Analysis of the functional interaction of arabidopsis starch synthase and branching enzyme isoforms reveals that the cooperative action of SSI and BEs results in glucans with polymodal chain length distribution similar to amylopectin

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Brust, Henrike ^a   Lehmann, Tanja ^a   D'Hulst, Christophe ^b   Fettke, Joerg ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 ALPHA GLUCAN BRANCHING ENZYME; 1,4 ALPHA GLUCAN BRANCHING ENZYME 2 ISOFORM; 1,4 ALPHA GLUCAN BRANCHING ENZYME 3 ISOFORM; AMYLOPECTIN; CARBOHYDRATE; GLUCAN; GLUCAN 1,4 ALPHA GLUCOSIDASE; GLUCOSE; ISOAMYLASE; ISOENZYME; MUTANT PROTEIN; PHOSPHORYLASE; RECOMBINANT ENZYME; STARCH SYNTHASE; STARCH SYNTHASE I ISOFORM; STARCH SYNTHASE II ISOFORM; STARCH SYNTHASE III ISOFORM; STARCH SYNTHASE IV ISOFORM; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; RECOMBINANT PROTEIN; STARCH;

ARABIDOPSIS THALIANA; ARTICLE; CARBOHYDRATE SYNTHESIS; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; GENE INACTIVATION; GLUCOSE ASSAY; IN VITRO STUDY; ISOENZYME ANALYSIS; PLANT LEAF; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; TWO DIMENSIONAL ELECTROPHORESIS; WILD TYPE; ANALOGS AND DERIVATIVES; ARABIDOPSIS; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; SIGNAL TRANSDUCTION;

1,4-ALPHA-GLUCAN BRANCHING ENZYME; AMYLOPECTIN; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; ISOENZYMES; PLANT LEAVES; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STARCH; STARCH SYNTHASE;

EID: 84904257702     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0102364     Document Type: Article

References (75)

1. Ball SG, Morell MK (2003) From bacterial glycogen to starch: Understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54: 207-233. (Pubitemid 37399993)
2. Fettke J, Fernie AR, Steup M (2012) Transitory starch and its degradation in higher plant cells. In: Essential Reviews in Experimental Biol. Vol. 5: The Synthesis and Breakdown of Starch, I.J. Tetlow, ed., The Society for Experimental Biology, London, 309-372.
3. Jenkins PJ, Cameron RE, Donald AM (1993) A universal feature in the structure of starch granules from different botanical sources. Starch-Stärke 45: 417-420.
4. Keeling PL, Myers AM (2010) Biochemistry and genetics of starch synthesis. Annu Rev Food Sci Technol 1: 271-303.
5. Pérez S, Bertoft E (2010) The molecular structures of starch components and their contribution to the architecture of starch granules: a comprehensive review. Starch-Stärke 62: 389-420.
6. Chauhan F, Seetharaman K (2013) On the organization of chains in amylopectin. Starch-Stärke 65: 191-199.
7. Peat S, Whelan WJ, Thomas GJ (1952) Evidence of multiple branching in waxy maize starch. J Chem Soc Chem Commun 4546-4548.
8. Hizukuri S (1986) Polymodal distribution of the chain lengths of amylopectins, and its significance. Carbohydr Res 147: 342-347.
9. Hanashiro I, Abe J, Hizukuri S (1996) A periodic distribution of chain length of amylopectin as revealed by high-performance anion-exchange chromatography. Carbohydr Res 283: 151-159. (Pubitemid 26092496)
10. Bertoft E (2004) On the nature of categories of chains in amylopectin and their connection to the super helix model. Carbohydr Res 57: 211-224.
11. Fujita N, Nakamura Y (2012) Distinct and overlapping functions of starch synthase isoforms. In: Essential Reviews in Experimental Biology Vol. 5: The Synthesis and Breakdown of Starch, I.J Tetlow, ed., The Society for Experimental Biology, London, 115-140.
12. Tetlow IJ (2012) Branching enzymes and their role in determining structural and functional properties of polyglucans. In: Essential Reviews in Experimental Biology Vol. 5: The Synthesis and Breakdown of Starch, I.J Tetlow, ed., The Society for Experimental Biology, London, 144-178.
13. Brust H, Orzechowski S, Fettke J, Steup M (2013) Starch Synthesizing Reactions and Paths: in vitro and in vivo Studies. J Appl Glycosci 60: 3-20.
14. Delvallé D, Dumez S, Wattebled F, Roldán I, Planchot V, et al. (2005) Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. Plant J 43: 398-412. (Pubitemid 41577007)
15. Roldán I, Wattebled F, Lucas MM, Delvallé D, Planchot V, et al. (2007) The phenotype of soluble starch synthase IV defective mutants of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant J 49: 492-504. (Pubitemid 46146628)
16. Szydlowski N, Ragel P, Raynaud S, Lucas MM, Roldán I, et al. (2009) Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 21: 2443-2457.
17. Szydlowski N, Ragel P, Hennen-Bierwagen TA, Planchot V, Myers AM, et al. (2011) Integrated functions among multiple starch synthases determine both amylopectin chain length and branch linkage location in Arabidopsis leaf starch. J Exp Bot 62: 4547-4559.
18. Zhang X, Myers AM, James MG (2005) Mutations affecting starch synthase III in Arabidopsis alter leaf starch structure and increase the rate of starch synthesis. Plant Physiol 138: 663-674. (Pubitemid 43793149)
19. Zhang X, Szydlowski N, Delvallé D, D'Hulst C, James MG, et al. (2008) Overlapping functions of the starch synthases SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biol 8: 96.
20. Fujita N, Yoshida M, Asakura N, Ohdan T, Miyao A, et al. (2006) Function and characterization of starch synthase I using mutants in rice. Plant Physiol 140: 1070-1084. (Pubitemid 43956258)
21. McMaugh SJ, Thistleton JL, Anschaw E, Luo J, Konik-Rose C, et al. (2014) Suppression of starch synthase I expression affects the granule morphology and granule size and fine structure of starch in wheat endosperm. J Exp Bot 65: 2189-2201.
22. Yamamori M, Fujita S, Hayakawa K, Matsuki J, Yasui T (2000) Genetic elimination of a starch granule protein, SGP-1, of wheat generates an altered starch with apparent high amylase. Theor Appl Genet 101: 21-29. (Pubitemid 30483592)
23. Morell MK, Kosar-Hashemi B, Cmiel M, Samuel MS, Chandler P, et al. (2003) Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties. Plant J 34: 173-185. (Pubitemid 36536680)
24. Zhang X, Colleoni C, Ratushna V, Sirghie-Colleoni M, James MG, et al. (2004) Molecular characterization demonstrates that the Zea mays gene sugary2 codes for the starch synthase isoform SSIIa. Plant Mol Biol 54: 865-879. (Pubitemid 40134253)
25. Umemoto T, Yano M, Shomura A, Nakamura Y (2002) Mapping of a gene responsible for the difference in amylopectin structure between japonica-type and indica-type rice varieties. Theor Appl Genet 104: 1-8. (Pubitemid 36064853)
26. Commuri PD, Keeling PL (2001) Chain-length specificities of maize starch synthase I enzyme: studies of glucan affinity and catalytic properties. Plant J 25: 475-486.
27. Senoura T, Isono N, Yoshikawa M, Asao A, Hamada S, et al. (2004) Characterization of starch synthase I and II expressed in early developing seeds of kidney bean (Phaseolus vulgaris L.). Biosci Biotechnol Biochem 68: 1949-1960. (Pubitemid 39415264)
28. Fujita N, Goto S, Yoshida M, Suzuki E, Nakamura Y (2008) The function of rice starch synthase I expressed in E.coli. J Appl Glycosci 55: 167-172.
29. Burton RA, Bewley JD, Smith AM, Bhattacharyya MK, Tatge H, et al. (1995) Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. Plant J 7: 3-15.
30. Sawada T, Francisco PB Jr, Aihara S, Utsumi Y, Yoshida M, et al. (2009) Chlorella starch branching enzyme II (BEII) can complement the function of BEIIb in rice endosperm. Plant Cell Physiol 50: 1062-1074.
31. Dumez S, Wattebled F, Dauvillee D, Delvalle D, Planchot V, et al. (2006) Mutants of Arabidopsis Lacking Starch Branching Enzyme II Substitute Plastidial Starch Synthesis by Cytoplasmic Maltose Accumulation. Plant Cell 18: 2694-2709. (Pubitemid 44749898)
32. Gao M, Fisher DK, Kim K-N, Boyer CD, Guiltinan MJ (1997) Independent Genetic Control of Maize Starch-Branching Enzymes IIa and IIb: Isolation and Characterization of Sbe2a cDNA. Plant Physiol 114: 69-78. (Pubitemid 28110895)
33. Blauth SL, Yao Y, Klucinec JD, Shannon JC, Thompson DB, et al. (2001) Identification of Mutator insertional mutants of starch-branching enzyme 2a in corn. Plant Physiol 125: 1396-1405. (Pubitemid 32224628)
34. Nishi A, Nakamura Y, Tanaka N, Satoh H (2001) Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiol 127: 459-472. (Pubitemid 32996749)
35. Ohdan T, Francisco PB Jr, Sawada T, Hirose T, Terao T, et al. (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot 56: 3229-3244. (Pubitemid 41746673)
36. Yandeau-Nelson MD, Laurens L, Shi Z, Xia H, Smith AM, et al. (2011) Starch-branching enzyme IIa is required for proper diurnal cycling of starch in leaves of maize. Plant Physiol 156: 479-490.
37. Tetlow IJ, Beisel KG, Cameron S, Makhmoudova A, Liu F, et al. (2008) Analysis of protein complexes in amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiol 146: 1878-1891. (Pubitemid 352844055)
38. Hennen-Bierwagen TA, Liu F, Marsh R, Kim S, Gan Q, et al. (2008) Multiple starch biosynthetic enzymes from developing Zea mays endosperm associate in multisubunit complexes. Plant Physiol 146: 1892-1908. (Pubitemid 352844056)
39. Hennen-Bierwagen TA, Lin Q, Grimaud F, Planchot V, Keeling PL, et al. (2009) Proteins from multiple metabolic pathways associate with starch biosynthetic enzymes in high molecular weight complexes: a model for regulation of carbon allocation in maize amyloplasts. Plant Physiol 149: 1541-1559.
40. Liu F, Makhmoudova A, Lee EA, Wait R, Emes MJ, et al. (2009) The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. J Exp Bot 60: 4423-4440.
41. Liu F, Romanova N, Lee EA, Ahmed R, Evans M, et al. (2012) Glucan affinity of starch synthase IIa determines binding of starch synthase I and starch-branching enzyme IIb to starch granules. Biochem J 448: 373-387.
42. Liu F, Ahmed Z, Lee EA, Donner E, Liu Q, et al. (2012) Allelic variants of the amylose extender mutation of maize demonstrate phenotypic variation in starch structure resulting from modified protein-protein interactions. J Exp Bot 63: 1167-1183.
43. Fettke J, Malinova I, Albrecht T, Hejazi M, Steup M (2011) Glucose 1-phosphate transport into protoplasts and chloroplasts from leaves of Arabidopsis thaliana. Plant Physiol 155: 1723-1734.
44. Fettke J, Leifels L, Brust H, Herbst K, Steup M (2012) 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.
45. Stitt M, Lilley RM, Gerhardt R, Heldt HW (1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods Enzymol 174: 971-977.
46. Waffenschmidt S, Jaenicke L (1987) Assay of reducing sugars in the nanomolar range with 2,29-bicinchoninate. Anal Biochem 165: 377-340.
47. Malinova I, Mahlow S, Alseekh S, Orawetz T, Fernie AR, 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: 907-921.
48. Fettke J, Albrecht T, Hejazi M, Mahlow S, Nakamura Y, et al. (2010) Glucose 1-phosphate is efficiently taken up by potato (Solanum tuberosum) tuber parenchyma cells and converted to reserve starch granules. New Phytol 185: 663-675.
49. Tetlow IJ, Wait R, Lu Z, Akkasaeng R, Bowsher CG, et al. (2004) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions. Plant Cell 16: 694-708. (Pubitemid 38335279)
50. Boos W, Shuman H (1998) Maltose/maltodextrin system of Escherichia coli. Transport, metabolism, and regulation. Microbiol Mol Biol Rev 62: 204-229. (Pubitemid 28130801)
51. Park JT, Shim J H, Tran P L, Hong IH, Yong HU, et al. (2011) Role of maltose enzymes in glycogen synthesis by Escherichia coli. J Bacteriol 193: 2517-2526.
52. Hawker JS, Ozbun JL, Ozaki H, Greenberg E, Preiss J (1974) Interaction of spinach leaf adenosine diphosphate glucose α-1,4-glucan α-4-glucosyl transferase and α-1,4-glucan, α-1,4-glucan-6- glycosyl transferase in synthesis of branched α-glucan. Arch Biochem Biophys 160: 530-551.
53. Pollock C, Preiss J (1980) The citrate-stimulated starch synthase of starchy maize kernels: purification and properties. Arch Biochem Biophys 204: 578-588.
54. Guan HP, Preiss J (1993) Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiol 102: 1269-1273.
55. Takeda Y, Guan HP, Preiss J (1993) Branching of amylose by the branching isoenzymes of maize endosperm. Carbohydr Res 240: 253-263. (Pubitemid 23068373)
56. Yoshimoto Y, Takenouchi T, Takeda Y (2002) Molecular structure and some physicochemical properties of waxy and low-amylose barley starches. Carbohydr Polym 47: 159-167. (Pubitemid 33018657)
57. Ao Z, Jane J (2007) Characterization and modeling of the A- and B-granule starches of wheat, triticale, and barley. Carbohydr Polym 67: 46-55. (Pubitemid 44738025)
58. Bertoft E, Kallman A, Koch K, Andersson R, Aman P (2011) The cluster structure of barley amylopectins of different genetic backgrounds. Int J Biol Macromol 49: 441-453.
59. Franco CML, OgawaI C, Rabachini T, de Souza Rocha T, Cereda MP, et al. (2010) Effect of Lactic Acid and UV Irradiation on the Cassava and Corn Starches. Brazil Arch Biol Technol 53: 443-454.
60. Gomand SV, Lamberts L, Derde LJ, Goesaert H, Vandeputte GE, et al. (2010) Structural properties and gelatinisation characteristics of potato and cassava starches and mutants thereof. Food Hydrocoll 24: 307-317.
61. Yasui T, Sasaki T, Matsuki J (2005) Variation in the Chain-length Distribution Profiles of Endosperm Starch from Triticum and Aegilops Species. Starch-Stärke 57: 521-530. (Pubitemid 41665086)
62. Broberg S, Koch K, Andersson R, Kenne L (2000) A comparison between MALDI-TOF mass spectrometry and HPAEC-PAD analysis of debranched starch. Carbohydr Polym 43: 285-289.
63. Yoo SH, Jane JL (2002) Structural and physical characteristics of waxy and other wheat starches. Carbohydr Polym 49: 297-305.
64. Hanashiro I, Ikeda I, Yamamori M, Takeda Y (2004) Increased amylose content and altered molecular structures of wheat starch by SGP-1 null mutation. J Appl Glycosci 51: 217-221.
65. Konik-Rose C, Thistleton J, Chanvrier H, Tan I,•Halley P, et al. (2007) Effects of starch synthase IIa gene dosage on grain, protein and starch in endosperm of wheat. Theor Appl Genet 115: 1053-1065. (Pubitemid 350043561)
66. Vrinten PL, Shimbata T, Yanase M, Sunohara A, Saito M, et al. (2012) Properties of a novel type of starch found in the double mutant "sweet wheat". Carbohydr Polym 89: 1250-1260.
67. Kalinga DN, Waduge R, Liu Q, Yada RY, Bertoft E, et al. (2013) On the differences in the granular architecture and starch structure between pericarp and endosperm wheat starches. Starch-Stärke 65: 791-800.
68. Lin Q, Huang B, Zhang M, Zhang X, Rivenbark J, et al. (2012) Functional interactions between starch synthase III and isoamylase-type starch-debranching enzyme in maize endosperm. Plant Physiol 158: 679-692.
69. Gérard C, Planchot V, Colonna P, Bertoft E (2000) Relationship between branching density and crystalline structure of A- and B-type maize mutant starches. Carbohydr Res 326: 130-144. (Pubitemid 30326731)
70. Jobling SA, Westcott RJ, Tayal A, Jeffcoat R, Schwall GP (2002) Production of a freeze-thaw-stable potato starch by antisense inhibition of three starch synthase genes. Nat Biotechnol 20: 295-299. (Pubitemid 34205424)
71. Crofts N, Abe K, Aihara S, Itoh R, Nakamura Y, et al. (2012) Lack of starch synthase IIIa and high expression of granule-bound starch synthase I synergistically increase the apparent amylose content in rice endosperm. Plant Science 193: 62-69.
72. Fujita N, Yoshida M, Kondo T, Saito K, Utsumi Y, et al. (2007) Characterization of SSIIIa-deficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm. Plant Physiol 144: 2009-2023. (Pubitemid 47258115)
73. Li Z, Li D, Du X, Wang H, Larroque O, et al. (2011) The barley amo1 locus is tightly linked to the starch synthase IIIa gene and negatively regulates expression of granule-bound starch synthetic genes. J Exp Bot 62: 5217-5231.
74. Cao H, Imparl-Radosevich J, Guan H, Keeling PL, James MG, et al. (1999) Identification of the soluble starch synthase activities of maize endosperm. Plant Physiol 120: 205-216.
75. Cuevas RP, Daygon VD, Morell MK, Gilbert RG, Fitzgerald MA (2010) Using chain-length distributions to diagnose genetic diversity in starch biosynthesis. Carbohydr Polym 81: 120-127.