Integrated functions among multiple starch synthases determine both amylopectin chain length and branch linkage location in Arabidopsis leaf starch

Journal of Experimental Botany

Volumn 62, Issue 13, 2011, Pages 4547-4559

  Szydlowski, Nicolas ^a   Ragel, Paula ^b   Hennen Bierwagen, Tracie A ^c   Planchot, Véronique ^d   Myers, Alan M ^c   Mérida, Angel ^b   D'Hulst, Christophe ^a   Wattebled, Fabrice ^a  

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

^b UNIVERSITY OF SEVILLE   (Spain)

^c IOWA STATE UNIVERSITY   (United States)

^d INRA   (France)

Author keywords

Amylopectin; amylose; branching; chain length distribution; glucans; SS1; SS2; SS3; starch; starch synthases

Indexed keywords

AMYLOPECTIN; AMYLOSE; PLANT EXTRACT; STARCH SYNTHASE;

ARABIDOPSIS; ARTICLE; CHEMISTRY; ENZYMOLOGY; FRACTIONATION; GEL CHROMATOGRAPHY; GENETICS; METABOLISM; MUTATION; PLANT LEAF; SOLUBILITY; ULTRASTRUCTURE;

AMYLOPECTIN; AMYLOSE; ARABIDOPSIS; CHEMICAL FRACTIONATION; CHROMATOGRAPHY, GEL; MUTATION; PLANT EXTRACTS; PLANT LEAVES; SOLUBILITY; STARCH SYNTHASE;

ARABIDOPSIS;

EID: 80052898059     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err172     Document Type: Article

References (37)

1. Ball SG, van de Wal MHBJ, Visser RGF. 1998. Progress in understanding the biosynthesis of amylose. Trends in Plant Science 3, 462-467. (Pubitemid 29014649)
2. Bertoft E, Piyachomkwan K, Chatakanonda P, Sriroth K. 2008. Internal unit chain composition in amylopectins. Carbohydrate Polymers 74, 527-543.
3. Buleon A, Colonna P, Planchot V, Ball S. 1998. Starch granules: structure and biosynthesis. International Journal of Biological Macromolecules 23, 85-112. (Pubitemid 28396136)
4. Commuri PD, Keeling PL. 2001. Chain-length specificities of maize starch synthase I enzyme: studies of glucan affinity and catalytic properties. The Plant Journal 25, 475-486. (Pubitemid 32442247)
5. Dauvillee 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. Journal of Bacteriology 187, 1465-1473. (Pubitemid 40299470)
6. Delrue B, Fontaine T, Routier F, Decq A, Wieruszeski JM, Van Den Koornhuyse N, Maddelein ML, Fournet B, Ball S. 1992. Waxy Chlamydomonas reinhardtii: monocellular algal mutants defective in amylose biosynthesis and granule-bound starch synthase activity accumulate a structurally modified amylopectin. Journal of Bacteriology 174, 3612-3620.
7. Delvallé D, Dumez S, Wattebled F, et al. 2005. Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. The Plant Journal 43, 398-412. (Pubitemid 41577007)
8. Deschamps P, Moreau H, Worden AZ, Dauvillee D, Ball SG. 2008. Early gene duplication within chloroplastida and its correspondence with relocation of starch metabolism to chloroplasts. Genetics 178, 2373-2387.
9. Dumez S, Wattebled F, Dauvillee D, Delvalle D, Planchot V, Ball SG, D'Hulst C. 2006. Mutants of Arabidopsis lacking Starch Branching Eenzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. The Plant Cell 18, 2694-2709. (Pubitemid 44749898)
10. Edwards A, Fulton DC, Hylton CM, Jobling SA, Gidley M, Rö ssner U, Martin C, Smith AM. 1999. A combined reduction in activity of starch synthases II and III of potato has novel effects on the starch of tubers. The Plant Journal 17, 251-261.
11. Fontaine T, D'Hulst C, Maddelein M, Routier F, Pepin T, Decq A, Wieruszeski J, Delrue B, Van den Koornhuyse N, Bossu J. 1993. Toward an understanding of the biogenesis of the starch granule. Evidence that Chlamydomonas soluble starch synthase II controls the synthesis of intermediate size glucans of amylopectin. Journal of Biological Chemistry 268, 16223-16230. (Pubitemid 23229919)
12. Guan H, Li P, Imparl-Radosevich J, Preiss J, Keeling P. 1997. Comparing the properties of Escherichia coli branching enzyme and maize branching enzyme. Archives of Biochemistry and Biophysics 342, 92-98. (Pubitemid 27217105)
13. Guan HP, Baba T, Preiss J. 1994. Expression of branching enzyme I of maize endosperm in Escherichia coli. Plant Physiology 104, 1449-1453.
14. Guan HP, Preiss J. 1993. Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiology 102, 1269-1273.
15. Hennen-Bierwagen TA, Lin Q, Grimaud F, Planchot V, Keeling PL, James MG, Myers AM. 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 Physiology 149, 1541-1559.
16. Hennen-Bierwagen TA, Liu F, Marsh RS, Kim S, Gan Q, Tetlow IJ, Emes MJ, James MG, Myers AM. 2008. Starch biosynthetic enzymes from developing maize endosperm associate in multisubunit complexes. Plant Physiology 146, 1892-1908. (Pubitemid 352844056)
17. Hizukuri S. 1986. Polymodal distribution of the chain lengths of amylopectin, and its significance. Carbohydrate Research 147, 342-347.
18. Imparl-Radosevich JM, Nichols DJ, Li P, McKean AL, Keeling PL, Guan H. 1999. Analysis of purified maize starch synthases IIa and IIb: SS isoforms can be distinguished based on their kinetic properties. Archives of Biochemistry and Biophysics 362, 131-138. (Pubitemid 29391659)
19. 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. Nature Biotechnology 20, 295-299. (Pubitemid 34205424)
20. Laby RJ, Kim D, Gibson SI. 2001. The ram1 mutant of Arabidopsis exhibits severely decreased b-amylase activity. Plant Physiology 127, 1798-1807. (Pubitemid 34050043)
21. Liu F, Makhmoudova A, Lee EA, Wait R, Emes MJ, Tetlow IJ. 2009. The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. Journal of Experimental Botany 60, 4423-4440.
22. Lloyd JR, Landschü tze V, Kossmann J. 1999 a. Simultaneous antisense inhibition of two starch-synthase isoforms in potato tubers leads to accumulation of grossly modified amylopectin. Biochemical Journal 338, 515-521.
23. Lloyd JR, Springer F, Buleon A, Müller-Rober B, Willmitzer L, Kossmann J. 1999 b. The influence of alterations in ADP-glucose pyrophosphorylase activities on starch structure and composition in potato tubers. Planta 209, 230-238.
24. Myers AM, Morell MK, James MG, Ball SG. 2000. Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiology 122, 989-997. (Pubitemid 30221378)
25. Perez S, Bertoft E. 2010. The molecular structures of starch components and their contribution to the architecture of starch granules: a comprehensive review. Starch-Starke 62, 389-420.
26. Roldan I, Wattebled F, Lucas MM, Delvalle D, Planchot V, Jimenez S, Perez R, Ball S, D'Hulst C, Merida A. 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. The Plant Journal 49, 492-504. (Pubitemid 46146628)
27. Rothblatt JA, Deshaies RJ, Sanders SL, Daum G, Schekman R. 1989. Multiple genes are required for proper insertion of secretory proteins into the endoplasmic reticulum in yeast. Journal of Cell Biology 109, 2641-2652. (Pubitemid 20011893)
28. Singletary GW, Banisadr R, Keeling PL. 1997. Influence of gene dosage on carbohydrate synthesis and enzymatic activities in endosperm of starch-deficient mutants of maize. Plant Physiology 113, 293-304. (Pubitemid 27111461)
29. Szydlowski N, Ragel P, Raynaud S, et al. 2009. Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. The Plant Cell 21, 2443-2457.
30. Tetlow IJ, Beisel KG, Cameron S, Makhmoudova A, Liu F, Bresolin NS, Wait R, Morell MK, Emes MJ. 2008. Analysis of protein complexes in wheat amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiology 146, 1878-1891. (Pubitemid 352844055)
31. 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 Physiology 138, 184-195. (Pubitemid 43138119)
32. Wattebled F, Planchot V, Dong Y, Szydlowski N, Pontoire B, Devin A, Ball S, D'Hulst C. 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 Physiology 148, 1309-1323. (Pubitemid 352847493)
33. Zeeman SC, Northrop F, Smith AM, ap Rees T. 1998. A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. The Plant Journal 15, 357-365.
34. Zeeman SC, Tiessen A, Pilling E, Kato KL, Donald AM, Smith AM. 2002. Starch synthesis in Arabidopsis. Granule synthesis, composition, and structure. Plant Physiology 129, 516-529. (Pubitemid 34689141)
35. Zeeman SC, Smith SM, Smith AM. 2007. The diurnal metabolism of leaf starch. Biochemical Journal 401, 13-28. (Pubitemid 46114596)
36. 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 Physiology 138, 663-674. (Pubitemid 43793149)
37. Zhang X, Szydlowski N, Delvallé D, D'Hulst C, James MG, Myers AM. 2008. Overlapping functions of the starch synthases SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biology 8, 96.