Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial β-amylases

Plant Physiology

Volumn 145, Issue 1, 2007, Pages 17-28

  Edner, Christoph ^a   Li, Jing ^b   Albrecht, Tanja ^a   Mahlow, Sebastian ^a   Hejazi, Mahdi ^a   Hussain, Hasnain ^c   Kaplan, Fatma ^d   Guy, Charles ^d   Smith, Steven M ^b   Steup, Martin ^a   Ritte, Gerhard ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITI MALAYSIA SARAWAK   (Malaysia)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOASSAY; MASS SPECTROMETRY; PHOSPHORYLATION; PLANTS (BOTANY); STARCH; WATER;

ARABIDOPSIS THALIANA; POTATO; STARCH GRANULES;

ENZYME ACTIVITY;

ARABIDOPSIS; ARABIDOPSIS THALIANA; SOLANUM TUBEROSUM;

EID: 34548679587     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.107.104224     Document Type: Article

References (51)

1. Alonso-Casajús N, Dauvillée D, Viale AM, Munoz J, Baroja-Fernández E, Morán-Zorzano MT, Eydallin G, Ball S, Pozueta-Romero J (2006) Glycogen phosphorylase, the product of the glgP gene, catalyzes glycogen breakdown by removing glucose units from the nonreducing ends in Escherichia coli. J Bacteriol 188: 5266-5272
2. Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenisis of the starch granule. Annu Rev Plant Biol 54: 207-233
3. 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: 595-695
4. Blennow A, Engelsen SB, Nielsen TH, Baunsgaard L, Mikkelsen R (2002) Starch phosphorylation: a new front line in starch research. Trends Plant Sci 7: 445-450
5. Caspar T, Lin TP, Kakefuda G, Benbow L, Preiss J, Somerville C (1991) Mutants of Arabidopsis with altered regulation of starch degradation. Plant Physiol 95: 1181-1188
6. Coppin A, Varre J-S, Lienard L, Dauvillee D, Guerardel Y, Soyer-Gobillard M-O, Buleon A, Ball S, Tomavo S (2005) Evolution of plant-like storage polysaccharides in the protozoan parasite Toxoplasma gondii argues for a red alga ancestry. J Mol Evol 60: 257-267
7. Critchley JH, Zeeman SC, Takaha T, Smith AM, Smith SM (2001) A critical role of disproportionating enzyme in starch breakdown is revealed by a knock-out mutation in Arabidopsis. Plant J 26: 89-100
8. Dauvillée D, Kinderf IS, Li Z, Kosar-Hashemi B, Samuel MS, Rampling L, Ball S, Morell MK (2005) Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol 187: 1465-1473
9. Delatte T, Umhang M, Trevisan M, Eicke S, Thorneycroft D, Smith SM, Zeeman SC (2006) Evidence for distinct mechanisms of starch granule breakdown in plants. J Biol Chem 281: 12050-12059
10. Dumez S, Wattebled F, Dauvillee D, Delvalle D, Planchot V, Ball SG, D'Hulst C (2006) Mutants of Arabidopsis lacking starch branching enzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. Plant Cell 18: 2694-2709
11. Fettke J, Eckermann N, Kötting O, Ritte G, Steup M (2007) Novel starch-related enzymes and carbohydrates. Cell Mol Biol 52: OL883-OL904
12. Fordham-Skelton AP, Chilley P, Lumbreras V, Reignoux S, Fenton TR, Dahm CC, Montserrat P, Gatehouse JA (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
13. Hoover R (2001) Composition, molecular structure, and physicochemical properties of tuber and root starches: a review. Carbohydr Polymer 45: 253-267
14. Hussain H, Mant A, Seale R, Zeeman S, Hincliffe E, Edwards A, Hylton C, Bornemann S, Smith AM, Martin C, et al (2003) Three isoforms of isoamylase contribute different catalytic properties for debranching of potato glucans. Plant Cell 15: 133-149
15. Hussain MH (2002) Analysis of debranching enzymes from pea and potato. PhD thesis. University of East Anglia, Norwich, UK
16. Imberty A, Chanzy H, Perez S, Buleon A, Tran V (1988) The double-helical nature of the crystalline part of A-starch. J Mol Biol 201: 365-378
17. Kaplan F, Guy CL (2004) β-Amylase induction and the protective role of maltose during temperature shock. Plant Physiol 135: 1674-1684
18. Kaplan F, Guy CL (2005) RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 44: 730-743
19. Kerk D, Conley TR, Rodriguez FA, Tran HT, Nimick M, Muench DG, Moorhead GBG (2006) A chloroplast-localized dual-specificity protein phosphatase in Arabidopsis contains a phylogenetically dispersed and ancient carbohydrate-binding domain, which binds the polysaccharide starch. Plant J 46: 400-413
20. 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 (PWD). Plant Physiol 137: 242-252
21. Lao NT, Schoneveld O, Mould RM, Hibberd J, Gray JC, Kavanagh TA (1999) An Arabidopsis gene encoding a chloroplast-targeted β-amylase. Plant J 20: 519-527
22. Lloyd JR, Kossmann J, Ritte G (2005) Leaf starch degradation comes out of the shadows. Trends Plant Sci 10: 130-137
23. 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. Nat Biotechnol 16: 473-477
24. Mikkelsen R, Baunsgaard L, Blennow A (2004) Functional characterization of α-glucan, water dikinase, the starch phosphorylating enzyme. Biochem J 377: 525-532
25. Mikkelsen R, Mutenda KE, Mant A, Schürmann P, Blennow A (2005) α-Glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci USA 102: 1785-1790
26. Miles M, Morris VJ, Orford PD, Ring S (1985) The roles of amylose and amylopectin in the gelation and retrogradation of starch. Carbohydr Res 135: 271-281
27. Nakamura Y, Takahashi JI, Sakurai A, Inaba Y, Suzuki E, Satoko N, Fujiwara S, Tsuzuki M, Miyashita H, Ikemoto H, et al (2005) Some cyanobacteria synthesize semi-amylopectin type α-polyglucans instead of glycogen. Plant Cell Physiol 46: 539-545
28. Niittylä T, Comparot-Moss S, Lue WL, Messerli G, Trevisan M, Seymour MDJ, 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
29. 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
30. 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
31. Ritte G, Lorberth R, Steup M (2000) Reversible binding of the starch-related R1 protein to the surface of transitory starch granules. Plant J 21: 387-391
32. Ritte G, Scharf A, Eckermann N, Haebel S, Steup M (2004) Phosphorylation of transitory starch is increased during degradation. Plant Physiol 135: 2068-2077
33. Ritte G, Steup M, Kossmann J, Lloyd JR (2003) Determination of the starch-phosphorylating enzyme activity in plant extracts. Planta 216: 798-801
34. Scheidig A, Fröhlich A, Schulze S, Lloyd JR, Kossmann J (2002) Down-regulation of a chloroplast-targeted β-amylase leads to a starch-excess phenotype in leaves. Plant J 30: 581-591
35. Smith AM (2001) The biosynthesis of starch granules. Biomacromolecules 2: 335-341
36. Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56: 73-97
37. 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
38. Sokolov LN, Dominguez-Solis JR, Allary AL, Buchanan BB, Luan S (2006) A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc Natl Acad Sci USA 103: 9732-9737
39. Sparla F, Costa A, Schiavo FL, Pupillo P, Trost P (2006) Redox regulation of a novel plastid-targeted β-amylase of Arabidopsis. Plant Physiol 141: 840-850
40. Steup M, Robenek H, Melkonian M (1983) In vitro degradation of starch granules isolated from spinach chloroplasts. Planta 158: 428-436
41. Stitt M, Lilley RMcC, Gerhardt R, Heldt HW (1989) Metabolite levels in specific cells and subcellular compartments in plant leaves. Methods Enzymol 174: 518-552
42. Takeda Y, Hizukuri S (1981) Re-examination of the action of sweet-potato betaamylase on phosphorylated 1,4-α-D-glucan. Carbohydr Res 89: 174-178
43. Tetlow IJ, Morell MK, Emes MJ (2004) Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 55: 2131-2145
44. Waffenschmidt S, Jaenicke L (1987) Assay of reducing sugars in the nanomole range with 2,2′-bicinchoninate. Anal Biochem 165: 337-340
45. Wattebled F, Dong Y, Dumez S, Delvalle D, Planchot V, Berbezy P, Vyas D, Colonna P, Chatterjee M, Ball S, et al (2005) Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin. Plant Physiol 138: 184-195
46. Worby CA, Gentry MS, Dixon JE (2006) Laforin: a dual specificity phosphatase that dephosphorylates complex carbohydrates. J Biol Chem 281: 30412-30418
47. Yano R, Nakamura M, Yoneyama T, Nishida I (2005) Starch related α-glucan/water dikinase is involved in the cold induced development of freezing tolerance in Arabidopsis. Plant Physiol 138: 837-846
48. Yu TS, Kofler H, Häusler RE, Hille D, Flügge UI, Zeeman SC, Smith AM, Kossmann J, Lloyd J, Ritte G, et al (2001) The Arabidopsis sex1 mutant is defective in the R1 protein, a general regulator of starch degradation in plants, and not in the chloroplast hexose transporter. Plant Cell 13: 1907-1918
49. Yu TS, Zeeman SC, Thorneycroft D, Fulton DC, Dunstan H, Lue WL, Hegemann B, Tung SY, Umemoto T, Chapple A, et al (2005) α-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280: 9773-9779
50. Zeeman S, Smith SM, Smith AM (2007) The diurnal metabolism of leaf starch. Biochem J 401: 13-28
51. Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM (2004) Plastidial α-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135: 849-858