Photosynthesis pp 301-320 | Cite as

Fructans: Synthesis and Regulation

  • A. J. Cairns
  • C. J. Pollock
  • J. A. Gallagher
  • J. Harrison
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 9)

Summary

Roughly ten percent of higher plant species possess a mechanism for reserve carbon allocation based on soluble fructose polymers (vacuolar fructan), which differs markedly in its enzymology, subcellular compartmentation and regulation from the more common starch-based carbon economy. This includes many economically important species, especially the temperate grasses and cereals. This chapter describes these novel elements associated with fructan metabolism, with particular emphasis on fructan synthesis in photosynthetic tissue.

Fructan structures, although based on variations in a few characters (polymer size, glycosidic linkage, etc.) are shown to be both varied and complex, differing markedly between species but possessing a consistency within species which argues for a biosynthetic mechanism with a high degree of specificity. The enzymological mechanisms currently thought to be involved are discussed, with particular reference to the involvement of multifunctional enzymes and the strong effects of both substrate and enzyme concentration on the chemical nature of the products in vitro. The enzymatic polymerization of authentic grass fructan has been achieved, but the conditions required in vitro do not coincide with those expected in the vacuole, the currently accepted site of synthesis. The properties of fructosyl transferases in general are shown to be unusual and we emphasize the need toreconcile the characteristics of enzymes in vitro with the patterns of metabolism and conditions observed in the tissue.

The regulation of fructan synthesis is discussed in relation to the pivotal role of sucrose as the sole substrate and as the key element in the coarse control of fructan accumulation, apparently acting at the level of gene expression and de novo enzyme synthesis. Sucrose mediated feedback inhibition of starch metabolism via phosphate transport does not apparently occur in grass leaves. This isolation of chloroplast metabolism from cytosolic sucrose accumulation indicates a fundamental difference in the fine control of centralcarbon metabolism between fructan and starch accumulators.

Recently, non-fructan, starch-accumulating plants such as maize, spinach and tobacco have been transformed with bacterial genes for fructan synthesis and shown to accumulate fructan. The current value of such transgenics is in terms of what they may tell us about the regulation of primary carbon metabolism in the recipient plants. Transgenics currently provide little insight into the nature or control of endogenous fructan metabolism. Some neglected aspects of the physiology these transgenics are considered by comparison with endogenous reserve carbon metabolism in untransformed plants.

Keywords

Sucrose Accumulation Jerusalem Artichoke Tuber Fructan Content Lolium Temulentum Fructan Synthesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

DP

degree of polymerization (number of hexose moieties)

FFT

fructan:fructan fructosyl transferase (EC 2.4.1.99)

Mr

molecualr mass

PEG

polyethylene glycol

SST

sucrose:sucrose fructosyl transferase (EC 2.4.1.100)

TLC

thin layer chromatography

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References

  1. Austin RB, Edrich JA, Ford MA and Blackwell RD (1977) The fate of the dry matter, carbohydrates and 14C lost from the leaves and stems of wheat during grain filling. Ann Bot 41: 1309–1321Google Scholar
  2. Bancal P and Triboi E (1993) Temperature effect on fructan oligomer contents and fructan-related enzyme activities in stems of wheat (Triticum oestivum L.) during grain filling. New Phytol 123: 247–253Google Scholar
  3. Bonnett GD and Incoll LD (1992) The potential pre-anthesis and post-anthesis contributions of stem interposed to grain yield in crops of winter barley. Ann Bot 69:219–225Google Scholar
  4. Bonnett GD and Simpson RJ (1993) Fructan hydrolase activities from Lolium rigidum Gaudin. New Phytol 123: 443–451Google Scholar
  5. Bonnett GD and Simpson RJ (1995) Fructanexo hydrolase activities from Lolium Rigidum that hydrolyze beta-2,1-glycosidic and beta-2, 6-glycosidic linkages at different rates. New Phytol 131:199–209Google Scholar
  6. Caimi PG, McCole LM, Klein TM and Kerr PS (1996) Fructan accumulation and sucrose metabolism in transgenic maize endosperm expressing a Bacillus amyloliquefaciens sacB gene. Plant Physiol 110: 355–363PubMedGoogle Scholar
  7. Cairns AJ (1992a) A reconsideration of fructan biosynthesis in storage roots of Asparagus officinalis L. New Phytol 120: 463–473Google Scholar
  8. Cairns AJ (1992b) Fructan biosynthesis in excised leaves of Lolium temulentum L. V. Enzymatic de novo synthesis of large fructans from sucrose. New Phytol 122: 253–259Google Scholar
  9. Cairns AJ (1993) Evidence for the de novo synthesis of fructan by enzymes from higher plants: A reappraisal of the SST/FFT model. New Phytol 123:15–24Google Scholar
  10. Cairns AJ (1995) Effects of enzyme concentration of oligo fructan synthesis from sucrose. Phytochemistry 40:705–708CrossRefGoogle Scholar
  11. Cairns AJ and Ashton JE (1993) Species-dependent patterns of fructan synthesis by enzymes from excised leaves of oat, wheat, barley and timothy. New Phytol 124: 381–388Google Scholar
  12. Cairns AJ and Ashton JE (1994) Fructan biosynthesis in excised leaves of Lolium temulentum L. VI Optimisation and stability of enzymatic fructan synthesis. New Phytol 126: 3–10Google Scholar
  13. Cairns AJ and Pollock CJ (1988a) Fructan biosynthesis in excised leaves of Lolium temulentum L. I. Chromatographic characterisation of oligo fructans and their labelling patterns following 14CO2 feeding. New Phytol 109: 399–405Google Scholar
  14. Cairns AJ and Pollock CJ (1988b) 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 109:407–413Google Scholar
  15. Cairns AJ, Winters AL and Pollock CJ (1989) Fructan biosynthesis in excised leaves of Lolium temulentum L. III A comparison of the invitro properties of fructosyl transferase activities with the characteristics of in vivo fructan accumulation. New Phytol 112: 343–352Google Scholar
  16. Cairns AJ, Bonnett GD, Gallagher JA, Simpson RJ and Pollock CJ (1997) Fructan biosynthesis in excised leaves of Lolium temulentum VII Sucrose and fructan hydrolysis by a fructan-polymerising enzyme preparation. New Phytol 136: 61–72CrossRefGoogle Scholar
  17. Cairns AJ, Nash R, Machado de Carvalho MA and Sims IM (1999) Characterisation of the enzymatic polymerisation of 2,6-linked fructan by leafextracts from timothy grass (Phleum pratense). New Phytol 142: 79–91CrossRefGoogle Scholar
  18. Chatterton NJ, Harrison PA, Thornley WR and Bennett JH (1993) Structures of fructan oligomers in orchard grass (Dactylis glomerata L.) J Plant Physiol 142: 552–556Google Scholar
  19. Collis BE. and Pollock CJ (1991) The control of sucrose synthesis in leaves of Lolium temulentum L., a fructan-accumulating grass. New Phytol 119: 483–489Google Scholar
  20. Collis BE and Pollock CJ (1992) Cytoplasmic carbohydrate metabolism in leaf tissues undergoing fructan synthesis and breakdown. J Plant Physiol 140:124–126Google Scholar
  21. Dedonder R (1966) Levansucrase from Bacillus subtilis. Meths Enzymol 8:500–505Google Scholar
  22. Dey PM (1980) Biochemistry of α-D-galactosidie linkages in the plant kingdom. Adv Carbohyd Chem Biochem 37: 283–372Google Scholar
  23. Dubois D, Winzeler M and Nösberger J (1990) Fructan accumulation and sucrose:sucrose fructosyl transferase activity in stems of spring wheat genotypes. Crop Sci 30:315–319Google Scholar
  24. Duchateau N, Bortlik K, Simmen U, Wiemken A and Bancal P (1995) Sucrose-fructan 6-fructosyl transferase: A key enzyme for diverting carbon from sucrose to fructan in barley leaves. Plant Physiol 107:1249–1255PubMedGoogle Scholar
  25. Ebskamp MJM, van der Meer IM, Spronk BA, Weisbeek PJ and Smeekens SCM (1994) Accumulation of fructose polymers in transgenic tobacco. Bio/Technology 12: 272–275CrossRefPubMedGoogle Scholar
  26. Edelman J and Dickerson AG (1966) The metabolism of fructose polymers in plants. Transfructosylation in tubers of Helianthus tuberosus L. Biochem J 98:787–794PubMedGoogle Scholar
  27. Edelman J and Jefford TG (1968) The mechanism of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus. New Phytol 67: 517–531Google Scholar
  28. Ernst M, Chatterton NJ and Harrison PA (1996) Purification and characterisation of a new fructan series from species of Asteraceae. New Phytol 132: 63–66Google Scholar
  29. Escalada JA and Moss DN (1976) Changes in the non-structural carbohydrate fractions of developing spring wheat kernels. Crop Sci 16: 627–631Google Scholar
  30. Frehner M, Keller F and Wiemken A (1984) Localisation of fructan metabolism in vacuoles isolated from protoplasts of Jerusalem artichoke tubers. J Plant Physiol 116: 197–208Google Scholar
  31. Fuchs A (1993a) Production and utilisation of inulin. Part I. Utilisation of inulin. In: Suzuki M and Chatterton NJ (eds) Science and Technology of Fructans, pp 320–352. CRC Press, Boca RatonGoogle Scholar
  32. Fuchs A (ed) (1993b) Inulin and Inulin-Containing Crops. Elsevier, AmsterdamGoogle Scholar
  33. Han Y (1990) Microbial Levan. Adv Appl Microbiol 35:171–194PubMedGoogle Scholar
  34. Hendrix JE (1983) Phloem function: An integrated view. What’s New in Plant Physiology, Physiol Plant 14: 45–48Google Scholar
  35. Hendry GAF and Wallace RK (1993) The origin, distribution and evolutionary significance of fructans. In: Suzuki M and Chatterton NJ (eds). Science and Technology of Fructans, pp 119–139. CRC Press, Boca RatonGoogle Scholar
  36. Henson CA and Livingston DP (1996) Purification and characterization of an oat fructan exohydrolase that preferentially hydrolyzes beta-2,6-fructans. Plant Physiol 110: 639–644CrossRefPubMedGoogle Scholar
  37. Housley TL and Daughtry CST (1987) Fructan content and fructosyl transferase activity during wheat seed growth. Plant Physiol 83: 4–7Google Scholar
  38. Housley TL and Pollock CJ (1985) Photosynthesis and carbohydrate metabolism in detached leaves of Lolium temulentum L. New Phytol 99: 499–502Google Scholar
  39. Housley TL and Pollock CJ (1993) The metabolism of fructan in higher plants. In Suzuki M and Chatterton NJ (eds) Science and Technology of Fructan, pp 191–225. CRC Press, Boca RatonGoogle Scholar
  40. Huber SC, Bachmann M, McMichael RW and Huber JC (1995) Regulation of sucrose phosphate synthase by reversible protein phosphorylation: Manipulation of activation and inactivation in vivo. In: Pontis H, Salerno GL and Echeverria EJ (eds) Sucrose Metabolism, Biochemistry, Physiology and Molecular Biology, pp 6–13. AmericanSociety of Plant Physiologists, RockvilleGoogle Scholar
  41. Jang JC and Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6: 1665–1679CrossRefPubMedGoogle Scholar
  42. Jellings AJ and Leach RM (1982) The importance of quantitative anatomy in the interpretation of whole leaf biochemistry in species of triticum, hordeum and avena. New Phytol 92:39–48Google Scholar
  43. Kaeser W (1983) Ultrastructure of storage cells in Jerusalem artichoke tubers (Helianthus tuberosus L.). Vesicle formation during inulin synthesis. Zeit Pflanz 111: 253–260Google Scholar
  44. Koops AJ and Jonker HH (1996) Purification and characterisation of the enzymes of fructan biosynthesis in tubers of Helianthus tuberosus (Colombia). 2. Purification of sucrose-sucrose 1-fructosyl transferase and reconstitution of fructan synthesis in vitro with purified sucrose-sucrose 1-fructosyl transferase and fructan-fructan 1-fructosyl transferase. Plant Physiol 110: 1167–1175PubMedGoogle Scholar
  45. Koroleva OA, Farrar JF, Tomos, AD and Pollock CJ (1997) Patterns of solute in individual mesophyll, bundle sheath and epidermal cells of barley leaves induced to accumulate carbohydrate. New Phytol 136: 97–104CrossRefGoogle Scholar
  46. Kingston-Smith AH and Pollock CJ (1996) Tissue level localisation of acid invertase in leaves: An hypothesis for the regulation of carbon export. New Phytol 134: 423–432Google Scholar
  47. Kühbauch W and Thome U (1989) Nonstructural carbohydrates of wheat stems as influenced by source-sink manipulations. J Plant Physiol 134: 243–250Google Scholar
  48. Lewis DH (1993) Nomenclature and diagrammatic representation of oligomericfructans: A paperfor discussion. New Phytol 123: 583–594Google Scholar
  49. Lüscher M, Erdin C, Sprenger N, Hochstrasser U, Boller T and Wiemken A (1996) Inulin synthesis by a combination of purified fructosyl transferases from tubers of Helianthus tuberosus. FEBS Lett 385: 39–42PubMedGoogle Scholar
  50. MacLeod AM and McCorquodale H (1958) Water-soluble carbohydrates of seeds of the Gramineae. New Phytol 57: 168–182Google Scholar
  51. Marx SP, Nosberger J and Frehner M (1997) Hydrolysis of fructan in grasses: A beta-(2–6)-linkage specific fructan-beta-fructosidase from stubble of Lolium perenne. New Phytol 135: 279–290Google Scholar
  52. McCree KJ (1972) Test of current definitions of photosynthetically active radiation against leaf photosynthetic data. Agric Meteorol 10: 443–453CrossRefGoogle Scholar
  53. Milthorpe FL and Moorby J (1974) An Introduction to Crop Physiology. Cambridge University Press. CambridgeGoogle Scholar
  54. Natr L (1969) Influence of assimilate accumulation on rate of photosynthesis of barley leaf segments. Photosynthetica 3: 120–126Google Scholar
  55. Obenland DM, Simmen U, Boller T and Wienken A (1991) Regulation of sucrose-sucrose fructosyl transferase in barley leaves. Plant Physiol 97: 811–813Google Scholar
  56. Ozbun JL, Hawker JS, Greenberg E, Lammel C and Preiss J (1973) Starch synthetase, phosphorylase, ADP glucose pyrophosphorylase and UDP glucose pyrophosphorylase in developing maize kernels. Plant Physiol 51: 1–5Google Scholar
  57. Pearman I, Thomas SM and Thome GN (1978) Effects of nitrogen fertiliser on the distribution of photosynthate during grain growth of spring wheat. Ann Bot 42: 91–99Google Scholar
  58. Pilon-Smits EAH, Ebskamp MJM, Paul MJ, Jeuken MJW, Weisbeek PJ and Smeekens SCM (1995a) Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiol 107: 125–130PubMedGoogle Scholar
  59. Pilon-Smits EAH, Ebskamp MJ, Weisbeek PJ and Smeekens SCM (1995b) Frucan-accumulation in transgenic plants: Effect on growth, carbohydrate partitioning and stress resistance. In: Pontis HG, Salerno GO and Echeverria EJ (eds) Sucrose Metabolism, Biochemistry, Physiology and Molecular Biology, pp 88–99. American Society of Plant Physiologists, RockvilleGoogle Scholar
  60. Pilon-Smits EAH, Ebskamp MJM, Jeuken MJW, van der Meer IM, Visser RGF, Weisbeek PJ and Smeekens SCM (1996) Microbial fructan production in transgenic potato plants and tubers. Indust Crops Prod 5: 35–46Google Scholar
  61. Pollock CJ (1979) Pathway of fructan synthesis in leaf bases of Dactylis glomerata. Phytochemistry 18: 777–779CrossRefGoogle Scholar
  62. Pollock CJ (1982) Patterns of turnover of fructans in leaves of Dactylis glomerata L. New Phytol 90: 645–650Google Scholar
  63. Pollock CJ and Cairns AJ (1991) Fructan metabolism in grasses and cereals. Ann Rev Plant Physiol Plant Mol Biol 42:77–101Google Scholar
  64. Pollock CJ and Jones T (1979) Seasonal patterns of fructan metabolism in forage grasses. New Phytol 83: 8–15Google Scholar
  65. Pollock CJ and Kingston-Smith AH (1997) The vacuole and carbohydrate metabolism. In: Leigh RA and Sanders D (eds) Advances in Botanical Research 25, pp 195–215. Academic Press, LondonGoogle Scholar
  66. Pollock CJ, Hall MA and Roberts DP (1979) Structural analysis of fructose polymers by gas-liquid chromatography and gel filtration. J Chromatogr 171: 411–415Google Scholar
  67. Pollock CJ, Eagles CE and Sims IM (1988) Effect of photoperiod and irradiance changes upon development of freezing tolerance and accumulation of soluble carbohydrate in seedlings of Lolium perenne grown at 2 °C. Ann Bot 62: 95–100Google Scholar
  68. Pollock CJ, Cairns AJ, Gallagher JA, Winters AL and Farrar J (1995) Cold affects partitioning. Does partitioning affect photosynthesis? In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol IV, pp 783–788. Kluwer Academic Publishers, DordrechtGoogle Scholar
  69. Pollock CJ, Cairns AJ, Sims IM and Housley TL (1996) Fructans as Reserve Carbohydrates in Crop Plants. In: Zamski E and Shaffer AA (eds) Photoassimilate Distribution in Plants and Crops: Source-Sink Relationships, pp 97–113. Marcel Dekker Inc, New YorkGoogle Scholar
  70. Pontis H (1995) A discussion on the present model of fructan biosynthesis. In: Pontis H, Salerno GL and Echeverria EJ (eds) Sucrose Metabolism, Biochemistry, Physiology and Molecular Biology, pp 190–197. American Society of Plant Physiologists, RockvilleGoogle Scholar
  71. Röber M, Geider K, Muller-Röber B and Willmitzer L (1996) Synthesis of fructans in tubers of transgenic starch-deficient potato plants does not result in an increased allocation of carbohydrates. Planta 199: 528–536PubMedGoogle Scholar
  72. Sachs J (1864) Uber die Spharokrystalle des Inulins und den mikroskopische Nachweisung in den Zellen. Botanische Zeitung 22: 77–81; 85–89Google Scholar
  73. Schnyder H (1986) Carbohydrate metabolism in the growth zone of tall fescue leaf blades. In: Randall DD, Miles CD, Nelson CJ, Blevins DG and Miernyk JA (eds) Current Topics in Plant Biochemistry and Physiology, pp. 47–58. University of Missouri, ColumbiaGoogle Scholar
  74. 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: 233–245Google Scholar
  75. Schnyder H and Nelson CJ (1987) Growth rates and carbohydrate fluxes within the elongation zone of tall fescue leaf blades at high and low irradiance. Plant Physiol 85: 548–553Google Scholar
  76. Schnyder H and Nelson CJ (1989) Growth rates and assimilate partitioning in the elongation zone of tall fescue leaf blades at high and low irradiance. Plant Physiol 90: 1201–1206Google Scholar
  77. Schnyder H, Nelson CJ and Spollen WG (1988) Diurnal growth of tall fescue leaf blades. II. Dry matter partitioning and carbohydrate metabolism in the elongation zone and adjacent expanded tissue. Plant Physiol 86: 1077–1083Google Scholar
  78. Silk WK. (1984) Quantitative descriptions of development. Ann Rev Plant Physiol 35: 479–518Google Scholar
  79. Simmen U, Obenland D, Boller T and Wiemken A (1993) Fructan synthesis in excised barley leaves. Identification of two sucrose-sucrose fructosyl transferases induced by light and their separation from constitutive invertases. Plant Physiol 101: 459–468PubMedGoogle Scholar
  80. Simpson RJ and Bonnett GD (1993) Fructan exohydrolese from grasses. New Phytol 123: 453–469Google Scholar
  81. Simpson RJ, Walker RP and Pollock CJ (1991) Fructan exohydrolase in leaves of Lolium temulentum L. New Phytol 119: 499–507Google Scholar
  82. Sims IM, Pollock CJ and Horgan R (1992) Structural analysis of oligomeric fructans from excised leaves of Lolium temulentum. Phytochemistry 31: 2989–2992CrossRefGoogle Scholar
  83. Sims IM, Horgan R and Pollock CJ (1993) The kinetic analysis of fructan biosynthesis in excised leaves of Lolium temulentum L. New Phytol 123: 25–29Google Scholar
  84. Slaughter LH and Livingston DP (1994) Separation of fructan isomers by high-performance anion-exchange chromatography. Carbohydr Res 253: 287–291CrossRefGoogle Scholar
  85. Sprenger N, Bortlik K, Brandt A, Boller T and Wiemken A (1995) Purification, cloning and functional expression of sucrose-fructan 6-transferase, a key enzyme of fructan synthesis in barley. Proc Nat Acad Sci USA 92: 11652–11656PubMedGoogle Scholar
  86. Stitt M (1996) Metabolic regulation of photosynthesis. In: Baker NR (ed) Photosynthesis and the Environment, pp 151–190. Kluwer Academic Publishers, DordrechtGoogle Scholar
  87. St John JA, Bonnett GD, Simpson RJ and Tanner GJ (1997a) A fructan: fructan fructosyl transferase activity from Lolium rigidum. New Phytol 135: 235–247Google Scholar
  88. St John JA, Sims IM, Bonnett GD and Simpson RJ (1997b) The identification of products formed by a fructan: fructan fructosyl transferase activity from Lolium rigidum. New Phytol 135: 249–257Google Scholar
  89. Tomos AD, Leigh RA, Palta JA and Williams JHH (1992) Sucrose and cell water relations. In: Pollock CJ, Farrar, JF and Gordon AJ (eds) Carbon Partitioning Within and Between Organisms, pp 71–89. Bios, OxfordGoogle Scholar
  90. van den Ende W and van Laere, A (1996) De novo synthesis of fructans from sucrose in vitro by a combination of 2 purified enzymes (sucrose-sucrose 1-fructosyl transferase and fructan-fructan 1-frucosyl transferase from chicory roots (Cichorium intybus) L. Planta 200: 335–342CrossRefGoogle Scholar
  91. van der Meer IM, Ebskamp MJM, Visser RGF, Weisbeek PJ and Smeekens SCM (1994) Fructan as a new carbohydrate sink in transgenic potato plants. Plant Cell 6: 561–570Google Scholar
  92. Wagner W and Wiemken A (1986) Properties and subcellular localisation of fructan hydrolase in the leaves of barley (Hordeum vulgare L. cv. Gerbel). J Plant Physiol 123: 429–439Google Scholar
  93. Wagner W and Wiemken A(1987) Enzymology of fructan synthesis in grasses. Properties of sucrose-sucrose fructosyl transferase in barley leaves (Hordeum vulgare L. cv. Gerbel). J Plant Physiol 85: 706–710Google Scholar
  94. Wagner W, Keller F and Wiemken A (1983) Fructan metabolism in cereals: Induction inleaves and compartmentation in protoplasts and vacuoles. Zeit Pflanz 112: 359–372Google Scholar
  95. Wagner W, Wiemken A and Matile PH (1986) Regulation of fructan metabolism in leaves of barley (Hordeum vulgare L. cv. Gerbel). J Plant Physiol 81: 444–447Google Scholar
  96. Wiemken A, Sprenger N and Boller T (1995) Fructan—an extension of sucrose by sucrose. In: Pontis HG, Salerno GL and Echeverria E.J (eds) Sucrose Metabolism, Biochemistry, Physiology and Molecular Biology, pp 179–189. American Society of Plant Physiologists, RockvilleGoogle Scholar
  97. Williams ML, Farrar JF and Pollock CJ (1989) Cell specialisation within the parenchymatous bundle sheath of barley. Plant Cell Env 12: 909–918Google Scholar
  98. Winter H, Robinson DG and Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191: 180–190CrossRefGoogle Scholar
  99. Winters AL, Williams JHH, Thomas DS and Pollock CJ (1994) Changes in gene expression in response to sucrose accumulation in leaf tissue of Lolium temulentum L. New Phytol 128: 591–600Google Scholar
  100. Winters AL, Gallagher JA, Pollock CJ and Farrar JF (1995) Isolation of a gene expressed during sucrose accumulation in leaves of Lolium temulentum L. J Exp Bot 46: 1345–1350Google Scholar
  101. Yamamoto S and Mino Y (1989) Mechanism of phleinase induction in the stem base of orchard grass after defoliation. J Plant Physiol 134: 258–260Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • A. J. Cairns
    • 1
  • C. J. Pollock
    • 1
  • J. A. Gallagher
    • 1
  • J. Harrison
    • 1
  1. 1.Environmental Biology DepartmentInstitute of Grassland and Environmental ResearchAberystwythWales, UK

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