The breakdown of starch in leaves

New Phytologist

Volumn 163, Issue 2, 2004, Pages 247-261

  Zeeman, Samuel C ^a   Smith, Steven M ^b   Smith, Alison M ^c  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c JOHN INNES CENTRE   (United Kingdom)

Author keywords

glucan phosphorylase; Amylase; Arabidopsis; Glucan; Glucanotransferase; Starch; Water dikinase

Indexed keywords

STARCH;

ARABIDOPSIS; SOLANUM TUBEROSUM;

EID: 3542995724     PISSN: 0028646X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2004.01101.x     Document Type: Review

References (134)

1. Ball S, Morell MK. 2003. From bacterial glycogen to starch: understanding the biogenesis of the starch granule. Annual Review of Plant Biology 54: 207-233.
2. Beck E. 1985. The degradation of transitory starch granules in chloroplasts. In: Heath RL, Preiss J, eds. Regulation of carbon partitioning in photosynthetic tissue. Baltimore, MD, USA: Waverly Press, 27-44.
3. Beck E, Ziegler P. 1989. Biosynthesis and degradation of statch in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 40: 95-117.
4. Beers EP, Duke SH, Henson CA. 1990. Partial characterization and subcellular localization of three α-glucosidase isoforms in pea (Pisum sativum L.) seedlings. Plant Physiology 94: 738-744.
5. Blennow A, Bay-Smidt AM, Olsen CE, Møller BL. 2000. The distribution of covalently bound phosphate in the starch granule in relation to starch crystallinity. International Journal of Biology Macromolecules 27: 211-218.
6. Boos W, Shuman H. 1998. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiology and Molecular Biology Reviews 62: 204-229.
7. Buléon A, Colonna P, Planchot V, Ball S. 1998. Starch granules: structure and biosynthesis. International Journal of Biology Macromolecules 23: 85-112.
8. Burton RA, Jenner H, Carrangis L, Fahy B, Fincher GB, Hylton C, Laurie DA, Parker M, Waite D, van Wegen S, Verhoeven T, Denyer K. 2002. Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. Plant Journal 31: 97-112.
9. Caspar T, Huber SC, Somerville C. 1985. Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomurase activity. Plant Physiology 79: 11-17.
10. Caspar T, Lin TP, Monroe J, Bernhard W, Spilatro S, Preiss J, Somerville C. 1989. Altered regulation of beta-amylase activity in mutants of Arabidopsis with lesions in starch metabolism. Proceedings of the National Academy of Sciences, USA 86: 5830-5833.
11. Caspar T, Lin T-P, Kakefuda G, Benbow L, Preiss J, Somerville C. 1991. Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiology 95: 1181-1188.
12. Chapman GW Jr, Pallas JE Jr, Mendicino J. 1972. The hydrolysis of maltodextrins by a β-amylase isolated from leaves of Vicia faba. Biochimica et Biophysica Acta 276: 491-507.
13. Chatterton NJ, Silvius JE. 1981. Photosynthate partitioning into starch in soybean leaves. II. Irradiance level and daily Photosynthetic period duration effects. Plant Physiology 67: 257-260.
14. Chia T, Thorneycroft D, Chapple A, Messerli G, Chen J, Zeeman SC, Smith SM, Smith AM. 2004. A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant Journal 37: 853-863.
15. Corbesier L, Lejeune P, Bernier G. 1998. The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: comparison between the wild type and a starchless mutant. Planta 206: 131-137.
16. Critchley JH, Zeeman SC, Takaha T, Smith AM, Smith SM. 2001. A critical role for disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant Journal 26: 89-100.
17. Dauvillée D, Colleoni C, Mouille G, Morell MK, d'Hulst C, Wattebled F, Liénard L, Devallé D, Ral J-P, Myers AM, Ball SG. 2001. Biochemical characterisation of wild type and mutant isoamylases of Chlamydomonas reinhardtii supports a function of the multimeric enzyme organisation in amylopectin maturation. Plant Physiology 125: 1723-1731.
18. Dinges JR, Colleoni C, James MG, Myers AM. 2003. Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism. Plant Cell 15: 666-680.
19. Doehlert DC, Duke SH. 1983. Specific determination of α-amylase activity in crude plant extracts containing β-amylase. Plant Physiology 71: 229-234.
20. Doehlert DC, Knutson CA. 1991. Two classes of starch debranching enzymes from developing maize kernels. Journal of Plant Physiology 138: 566-572.
21. Ehrmann MA, Vogel RF. 1998. Maltose metabolism of Lactobacillus sanfranciscensis: cloning and heterologous expression of the key enzymes maltose phosphorylase and phosphoglucomutase. FEMS Microbiology Letters 169: 81-86.
22. Eimert K, Wang S-M, Lue W-L, Chen JC. 1995. Monogenic recessive mutations causing both late floral initiation and excess starch accumulation in Arabidopsis. Plant Cell 7: 1703-1712.
23. Fincher GB. 1989. Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annual Review of Plant Physiology and Plant Molecular Biology 40: 305-346.
24. Flügge U-I, Heldt HW. 1991. Metabolite transporters of the chlotoplast envelope. Annual Review of Plant Physiology and Plant Molecular Biology 42: 129-144.
25. Fondy BR, Geiger DR. 1982. Diurnal pattern of translocation and carbohydrate metabolism in source leaves of Beta vulgaris L. Plant Physiology 70: 671-676.
26. Fondy BR, Geiger DR, Servaites JC. 1989. Photosynthesis, carbohydrate metabolism and export in Beta vulgaris L. and Phaseolus vulgaris L. during square and sinusoidal light regimes. Plant Physiology 89: 396-402.
27. Frandsen TP, Svensson B. 1998. Plant α-glucosidases of the glycoside hydrolase family 31. Molecular properties, substrate specificity, reaction mechanism, and comparison with family members of different origin. Plant Molecular Biology 37: 1-13.
28. Fredeen AL, Raab TK, Rao IM, Terry N. 1989. Effects of phosphorus nutrition on photosynthesis in Glycine max (L.) Merr. Planta 181: 399-405.
29. Gordon AJ, Ryle GJA, Webb G. 1980. The relationship between sucrose and starch during 'dark' export from leaves of uniculm barley. Journal of Experimental Botany 31: 845-850.
30. Grange RI. 1985. Carbon partitioning in mature leaves of pepper: effects of daylength. Journal of Experimental Botany 36: 1749-1759.
31. Harmer SL, Hogenesch JB, Straume M, Chang H-S, Han B, Zhu T, Wang X, Kreps JA, Kay SA. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290: 2110-2113.
32. Häusler RE, Schlichen NH, Schulz B, Flügge U-I. 1998. Compensation of decreased triose phosphate/phosphate translocator activity by accelerated starch turnover and glucose transport in transgenic tobacco. Planta 204: 366-376.
33. Heineke D, Kruse A, Flügge U-I, Frommer WB, Riesmeier JW, Willmitzer L, Heldt HW. 1994. Effect of antisense repression of the chloroplast triose-phosphate translocator on photosynthetic metabolism in transgenic potato plants. Planta 193: 174-180.
34. Herold A, Leegood RC, McNeil PH, Robinson SP. 1981. Accumulation of maltose during photosynthesis in protoplasts isolated from spinach leaves treated with mannose. Plant Physiology 67: 85-88.
35. Hildebrand DF, Hymowitz T. 1981. Role of β-amylase in starch metabolism during soybean seed development and germination. Physiolagia Plantarum 53: 429-434.
36. Huber SC, Hanson KR. 1992. Carbon partitioning and growth of a starchless mutant of Nicotiana sylvestris. Plant Physiology 99: 1449-1454.
37. Hussain H, Mant A, Seale R, Zeeman SC, Hinchliffe E, Edwards A, Hylton C, Bornemann S, Smith AM, Martin C, Bustos R. 2003. Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans. Plant Cell 15: 133-149.
38. Ishizaki Y, Taniguchi H, Maruyama Y, Nakamura M. 1983. Debranching enzymes of potato tubers (Solanum tuberosum L). II. Purification of a pullulanase (R-enzyme) from potato tubers and comparison of its properties with those of the potato isoamylase. Journal of the Japanese Society of Starch Science 30: 19-29.
39. James MG, Robertson DS, Myers AM. 1995. Characterisation of the maize gene sugaryI, a determinant of starch composition in kernels. Plant Cell 7: 417-429.
40. Kakefuda G, Duke SH. 1989. Characterisation of pea chloroplast D-enzyme (4-α-D-glucanotransferase). Plant Physiology 91: 136-143.
41. Kakefuda G, Duke SH, Hostak MS. 1986. Chloroplast and extrachloroplastic starch-degrading enzymes in Pisum sativum L. Planta 168: 175-182.
42. Kakefuda G, Preiss J. 1997. Partial purification and characterization of a diurnally fluctuating novel endoamylase from Arabidopsis thaliana leaves. Plant Physiology and Biochemistry 35: 907-913.
43. Kerr PS, Rufty TW, Huber SC. 1985. Endogenous rhythms in photosynthesis, sucrose-phosphate synthase activity and stomatal resistance in leaves of soybean (Glycine max [L.] Merr). Plant Physiology 77: 275-280.
44. Kruger NJ, ap Rees T. 1983a. Properties of α-glucan phosphorylase from pea. Phytochemistry 22: 1891-1898.
45. Kruger NJ, ap Rees T. 1983b. Maltose metabolism by pea chloroplasts. Planta 158: 179-184.
46. Kruger NJ, Bulpin PV, ap Rees T. 1983. The extent of starch degradation in the light in pea leaves. Planta 157: 271-273.
47. Laby RJ, Kim D, Gibson SI. 2001. The ram1 mutant of Arabidopsis exhibits severely decreased β-amylase activity. Plant Physiology 127: 1798-1807.
48. Lao NT, Schoneveld O, Mould RM, Hibberd JM, Gray JC, Kavanagh TA. 1999. An Arabidopsis gene encoding a chloroplast-targeted beta-amylase. Plant Journal 20: 519-527.
49. Levi C, Gibbs M. 1976. Starch degradation in isolated chloroplasts. Plant Physiology 57: 933-935.
50. Levi C, Preiss J. 1978. Amylopectin degradation in pea chloroplast extracts. Plant Physiology 61: 218-220.
51. Li B, Servaites JC, Geiger DR. 1992a. Characterization and subcellular localization of debranching enzyme and endoamylase from the leaves of sugar beet. Plant Physiology 98: 1277-1284.
52. Li B, Geiger DR, Shieh W-J. 1992b. Evidence for circadian regulation of starch and sucrose synthesis in sugar beet leaves. Plant Physiology 99: 1393-1399.
53. Lim ST, Kasemsuwan T, Jane JL. 1994. Characterization of phosphorus in starch by P-31 nuclear magnetic resonance spectroscopy. Cereal Chemistry 71: 488-493.
54. Lin T-P, Caspar T, Somerville CR, Preiss J. 1988b. A starch deficient mutant of Arabidopsis thaliana with low ADPglucose pytophosphorylase activity lacks one of the two subunits of the enzyme. Plant Physiology 88: 1175-1181.
55. Lin T, Preiss J. 1988. Characterisation of D-enzyme (4-α-D- glucanotransferase) in Arabidopsis leaf. Plant Physiology 86: 260-265.
56. Lin T-P, Spilatro SR, Preiss J. 1988a. Subcellular localization and characterization of amylases in Arabidopsis leaf. Plant Physiology 86: 251-259.
57. Lorberth R, Ritte G, Willmitzer L, Kossmann J. 1998. Inhibition of a starch-granule-bound protein leads to modified starch and repression of cold sweetening. Nature Biotechnology 16: 473-477.
58. Lu Y, Sharkey TD. 2004. The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218: 466-473.
59. Ludwig I, Ziegler P, Beck E. 1984. Purification and properties of spinach leaf debranching enzyme. Plant Physiology 74: 856-861.
60. Maeda I, Kiribuchi S, Nakamura M. 1978. Digestion of barley starch granules by the combined action of α- and β-amylases purified from barley and barley malt. Agricultural and Biological Chemistry 42: 259-267.
61. 2 assimilation and carbon partitioning. Journal of Experimental Botany 48: 1865-1872.
62. Matheson NK. 1996. The chemical structure of amylose and amylopectin fractions of starch from tobacco leaves during development and diurnally-nocturnally. Carbohydrate Research 282: 247-262.
63. Monroe JD, Preiss J. 1990. Purification of a β-amylase that accumulates in Arabidopsis thaliana mutants defective in starch metabolism. Plant Physiology 94: 1033-1039.
64. Moore B, Zhou L, Rolland F, Hall Q, Cheng W-H, Liu Y-X, Hwang I, Jones T, Sheen J. 2003. Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signalling. Science 300: 332-336.
65. Mouille G, Maddelein M-L, Libessart N, Talaga P, Decq A, Delrue B, Ball SG. 1996. Preamylopectin processing: a mandatory step for starch biosynthesis in plants. Plant Cell 8: 1353-1366.
66. Myers AM, Morell MK, James MG, Ball SG. 2000. Recent progress towards understanding the biogenesis of the amylopectin crystal. Plant Physiology 122: 989-997.
67. Nakamura Y, Kubo A, Shimamune T, Matsuda T, Harada K, Satoh H. 1997. Correlation between activities of starch debranching enzyme and α-polyglucan structure in endosperms of sugary-1 mutants of rice. Plant Journal 12: 143-153.
68. 3 or CAM (Crassulacean acid metabolism)-induced Mesembryanthemum crystallinum L. Biochemical Journal 318: 945-953.
69. Newgard CB, Hwang PK, Fletterick RJ. 1989. The family of glycogen phosphorylases: structure and function. Critical Reviews in Biochemistry and Molecular Biology 24: 69-99.
70. Nielsen TH, Wischmann B, Enevoldsen K, Møller BL. 1994. Starch phosphorylation in potato tubers proceeds concurrently with de novo biosynthesis of starch. Plant Physiology 105: 111-117.
71. Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC. 2004. A previously unknown maltose transporter essential for starch degradation in leaves. Science 303: 87-89.
72. Okita TW, Greenberg E, Kuhn DN, Preiss J. 1979. Subcellular localization of the starch degradative and biosynthetic enzymes of spinach leaves. Plant Physiology 64: 187-192.
73. Okita TW, Preiss J. 1980. Starch degradation in spinach leaves. Plant Physiology 66: 870-976.
74. Olsson T, Thelander M, Ronne H. 2003. A novel type of chloroplast stromal hexokinase is the major phosphorylating enzyme in the moss Physcomitrella patens. Journal of Biological Chemistry 278: 44439-44447.
75. Paul MJ, Stitt M. 1993. Effects of nitrogen and phosphorus deficiencies on levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their responses to exogenous sucrose. Plant, Cell & Environment 16: 1047-1057.
76. Preiss J. 1982. Regulation of the biosynthesis and degradation of starch. Annual Review of Plant Physiology 33: 431-454.
77. Qui J, Israel DW. 1992. Diurnal starch accumulation and utilisation in phosphorus-deficient soybean plants. Plant Physiology 98: 316-232.
78. Quick WP, Scheibe R, Neuhaus HE. 1995. Induction of hexose-phosphate translocator activity in spinach chloroplasts. Plant Physiology 109: 113-121.
79. Riesmeier JW, Flügge U-I, Schulz B, Heineke D, Heldt HW, Willmitzer L, Frommer WB. 1993. Antisense repression of the chloroplast triose phosphate translocator affects carbon partitioning in transgenic potato plants. Proceedings of the National Academy of Science of the USA 90: 6160-6164.
80. Ritte G, Lorberth R, Steup M. 2000a. Reversible binding of the starch-related R1 protein to the surface of transitory starch granules. Plant Journal 21: 387-391.
81. Ritte G, Eckermann N, Haebel S, Lorberth R, Steup M. 2000b. Compartmentation of the starch-related R1 protein in higher plants. Starch-Stärke 52: 145-149.
82. Ritte G, Lloyd JR, Eckermann N, Rottmann A, Kossmann J, Steup M, 2002. The starch-related R1 protein is an alpha-glucan, water dikinase. Proceedings of the National Academy of Sciences, USA 99: 7166-7171.
83. Robertson JG, Lytleton P, Williamson KI, Batt RD. 1975. The effect of fixation procedures on the electron density of polysacchande granules in Nordica corallina. Journal of Ultrastructural Research 52: 321-332.
84. Rolland F, Moore B, Sheen J. 2002. Sugar sensing and signaling in plants. Plant Cell Supplement 2002: S185-S205.
85. Rost S, Frank C, Beck E. 1996. The chloroplast envelope is permeable for maltose but not for maltodextrins. Biochimica et Biophysica Acta 1291: 221-227.
86. Schächtele C, Steup M. 1986. Alpha-1,4-glucan phosphorylase forms from leaves of spinach (Spinacia oleracea L.). 1. In situ localization by indirect immunofluorescence. Planta 167: 444-451.
87. Schäfer G, Heber U, Heldt HW. 1977. Glucose transport into spinach chloroplasts. Plant Physiology 60: 286-289.
88. Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E. 2001. Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13: 113-123.
89. Scheidig A, Frohlich A, Schulze S, Lloyd JR, Kossmann J. 2002. Down regulation of a chloroplast-targeted beta-amylase leads to a starch-excess phenotype in leaves. Plant Journal 10: 581-591.
90. Schleucher J, Vanderveer PJ, Sharkey TD. 1998. Export of carbon from chloroplasts at night. Plant Physiology 118: 1439-1445.
91. Schneider A, Häusler RE, Kolukisaoglu Ü, Kunze R, van der Graaff E, Schwacke R, Catoni E, Desimone M, Flügge U-I. 2002. An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant Journal 32: 685-699.
92. Schulze W, Stitt M, Schulze ED, Neuhause HE, Fichtner K. 1991. A quantification of the significance of assimilatory starch for growth of Arabidopsis thaliana L. Heynh. Plant Physiology 95: 890-895.
93. Scott P, Kruger NJ. 1994. Fructose 2,6-bisphosphate levels in mature leaves of tobacco (Nicotiana tabacum) and potato (Solanum tuberosum). Planta 193: 16-20.
94. Servaites JC, Geiger DR, Tucci MA, Fondy BR. 1989a. Leaf carbon metabolism and metabolite levels during a period of sinusoidal light. Plant Physiology 89: 403-408.
95. Servaites JC, Fondy BR, Geiger DR. 1989b. Sources of carbon for export from spinach leaves throughout the day. Plant Physiology 90: 1168-1174.
96. Servaites JC, Geiger DR. 2002. Kinetic characteristics of chloroplast glucose transport. Journal of Experimental Botany 53: 1581-1591.
97. Sharkey TD, Savitch LV, Vanderveer PJ, Micallef BJ. 1992. Carbon partitioning in a Flaveria linearis mutant with reduced cytosolic fructose bisphosphatase. Plant Physiology 100: 210-215.
98. Shimomura S, Nagai M, Fukui T. 1982. Comparative glucan specificities of two types of spinach leaf phosphorylase. Journal of Biochemistry 91: 703-717.
99. Sonnewald U, Basner A, Greve B, Steup M. 1995. A second 1-type isozyme of potato glucan phosphorylase: cloning, antisense inhibition and expression analysis. Plant Molecular Biology 27: 567-576.
100. Stanley D, Fitzgerald AM, Farnden KJF, McRae EA. 2002. Characterization of putative amylases from apple (Malus domestica) and Arabidopsis thaliana. Biologia 57: 137-148.
101. Steup M. 1988. Starch degradation. In: Preiss J, ed. Biochemistry of plants, Vol. 14. Carbohydrates. New York, NY, USA: Academic Press, 255-296.
102. Steup M, Robenek H, Melkonian M. 1983. In-vitro degradation of starch granules isolated from spinach chloroplasts. Planta 158: 428-436.
103. Steup M, Schächtele C. 1981. Mode of glucan degradation by purified phosphorylase forms from spinach leaves. Planta 153: 351-361.
104. Stitt M, ap Rees T. 1980. Carbohydrate breakdown by chloroplasts of Pisum sativum. Biochimica et Biophysica Acta 627: 131-143.
105. Stitt M, Bulpin PV, ap Rees T. 1978. Pathways of starch breakdown in photosynthetic tissues of Pisum sativum. Biochimica et Biophysica Acta 544: 200-214.
106. Stitt M, Heldt HW. 1981. Physiological rates of starch breakdown in isolated intact spinach chloroplasts. Plant Physiology 68: 755-761.
107. Stitt M, Quick P. 1989. Photosynthetic carbon partitioning: its regulation and possibilities for manipulation. Physiologia Plantarum 77: 663-641.
108. Strand A, Hurry V, Gustafsson P, Gardestrom P. 1997. Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant Journal 12: 605-614.
109. Sun Z, Duke SH, Henson CA. 1995. The role of pea chloroplast α-glucosidase in transitory starch degradation. Plant Physiology 108: 211-217.
110. Sun Z, Henson CA. 1990. Degradation of native starch granules by barley α-glucosidases. Plant Physiology 94: 320-327.
111. Takaha T, Yanase M, Okada S, Smith SM. 1993. Disproportionating enzyme (4-alpha-glucanotransferase - EC 2.4.1.25) of potato - purification, molecular-cloning, and potential role in starch metabolism. Journal of Biological Chemistry 268: 1391-1396.
112. Trethewey RN, ap Rees T. 1994a. A mutant of Arabidopsis thaliana lacking the ability to transport glucose across the chloroplast envelope. Biochemical Journal 301: 449-454.
113. Trethewey RN, ap Rees T. 1994b. The role of the hexose transporter in the chloroplasts of Arabidopsis thaliana L. Planta 195: 168-174.
114. Trethewey RN, Smith AM. 2000. Starch metabolism in leaves. In: Leegood RC, Sharkey TD, von Caemmeter S, eds. Advances in photosynthesis, Vol. 9. Photosynthesis: physiology and metabolism. Dordrecht, The Netherlands: Kluwer Academic Publishers, 205-231.
115. Trevanion SJ. 2002. Regulation of sucrose and starch synthesis in wheat (Triticum aestivum L.) leaves: role of fructose 2,6-bisphosphate. Planta 215: 653-665.
116. Waigh TA, Kato KL, Donald AM, Gidley MJ, Clarke CJ, Riekel C. 2000. Side-chain liquid-crystalline model for starch. Starch-Stärke 52: 450-460.
117. Wang Q, Monroe J, Sjölund RD. 1995. Identification and characterisation of a phloem-specific β-amylase. Plant Physiology 109: 743-750.
118. Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Gröner F, Hebbeker U, Flügge U-I. 2000. Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12: 787-801.
119. Wiese A, Groner F, Sonnewald U, Deppner H, Lerchl J, Hebbeker U, Flügge U-I, Weber A. 1999. Spinach hexokinase I is located in the outer envelope membrane of plastids. FEBS Letters 461: 13-18.
120. Weise SE, Weber APM, Sharkey TD. 2004. Maltose is the major form of carbon exported from the chloroplast at night. Planta 218: 474-482.
121. Witt W, Sauter JJ. 1994. Enzymes of starch metabolism in poplar wood during fall and winter. Journal of Plant Physiology 143: 625-631.
122. Yang Y, Steup M. 1990. Polysaccharide fraction from higher-plants which strongly interacts with the cytosolic phosphorylase isozyme. I. Isolation and characterization. Plant Physiology 94: 960-969.
123. Yu T-S, Kofler H, Häusler RE, Hille D, Flügge U-I, Zeeman SC, Smith AM, Kossmann J, Lloyd J, Ritte G, Steup M, Lue W-L, Chen J, Weber A. 2001. SEX1 is a general regulator of starch degradation in plants and not the chloroplast hexose transporter. Plant Cell 13: 1907-1918.
124. Zeeman SC, ap Rees T. 1999. Changes in carbohydrate metabolism and assimilate partitioning in starch-excess mutants of Arabidopsis. Plant, Cell & Environment 22: 1445-1453.
125. Zeeman SC, Umemoto T, Lue W-L, Au-Yeung P, Martin C, Smith AM, Chen J. 1998a. A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10: 1699-1711.
126. Zeeman SC, Northrop F, Smith AM, ap Rees T. 1998b. A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant Journal 15: 357-365.
127. Zeeman SC, Smith SM, Smith AM. 2002a. The priming of amylose synthesis in Arabidopsis leaves. Plant Physiology 128: 1069-1076.
128. Zeeman SC, Pilling E, Tiessen A, Kato L, Donald AM, Smith AM. 2002b. Starch synthesis in Arabidopsis; granule synthesis, composition and structure. Plant Physiology 129: 516-529.
129. Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Week M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM. 2004. The role of plastidial α-glucan phosphorylase in starch degradation and tolerance of abiotic stress in Arabidopsis leaves. Plant Physiology (In press).
130. Zhu ZP, Hylton CM, Rossner U, Smith AM. 1998. Characterization of starch-debranching enzymes in pea embryos. Plant Physiology 118: 581-590.
131. Ziegler P. 1988. Partial purification and characterization of the major endoamylase of mature pea leaves. Plant Physiology 86: 659-666.
132. Ziegler P. 1999. Cereal beta-amylases. Journal of Cereal Science 29: 195-204.
133. Ziegler P, Beck E. 1986. Exoamylase activity in vacuoles isolated from pea and wheat leaf protoplasts. Plant Physiology 82: 1119-1121.
134. Zrenner R, Krause KP, Apel P, Sonnewald U. 1996. Reduction of the cytosolic fructose-1,6-bisphosphatase in transgenic potato plants limits photosynthetic sucrose biosynthesis with no impact on plant growth and tuber yield. Plant Journal 9: 671-681.