Feedback inhibition of starch degradation in Arabidopsis leaves mediated by trehalose 6-phosphate

Plant Physiology

Volumn 163, Issue 3, 2013, Pages 1142-1163

  Martins, Marina Camara Mattos ^a   Hejazi, Mahdi ^b,c   Fettke, Joerg ^b   Steup, Martin ^b   Feil, Regina ^a   Krause, Ursula ^a   Arrivault, Stéphanie ^a   Vosloh, Daniel ^a,d   Figueroa, Carlos María ^a   Ivakov, Alexander ^a   Yadav, Umesh Prasad ^a,e   Piques, Maria ^a   Metzner, Daniela ^a   Stitt, Mark ^a   Lunn, John Edward ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b UNIVERSITY OF POTSDAM   (Germany)

^c BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^d STELLENBOSCH UNIVERSITY   (South Africa)

^e UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ALCOHOL; ARABIDOPSIS PROTEIN; DRUG DERIVATIVE; GLUCOSYLTRANSFERASE; MALTOSE; MALTOTRIOSE; PHOSPHATE; STARCH; SUGAR PHOSPHATE; TREHALOSE; TREHALOSE 6 PHOSPHATE; TREHALOSE 6 PHOSPHATE SYNTHETASE; TREHALOSE-6-PHOSPHATE; TREHALOSE-6-PHOSPHATE SYNTHASE; TRISACCHARIDE;

ARABIDOPSIS; ARTICLE; CELL GRANULE; CHLOROPLAST; CYTOSOL; DRUG EFFECT; FEEDBACK SYSTEM; GENETICS; HYDROLYSIS; IMMUNOBLOTTING; METABOLISM; PHYSIOLOGY; PLANT LEAF; SCANNING ELECTRON MICROSCOPY; TIME; TRANSGENIC PLANT; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPLASTS; CYTOPLASMIC GRANULES; CYTOSOL; ETHANOL; FEEDBACK, PHYSIOLOGICAL; GLUCOSYLTRANSFERASES; HYDROLYSIS; IMMUNOBLOTTING; MALTOSE; MICROSCOPY, ELECTRON, SCANNING; PHOSPHATES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; STARCH; SUGAR PHOSPHATES; TIME FACTORS; TREHALOSE; TRISACCHARIDES;

EID: 84886783847     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.226787     Document Type: Article

References (107)

1. Andriotis VME, Pike MJ, Schwarz SL, Rawsthorne S, Wang TL, Smith AM (2012) Altered starch turnover in the maternal plant has major effects on Arabidopsis fruit growth and seed composition. Plant Physiol 160: 1175-1186
2. Arrivault S, Guenther M, Ivakov A, Feil R, Vosloh D, van Dongen JT, Sulpice R, Stitt M (2009) Use of reverse-phase liquid chromatography, linked to tandem mass spectrometry, to profile the Calvin cycle and other metabolic intermediates in Arabidopsis rosettes at different carbon dioxide concentrations. Plant J 59: 826-839
3. Ballicora MA, Frueauf JB, Fu Y, Schürmann P, Preiss J (2000) Activation of the potato tuber ADP-glucose pyrophosphorylase by thioredoxin. J Biol Chem 275: 1315-1320
4. Baunsgaard L, Lütken H, Mikkelsen R, Glaring MA, Pham TT, Blennow A (2005) A novel isoform of glucan, water dikinase phosphorylates prephosphorylated α-glucans and is involved in starch degradation in Arabidopsis. Plant J 41: 595-605
5. Blázquez MA, Santos E, Flores CL, Martínez-Zapater JM, Salinas J, Gancedo C (1998) Isolation and molecular characterization of the Arabidopsis TPS1 gene, encoding trehalose-6-phosphate synthase. Plant J 13: 685-689
6. Blennow A, Engelsen SB (2010) Helix-breaking news: fighting crystalline starch energy deposits in the cell. Trends Plant Sci 15: 236-240
7. Blennow A, Nielsen TH, Baunsgaard L, Mikkelsen R, Engelsen SB (2002) Starch phosphorylation: a new front line in starch research. Trends Plant Sci 7: 445-450
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
9. Caddick MX, Greenland AJ, Jepson I, Krause KP, Qu N, Riddell KV, Salter MG, Schuch W, Sonnewald U, Tomsett AB (1998) An ethanol inducible gene switch for plants used to manipulate carbon metabolism. Nat Biotechnol 16: 177-180
10. Carillo P, Feil R, Gibon Y, Satoh-Nagasawa N, Jackson D, Bläsing OE, Stitt M, Lunn JE (2013) A fluorometric assay for trehalose in the picomole range. Plant Methods 9: 21-35
11. Chatterton NJ, Silvius JE (1980) Photosynthate partitioning into leaf starch as affected by daily photosynthetic period duration in six species. Physiol Plant 49: 141-144
12. Cheng SH, Moore B, Seemann JR (1998) Effects of short-and long-term elevated CO2 on the expression of ribulose-1,5-bisphosphate carboxylase/ oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L.) Heynh. Plant Physiol 116: 715-723
13. 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 J 37: 853-863
14. Cho MH, Lim H, Shin DH, Jeon JS, Bhoo SH, Park YI, Hahn TR (2011) Role of the plastidic glucose translocator in the export of starch degradation products from the chloroplasts in Arabidopsis thaliana. New Phytol 190: 101-112
15. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
16. Comparot-Moss S, Kötting O, Stettler M, Edner C, Graf A, Weise SE, Streb S, Lue W-L, MacLean D, Mahlow S, et al (2010) A putative phosphatase, LSF1, is required for normal starch turnover in Arabidopsis leaves. Plant Physiol 152: 685-697
17. 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 J 26: 89-100
18. Cseke C, Balogh A, Wong JH, Buchanan BB, Stitt M, Herzog B, Heldt HW (1994) Fructose 2,6-bisphosphate: a regulator of carbon processing in leaves. Trends Biochem Sci 9: 533-535
19. Debast S, Nunes-Nesi A, Hajirezaei MR, Hofmann J, Sonnewald U, Fernie AR, Börnke F (2011) Altering trehalose-6-phosphate content in transgenic potato tubers affects tuber growth and alters responsiveness to hormones during sprouting. Plant Physiol 156: 1754-1771
20. de Dios Barajas-López J, Tezycka J, Travaglia CN, Serrato AJ, Chueca A, Thormählen I, Geigenberger P, Sahrawy M (2012) Expression of the chloroplast thioredoxins f and m is linked to short-term changes in the sugar and thiol status in leaves of Pisum sativum. J Exp Bot 63: 4887-4900
21. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AA (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309: 630-633
22. Edner C, Li J, Albrecht T, MahlowS, HejaziM, Hussain H, Kaplan F, Guy C, Smith SM, Steup M, et al (2007) Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial β-amylases. Plant Physiol 145: 17-28
23. Fettke J, Chia T, Eckermann N, Smith A, Steup M (2006) A transglucosidase necessary for starch degradation and maltose metabolism in leaves at night acts on cytosolic heteroglycans (SHG). Plant J 46: 668-684
24. Fettke J, Eckermann N, Poeste S, Pauly M, Steup M (2004) The glycan substrate of the cytosolic (Pho 2) phosphorylase isozyme from Pisum sativum L.: identification, linkage analysis and subcellular localization. Plant J 39: 933-946
25. Fettke J, Hejazi M, Smirnova J, Höchel E, Stage M, Steup M (2009) Eukaryotic starch degradation: integration of plastidial and cytosolic pathways. J Exp Bot 60: 2907-2922
26. Fettke J, Poeste S, Eckermann N, Tiessen A, Pauly M, Geigenberger P, Steup M (2005) Analysis of cytosolic heteroglycans from leaves of transgenic potato (Solanum tuberosum L.) plants that under-or overexpress the Pho 2 phosphorylase isozyme. Plant Cell Physiol 46: 1987-2004
27. Fu Y, Ballicora MA, Leykam JF, Preiss J (1998) Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. J Biol Chem 273: 25045-25052
28. Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, et al (2008) β-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell 20: 1040-1058
29. Gerhardt R, Heldt HW (1984) Measurement of subcellular metabolite levels in leaves by fractionation of freeze-stopped material in nonaqueous media. Plant Physiol 75: 542-547
30. Gibon Y, Bläsing OE, Palacios-Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Höhne M, Günther M, Stitt M (2004) Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 39: 847-862
31. Gibon Y, Pyl ET, Sulpice R, Lunn JE, Höhne M, Günther M, Stitt M (2009) Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ 32: 859-874
32. Glaring MA, Skryhan K, Kötting O, Zeeman SC, Blennow A (2012) Comprehensive survey of redox sensitive starch metabolising enzymes in Arabidopsis thaliana. Plant Physiol Biochem 58: 89-97
33. Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci USA 107: 9458-9463
34. Graf A, Smith AM (2011) Starch and the clock: the dark side of plant productivity. Trends Plant Sci 16: 169-175
35. Hädrich N, Hendriks JHM, Kötting O, Arrivault S, Feil R, Zeeman SC, Gibon Y, Schulze WX, Stitt M, Lunn JE (2012) Mutagenesis of cysteine 81 prevents dimerization of the APS1 subunit of ADP-glucose pyrophosphorylase and alters diurnal starch turnover in Arabidopsis thaliana leaves. Plant J 70: 231-242
36. Haebel S, Hejazi M, Frohberg C, Heydenreich M, Ritte G (2008) Mass spectrometric quantification of the relative amounts of C6 and C3 position phosphorylated glucosyl residues in starch. Anal Biochem 379: 73-79
37. Harder KW, Owen P, Wong LKH, Aebersold R, Clark-Lewis I, Jirik FR (1994) Characterization and kinetic analysis of the intracellular domain of human protein tyrosine phosphatase β (HPTP β) using synthetic phosphopeptides. Biochem J 298: 395-401
38. Harthill JE, Meek SEM, Morrice N, Peggie MW, Borch J, Wong BHC, Mackintosh C (2006) Phosphorylation and 14-3-3 binding of Arabidopsis trehalose-phosphate synthase 5 in response to 2-deoxyglucose. Plant J 47: 211-223
39. Hejazi M, Fettke J, Haebel S, Edner C, Paris O, Frohberg C, Steup M, Ritte G (2008) Glucan, water dikinase phosphorylates crystalline maltodextrins and thereby initiates solubilization. Plant J 55: 323-334
40. Hejazi M, Fettke J, Kötting O, Zeeman SC, Steup M(2010) The laforin-like dual-specificity phosphatase SEX4 from Arabidopsis hydrolyzes both C6-and C3-phosphate esters introduced by starch-related dikinases and thereby affects phase transition of α-glucans. Plant Physiol 152: 711-722
41. Hendriks JHM, Kolbe A, Gibon Y, Stitt M, Geigenberger P (2003) ADPglucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol 133: 838-849
42. Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47: 431-444
43. Klie S, Krueger S, Krall L, Giavalisco P, Flügge UI, Willmitzer L, Steinhauser D (2011) Analysis of the compartmentalized metabolome: a validation of the non-aqueous fractionation technique. Front Plant Sci 2: 55
44. Kolbe A, Tiessen A, Schluepmann H, Paul M, Ulrich S, Geigenberger P (2005) Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADP-glucose pyrophosphorylase. Proc Natl Acad Sci USA 102: 11118-11123
45. Kötting O, Kossmann J, Zeeman SC, Lloyd JR (2010) Regulation of starch metabolism: the age of enlightenment? Curr Opin Plant Biol 13: 321-329
46. Kötting O, Pusch K, Tiessen A, Geigenberger P, Steup M, Ritte G (2005) Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves: the phosphoglucan, water dikinase. Plant Physiol 137: 242-252
47. Kötting O, Santelia D, Edner C, Eicke S, Marthaler T, Gentry MS, Comparot-Moss S, Chen J, Smith AM, SteupM, et al (2009) STARCHEXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21: 334-346
48. Krueger S, Niehl A, Lopez Martin MC, Steinhauser D, Donath A, Hildebrandt T, Romero LC, Hoefgen R, Gotor C, Hesse H (2009) Analysis of cytosolic and plastidic serine acetyltransferase mutants and subcellular metabolite distributions suggests interplay of the cellular compartments for cysteine biosynthesis in Arabidopsis. Plant Cell Environ 32: 349-367
49. Lu Y, Gehan JP, Sharkey TD (2005) Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol 138: 2280-2291
50. Lu Y, Sharkey TD (2004) The role of amylomaltase in maltose metabolism in the cytosol of photosynthetic cells. Planta 218: 466-473
51. Lunn JE (2007) Gene families and evolution of trehalose metabolism in plants. Funct Plant Biol 34: 550-563
52. Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R, Osuna D, Scheible W-R, Carillo P, Hajirezaei MR, Stitt M (2006) Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of starch synthesis in Arabidopsis thaliana. Biochem J 397: 139-148
53. Lunn JE, Price GD, Furbank RT (1999) Cloning and expression of a prokaryotic sucrose-phosphate synthase gene from the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 40: 297-305
54. MacRae EA, Lunn JE (2006) Control of sucrose biosynthesis. In WC Plaxton, MT McManus, eds, Advances in Plant Research: Control of Primary Metabolism in Plants, Vol 22. Blackwell, Oxford, pp 234-257
55. Michalska J, Zauber H, Buchanan BB, Cejudo FJ, Geigenberger P (2009) NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts. Proc Natl Acad Sci USA 106: 9908-9913
56. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco cultures. Physiol Plant 15: 473-497
57. Neuhaus HE, Kruckeberg AL, Feil R, Gottlieb L, Stitt M (1989) Dosage mutants of phosphoglucose isomerase in the cytosol and chloroplasts of Clarkia xantiana. II. Study of the mechanisms which regulate photosynthate partitioning. Planta 178: 110-122
58. Neuhaus HE, Quick WP, Siegl G, Stitt M (1990) Control of photosynthate partitioning in spinach leaves: analysis of the interaction between feedforward and feedback regulation of sucrose synthesis. Planta 181: 583-592
59. Neuhaus HE, Stitt M (1990) Control analysis of photosynthate partitioning: impact of reduced activity of ADP-glucose pyrophosphorylase or plastid phosphoglucomutase on the fluxes to starch and sucrose in Arabidopsis thaliana. Planta 182: 445-454
60. Niittylä T, Comparot-Moss S, Lue WL, Messerli G, Trevisan M, Seymour MD, Gatehouse JA, Villadsen D, Smith SM, Chen J, et al (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J Biol Chem 281: 11815-11818
61. 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
62. Pal SK, Liput M, Piques M, Ishihara H, Obata T, Martins MCM, Sulpice R, van Dongen JT, Fernie AR, Yadav UP, et al (2013) Diurnal changes of polysome loading track sucrose content in the rosette of wild-type Arabidopsis and the starchless pgm mutant. Plant Physiol 162: 1246-1265
63. Pellny TK, Ghannoum O, Conroy JP, Schluepmann H, Smeekens S, Andralojc J, Krause KP, Goddijn O, Paul MJ (2004) Genetic modification of photosynthesis with E. coli genes for trehalose synthesis. Plant Biotechnol J 2: 71-82
64. Piques M, Schulze WX, Höhne M, Usadel B, Gibon Y, Rohwer J, Stitt M (2009) Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Mol Syst Biol 5: 314-330
65. Preiss J (1988) Biosynthesis of starch and its regulation. In J Preiss, ed, The Biochemistry of Plants, Vol 14. Academic Press, San Diego, pp 181-254
66. Pyl ET, Piques M, Ivakov A, Schulze WX, Ishihara H, Stitt M, Sulpice R (2012) Metabolism and growth in Arabidopsis depend on the daytime temperature but are temperature-compensated against cool nights. Plant Cell 24: 2443-2469
67. Raines CA (2003) The Calvin cycle revisited. Photosynth Res 75: 1-10
68. Ramon M, De Smet I, Vandesteene L, Naudts M, Leyman B, Van Dijck P, Rolland F, Beeckman T, Thevelein JM (2009) Extensive expression regulation and lack of heterologous enzymatic activity of the class II trehalose metabolism proteins from Arabidopsis thaliana. Plant Cell Environ 32: 1015-1032
69. Ramon M, Rolland F, Thevelein JM, Van Dijck P, Leyman B (2007) ABI4 mediates the effects of exogenous trehalose on Arabidopsis growth and starch breakdown. Plant Mol Biol 63: 195-206
70. Ritte G, Heydenreich M, Mahlow S, Haebel S, Kötting O, Steup M (2006) Phosphorylation of C6-and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Lett 580: 4872-4876
71. Ritte G, Lloyd JR, Eckermann N, Rottmann A, Kossmann J, Steup M (2002) The starch-related R1 protein is an α-glucan, water dikinase. Proc Natl Acad Sci USA 99: 7166-7171
72. Santelia D, Kötting O, Seung D, Schubert M, Thalmann M, Bischof S, Meekins DA, Lutz A, Patron N, Gentry MS, et al (2011) The phosphoglucan phosphatase like sex Four2 dephosphorylates starch at the C3-position in Arabidopsis. Plant Cell 23: 4096-4111
73. Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 6849-6854
74. Scialdone A, Mugford ST, Feike D, Skeffington A, Borrill P, Graf A, Smith AM, Howard M (2013) Arabidopsis plants perform arithmetic division to prevent starvation at night. eLife 2: e00669
75. Scott P, Lange AJ, Kruger NJ (2000) Photosynthetic carbon metabolism in leaves of transgenic tobacco (Nicotiana tabacum L.) containing decreased amounts of fructose 2,6-bisphosphate. Planta 211: 864-873
76. Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30: 1126-1149
77. Smith SM, Fulton DC, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman SC, Smith AM (2004) Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves. Plant Physiol 136: 2687-2699
78. Steup M (1990) Starch degrading enzymes. In PJ Lea, ed, Methods in Plant Biochemistry, Vol 3. Academic Press, London, pp 103-128
79. Stitt M, Gibon Y, Lunn JE, Piques M (2007) Multilevel genomics analysis of carbon signaling during diurnal cycles: balancing supply and utilization by responding to changes in the nonlimiting range. Funct Plant Biol 34: 526-549
80. Stitt M, Lilley RM, Gerhardt R, Heldt HW (1989) Determination of metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol 174: 518-552
81. Stitt M, Lunn J, Usadel B (2010) Arabidopsis and primary photosynthetic metabolism: more than the icing on the cake. Plant J 61: 1067-1091
82. Stitt M, Sonnewald U (1995) Regulation of metabolism in transgenic plants. Annu Rev Plant Physiol Plant Mol Biol 46: 341-368
83. Stitt M, Wilke I, Feil R, Heidt HW (1988) Coarse control of sucrosephosphate synthase in leaves: alterations of the kinetic properties in response to the rate of photosynthesis and the accumulation of sucrose. Planta 174: 217-230
84. Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15: 282-292
85. Strand A, Zrenner R, Stitt M, Gardestrom P (2000) Antisense inhibition of two key enzymes in the sucrose biosynthesis pathway, cytosolic fructose bisphosphatase and sucrose phosphate synthase, has different consequences for photosynthetic carbon metabolism in transgenic Arabidopsis thaliana. Plant J 23: 751-770
86. Streb S, Eicke S, Zeeman SC (2012) The simultaneous abolition of three starch hydrolases blocks transient starch breakdown in Arabidopsis. J Biol Chem 287: 41745-41756
87. Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D, Huege J, Feil R, Lunn J, Nikoloski Z, Stitt M, et al (2013) Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell 25: 694-714
88. Tagliabracci VS, Roach PJ (2010) Insights into the mechanism of polysaccharide dephosphorylation by a glucan phosphatase. Proc Natl Acad Sci USA 107: 15312-15313
89. Tanz SK, Castleden I, Hooper CM, Vacher M, Small I, Millar AH (2012) SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res 41: D1185-D1191
90. Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14: 2191-2213
91. Usadel B, Bläsing OE, Gibon Y, Retzlaff K, Höhne M, Günther M, Stitt M (2008) Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 146: 1834-1861
92. Valerio C, Costa A, Marri L, Issakidis-Bourguet E, Pupillo P, Trost P, Sparla F (2011) Thioredoxin-regulated beta-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. J Exp Bot 62: 545-555
93. Vandesteene L, López-Galvis L, Vanneste K, Feil R, Maere S, Lammens W, Rolland F, Lunn JE, Avonce N, Beeckman T, et al (2012) Expansive evolution of the trehalose-6-phosphate phosphatase gene family in Arabidopsis. Plant Physiol 160: 884-896
94. Van Dijck P, Mascorro-Gallardo JO, De Bus M, Royackers K, Iturriaga G, Thevelein JM (2002) Truncation of Arabidopsis thaliana and Selaginella lepidophylla trehalose-6-phosphate synthase unlocks high catalytic activity and supports high trehalose levels on expression in yeast. Biochem J 366: 63-71
95. Weber A, Servaites JC, Geiger DR, Kofler H, Hille D, Gröner F, Hebbeker U, Flügge UI (2000) Identification, purification, and molecular cloning of a putative plastidic glucose translocator. Plant Cell 12: 787-802
96. Weise SE, Schrader SM, Kleinbeck KR, Sharkey TD (2006) Carbon balance and circadian regulation of hydrolytic and phosphorolytic breakdown of transitory starch. Plant Physiol 141: 879-886
97. Weise SE, Weber APM, Sharkey TD (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta 218: 474-482
98. Wingler A, Delatte TL, O'Hara LE, Primavesi LF, Jhurreea D, Paul MJ, Schluepmann H (2012) Trehalose 6-phosphate is required for the onset of leaf senescence associated with high carbon availability. Plant Physiol 158: 1241-1251
99. Wingler A, Fritzius T, Wiemken A, Boller T, Aeschbacher RA (2000) Trehalose induces the ADP-glucose pyrophosphorylase gene, ApL3, and starch synthesis in Arabidopsis. Plant Physiol 124: 105-114
100. Winter H, Robinson DG, Heldt HW (1993) Subcellular volumes and metabolite concentrations in barley leaves. Planta 191: 180-190
101. Winter H, Robinson DG, Heldt HW (1994) Subcellular volumes and metabolite concentrations in spinach leaves. Planta 193: 530-535
102. Worby CA, Gentry MS, Dixon JE (2006) Laforin, a dual specificity phosphatase that dephosphorylates complex carbohydrates. J Biol Chem 281: 30412-30418
103. Wuyts N, Palauqui JC, Conejero G, Verdeil JL, Granier C, Massonnet C (2010) High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll. Plant Methods 6: 17-30
104. Yazdanbakhsh N, Sulpice R, Graf A, Stitt M, Fisahn J (2011) Circadian control of root elongation and C partitioning in Arabidopsis thaliana. Plant Cell Environ 34: 877-894
105. Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61: 15.1-15.26
106. Zeeman SC, Tiessen A, Pilling E, Kato KL, Donald AM, Smith AM (2002) Starch synthesis in Arabidopsis: granule synthesis, composition, and structure. Plant Physiol 129: 516-529
107. Zhang Y, Primavesi LF, Jhurreea D, Andralojc PJ, Mitchell RAC, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of SNF1 related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol 149: 1860-1871