Phosphoglucan phosphatase function sheds light on starch degradation

Trends in Plant Science

Volumn 19, Issue 7, 2014, Pages 471-478

  Silver, Dylan M ^a   Kötting, Oliver ^b   Moorhead, Greg B G ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b ETH ZURICH   (Switzerland)

Author keywords

Dual specificity phosphatase; Phosphoglucan phosphatase; Phosphorylation; Redox; Starch degradation

Indexed keywords

ARABIDOPSIS PROTEIN; GLUCAN; PHOSPHATASE; PHOSPHATE; STARCH;

AMINO ACID SEQUENCE; ARABIDOPSIS; CHEMISTRY; LIGHT; METABOLISM; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PHOSPHORYLATION; PLANT LEAF; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GLUCANS; LIGHT; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHOSPHATES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PLANT LEAVES; SEQUENCE ALIGNMENT; STARCH;

EID: 84903618324     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2014.01.008     Document Type: Review

References (80)

1. Tonks N.K. Protein tyrosine phosphatases: from housekeeping enzymes to master regulators of signal transduction. FEBS J. 2013, 280:346-378.
2. Brautigan D.L. Protein Ser/Thr phosphatases: the ugly ducklings of cell signalling. FEBS J. 2013, 280:324-345.
3. Moorhead G.B., et al. Evolution of protein phosphatases in plants and animals. Biochem. J. 2009, 417:401-409.
4. Kerk D., et al. Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol. 2008, 146:351-367.
5. Gentry M.S., et al. Laforin, a protein with many faces: glucan phosphatase, adapter protein, et alii. FEBS J. 2013, 280:525-537.
6. Tagliabracci V.S., et al. Phosphate incorporation during glycogen synthesis and Lafora disease. Cell Metab. 2011, 13:274-282.
7. Sokolov L.N., et al. A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:9732-9737.
8. Kerk D., et al. 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. 2006, 46:400-413.
9. Niittyla T., et al. Similar protein phosphatases control starch metabolism in plants and glycogen metabolism in mammals. J. Biol. Chem. 2006, 281:11815-11818.
10. Comparot-Moss S., et al. A putative phosphatase, LSF1, is required for normal starch turnover in Arabidopsis leaves. Plant Physiol. 2010, 152:685-697.
11. Santelia D., et al. The phosphoglucan phosphatase like sex four2 dephosphorylates starch at the C3-position in Arabidopsis. Plant Cell 2011, 23:4096-4111.
12. Vander Kooi C.W., et al. Structural basis for the glucan phosphatase activity of Starch Excess4. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15379-15384.
13. Hsu S., et al. Structural insights into glucan phosphatase dynamics using amide hydrogen-deuterium exchange mass spectrometry. Biochemistry 2009, 48:9891-9902.
14. Guillen D., et al. Carbohydrate-binding domains: multiplicity of biological roles. Appl. Microbiol. Biotechnol. 2010, 85:1241-1249.
15. Schuhmann H., et al. The family of Deg/HtrA proteases in plants. BMC Plant Biol. 2012, 12:52.
16. Lee H.J., Zheng J.J. PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun. Signal. 2010, 8:8.
17. Gardiner J., et al. PDZ domain proteins: 'dark matter' of the plant proteome?. Mol. Plant 2011, 4:933-937.
18. Zeeman S.C., et al. The diurnal metabolism of leaf starch. Biochem. J. 2007, 401:13-28.
19. Buléon A., et al. Starch granules: structure and biosynthesis. Int. J. Biol. Macromol. 1998, 23:85-112.
20. Pérez S., Bertoft E. The molecular structures of starch components and their contribution to the architecture of starch granules: a comprehensive review. Starch 2010, 62:389-420.
21. Smith A.M., et al. Starch degradation. Annu. Rev. Plant Biol. 2005, 56:73-98.
22. Blennow A., et al. The distribution of covalently bound phosphate in the starch granule in relation to starch crystallinity. Int. J. Biol. Macromol. 2000, 27:211-218.
23. Blennow A., et al. Starch phosphorylation: a new front line in starch research. Trends Plant Sci. 2002, 7:445-450.
24. Takeda Y., Hizukuri S. Location of phosphate groups in potato amylopectin. Carbohydr. Res. 1982, 102:321-327.
25. Ritte G., et al. Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Lett. 2006, 580:4872-4876.
26. Haebel S., et al. Mass spectrometric quantification of the relative amounts of C6 and C3 position phosphorylated glucosyl residues in starch. Anal. Biochem. 2008, 379:73-79.
27. Kötting O., et al. STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 2009, 21:334-346.
28. Blennow A., Engelsen S.B. Helix-breaking news: fighting crystalline starch energy deposits in the cell. Trends Plant Sci. 2010, 15:236-240.
29. Ritte G., et al. Phosphorylation of transitory starch is increased during degradation. Plant Physiol. 2004, 135:2068-2077.
30. Hejazi M., et al. The two plastidial starch-related dikinases sequentially phosphorylate glucosyl residues at the surface of both the A- and B-type allomorphs of crystallized maltodextrins but the mode of action differs. Plant Physiol. 2009, 150:962-976.
31. Nitschke F., et al. Hyperphosphorylation of glucosyl C6 carbons and altered structure of glycogen in the neurodegenerative epilepsy Lafora disease. Cell Metab. 2013, 17:756-767.
32. Takeda Y., Hizukuri S. Reexamination of the action of sweet-potato beta-amylase on phosphorylated (1→4)-α-D-glucan. Carbohydr. Res. 1981, 89:174-178.
33. Hejazi M., et al. 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 alpha-glucans. Plant Physiol. 2010, 152:711-722.
34. Kötting O., et al. Regulation of starch metabolism: the age of enlightenment?. Curr. Opin. Plant Biol. 2010, 13:321-329.
35. Zeeman S.C., et al. A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 1998, 10:1699-1712.
36. Zeeman S.C., ap Rees T. Changes in carbohydrate metabolism and assimilate export in starch-excess mutants of Arabidopsis. Plant Cell Environ. 1999, 22:1445-1453.
37. Zeeman S.C., et al. A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J. 1998, 15:357-365.
38. Edner C., et al. Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial beta-amylases. Plant Physiol. 2007, 145:17-28.
39. Robinson F.L., Dixon J.E. Myotubularin phosphatases: policing 3-phosphoinositides. Trends Cell Biol. 2006, 16:403-412.
40. Gentry M.S., et al. The phosphatase laforin crosses evolutionary boundaries and links carbohydrate metabolism to neuronal disease. J. Cell Biol. 2007, 178:477-488.
41. Silver D.M., et al. Insight into the redox regulation of the phosphoglucan phosphatase SEX4 involved in starch degradation. FEBS J. 2013, 280:538-548.
42. Tiessen A., et al. 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 2002, 14:2191-2213.
43. Hendriks J.H., et al. ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species. Plant Physiol. 2003, 133:838-849.
44. Mikkelsen R., et al. α-glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:1785-1790.
45. Sparla F., et al. Redox regulation of a novel plastid-targeted beta-amylase of Arabidopsis. Plant Physiol. 2006, 141:840-850.
46. Seung D., et al. Arabidopsis thaliana AMY3 Is a unique redox-regulated chloroplastic α-amylase. J. Biol. Chem. 2013, 288:33620-33633.
47. Glaring M.A., et al. Comprehensive survey of redox sensitive starch metabolising enzymes in Arabidopsis thaliana. Plant Physiol. Biochem. 2012, 58:89-97.
48. Meekins D.A., et al. Structure of the Arabidopsis glucan phosphatase LIKE SEX FOUR2 reveals a unique mechanism for starch dephosphorylation. Plant Cell 2013, 25:2302-2314.
49. Kerk D., et al. The complement of protein phosphatase catalytic subunits encoded in the genome of Arabidopsis. Plant Physiol. 2002, 129:908-925.
50. Fordham-Skelton A.P., et al. A novel higher plant protein tyrosine phosphatase interacts with SNF1-related protein kinases via a KIS (kinase interaction sequence) domain. Plant J. 2002, 29:705-715.
51. Zhang Z.Y., Dixon J.E. Active site labeling of the Yersinia protein tyrosine phosphatase: the determination of the pK of the active site cysteine and the function of the conserved histidine 402. Biochemistry 1993, 32:9340-9345.
52. Li J., et al. Catalytically-inactive beta-amylase BAM4 required for starch breakdown in Arabidopsis leaves is a starch-binding-protein. Arch. Biochem. Biophys. 2009, 489:92-98.
53. Fulton D.C., et al. Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts. Plant Cell 2008, 20:1040-1058.
54. Streb S., Zeeman S.C. Starch metabolism in Arabidopsis. Arabidopsis Book 2012, 10:e0160.
55. Delatte T., et al. 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. 2005, 41:815-830.
56. Kerk D., Moorhead G.B. A phylogenetic survey of myotubularin genes of eukaryotes: distribution, protein structure, evolution, and gene expression. BMC Evol. Biol. 2010, 10:196.
57. Tonks N.K. Protein tyrosine phosphatases: from genes, to function, to disease. Nat. Rev. Mol. Cell Biol. 2006, 7:833-846.
58. Hung A.Y., Sheng M. PDZ domains: structural modules for protein complex assembly. J. Biol. Chem. 2002, 277:5699-5702.
59. Harris B.Z., Lim W.A. Mechanism and role of PDZ domains in signaling complex assembly. J. Cell Sci. 2001, 114:3219-3231.
60. Blennow A., et al. The degree of starch phosphorylation is related to the chain length distribution of the neutral and the phosphorylated chains of amylopectin. Carbohydr. Res. 1998, 307:45-54.
61. Wen Y., et al. Mammalian capping enzyme binds RNA and uses protein tyrosine phosphatase mechanism. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:12226-12231.
62. Begley M.J., Dixon J.E. The structure and regulation of myotubularin phosphatases. Curr. Opin. Struct. Biol. 2005, 15:614-620.
63. Patterson K.I., et al. Dual-specificity phosphatases: critical regulators with diverse cellular targets. Biochem. J. 2009, 418:475-489.
64. Lee J.O., et al. Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association. Cell 1999, 99:323-334.
65. Singh A., et al. Protein phosphatase complement in rice: genome-wide identification and transcriptional analysis under abiotic stress conditions and reproductive development. BMC Genomics 2010, 11:435.
66. Denu J.M., Dixon J.E. Protein tyrosine phosphatases: mechanisms of catalysis and regulation. Curr. Opin. Biotechnol. 1998, 2:633-641.
67. Denu J.M., et al. Form and function in protein dephosphorylation. Cell 1996, 87:361-364.
68. Denu J.M., et al. Visualization of intermediate and transition-state structures in protein-tyrosine phosphatase catalysis. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:2493-2498.
69. Peters G.H., et al. Electrostatic evaluation of the signature motif (H/V)CX5R(S/T) in protein-tyrosine phosphatases. Biochemistry 1998, 37:5383-5393.
70. Denu J.M., Tanner K.G. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 1998, 37:5633-5642.
71. Salmeen A., Barford D. Functions and mechanisms of redox regulation of cysteine-based phosphatases. Antioxid. Redox Signal. 2005, 7:560-577.
72. Salmeen A., et al. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 2003, 423:769-773.
73. Meng T.C., et al. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 2002, 9:387-399.
74. Gupta R., Luan S. Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol. 2003, 132:1149-1152.
75. Punta M., et al. The Pfam protein families database. Nucleic Acids Res. 2012, 40:D290-D301.
76. Letunic I., et al. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 2012, 40:D302-D305.
77. Cho K.O., et al. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 1992, 9:929-942.
78. Woods D.F., Bryant P.J. The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 1991, 66:451-464.
79. Itoh M., et al. The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J. Cell Biol. 1993, 121:491-502.
80. Schrodinger, L.L.C. (2010) The PyMOL Molecular Graphics System, Version 1.3r1.