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Fructan Metabolism in Plant Growth and Development and Stress Tolerance

  • Alejandro del PozoEmail author
  • Ana María Méndez-Espinoza
  • Alejandra Yáñez
Chapter

Abstract

Photosynthesis is a fundamental process for life, converting solar energy into chemical energy. This then powers the assimilation of carbon into organic compounds, like carbohydrates, which are used to synthesize other compounds such as organic acids, amino acids and lipids to form the basic components for biomass accumulation. Water-soluble carbohydrates (WSCs) play a central role in the metabolism of plants as carbon and energy sources in cells, and their levels are continuously adjusted as a result of the balance between supply and demand of carbon at the whole plant level. As a consequence, the metabolism of sugars is very dynamic and varies with the stage of development of plants and in response to the environment. Fructans are the largest reserve of carbohydrates in approximately 15% of higher plants. They are synthesized from sucrose in the vacuole by a group of fructosyltransferase (FT) enzymes and catalysed by fructan exohydrolase (FEH) enzymes. They can be found in vegetative organs – stem, leaves and roots – and in the grain, depending on the state of development of the plant and environmental conditions, such as light intensity, temperature and water availability. Along with its role as a carbohydrate reserve, fructans confer tolerance to cold and drought, contribute to the maintenance of osmotic potential, participate in the stabilization of the membranes and play an important role during grain filling. In temperate cereals, such as wheat (Triticum aestivum) and barley (Hordeum vulgare), carbohydrates are stored mainly in the stem as WSCs and are composed predominantly of grass-type fructans, which may represent more than 80% of the WSCs, followed by sucrose and, to a lesser extent, glucose and fructose. In the absence of stress, fructans accumulate in the stem until they reach a maximum content at early grain filling; later they are degraded and partially remobilized to the grain for the synthesis of starch in late stages of grain filling. However, under unfavourable environmental conditions, fructans can be degraded in the early stages of grain filling to effectively compensate for the decrease in photosynthates and to sustain the rate of grain filling. Therefore, stem fructans can play an important role in grain yield under stressed conditions, and they contribute significantly to the final grain weight in cereals. In addition, genotypic differences in the pattern of fructan accumulation and in the expression genes regulating fructan metabolism have been reported for wheat and other cereals.

Keywords

Cereals Enzymes Gene expression Grain weight Water-soluble carbohydrates 

References

  1. Aranjuelo I, Cabrera-Bosquet L, Morcuende R, Avice JC, Nogués S, Araus JL, Martínez-Carrasco R, Pérez P (2011) Does ear C sink strength contribute to overcoming photosynthetic acclimation of wheat plants exposed to elevated CO2? J Exp Bot 62:3957–3969PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bagherikia S, Pahlevani M, Yamchi A, Zaynalinezhad K, Mostafaie A (2019) Transcript profiling of genes encoding fructan and sucrose metabolism in wheat under terminal drought stress. J Plant Growth Regul 38(1):148–163.  https://doi.org/10.1007/s00344-018-9822-yCrossRefGoogle Scholar
  3. Bancal P, Carpita NC, Gaudillere JP (1992) Differences in fructan accumulated in induced and field-grown wheat plants: an elongation-trimming pathway for their synthesis. New Phytol 120:313–321CrossRefGoogle Scholar
  4. Bancal P, Triboï E (1993) Temperature effect on fructan oligomer contents and fructan-related enzyme activities in stems of wheat (Triticum aestivum L.) during grain filling. New Phytol 123:247–253CrossRefGoogle Scholar
  5. Blum A (1998) Improving wheat grain filling under stress by stem reserve mobilisation. Euphytica 100:77–83CrossRefGoogle Scholar
  6. Blum A, Sinmena B, Mayer J, Golan G, Shpiler L (1994) Stem reserve mobilisation supports wheat-grain filling under heat stress. Funct Plant Biol 21:771–781CrossRefGoogle Scholar
  7. Bogeat-Triboulot M-B, Brosché M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T (2007) Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiol 143:876–892PubMedPubMedCentralCrossRefGoogle Scholar
  8. Cairns AJ, Pollock CJ (1988) Fructan biosynthesis in excised leaves of Lolium temulentum L. II. Changes in fructosyl transferase activity following excision and application of inhibitors of gene expression. New Phytol 109:407–413CrossRefGoogle Scholar
  9. Carpita NC, Housley TL, Hendrix JE (1991) New features of plant-fructan structure revealed by methylation analysis and carbon-13 nmr spectroscopy. Carbohydr Res 217:127–136CrossRefGoogle Scholar
  10. Cramer G, Ergül A, Grimplet J, Tillett R, Tattersall ER, Bohlman M, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch K, Schooley D, Cushman J (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7:111–134PubMedCrossRefPubMedCentralGoogle Scholar
  11. Chalmers J, Lidgett A, Cummings N, Cao Y, Forster J, Spangenberg G (2005) Molecular genetics of fructan metabolism in perennial ryegrass. Plant Biotechnol J 3:459–474PubMedCrossRefPubMedCentralGoogle Scholar
  12. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560PubMedPubMedCentralCrossRefGoogle Scholar
  13. 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 210:808–814PubMedCrossRefPubMedCentralGoogle Scholar
  14. del Pozo A, Castillo D, Inostroza L, Matus I, Méndez AM, Morcuende R (2012) Physiological and yield responses of recombinant chromosome substitution lines of barley to terminal drought in a Mediterranean-type environment. Ann Appl Biol 160:157–167CrossRefGoogle Scholar
  15. del Pozo A, Yáñez A, Matus I, Tapia G, Castillo D, Araus JL, Sanchez-Jardón L (2016) Physiological traits associated with wheat yield potential and performance under water-stress in a Mediterranean environment. Front Plant Sci 7:987.  https://doi.org/10.3389/fpls.2016.00987CrossRefPubMedPubMedCentralGoogle Scholar
  16. Del Viso F, Puebla A, Hopp H, Heinz R (2009) Cloning and functional characterization of a fructan 1-exohydrolase (1-FEH) in the cold tolerant Patagonian species Bromus pictus. Planta 231:13–25PubMedCrossRefPubMedCentralGoogle Scholar
  17. Dreccer MF, van Herwaarden AF, Chapman SC (2009) Grain number and grain weight in wheat lines contrasting for stem water soluble carbohydrate concentration. Field Crops Res 112:43–54CrossRefGoogle Scholar
  18. Dolferus R, Powell N, Ji X, Ravash R, Edlington J, Oliver S, van Dongen J, Shiran B (2013) Chapter 8: The physiology of reproductive-stage abiotic stress tolerance in cereals. In: Rout G, Das A (Eds) Molecular stress physiology of plants. Springer India, pp 193–218Google Scholar
  19. Dong Y, Liu J, Zhang Y, Geng H, Rasheed A, Xiao Y, Cao S, Fu L, Yan J, Wen W, Zhang Y, Jing R, Xia X, He Z (2016) Genome-wide association of stem water soluble carbohydrates in bread wheat. PLoS One 11:e0164293.  https://doi.org/10.1371/journal.pone.0164293CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 Physiol 107:1249–1255PubMedPubMedCentralCrossRefGoogle Scholar
  21. Ehdaie B, Alloush GA, Madore MA, Waines JG (2006) Genotypic variation for stem reserves and mobilization in wheat: II. Postanthesis changes in internode water-soluble carbohydrates. Crop Sci 46:2093–2103CrossRefGoogle Scholar
  22. Ehdaie B, Alloush GA, Waines JG (2008) Genotypic variation in linear rate of grain growth and contribution of stem reserves to grain yield in wheat. Field Crops Res 106:34–43CrossRefGoogle Scholar
  23. Foulkes MJ, Sylvester-Bradley R, Weightman R, Snape JW (2007) Identifying physiological traits associated with improved drought resistance in winter wheat. Field Crops Res 103:11–24CrossRefGoogle Scholar
  24. Gadegaard G, Didion T, Folling M, Storgaard M, Andersen CH, Nielsen KK (2008) Improved fructan accumulation in perennial ryegrass transformed with the onion fructosyltransferase genes 1-SST and 6G-FFT. J Plant Physiol 165:1214–1225PubMedCrossRefPubMedCentralGoogle Scholar
  25. Gallagher JN, Biscoe PV, Hunter B (1976) Effects of drought on grain growth. Nature 264:541–542CrossRefGoogle Scholar
  26. Gebbing T, Schnyder H, Kühbauch W (1999) The utilization of pre-anthesis reserves in grain filling of wheat. Assessment by steady-state 13CO2/12CO2 labelling. Plant Cell Environ 22:851–858CrossRefGoogle Scholar
  27. Geigenberger P, Kolbe A, Tiessen A (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 56:1469–1479PubMedCrossRefPubMedCentralGoogle Scholar
  28. Halford NG, Curtis TY, Muttucumaru N, Postles J, Mottram DS (2011) Sugars in crop plants. Ann Appl Biol 158:1–25CrossRefGoogle Scholar
  29. Hendry GAF (1993) Evolutionary origins and natural functions of fructans -a climatological, biogeographic and mechanistic appraisal. New Phytol 123:3–14CrossRefGoogle Scholar
  30. Hincha DK, Livingston DP III, Premakumar R, Zuther E, Obel N, Cacela C, Heyer AG (2007) Fructans from oat and rye: Composition and effects on membrane stability during drying. Biochim Biophys Acta Biomembr 1768:1611–1619CrossRefGoogle Scholar
  31. Hou J, Huang X, Sun W, Du C, Wang C, Xie Y, Ma Y, Ma D (2018) Accumulation of water-soluble carbohydrates and gene expression in wheat stems correlates with drought resistance. J Plant Physiol 231:182–191.  https://doi.org/10.1016/j.jplph.2018.09.017CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hummel I, Pantin F, Sulpice R, Piques M, Rolland G, Dauzat M, Christophe A, Pervent M, Bouteillé M, Stitt M, Gibon Y, Muller B (2010) Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol 154:357–372PubMedPubMedCentralCrossRefGoogle Scholar
  33. Jiang Y, Huang B (2001) Osmotic adjustment and root growth associated with drought preconditioning-enhanced heat tolerance in kentucky bluegrass. Crop Sci 41:1168–1173CrossRefGoogle Scholar
  34. Joudi M, Ahmadi A, Mohamadi V, Abbasi A, Vergauwen R, Mohammadi H, Van den Ende W (2012) Comparison of fructan dynamics in two wheat cultivars with different capacities of accumulation and remobilization under drought stress. Physiol Plant 144:1–12PubMedCrossRefPubMedCentralGoogle Scholar
  35. Kawakami A, Sato Y, Yoshida M (2008) Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. J Exp Bot 59:793–802PubMedCrossRefPubMedCentralGoogle Scholar
  36. Kawakami A, Yoshida M (2005) Fructan:fructan 1-fructosyltransferase, a key enzyme for biosynthesis of graminan oligomers in hardened wheat. Planta 223:90–104PubMedCrossRefGoogle Scholar
  37. 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
  38. Khoshro H, Taleei A, Bihamta M, Shahbazi M, Abbasi A, Ramezanpour S (2014) Expression analysis of the genes involved in accumulation and remobilization of assimilates in wheat stem under terminal drought stress. Plant Growth Regul 74:165–176CrossRefGoogle Scholar
  39. Kim J-Y, Mahé A, Brangeon J, Prioul JL (2000) A maize vacuolar invertase, IVR2, is induced by water stress. Organ/tissue specificity and diurnal modulation of expression. Plant Physiol 124:71–84PubMedPubMedCentralCrossRefGoogle Scholar
  40. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246PubMedCrossRefPubMedCentralGoogle Scholar
  41. Lasseur B, Lothier J, Djoumad A, De Coninck B, Smeekens S, Van Laere A, Morvan-Bertrand A, Van den Ende W, Prud’homme M-P (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 57:2719–2734PubMedCrossRefPubMedCentralGoogle Scholar
  42. 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 (Asp-239) substitution transforms Arabidopsis cell wall invertase1 into a fructan 1-exohydrolase. Plant Physiol 145:616–625PubMedPubMedCentralCrossRefGoogle Scholar
  43. Li H, Cai J, Jiang D, Liu F, Dai T, Cao W (2013) Carbohydrates accumulation and remobilization in wheat plants as influenced by combined waterlogging and shading stress during grain filling. J Agric Crop Sci 199:38–48CrossRefGoogle Scholar
  44. Li W, Zhang B, Li R, Chang X, Jing R (2015) Favorable Alleles for Stem Water-Soluble Carbohydrates Identified by Association Analysis Contribute to Grain Weight under Drought Stress Conditions in Wheat. PLoS One 10:e0119438PubMedPubMedCentralCrossRefGoogle Scholar
  45. Liu F, Jensen CR, Andersen MN (2004) Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implication in altering pod set. Field Crops Res 86:1–13CrossRefGoogle Scholar
  46. Livingston DP, Henson CA (1998) Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: Responses to second-phase cold hardening. Plant Physiol 116:403–408PubMedCentralCrossRefGoogle Scholar
  47. Livingston DP, Hincha D, Heyer A (2009) Fructan and its relationship to abiotic stress tolerance in plants. Cell Mol Life Sci 66:2007–2023PubMedPubMedCentralCrossRefGoogle Scholar
  48. Lunn JE (2007) Compartmentation in plant metabolism. J Exp Bot 58:35–47PubMedCrossRefPubMedCentralGoogle Scholar
  49. Martínez-Carrasco R, Cervantes E, Pérez P, Morcuende R, Del Molino IMM (1993) Effect of sink size on photosynthesis and carbohydrate content of leaves of three spring wheat varieties. Physiol Plant 89:453–459CrossRefGoogle Scholar
  50. Martínez-Vilalta SA, Asensio D, Galiano L, Hoch G, Palacio S, Piper FI, Lloret F (2016) Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis. Ecol Monogr 86:495–516CrossRefGoogle Scholar
  51. McIntyre C, Casu R, Rattey A, Dreccer M, Kam J, van Herwaarden A, Shorter R, Xue G (2011) Linked gene networks involved in nitrogen and carbon metabolism and levels of water-soluble carbohydrate accumulation in wheat stems. Funct Integr Genomics 11:585–597PubMedCrossRefPubMedCentralGoogle Scholar
  52. McIntyre CL, Seung D, Casu RE, Rebetzke GJ, Shorter R, Xue GP (2012) Genotypic variation in the accumulation of water soluble carbohydrates in wheat. Funct Plant Biol 39:560.  https://doi.org/10.1071/fp12077CrossRefGoogle Scholar
  53. Medrano H, Flexas J (2000) Fijación del dióxido de carbono y biosíntesis de fotoasimilados. In: Azcón-Bieto J, Talón M (eds) Fundamentos de Fisiología Vegetal. McGraw-Hill-Interamericana, Barcelona, España, pp 173–187Google Scholar
  54. Méndez AM, Castillo D, Del Pozo A, Matus I, Morcuende R (2011) Differences in stem soluble carbohydrate contents among recombinant chromosome substitution lines (RCSLs) of barley under drought in a Mediterranean-type environment. Agron Res 9:433–438Google Scholar
  55. Mercier V, Bussi C, Lescourret F, Génard M (2009) Effects of different irrigation regimes applied during the final stage of rapid growth on an early maturing peach cultivar. Irrig Sci 27:297–306CrossRefGoogle Scholar
  56. Monneveux P, Rekika D, Acevedo E, Merah O (2006) Effect of drought on leaf gas exchange, carbon isotope discrimination, transpiration efficiency and productivity in field grown durum wheat genotypes. Plant Sci 170:867–872CrossRefGoogle Scholar
  57. Morcuende R, Kostadinova S, Pérez P, IMM DM, Martínez-Carrasco R (2004) Nitrate is a negative signal for fructan synthesis, and the fructosyltransferase-inducing trehalose inhibits nitrogen and carbon assimilation in excised barley leaves. New Phytol 161:749–759CrossRefGoogle Scholar
  58. Morcuende R, Kostadinova S, Pérez P, Martínez-Carrasco R (2005) Fructan synthesis is inhibited by phosphate in warm-grown, but not in cold-treated, excised barley leaves. New Phytol 168:567–574PubMedCrossRefPubMedCentralGoogle Scholar
  59. 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 213:109–120PubMedCrossRefPubMedCentralGoogle Scholar
  60. Müller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. J Exp Bot 62:1715–1729PubMedCrossRefPubMedCentralGoogle Scholar
  61. Müller J, Aeschbacher RA, Sprenger N, Boller T, Wiemken A (2000) Disaccharide-mediated regulation of sucrose:fructan-6-fructosyltransferase, a key enzyme of fructan synthesis in barley leaves. Plant Physiol 123:265–274PubMedPubMedCentralCrossRefGoogle Scholar
  62. Osuna D, Usadel B, Morcuende R, Gibon Y, Bläsing OE, Höhne M, Günter M, Kamlage B, Trethewey R, Scheible W-R, Stitt M (2007) Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 49:463–491PubMedPubMedCentralCrossRefGoogle Scholar
  63. Peleg Z, Fahima T, Krugman T, Abbo S, Yakir D, Korol AB, Saranga Y (2009) Genomic dissection of drought resistance in durum wheat x wild emmer wheat recombinant inbreed line population. Plant Cell Environ 32:758–779PubMedCrossRefPubMedCentralGoogle Scholar
  64. Pérez P, Morcuende R, Martı́n del Molino I, Martı́nez-Carrasco R (2005) Diurnal changes of Rubisco in response to elevated CO2, temperature and nitrogen in wheat grown under temperature gradient tunnels. Environ Exper Bot 53:13–27CrossRefGoogle Scholar
  65. Pérez P, Morcuende R, Martín del Molino I, Sánchez de la Puente L, Martínez-Carrasco R (2001) Contrasting responses of photosynthesis and carbon metabolism to low temperatures in tall fescue and clovers. Physiol Plant 112:478–486PubMedCrossRefPubMedCentralGoogle Scholar
  66. Peshev D, Vergauwen R, Moglia A, Hideg É, Van den Ende W (2013) Towards understanding vacuolar antioxidant mechanisms: a role for fructans? J Exp Bot 64:1025–1038PubMedPubMedCentralCrossRefGoogle Scholar
  67. Pilon-Smits E, Ebskamp M, Paul MJ, Jeuken M, Weisbeek PJ, Smeekens S (1995) Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiol 107:125–130PubMedPubMedCentralCrossRefGoogle Scholar
  68. Pilon-Smits EAH, Hwang S, Mel Lytle C, Zhu Y, Tai JC, Bravo RC, Chen Y, Leustek T, Terry N (1999) Overexpression of ATP sulfurylase in indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol 119:123–132PubMedPubMedCentralCrossRefGoogle Scholar
  69. Pollock CJ, Cairns AJ (1991) Fructan metabolism in grasses and cereals. Annu Rev Plant Biol 42:77–101CrossRefGoogle Scholar
  70. Ramel F, Sulmon C, Gouesbet G, Couée I (2009) Natural variation reveals relationships between pre-stress carbohydrate nutritional status and subsequent responses to xenobiotic and oxidative stress in Arabidopsis thaliana. Ann Bot 104:1323–1337PubMedPubMedCentralCrossRefGoogle Scholar
  71. Rao RSP, Andersen JR, Dionisio G, Boelt B (2011) Fructan accumulation and transcription of candidate genes during cold acclimation in three varieties of Poa pratensis. J Plant Physiol 168:344–351PubMedCrossRefPubMedCentralGoogle Scholar
  72. Rebetzke GJ, van Herwaarden AF, Jenkins C, Weiss M, Lewis D, Ruuska S, Tabe L, Fettell NA, Richards RA (2008) Quantitative trait loci for water-soluble carbohydrates and associations with agronomic traits in wheat. Aust J Agric Res 59:891–905CrossRefGoogle Scholar
  73. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709PubMedPubMedCentralCrossRefGoogle Scholar
  74. Ruuska SA, Lewis DC, Kennedy G, Furbank RT, Jenkins CLD, Tabe LM (2008) Large scale transcriptome analysis of the effects of nitrogen nutrition on accumulation of stem carbohydrate reserves in reproductive stage wheat. Plant Mol Biol 66:15–32PubMedCrossRefPubMedCentralGoogle Scholar
  75. Ruuska SA, Rebetzke GJ, van Herwaarden AF, Richards RA, Fettell NA, Tabe L, Jenkins CLD (2006) Genotypic variation in water-soluble carbohydrate accumulation in wheat. Funct Plant Biol 33:799–809CrossRefGoogle Scholar
  76. Salinas C, Handford M, Pauly M, Dupree P, Cardemil L (2016) Structural modifications of fructans in Aloe barbadensis Miller (aloe vera) grown under water stress. PLoS One 11:e0159819PubMedPubMedCentralCrossRefGoogle Scholar
  77. Salem K, Röder M, Börner A (2007) Identification and mapping quantitative trait loci for stem reserve mobilisation in wheat (Triticum aestivum L.). Cereal Res Commun 35(3):1367–1374CrossRefGoogle Scholar
  78. Scofield GN, Ruuska SA, Aoki N, Lewis DC, Tabe LM, Jenkins CLD (2009) Starch storage in the stems of wheat plants: localization and temporal changes. Ann Bot 103:859–868PubMedPubMedCentralCrossRefGoogle Scholar
  79. Schnyder H (1993) The role of carbohydrate storage and redistribution in the source-sink relations of wheat and barley during grain filling-a review. New Phytol 123:233–245CrossRefGoogle Scholar
  80. Shiomi N, Benkeblia N, Onodera S, Yoshihira T, Kosaka S, Osaki M (2006) Fructan accumulation in wheat stems during kernel filling under varying nitrogen fertilization. Can J Plant Sci 86:1027–1035CrossRefGoogle Scholar
  81. 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 101:459–468PubMedPubMedCentralCrossRefGoogle Scholar
  82. Snape JW, Foulkes MJ, Simmonds J, Leverington M, Fish LJ, Wang Y, Ciavarrella M (2007) Dissecting gene x environmental effects on wheat yields via QTL and physiological analysis. Euphytica 154:401–408.  https://doi.org/10.1007/s10681-006-9208-2CrossRefGoogle Scholar
  83. Teulat B, Borries C, This D (2001) New QTLs identified for plant water status, water-soluble carbohydrate and osmotic adjustment in a barley population grown in a growth-chamber under two water regimes. Theor Appl Genet 103:161–170CrossRefGoogle Scholar
  84. Turner LB, Cairns AJ, Armstead IP, Thomas H, Humphreys MW, Humphreys MO (2008) Does fructan have a functional role in physiological traits?. Investigation by quantitative trait locus mapping. New Phytol 179:765–775PubMedCrossRefPubMedCentralGoogle Scholar
  85. 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 Physiol 131:621–631PubMedCentralCrossRefGoogle Scholar
  86. Van den Ende W, Coopman M, Clerens S, Vergauwen R, Le Roy K, Lammens W, Van Laere A (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 155:603–614PubMedCrossRefPubMedCentralGoogle Scholar
  87. Van den Ende W, De Coninck B, Van Laere A (2004) Plant fructan exohydrolases: a role in signaling and defense? Trends Plant Sci 9:523–528PubMedCrossRefPubMedCentralGoogle Scholar
  88. 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 166:917–932PubMedCrossRefPubMedCentralGoogle Scholar
  89. Van Laere A, Van Den Ende W (2002) Inulin metabolism in dicots: chicory as a model system. Plant Cell Environ 26:803–813CrossRefGoogle Scholar
  90. Lynn D. Veenstra, Jean-Luc Jannink, Mark E. Sorrells, (2017) Wheat Fructans: A Potential Breeding Target for Nutritionally Improved, Climate-Resilient Varieties. Crop Science 57(3):1624CrossRefGoogle Scholar
  91. Veenstra LD, Jannink J, Sorrells ME (2017) Wheat fructans: A potential breeding target for nutritionally improved, climate-resilient varieties. Crop Sci 57:1624–1640CrossRefGoogle Scholar
  92. Verhaest M, Lammens W, Le Roy K, De Ranter CJ, Van Laere A, Rabijns A, Van den Ende W (2007) Insights into the fine architecture of the active site of chicory fructan 1-exohydrolase: 1-kestose as substrate vs sucrose as inhibitor. New Phytol 174:90–100PubMedCrossRefPubMedCentralGoogle Scholar
  93. Versluys M, Kirtel O, Toksoy Öner E, Van den Ende W (2017a) The fructan syndrome: Evolutionary aspects and common themes among plants and microbes. Plant Cell Environ 41:16–38.  https://doi.org/10.1111/pce.13070CrossRefPubMedPubMedCentralGoogle Scholar
  94. Versluys M, Tarkowski ŁP, Van den Ende W (2017b) Fructans As DAMPs or MAMPs: Evolutionary prospects, cross-tolerance, and multistress resistance potential. Front Plant Sci 7:2061PubMedPubMedCentralCrossRefGoogle Scholar
  95. Verspreet J, Cimini S, Vergauwen R, Dornez E, Locato V, Le Roy K, De Gara L, Van den Ende W, Delcour JA, Courtin CM (2013) Fructan metabolism in developing wheat (Triticum aestivum L.) kernels. Plant Cell Physiol 54:2047–2057PubMedCrossRefPubMedCentralGoogle Scholar
  96. Verspreet J, Dornez E, Van den Ende W, Delcour JA, Courtin CM (2015) Cereal grain fructans: Structure, variability and potential health effects. Trends Food Sci Technol 43:32–42CrossRefGoogle Scholar
  97. Vijn I, Smeekens S (1999) Fructan: More than a reserve carbohydrate? Plant Physiol 120:351–360PubMedPubMedCentralCrossRefGoogle Scholar
  98. Virgona J, Barlow E (1991) Drought stress induces changes in the non-structural carbohydrate composition of wheat stems. Funct Plant Biol 18:239–247CrossRefGoogle Scholar
  99. Wagner W (1986) Regulation of fructan metabolism in leaves of barley (Hordeum vulgare L. cv Gerbel). Plant Physiol 81:444PubMedPubMedCentralCrossRefGoogle Scholar
  100. Wang C, Van den Ende W, Tillberg J-E (2000) Fructan accumulation induced by nitrogen deficiency in barley leaves correlates with the level of sucrose:fructan 6-fructosyltransferase mRNA. Planta 211:701–707PubMedCrossRefPubMedCentralGoogle Scholar
  101. Xiang GAO, She MY, Yin GX, Yang YU, Qiao WH, Du LP, Ye XG (2010) Cloning and characterization of genes coding for fructan biosynthesis enzymes (FBEs) in Triticeae plants. Agric Sci China 9:313–324CrossRefGoogle Scholar
  102. Xue G, McIntyre CL, Jenkins CLD, Glassop D, van Herwaarden AF, Shorter R (2008a) Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiol 146:441–454PubMedPubMedCentralCrossRefGoogle Scholar
  103. Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008b) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761PubMedCrossRefPubMedCentralGoogle Scholar
  104. Yang DL, Jing RL, Chang XP, Li W (2007) Identification of quantitative trait loci and environmental interactions for accumulation and remobilization of water-soluble carbohydrates in wheat (Triticum aestivum L.) stems. Genetics 176:571–584.  https://doi.org/10.1534/genetics.106.068361CrossRefPubMedPubMedCentralGoogle Scholar
  105. Yang J, Zhang J (2006) Grain filling of cereals under soil drying. New Phytol 169:223–236PubMedCrossRefPubMedCentralGoogle Scholar
  106. Yang J, Zhang J, Wang Z, Zhu Q, Liu L (2004) Activities of fructan- and sucrose-metabolizing enzymes in wheat stems subjected to water stress during grain filling. Planta 220:331–343CrossRefGoogle Scholar
  107. Yañez A, Tapia G, Guerra F, del Pozo A (2017) Stem carbohydrate dynamics and expression of genes involved in fructan accumulation and remobilization during grain growth in wheat (Triticum aestivum L.) genotypes with contrasting tolerance to water stress. PLoS One 12(5):e0177667.  https://doi.org/10.1371/journal.pone.0177667CrossRefPubMedPubMedCentralGoogle Scholar
  108. Yoshida M, Kawakami A (2013) Molecular analysis of fructan metabolism associated with freezing tolerance and snow mold resistance of winter wheat. In: Imai R, Yoshida M, Matsumoto N (eds) Plant and microbe adaptations to cold in a changing world. Springer, New York, NYGoogle Scholar
  109. Yue A, Li A, Mao X, Chang X, Li R, Jing R (2015) Identification and development of a functional marker from 6-SFT-A2 associated with grain weight in wheat. Mol Breed 35:1–10CrossRefGoogle Scholar
  110. Zeeman SC, Delatte T, Messerli G, Umhang M, Stettler M, Mettler T, Streb S, Reinhold H, Kötting O (2007) Starch breakdown: recent discoveries suggest distinct pathways and novel mechanisms. Funct Plant Biol 34:465–473CrossRefGoogle Scholar
  111. Zhang J, Dell B, Conocono E, Waters I, Setter T, Appels R (2009) Water deficits in wheat: fructan exohydrolase (1-FEH) mRNA expression and relationship to soluble carbohydrate concentrations in two varieties. New Phytol 181:843–850PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Alejandro del Pozo
    • 1
    Email author
  • Ana María Méndez-Espinoza
    • 1
  • Alejandra Yáñez
    • 2
  1. 1.Centro de Mejoramiento Genético y Fenómica Vegetal, Facultad de Ciencias Agrarias, Universidad de TalcaTalcaChile
  2. 2.Facultad de Ciencias Agrarias y Forestales, Universidad Católica del MauleCuricóChile

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