Starch degradation

Starch: Metabolism and Structure

Volumn , Issue , 2015, Pages 239-290

  Smirnova, Julia ^a,b,c   Fernie, Alisdair R ^a   Steup, Martin ^b,d  

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

^b UNIVERSITY OF POTSDAM   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d UNIVERSITY OF GUELPH   (Canada)

Author keywords

Amylopectin; Amylose; Carbohydrate active enzymes; Carbohydrate binding nodule (CBM); Glycogen; Reserve starch; Secondary binding site (SBS); Starch degradation; Starch modification; Transitory starch

Indexed keywords

EID: 84943234523     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-4-431-55495-0_7     Document Type: Chapter

References (245)

1. Aguado C, Sarkar S, Korolchuk VI et al (2010) Laforin, the most common protein mutated inLafora disease, regulates autophagy. Hum Mol Genet 19:2867–2876
2. Albrecht T, Koch A, Lode A et al (2001) Plastidic (Pho1-type) phosphorylase isoforms in potato (Solanum tuberosum L.) plants: expression analysis and immunochemical characterization. Planta 213:602–613
3. Asatsuma S, Sawada C, Itoh K et al (2005) Involvement of ‘-amylase I-1 in starch degradation in rice chloroplasts. Plant Cell Physiol 46:858–869
4. Atmodjo MA, Hao Z, Mohnen D (2013) Evolving views of pectin biosynthesis. Annu Rev PlantBiol 64:747–779
5. Baginsky S (2009) Plant proteomics: concepts, applications, and novel strategies for data interpretation. Mass Spectrom Rev 28:93–120
6. Bailey JM, Whelan WJ (1961) Physical properties of starch I. Relationship between iodine stain and chain length. J Biol Chem 236:969–972
7. Ball S (2012) Evolution of the starch pathway. In: Tetlow IA (ed) Starch: origins, structure and metabolism, vol 5, Essential reviews in experimental biology. Society for Experimental Biology, London, pp 29–54
8. Ball S, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the starch granule. Annu Rev Plant Biol 54:207–233
9. Ball S, Colleoni C, Cenci U et al (2011) The evolution of glycogen and starch metabolism gives molecular clues to understand the establishment of plastid endosymbiosis. J Exp Bot 62:1775–1801
10. Bertoft E (2013) On the building block and backbone concepts of amylopectin structure. CerealChem 90:294–311
11. Bewley DJ (1997) Seed germination and dormancy. Plant Cell 9:1055–1066
12. Bischof S, Umhang M, Eicke S et al (2013) Cecropia peltata accumulates starch or soluble glycogen by differentially regulation starch biosynthetic genes. Plant Cell 25:1400–1415
13. Blazek J, Copeland L (2010) Amylolysis of wheat starches. II. Degradation patterns of native starch granules with varying functional properties. J Cereal Sci 52:295–302
14. Boraston AB, Bolam DN, Gilbert HJ et al (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781
15. Buléon A, Colonna P, Planchot V et al (1998) Starch granules: structure and biosynthesis. Intern J Biolo Macromol 23:85–112
16. Buléon A, Cotte M, Putaux J-L et al (2014) Tracking sulfur and phosphorus within single starch granules using synchrotron X-ray micro fluorescence mapping. Biochim Biophys Acta 1840:113–119
17. Bustos R, Fahy B, Hylton CM et al (2004) Starch granule initiation is controlled by heteromultimeric isoamylase in potato tubers. Proc Natl Acad Sci U S A 101:2215–2220
18. Cantarel BL, Coutinho PM, Rancurel C et al (2009) The carbohydrate-active enzymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238
19. Carillo P, Feil R, Gibon Y et al (2013) A fluorometric assay for trehalose in the picomole range. Plant Methods 9:21
20. Cenci U, Nitschke F, Steup M et al (2014) Transition from glycogen to starch metabolism in archaeplastida. Trends Plant Sci 19:18–28
21. Chen K, An Y-QC (2006) Transcriptional responses to gibberellin and abscisic acid in barley aleurone. J Integr Plant Biol 48:591–612
22. Chia T, Thorneycroft D, Chapple A et al (2004) A cytosolic glucosyl transferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J 37:853–863
23. Chikwana VM, Khanna M, Baskaran S et al (2013) Structural basis for 20-phosphate incorporation into glycogen by glycogen synthase. Proc Natl Acad Sci U S A 110:20976–20981
24. Cho M-H, Lim H, Shin DH et al (2011) Role of the plastidic glucose transporter in the export of starch degradation products from the chloroplasts in Arabidopsis thaliana. New Phytol 190:101–112
25. Christiansen C, Hachem NA, Glaring MA et al (2009) A CBM20 low-affinity starch-binding domains from glucan, water dikinase. FEBS Lett 583:1159–1163
26. Claessen É, Rivoal J (2007) Isoenzymes of plant hexokinase: occurrence, properties and functions. Phytochemistry 68:709–713
27. Claeys H, De Bodt S, Inzé D (2014) Gibberellins and DELLAs: central nodes in growth regulatory networks. Trends Plant Sci 19:231–239
28. Collén J, Porcel B, Carré W et al (2013) Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad SciU S A 110:5247–5252
29. Comparat-Moss S, Kötting O, Stettler M et al (2010) A putative phosphatase, LSF1, is required for normal starch turnover in Arabidopsis leaves. Plant Physiol 152:685–697
30. Crumpton-Taylor M, Grandison S, Png KMY et al (2012) Control of starch granule number inArabidopsis chloroplasts. Plant Physiol 158:905–916
31. Crumpton-Taylor M, Pike M, Lu K-J et al (2013) Starch synthase 4 is essential for coordination of starch granule formation with chloroplast division during Arabidopsis leaf expansion. New Phytol 200:1064–1074
32. Cuyvers S, Dornez E, Delcour JA et al (2012) Occurrence and functional significance of secondary carbohydrate binding sites in glycoside hydrolases. Crit Rev Biotechnol 32:93–107
33. Daussant J, Zbaszyniak B, Sadowski J et al (1981) Cereal “-amylase: immunochemical study on two enzyme-deficient inbred lines of rye. Planta 151:176–179
34. De Schepper V, De Swaef T, Bauweraerts I et al (2013) Phloem transport: a review of mechanisms and controls. J Exp Bot 64:4839–4850
35. Delatte T, Trevisan M, Parker M et al (2005) Arabidopsis mutants Atisa1 and Atisa2 have identical phenotypes and lack the same multimeric isoamylase, which influences the branch point distribution of amylopectin during starch synthesis. Plant J 41:815–830
36. Delatte T, Umhang M, Trevisan M et al (2006) Evidence for distinct mechanisms of starch granule breakdown. J Biol Chem 281:12050–12059
37. Denison FC, Paul A-L, Zupanska AK et al (2011) 14-3-3 proteins in plant physiology. Semin Cell Dev Biol 22:720–727
38. DePaoli A, Contreras CJ, Segvich DM et al (2015) Glycogen phosphomonoester distribution in mouse models of the progressive myoclonic epilepsy, Lafora disease. J Biol Chem 290:841–850
39. Deschamps P, Colleoni C, Nakamura Y et al (2008) Metabolic symbiosis and the birth of the plant kingdom. Mol Biol Evol 25:536–548
40. Dippel R, Boos W (2005) The maltodextrin system of Escherichia coli. Metabolism and transport. J Bacteriol 187:8322–8331
41. Dumez S, Wattebled F, Dauvillee D et al (2006) Mutants of Arabidopsis lacking starch branching enzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. PlantCell 18:2694–2709
42. Edner C, Li J, Albrecht T, Mahlow S et al (2007) Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial “-amylases. Plant Physiol 145:17–28
43. Emes MJ, Tetlow IJ (2012) The role of heteromeric protein complexes in starch synthesis. In: Tetlow IJ (ed) Starch: origins, structure and metabolism, Essential reviews in experimental biology. Society for Experimental Biology, London, pp 255–278
44. Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63:3367–3377
45. Facchinelli F, Colleoni C, Ball SG et al (2013) Chlamydia, cyanobion, or host: who was on top in the ménage à trios? Trends Plant Sci 18:673–679
46. Facon M, Lin Q, Azzaz AM et al (2013) Distinct functional properties if isoamylase-type starch debranching enzymes in monocot and dicot leaves. Plant Physiol 163:1363–1375
47. Fazedas E, Szabó K, Kandra L et al (2013) Unexpected mode of action of sweet potato “-amylase on maltooligomers. Biochim Biophys Acta 1834:1976–1981
48. Fettke J, Eckermann N, Poeste S et al (2004) The glycan substrate of the cytosolic (pho2) phosphorylase isozyme from Pisum sativum L.: identification, linkage analysis and subcellular localization. Plant J 39:933–946
49. Fettke J, Eckermann N, Tiessen A et al (2005a) Identification, subcellular localization and biochemical characterization of water-soluble heteroglycans (SHG) in leaves of Arabidopsis thaliana L.: distinct SHG reside in the cytosol and in the apoplast. Plant J 43:568–586
50. Fettke J, Poeste S, Eckermann N et al (2005b) Analysis of cytosolic heteroglycans from leaves of transgenic potato (Solanum tuberosum L.) plants that under- or over-express the Pho2 phosphorylase isozyme. Plant Cell Physiol 46:1987–2004
51. Fettke J, Chia T, Eckermann N et al (2006) A transglucosidase necessary for starch degradation and maltose metabolism in leaves at night acts on cytosolic heteroglycans (SHG). Plant J 46:668–684
52. Fettke J, Nunes-Nesi A, Alpers J et al (2008) Alterations in cytosolic glucose-phosphate metabolism affect structural features and biochemical properties of starch-related heteroglycans. Plant Physiol 148:1614–1629
53. Fettke J, Hejazi M, Smirnova J et al (2009) Eukaryotic starch degradation: integration of plastidial and cytosolic pathways. J Exp Bot 60:2907–2922
54. Fettke J, Albrecht T, Hejazi M et al (2010) Glucose 1-phosphate is efficiently taken up by potato (Solanum tuberosum) tuber parenchyma cells and converted to reserve starch granules. NewPhytol 185:663–675
55. Fettke J, Malinova I, Albrecht T et al (2011) Glucose 1-phosphate transport into protoplasts and chloroplasts from leaves of Arabidopsis. Plant Physiol 155:1723–1734
56. Fettke J, Fernie AR, Steup M (2012a) Transitory starch and its degradation in higher plants. In: Tetlow IJ (ed) Starch: origins, structure and metabolism, vol 5, Essential reviews in experimental biology. Society for Experimental Biology, London, pp 311–374
57. Fettke J, Leifels L, Brust H et al (2012b) Two carbon fluxes to reserve starch in potato (Solanum tuberosum L.) tuber cells are closely interconnected but differently modulated by temperature. J Exp Bot 63:3011–3029
58. Fontes CMGA, Gilbert HJ (2010) Cellulosomes: highly efficient nanomachines designated to deconstruct plant cell wall complex carbohydrates. Annu Rev Biochem 79:655–681
59. Fordham-Skelton AP, Chilley P, Lumbreras V et al (2002) A novel higher plant protein tyrosine phosphatase interacts with SNF1-related protein kinases via a KIS (kinase interaction sequence) domain. Plant J 29:705–715
60. Fu F-F, Xue H-W (2010) Coexpression analyses identifies rice starch regulator1, a riceAP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. PlantPhysiol 154:927–938
61. Fujita N, Nakamura Y (2012) Distinct and overlapping functions of starch synthase isoforms. In: Tetlow IA (ed) Starch: origin, structure and metabolism, vol 5, Essential reviews in experimental biology. Society for Experimental Biology, London, pp 115–140
62. Fujita N, Kubo A, Suh DS et al (2003) Antisense inhibition of isoamylase alters the structure of amylopectin and physicochemical properties of starch in rice endosperm. Plant Cell Physiol 44:607–618
63. Fujita N, Toyosawa Y, Yoshinori U et al (2009) Characterization of pullulanase (PUL)-deficient mutants of rice (Oryza sativa L.) and the function of PUL on starch biosynthesis in the developing rice endosperm. J Exp Bot 60:1009–1023
64. Fulton DC, Stettler M, Mettler T et al (2008) Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of the active beta-amylases in Arabidopsis chloroplasts. Plant Cell 20:1040–1058
65. Garz A, Sandmann M, Rading M et al (2012) Cell-to-cell diversity in a synchronized Chlamydomonas culture as revealed by single cell analyses. Biophys J 103:1078–1086
66. Gayarre J, Duran-Trío L, Garcia OC et al (2014) The phosphatase activity of laforin is dispensable to rescue EPM2a_/_ mice from Lafora disease. Brain 137:806–818
67. Gentry MS, Dowen RH III, Worby CA et al (2007) The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neutral disease. J Cell Biol 178:477–488
68. Gentry MS, Dixon JE, Worby CA (2009) Lafora disease: insights into neurodegeneration from plant metabolism. Trends Biochem Sci 34:628–639
69. Gentry MS, Pace RM (2009) Conservation of the glucan phosphatase laforin is linked to rates of molecular evolution and the glucan metabolism of the organism. BMC Evol Biol 9:138
70. Gentry MS, Romá-Mateo C, Sanz P (2013) Laforin, a protein with many faces: glucan phosphatase, adapter protein, et alii. FEBS J 280:525–537
71. Gilbert HJ (2010) The biochemistry and structural biology of plant cell wall deconstruction. Plant Physiol 153:444–455
72. Glaubitz U, Li X, Köhl K et al (2014) Differential physiological responses of different rice (Oryza sativa) cultivars to elevated night temperature during vegetative growth. Funct Plant Biol 41:437–448
73. Goldberg RN, Bell D, Tewari YB et al (1991) Thermodynamics of hydrolysis of oligosaccharides. Biophys Chem 40:69–76
74. Graf A, Smith AM (2011) Starch and the clock: the dark side of the plant productivity. Trends Plant Sci 16:169–175
75. Graf A, Schlereth A, Stitt M et al (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci U S A 107:9458–9463
76. Guillén D, Sánchez S, Rodríguez-Sanoja R (2010) Carbohydrate-binding domains: multiplicity of biological roles. Appl Microbiol Biotechnol 85:1241–1249
77. Häusler RE, Heinrichs L, Schmitz J et al (2014) How sugars might coordinate chloroplast and nuclear gene expression during acclimation to high light intensities. Mol Plant 7:1121–1137
78. Heazlewood JL, Durek P, Hummel J et al (2009) PhosPhAt: a database of phosphorylation sites in Arabidopsis thaliana and a plant-specific phosphorylation site predictor. Nucleic Acid Res 36:D1015–D1021
79. Hehre EJ, Brewer CF, Henghof DS (1979) Scope and mechanism of carbohydrase action. Hydrolytic and nonhydrolytic actions of beta-amylase on alpha- and beta-maltosyl fluoride. J Biol Chem 254:5942–5950
80. Hehre EJ, Kitabata S, Brewer CF (1986) Catalytic flexibility of glycosidases. The hydration of maltal by “-amylase to form 2-deoxymaltose. J Biol Chem 261:2147–2153
81. Hejazi M, Fettke J, Haebel S et al (2008) Glucan, water dikinase phosphorylates crystalline maltodextrins and thereby initiates solubilisation. Plant J 55:323–334
82. Hejazi M, Fettke J, Paris O et al (2009) The two plastidial starch-related dikinases sequentially phosphorylate glucosyl residues at the surface of both the A- and the B-type allomorphs of crystalline maltodextrins but the mode of action differs. Plant Physiol 150:962–976
83. Hejazi M, Fettke J, Kötting O et al (2010) The laforin-like dual-specificity phosphatase SEX4 from Arabidopsis hydrolyses both C6- and C3-monophosphate esters introduced by starch-related dikinases and thereby affects phase transition of alpha-glucans. Plant Physiol 152:711–722
84. Hejazi M, Fettke J, Steup M (2012) Starch phosphorylation and dephosphorylation: the consecutive action of starch-related dikinases and phosphatases. In: Tetlow IA (ed) Starch: origins, structure and metabolism, vol 5, Essential reviews in experimental biology. Society for Experimental Biology, London, pp 279–309
85. Henry C, Bledsoe SW, Siekman A et al (2014) The trehalose pathway in maize: conservation and gene regulation in response to the diurnal cycle and extended darkness. J Exp Bot 65:5959–5973
86. Hong YF, Ho T-HD, Wu CF et al (2012) Convergent starvation signals and hormone crosstalk in regulating nutrient mobilization upon germination in cereals. Plant Cell 24:2857–2873
87. Huang X-F, Nazarin-Fironzabadi F, Vincken J-P et al (2014) Expression of an amylosucrase in potato results in larger starch granules with novel properties. Planta 240:409–421
88. Hussain H, Mant A, Seale R et al (2003) Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans. Plant Cell 15:133–149
89. Hwang SK, Nishi A, Satoh H et al (2010) Rice endosperm-specific plastidial alpha-phosphorylase is important for synthesis opf short-chain malto-oligosaccharides. Arch Biochem Biophys 495:82–92
90. Ingkasuwan P, Netrphan S, Prasitwattanaseree S et al (2012) Inferring transcriptional gene regulation network of starch metabolism in Arabidopsis thaliana leaves using graphical Gaussian model. MBC Syst Biol 6:100
91. Ishikawa K, Nakatani H, Katsuya Y et al (2007) Kinetic and structural analysis of enzyme sliding on a substrate: multiple attack in “-amylase. Biochemistry 46:792–798
92. Isshiki M, Matsuda Y, Takasaki A et al (2008) Du3, a mRNA cap-binding protein gene, regulates amylose content in Japonica rice seeds. Plant Biotechnol 25:483–487
93. Izumi M, Hidema J, Makino A et al (2013) Autophagy contributes to nighttime energy availability for growth in Arabidopsis. Plant Physiol 161:1682–1693
94. Jane JL, Kasemsuwaran T, Leas S et al (1994) Anthology of starch granule morphology by scanning electron microscopy. Starch-Starke 46:121–129
95. Kainuma K, French D (1970) Action of pancreatic alpha-amylase and sweet potato beta-amylase on 62 and 62 ‘-glucosylmaltooligosaccharides. FEBS Lett 6:182–186
96. Kammerer B, Fischer K, Hilpert B et al (1998) Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell 10:105–117
97. Kartal Ö, Mahlow S, Skupin A et al (2011) Carbohydrate-active enzymes exemplify entropic principles in metabolism. Mol Syst Biol 7:542
98. Keeling PL, Myers AM (2010) Biochemistry and genetics of starch synthesis. Annu Rev Food Sci 1:271–303
99. Kerk D, Conley TR, Rodriguez FA et al (2006) A chloroplast-localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydratebinding module, which binds the polysaccharide starch. Plant J 46:400–413
100. Kiessling LL, Young T, Gruber TD et al (2008) Multivalency in protein-carbohydrate recognition. In: Fraser-Reid B, Tatsuata K, Thiem J (eds) Glycoscience. Springer, Berlin/Heidelberg, pp 2483–2523
101. Kihara M, Kaneko T, Ito K et al (1999) Geographic variation of “-amylase thermostability among varieties of barley (Hordeum vulgare) and “-amylase deficiency. Plant Breed 118:453–455
102. Kim T-J, Kim M-J, Kim B-C et al (1999) Modes of action of acarbose hydrolysis and transglycosylation catalyzed by a thermo-stable maltogenic amylase, the gene for which was cloned from a Thermus strain. Appl Environ Microbiol 65:1644–1651
103. Kötting O, Santelia D, Edner C et al (2009) STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 21:334–346
104. Kötting O, Kossmann J, Zeeman SC et al (2010) Regulation of starch metabolism: the age of enlightenment? Curr Opin Plant Biol 13:321–329
105. Kramhøft B, Bak-Jensen KS, Mori H et al (2005) Multiple attack, kinetic parameters, and product profiles in amylose hydrolysis by barley ‘-amylase 1 variants. Biochemistry 44:1824–1832
106. Kreis M, Williamson M, Buxton B et al (1987) Primary structure and differential expression of “-amylase in normal and mutant barley. Eur J Biochem 169:517–525
107. Kubo A, Rahman S, Utsumi Y et al (2005) Complementation of sugary-1 phenotype in rice endosperm with the wheat isoamylase1 gene supports a direct role for isoamylase1 in amylopectin biosynthesis. Plant Physiol 137:43–56
108. Kubo A, Colleoni C, Dinges J et al (2010) Functions of heteromeric and homomeric isoamylasetype starch-debranching enzymes in developing maize endosperm. Plant Physiol 153:956–969
109. Lastdrager J, Hanson J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65:799–807
110. Leivar P, Quail PH (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 2011:19–28
111. Li J, Francisco P, Zhou W, Edner C et al (2009) Catalytically-inactive “-amylase BAM4 required for starch breakdown in Arabidopsis leaves is a starch-binding protein. Arch Biochem Biophys 489:92–98
112. Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63:215–237
113. Lloyd JR, Kossmann J (2015) Transitory and storage starch metabolism: two sides do the same coin? Curr Opin Biotechnol 32:143–148
114. Lohmeyer-Vogel EM, Kerk D, Nimick M et al (2008) Arabidopsis At5g39790 encodes a chloroplast-localized carbohydrate-binding coiled-coil domain-containing putative scaffold protein. BCM Plant Biol 8:120
115. López CA, de Vries AH, Marrink SJ (2012) Amylose folding under the influence of lipids. Carbohydr Res 364:1–7
116. Lu CA, Lin CC, Lee KW et al (2007) The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice. Plant Cell 19:2484–2499
117. Luís AS, Venditto I, Temple MJ et al (2013) Understanding how noncatalytic carbohydrate binding modules can display specificity for xyloglucan. J Biol Chem 288:4799–4809
118. Lunn JE (2007) Gene families and evolution of trehalose metabolism in plants. Funct Plant Biol 34:550–563
119. Lunn JE, Delorge I, Figueroa CM et al (2014) Trehalose metabolism in plants. Plant J 79: 544–567
120. Ma J, Jiang Q-T, Wei L et al (2014) Conserved structure and varied expression reveal key roles of phosphoglucan phosphatase gene starch excess 4 in barley. Planta 240:1179–1190
121. Mahlow S, Hejazi M, Kuhnert F et al (2014) Phosphorylation of transitory starch by ‘-glucan, water dikinase during starch turnover affects the surface properties and morphology of starch granules. New Phytol 203:495–507
122. Malinova I, Steup M, Fettke J (2011) Starch related heteroglycans in roots from Arabidopsis thaliana. J Plant Physiol 168:1406–1414
123. Malinova I, Steup M, Fettke J (2013) Carbon transitions from either Calvin cycle or transitory starch to heteroglycans as revealed by 14C-labeling experiments using protoplasts fromArabidopsis. Physiol Plant 149:25–44
124. Malinova I, Mahlow S, Alseekh S et al (2014) Double knock-out mutants of Arabidopsis thaliana grown under normal conditions reveal that the plastidial phosphorylase isozyme (PHS1) participates in transitory starch metabolism. Plant Physiol 164:607–621
125. Martins MCM, Hejazi M, Fettke J et al (2013) Feedback inhibition of starch degradation inArabidopsis leaves mediated by trehalose 6-phosphate. Plant Physiol 163:1142–1163
126. Matsushima R, Maekawa M, Kurano M et al (2014) Amyloplast-localized SSG4 protein influences the size of starch grains in rice endosperm. Plant Physiol 164:623–636
127. Meekins DA, Guo H-F, Husodo S et al (2013) Structure of the Arabidopsis glucan phosphataseLIKE SEX FOUR2 reveals a unique mechanism for starch dephosphorylation. Plant Cell 25:2302–2314
128. Meekins DA, Raththagala M, Husodo S et al (2014) Phosphoglucan-bound structure of starch phosphatase starch excess4 reveals the mechanism for C6 specificity. Proc Natl Acad Sci U S A 111:7272–7277
129. Meléndez-Hevia E, Waddell TG, Shelton ED (1993) Optimization of molecular design in the evolution of metabolism: the glycogen molecule. Biochem J 295:477–483
130. Mikami B, Degano M, Hehre EJ et al (1994) Crystal structure of soybean “-amylase reacted with “-maltose and maltal: active site components and their apparent role in catalysis. Biochemistry 33:7779–7787
131. Minassian BA, Lee JR, Herbick JA et al (1998) Mutations in a gene encoding a novel protein tyrosine phosphatase cause progressive myoclonus epilepsy. Nat Genet 20:171–174
132. Mizushima N, Yoshimori T, Ohsumi Y (2011) The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27:107–132
133. Moghaddam MRB, Van den Ende W (2012) Sugar and plant immunity. J Exp Bot 63:3989–3998
134. Nielsen TH, Wischmann B, Enevoldsen K et al (1994) Starch phosphorylation in potato tubers proceeds concurrently with de novo biosynthesis of starch. Plant Physiol 105:111–117
135. Nielsen MM, Bozonnet S, Seo ES et al (2009) Two secondary carbohydrate binding sites on the surface of barley alpha-amylase I have distinct functions and display synergy in hydrolysis of starch granules. Biochemistry 48:7686–7697
136. Nielsen JW, Kramhøft B, Boyonnet S et al (2012) Degradation of the starch components amylopectin and amylose by barley ‘-amylase 1: role of surface binding site 2. Arch BiochemBiophys 528:1–6
137. Niittylä T, Messerli G, Trevisan M et al (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303:87–89
138. Niittylä T, Comparat-Moss S, Lue WL et al (2006) Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J Biol Chem 281:11815–11818
139. Nishimo H, Murakawa A, Mori T et al (2004) Kinetic studies of AMP-dependent phosphorolysis of amylopectin catalyzed by phosphorylase b on a 27 MHz microbalance quartz-crystal. J AmChem Soc 126:14752–14757
140. Nishiyama Y, Mazeau K, Morin M et al (2010) Molecular and crystal structure of 7-fold V-amylose complexed with 2-propanol. Macromolecules 43:8628–8636
141. Nitschke F, Wang P, Schmieder P et al (2013) Hyperphosphorylation of glucosyl C6 carbons and altered structure of glycogen in the neurodegenerative epilepsy Lafora disease. Cell Metab 17:756–767
142. Nougué O, Corbi J, Ball SG et al (2014) Molecular evolution accompanying functional divergence of duplicated genes along the plant starch biosynthesis path. BMC Evol Biol 14(1):103. doi:10.1186/1471-2148-103
143. Pal SK, Liput M, Piques M 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
144. Palm DC, Rohwer JM, Hofmeyr J-HS (2013) Regulation of glycogen synthase from mammalian skeletal muscle – a unifying view of allosteric and covalent regulation. FEBS J 280:2–27
145. Paparelli E, Parlanti S, Gonzali S et al (2013) Nighttime sugar starvation orchestrates gibberellin biosynthesis and plant growth in Arabidopsis. Plant Cell 25:3760–3769
146. Park J-T, Shim J-H, Tran P et al (2011) Role of maltose enzymes in glycogen synthesis byEscherichia coli. J Bacteriol 193:2517–2526
147. Paul MJ, Primavesi F, Jhurreea D et al (2008) Trehalose metabolism and signalling. Annu RevPlant Biol 59:417–441
148. Payne CM, Baban J, Horn SJ et al (2012) Hallmarks of processivity in glycoside hydrolases from crystallographic and computational studies of the Serratia marcescens chitinases. J Biol Chem 287:36322–36330
149. Payne CM, Resch MG, Chen L et al (2013) Glycosylated linkers in multimodular lignocellulosedegrading enzymes dynamically bind to cellulose. Proc Natl Acad Sci U S A 110:14646–14651
150. Pederson BA, Turnbull J, Epp JR et al (2013) Inhibiting glycogen synthesis prevents Lafora disease in a mouse model. Ann Neurol 74:297–300
151. Peng M, Gao M, Båga M et al (2000) Starch-branching enzymes preferentially associated withA-type starch granules in wheat endosperm. Plant Physiol 124:265–272
152. Peng C, Wang Y, Liu F et al (2014) FLOURY ENDOSPERM6 encodes a CBM48 domaincontaining protein involved in compound granule formation and starch synthesis in rice endosperm. Plant J 77:917–930
153. Pérez S, Bertoft E (2010) The molecular structure of starch components and their contribution to the architecture of starch granules: a comprehensive review. Starch-Starke 62:389–420
154. Pfister B, Lu K-J, Eicke S et al (2014) Genetic evidence that chain length and branch point distributions are linked determinants of starch granule formation in Arabidopsis. Plant Physiol 165:1467–1474
155. Pulido R, Hooft van Huijsduijnen R (2008) Protein tyrosine phosphatases: dual-specificity phosphatases in health and disease. FEBS J 275:848–866
156. Purdy SJ, Bussell JD, Nunn CP et al (2013) Leaves from the Arabidopsis maltose exporter1 mutant exhibits a metabolic profile with features of cold acclimation in the warm. PLoS ONE 8:e79412
157. Putaux J-L, Montesanti N, Véronèse G et al (2011) Morphology and structure of A-amylose single crystals. Polymer 52:2198–2205
158. Pyl E-T, Piques M, Ivakov A et al (2012) Metabolism and growth in Arabidopsis depend on the daytime temperature but are temperature-compensated against cool nights. Plant Cell 24:2443–2469
159. Qian M, Nahoum V, Bumiel J et al (2001) Enzyme-catalyzed condensation reaction in a mammalian ‘-amylase. High-resolution structural analysis of an enzyme-inhibitor complex. Biochemistry 40:7700–7709
160. Ragauskas AJ, Williams CK, Davison BH et al (2006) The path for biofuels and biomaterials. Science 311:484–489
161. Ragel P, Streb S, Feil R et al (2013) Loss of starch granule initiation has a deleterious effect on the growth of Arabidopsis plants due to an accumulation of ADP-glucose. Plant Physiol 163:75–85
162. Rao SNR, Maity R, Sharma J et al (2010) Sequestration of chaperones and proteasome into Lafora bodies and proteasomal dysfunction induced by Lafora disease-associated mutations. Hum MolGenet 19:4726–4734
163. Raththagala M, Brewer MK, Parker MW et al (2015) Structural mechanism of laforin function in glycogen dephosphorylation and Lafora disease. Mol Cell 57:261–272
164. Regina A, Blazek J, Gilbert E et al (2012) Differential effects of genetically distinct mechanisms of elevating amylose on barley starch characteristics. Carbohydr Polym 89:979–991
165. Reiland S, Messerli G, Baerenfaller K et al (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast-kinase substrates and phosphorylation networks. Plant Physiol 150:889–903
166. Reinhold H, Soyk S, Šimková K et al (2011) “-amylase-like proteins function as transcription factors in Arabidopsis, controlling shoot growth and development. Plant Cell 23:1391–1403
167. Rejek M, Stevenson CE, Southard AM et al (2011) Chemical genetics and cereal starch metabolism: structural basis of the non-covalent and covalent inhibition of barley “-amylase. Mol BioSyst 7:718–730
168. Ritte G, Lloyd JR, Eckermann N et al (2002) The starch-related R1 protein is an alpha-glucan, water dikinase. Proc Natl Acad Sci U S A 99:7166–7171
169. Ritte G, Scharf A, Eckermann N et al (2004) Phosphorylation of transitory starch is increased during degradation. Plant Physiol 135:2068–2077
170. Roach PJ, DePaoli AA, Hurley TD et al (2012) Glycogen and its metabolism: some new developments and old themes. Biochem J 441:763–787
171. Roberts EH (1973) Predicting the storage life of seeds. Seed Sci Technol 1:499–514
172. Roblin P, Potocki-Véronèse G, Guieysse D et al (2013) SAXS Conformational tracking of amylose synthesized by amylosucrase. Biomacromolecules 14:232–239
173. Ruan Y-L (2014) Sucrose metabolism: gateway to diverse carbon use and sugar signaling. AnnuRev Plant Biol 65:26.1–26.35
174. Ruzanski C, Smirnova J, Rejzek M et al (2013) A bacterial glucanotransferase can replace the complex maltose metabolism required for starch-to-sucrose conversion in leaves at night. J Biol Chem 288:28581–28598
175. Ryu J-H, Drain J, Kim JH et al (2009) Comparative structural analyses of purified glycogen particles from rat liver, human skeletal muscle and commercial preparations. Int J Biol Macromol 45:478–482
176. Salazar C, Höfer T (2009) Multiple protein phosphorylation – from molecular mechanisms to kinetic models. FEBS J 276:3177–3198
177. Sankhala RS, Koksai AC, Ho L et al (2015) Dimeric quarternary structure of human laforin. J BiolChem 290:4552–4559
178. Santelia D, Kötting O, Seung D et al (2011) The phosphoglucan phosphatase like SEX Four2 dephosphorylates starch at the C3-position in Arabidopsis. Plant Cell 23:4096–4111
179. Satoh H, Shibahara K, Tokunaga T et al (2008) Mutation of the plastidial alpha-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. Plant Cell 20:1833–1849
180. Scheidig A, Fröhlich A, Schulze S et al (2002) Downregulation of a chloroplast-targeted “-amylase leads to a starch-excess phenotype in leaves. Plant J 30:581–591
181. Schmitz J, Heinrichs L, Scossa F et al (2014) The essential role of sugar metabolism in the acclimation response of Arabidopsis thaliana to high light intensities. J Exp Bot 65:1619–1636
182. Schönknecht G, Chen W-H, Ternes CM et al (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–1210
183. Shaik SS, Carciofi M, Martens HJ et al (2014) Starch bioengineering affects cereal grain germination and seedling establishment. J Exp Bot 65:2257–2270
184. Shang BZ, Chang R, Chu J-W (2013) Systems-level modelling with molecular resolution elucidates the rate-limiting mechanisms of cellulose decomposition by cellobiohydrolases. J Biol Chem 288:29081–29089
185. Shimonaga T, Konishi M, Oyama Y et al (2008) Variation in storage ‘-glucans of the Porphyridiales (Rhodophyta). Plant Cell Physiol 49:103–116
186. Silver DM, Silva LP, Issakidis-Bourguet E et al (2013) Insight into the redox regulation of the phosphoglucan phosphatase SEX4 involved in starch degradation. FEBS J 280:538–548
187. Silver DM, Kötting O, Moorhead GB (2014) Phosphoglucan phosphatase function sheds light on starch degradation. Trends Plant Sci 19:471–478
188. Sim L, Beeren SR, Findinier J et al (2014) Crystal structure of the Chlamydomonas starch debranching isoamylase ISA1 reveals insights into the mechanism of branch trimming and complex assembly. J Biol Chem 289:22991–23003
189. Skeffington AW, Graf A, Duxbury Z et al (2014) Glucan, water dikinase exerts little control over starch degradation in Arabidopsis leaves at night. Plant Physiol 165:866–879
190. Smirnova J (2013) Carbohydrate-active enzymes metabolising maltose: kinetic and structural features. Dissertation, University of Potsdam
191. Smith SM, Fulton DC, Chia T et al (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
192. Sokolov LN, Dominguez-Solis JR, Allary AL et al (2006) A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc Natl Acad SciUSA 103:9732–9737
193. Sonnewald U, Kossmann J (2013) Starches – from current models to genetic engineering. PlantBiotechnol J 11:223–232
194. Soyk S, Šimková K, Zürcher E et al (2014) The enzyme-like domain of Arabidopsis nuclear “-amylases is critical for DNA sequence recognition and transcriptional activity. Plant Cell 26:1746–1763
195. Sparks E, Wachsmann G, Benfey PN (2013) Spatiotemporal signaling in plant development. NatRev Genet 14:631–644
196. Sreenivaculu N, Usadel B, Winter A et al (2008) Barley grain maturation and germination: metabolic pathway and regulatory network commonalities and differences highlighted by newMapMan/PageMan profiling tools. Plant Physiol 146:310–327
197. Sreenivasulu N, Wobus U (2013) Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu Rev Plant Biol 64:189–217
198. Steichen JM, Petty RV, Sharkey TD (2008) Domain characterization of a 4-alphaglucanotransferase essential for maltose metabolism in photosynthetic leaves. J Biol Chem 283:20797–20804
199. Stettler M, Eicke S, Mettler T et al (2009) Blocking the metabolism of starch breakdown products in Arabidopsis leaves triggers chloroplast degradation. Mol Plant 2:1233–1246
200. Steup M, Schächtele C (1981) Mode of glucan degradation by purified phosphorylase forms from spinach leaves. Planta 153:351–361
201. Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15:282–292
202. Stoddard FL (1999) Survey of starch particle-size distribution in wheat and related species. CerealChem 67:59–63
203. Streb S, Delatte T, Umhang M et al (2008) Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell 20:3448–3466
204. 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
205. Sullivan MA, Aroney STN, Li S et al (2014) Changes in glycogen structure over feeding cycles sheds new light on blood-glucose control. Biomacromolecules 15:660–665
206. Sulpice R, Flis A, Ivakov AA, Apelt F et al (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol Plant 7:137–155
207. Sun T-P (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21:R338–R345
208. Sun X, Jones WT, Rikkerink EHA (2012) GRAS proteins: the versatile roles of intrinsically disordered proteins in plant signalling. Biochem J 442:1–12
209. Sundberg M, Pfister B, Fulton D et al (2013) The heteromultimeric debranching enzyme involved in starch synthesis in Arabidopsis requires both isoamylase1 and isoamyoase2 subunits for complex stability and activity. PLos ONE 8:e75223
210. Szecowka M, Heise R, Tohge T et al (2013) Metabolic fluxes of an illuminated Arabidopsis thaliana rosette. Plant Cell 25:694–714
211. Tagliabracci VS, Heiss C, Karthlic C et al (2011) Phosphate incorporation during glycogen biosynthesis and Lafora disease. Cell Metab 13:274–282
212. Takeda Y, Hizukuri S (1981) Re-examination of the action of sweet-potato beta-amylase on phosphorylated (1!4)-’-D-glucan. Carbohydr Res 89:174–178
213. Tanackovic V, Svenson JT, Jensen S et al (2014) The deposition and characterization of starch in Brach ypodium distachyon. J Exp Bot 65:5179–5192
214. Tan-Wilson AL, Wilson KA (2012) Mobilization of seed protein reserves. Physiol Plant 145:140–153
215. Tsuji H, Aya K, Ueguchi-Tanaka M et al (2006) GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J 47:427–444
216. Turgeon R, Wolf S (2009) Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol 60:207–221
217. Turnbull J, Wang P, Girard J-M et al (2010) Glycogen hyperphosphorylation underlies lafora body formation. Ann Neurol 68:925–933
218. van Wijk KJ, Friso G, Walther D, Schulze WX (2014) Meta-analysis of Arabidopsis thaliana phospho-proteomics data reveals compartmentalization of phosphorylation motifs. Plant Cell 26:2367–2389
219. Vander Kooi CW, Taylor AO, Pace RM et al (2010) Structural basis for the glucan phosphatase activity of Starch Excess4. Proc Natl Acad Sci U S A 107:15379–15384
220. Vilaplana F, Hasjim J, Gilbert RG (2012) Amylose content in starches: towards optimal definition and validating experimental methods. Carbohydr Polym 88:103–111
221. Vriet C, Welham T, Brachmann A et al (2010) A suite of Lotus japonicus starch mutants reveals both conserved and novel features of starch metabolism. Plant Physiol 154:643–655
222. Walley JW, Shen Z, Sartor R et al (2013) Reconstruction of protein networks from an atlas of maize seed proteotypes. Proc Natl Acad Sci U S A 110:E4808–E4817
223. Wattebled F, Dong Y, Dumez S et al (2005) Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin. Plant Physiol 138:184–195
224. Wattebled F, Planchot V, Szydlowski N et al (2008) Further evidence for the mandatory nature of polysaccharide debranching for the aggregation of semicrystalline starch and for overlapping functions of debranching enzymes in Arabidopsis leaves. Plant Physiol 148:1309–1323
225. Webber BL, Abaloz BA, Woodrow IE (2007) Myrmecophilic food body production in the understorey tree, Ryparosa kurrangii (Archariaceae), a rare Australian rainforest taxon. NewPhytol 173:250–263
226. Weidberg H, Shvets E, Elazar Z (2011) Biogenesis and cargo selectivity of autophagosomes. AnnuRev Biochem 80:125–156
227. Weise SE, Weber APM, Sharkey TD (2004) Maltose is the major form of carbon exported from the chloroplast at night. Planta 218:474–482
228. Weise SE, Kim KS, Stewart RP et al (2005) “-Maltose is the metabolically active anomer of maltose during transitory starch degradation. Plant Physiol 137:756–761
229. Weise SE, Aung K, Jarou ZJ et al (2012) Engineering starch accumulation by manipulation of phosphate metabolism of starch. Plant Biotechnol J 10:545–554
230. Weitbrecht K, Muller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309
231. Wilson WA, Roach PJ, Montero M et al (2010) Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev 34:952–985
232. Worby CA, Gentry MS, Dixon JE (2006) Laforin, a dual specificity phosphatase that dephosphorylates complex carbohydrates. J Biol Chem 281:30412–30418
233. Yadav UP, Ivakov A, Feil R et al (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65:1051–1068
234. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251
235. Yin LL, Xue HW (2012) TheMADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. Plant Cell 24:1049–1065
236. Yu TS, Zeeman SC, Thorneycroft D et al (2005) ‘-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280:9773–9779
237. Yun M-S, Kawagoe Y (2010) Septum formation in amyloplasts produces compound granules in the endosperm and is regulated by plastid division proteins. Plant Cell Physiol 51:1469–1479
238. Zeeman SC, Umemoto T, Lue WL et al (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10:1699–1712
239. Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234
240. Zeng D, Yan M, Wang Y et al (2007) Du1, encoding a novel Prp1 protein, regulates starch biosynthesis through affecting the splicing of Wxb pre-mRNAs in rice (Oryza sativa L.). PlantMol Biol 65:501–509
241. Zhang Q, Wing R (2013) Genome studies and molecular genetics: understanding the functional genome based on the rice model. Curr Opin Plant Biol 16:129–132
242. Zhou S-R, Yin L-L, Xue H-W (2013) Functional genomics based understanding of rice endosperm development. Curr Opin Plant Biol 16:236–246
243. Zi J, Mafu S, Peters RJ (2014) To gibberellins and beyond! Surveying the evolution of (di)terpenoid metabolism. Annu Rev Plant Biol 65:10.1–10.28
244. Zirin J, Nieuwenhius J, Perrimon N (2013) Role of autophagy in glycogen breakdown and its relevance to chloroquine myopathy. PLoS Biol 11:e1001708
245. Zulawski M, Braginets R, Schulze WX (2013) PhosPhAt goes kinases – searchable protein kinase target information in the plant phosphorylation site database PhosPhAt. Nucleic Acids Res 41:D1176–D1184