedCrossRefGoogle Scholar
  109. Vanhaecke M, Dyubankova N, Lescrinier E, Van den Ende W (2010) Metabolism of galactosyl-oligosaccharides in Stellaria media—discovery of stellariose synthase, a novel type of galactosyltransferase. Phytochemistry 71:1095–1103PubMedCrossRefGoogle Scholar
  110. Vereyken IJ, van Kuik JA, Evers TH, Rijken PJ, de Kruijff B (2003) Structural requirements of the fructan-lipid interaction. Bioph J 84:3147–3154CrossRefGoogle Scholar
  111. Vergauwen R, Van den Ende W, Van Laere A (2000) The role of fructan in flowering of Campanula rapunculoides. J Exp Bot 51:1261–1266CrossRefGoogle Scholar
  112. Vijn I, van Dijken A, Sprenger N et al (1997) Fructan of the inulin neoseries is synthesized in transgenic chicory plants (Cichorium intybus L) harbouring onion (Allium cepa L) fructan: fructan 6G-fructosyltransferase. Plant J 11:387–398PubMedCrossRefGoogle Scholar
  113. Weber H, Borisjuk L, Heim U, Buchner P, Wobus U (1995) Seed coat-associated invertases of fava-bean control both unloading and storage functions—cloning of cDNA and cell-type-specific expression. Plant Cell 7:1835–1846PubMedGoogle Scholar
  114. Wolfe J, Bryant G (1999) Freezing, drying, and/or vitrification of membrane-solute-water systems. Cryobiology 39:103–129PubMedCrossRefGoogle Scholar
  115. Xiang L, Le Roy K, Bolouri-Moghaddam MR et al (2011) Exploring the neutral invertase—oxidative stress defence connection in Arabidopsis thaliana. J Exp Bot 62:1871–1885Google Scholar
  116. 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 Physiol 146:441–454PubMedCrossRefGoogle Scholar
  117. Yang JC, Zhang JH (2006) Grain filling of cereals under soil drying. New Phytol 169:223–236PubMedCrossRefGoogle Scholar
  118. Zechmann B, Stumpe M, Mauch F (2011) Immunocytochemical determination of the subcellular distribution of ascorbate in plants. Planta 233:1–12PubMedCrossRefGoogle Scholar
  119. Zhang YH, Primavesi LF, Jhurreea D et al (2009) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149:1860–1871PubMedCrossRefGoogle Scholar
  120. Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: Uncovering the weakest links. J Exp Bot 61:1959–1968PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Laboratory for Molecular Plant BiologyKatholieke Universiteit LeuvenHeverleeBelgium

Personalised recommendations