Explain one way in which starch molecules are adapted for their function in plant cells

Explain one way in which starch molecules are adapted for their function in plant cells

Unlike humans, plants are not able to eat food in order to meet their energy needs, instead they have to make their energy by photosynthesis.

As every GCSE student can tell you, photosynthesis is the process through which light energy is converted into either chemical energy or sugar. When it is converted to sugar, that is in turn used by the plant for things like respiration, growth and reproduction. Some of the sugar is also stored for use later, by being converted into starch.

Plants make, and store temporary supplies of starch in their leaves, which they use during the night when there is no light available for photosynthesis. Many plants, including crop plants like wheat and potatoes, also make starch in their seeds and storage organs (their grains and tubers), which is used for germination and sprouting.

But what exactly is starch? Starch is a chain of glucose molecules which are bound together, to form a bigger molecule, which is called a polysaccharide. There are two types of polysaccharide in starch:

  • Amylose – a linear chain of glucose
  • Amylopectin – a highly branched chain of glucose

Depending on the plant, starch is made up of between 20-25% amylose and 75-80% amylopectin.

As well as being important for plants, starch is also extremely important to humans. Starchy food for example is the main source of digestible carbohydrates in our diet.

The structure of starch can affect digestibility, with high amylose being more resistant to degradation. As such, foods with high levels of amylose are an important source of ‘resistant starch’, which has the potential to provide a range of health benefits by lowering elevated blood glucose levels and insulin response to carbohydrate-based meals that are low in fibre.

Starch also has many non-food applications, including use within the papermaking industry (providing strength to paper), manufacturing of adhesives, the textile industry (as a stiffener), and the production of bioplastics.

The many varied uses of starch depend on its structure, with granule shape and size affecting the properties of starch, and therefore its uses.  For this reason, it is important for us to understand more about starch granules; including how starch polymer growth is directed, how different shaped and sized granules are formed, and how the plant controls the number of granules made.

A lot of our understanding about starch initiation and formation in leaves has come from work on the model plant Arabidopsis thaliana.

However, there is still a lot of work to do to understand granule initiation and formation within cereal grains. As cereals are one of the major food crops, and a major source of starch for industrial processes, understanding granule initiation and formation in grains is crucial.

At the John Innes Centre we are using a large mutant collection of wheat to investigate the granule initiation and have already isolated several promising mutants with radically altered starch granules. By investigating these further, we hope to identify key candidates involved in granule initiation in wheat, which may allow the development of new tools to improve crop quality and tailor starch production properties for different uses.

1. Ellis RP, Cochrane MP, Dale MFB, Duþus CM, Lynn A, Morrison IM, Prentice RDM, Swanston JS, Tiller SA. Starch production and industrial use. J Sci Food Agric. 1998;77:289–311. doi: 10.1002/(SICI)1097-0010(199807)77:3<289::AID-JSFA38>3.0.CO;2-D. [CrossRef] [Google Scholar]

2. Blennow A, Bay-Smidt AM, Leonhardt P, Bandsholm O, Madsen MH. Starch paste stickiness is a relevant native starch selection criterion for wet-end paper manufacturing. Starch/Stärke. 2003;55:381–389. doi: 10.1002/star.200300169. [CrossRef] [Google Scholar]

3. Zhang Y, Rempel C, Liu Q. Thermoplastic starch processing and characteristics—a review. Crit Rev Food Sci Nutr. 2014;54:1353–1370. doi: 10.1080/10408398.2011.636156. [PubMed] [CrossRef] [Google Scholar]

4. Pal SK, Liput M, Piques M, Ishihara H, Obata T, Martins MCM, Sulpice R, et al. Diurnal changes of polysome loading track sucrose content in the rosette of wild-type Arabidopsis and the starchless pgm mutant. Plant Physiol. 2013;162:1246–1265. doi: 10.1104/pp.112.212258. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

5. Fujita N, Satoh R, Hayashi A, Kodama M, Itoh R, Aihara S, Nakamura Y. Starch biosynthesis in rice endosperm requires the presence of either starch synthase I or IIIa. J Exp Bot. 2011;62:4819–4831. doi: 10.1093/jxb/err125. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

6. Abe N, Asai H, Yago H, Oitome NF, Itoh R, Crofts N, Nakamura Y, Fujita N. Relationships between starch synthase I and branching enzyme isozymes determined using double mutant rice lines. BMC Plant Biol. 2014;14:80. doi: 10.1186/1471-2229-14-80. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

7. Lafiandra D, Riccardi G, Shewry PR. Improving cereal grain carbohydrates for diet and health. J Cereal Sci. 2014;59:312–326. doi: 10.1016/j.jcs.2014.01.001. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

8. Ceballos H, Sánchez T, Morante N, Fregene M, Dufour D, Smith AM, Denyer K, Pérez JC, Calle F, Mestres C. Discovery of an amylose-free starch mutant in cassava (Manihot esculenta Crantz) J Agric Food Chem. 2007;55:7469–7476. doi: 10.1021/jf070633y. [PubMed] [CrossRef] [Google Scholar]

9. Wang K, Henry RJ, Gilbert RG. Causal relations among starch biosynthesis, structure, and properties. Springer Sci Rev. 2014;2:15–33. doi: 10.1007/s40362-014-0016-0. [CrossRef] [Google Scholar]

10. Tharanathan RN. Starch—value addition by modification. Crit Rev Food Sci Nutr. 2005;45:371–384. doi: 10.1080/10408390590967702. [PubMed] [CrossRef] [Google Scholar]

11. Raigond P, Ezekiel R, Raigond B. Resistant starch in food: a review. J Sci Food Agric. 2014;95:1968–1978. doi: 10.1002/jsfa.6966. [PubMed] [CrossRef] [Google Scholar]

12. Pérez S, Bertoft E. The molecular structures of starch components and their contribution to the architecture of starch granules: a comprehensive review. Starch/Stärke. 2010;62:389–420. doi: 10.1002/star.201000013. [CrossRef] [Google Scholar]

13. Manners DJ. Recent developments in our understanding of amylopectin structure. Carbohydr Polym. 1989;11:87–112. doi: 10.1016/0144-8617(89)90018-0. [CrossRef] [Google Scholar]

14. French D. Fine structure of starch and its relationship to the organisation of starch granules. J Jpn Soc Starch Sci. 1972;19:8–25. doi: 10.5458/jag1972.19.8. [CrossRef] [Google Scholar]

15. Nikuni Z. Studies on starch granules. Starch/Stärke. 1978;30:105–111. doi: 10.1002/star.19780300402. [CrossRef] [Google Scholar]

16. Hizukuri S. Polymodal distribution of the chain lengths of amylopectins, and its significance. Carbohydr Res. 1986;147:342–347. doi: 10.1016/S0008-6215(00)90643-8. [CrossRef] [Google Scholar]

17. Bertoft E. On the nature of categories of chains in amylopectin and their connection to the super helix model. Carbohydr Polym. 2004;57:211–224. doi: 10.1016/j.carbpol.2004.04.015. [CrossRef] [Google Scholar]

18. Jenkins PJ, Cameron RE, Donald AM. A universal feature in the structure of starch granules from different botanical sources. Starch/Stärke. 1993;45:417–420. doi: 10.1002/star.19930451202. [CrossRef] [Google Scholar]

19. Kassenbeck P. Beitrag zur Kenntnis der Verteilung von Amylose und Amylopektin in Stärkekörnern. Starch/Stärke. 1978;30:40–46. doi: 10.1002/star.19780300203. [CrossRef] [Google Scholar]

20. Imberty A, Perez S. A revisit to the three-dimensional structure of B-type starch. Biopolymers. 1988;27:1205–1221. doi: 10.1002/bip.360270803. [CrossRef] [Google Scholar]

21. Imberty A, Chanzy H, Pérez S, Buléon A, Tran V. The double-helical nature of the crystalline part of A-starch. J Mol Biol. 1988;201:365–378. doi: 10.1016/0022-2836(88)90144-1. [PubMed] [CrossRef] [Google Scholar]

22. Pilling E, Smith AM. Growth ring formation in the starch granules of potato tubers. Plant Physiol. 2003;132:365–371. doi: 10.1104/pp.102.018044. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

23. Gallant DJ, Bouchet B, Baldwin PM. Microscopy of starch: evidence of a new level of granule organization. Carbohydr Polym. 1997;32:177–191. doi: 10.1016/S0144-8617(97)00008-8. [CrossRef] [Google Scholar]

24. Oostergetel GT, van Bruggen EFJ. The crystalline domains in potato starch granules are arranged in a helical fashion. Carbohydr Polym. 1993;21:7–12. doi: 10.1016/0144-8617(93)90110-P. [CrossRef] [Google Scholar]

25. Jane J-L, Kasemsuwan T, Leas S, Zobel H, Robyt JF. Anthology of starch granule morphology by scanning electron microscopy. Starch/Stärke. 1994;46:121–129. doi: 10.1002/star.19940460402. [CrossRef] [Google Scholar]

26. Zeeman SC, Tiessen A, Pilling E, Kato KL, Donald AM, Smith AM. Starch synthesis in Arabidopsis. Granule synthesis, composition, and structure. Plant Physiol. 2002;129:516–529. doi: 10.1104/pp.003756. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

27. Buléon A, Cotte M, Putaux J-L, D’Hulst C, Susini J. Tracking sulfur and phosphorus within single starch granules using synchrotron X-ray microfluorescence mapping. Biochim Biophys Acta. 2014;1840:113–119. doi: 10.1016/j.bbagen.2013.08.029. [PubMed] [CrossRef] [Google Scholar]

28. Grimaud F, Rogniaux H, James MG, Myers AM, Planchot V. Proteome and phosphoproteome analysis of starch granule-associated proteins from normal maize and mutants affected in starch biosynthesis. J Exp Bot. 2008;59:3395–3406. doi: 10.1093/jxb/ern198. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

29. Blennow A, Bay-Smidt AM, Olsen CE, Møller BL. The distribution of covalently bound phosphate in the starch granule in relation to starch crystallinity. Int J Biol Macromol. 2000;27:211–218. doi: 10.1016/S0141-8130(00)00121-5. [PubMed] [CrossRef] [Google Scholar]

30. Santelia D, Zeeman SC. Progress in Arabidopsis starch research and potential biotechnological applications. Curr Opin Biotechnol. 2011;22:271–280. doi: 10.1016/j.copbio.2010.11.014. [PubMed] [CrossRef] [Google Scholar]

31. Viola R, Nyvall P, Pedersen M. The unique features of starch metabolism in red algae. Proc R Soc B Biol Sci. 2001;268:1417–1422. doi: 10.1098/rspb.2001.1644. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

32. Dauvillée D, Deschamps P, Ral J-P, Plancke C, Putaux J-L, Devassine J, Durand-Terrasson A, Devin A, Ball SG. Genetic dissection of floridean starch synthesis in the cytosol of the model dinoflagellate Crypthecodinium cohnii. Proc Natl Acad Sci. 2009;106:21126–21130. doi: 10.1073/pnas.0907424106. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

33. Deschamps P, Haferkamp I, D’Hulst C, Neuhaus HE, Ball SG. The relocation of starch metabolism to chloroplasts: when, why and how. Trends Plant Sci. 2008;13:574–582. doi: 10.1016/j.tplants.2008.08.009. [PubMed] [CrossRef] [Google Scholar]

34. Stitt M, Zeeman SC. Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol. 2012;15:1–11. doi: 10.1016/j.pbi.2012.03.016. [PubMed] [CrossRef] [Google Scholar]

35. Gross P, Rees T. Alkaline inorganic pyrophosphatase and starch synthesis in amyloplasts. Planta. 1986;167:140–145. doi: 10.1007/BF00446381. [PubMed] [CrossRef] [Google Scholar]

36. George GM, van der Merwe MJ, Nunes-Nesi A, Bauer R, Fernie AR, Kossmann J, Lloyd JR. Virus-induced gene silencing of plastidial soluble inorganic pyrophosphatase impairs essential leaf anabolic pathways and reduces drought stress tolerance in Nicotiana benthamiana. Plant Physiol. 2010;154:55–66. doi: 10.1104/pp.110.157776. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

37. Ragel P, Streb S, Feil R, Sahrawy M, Annunziata MG, Lunn JE, Zeeman S, Mérida Á. Loss of starch granule initiation has a deleterious effect on the growth of Arabidopsis plants due to an accumulation of ADP-glucose. Plant Physiol. 2013;163:75–85. doi: 10.1104/pp.113.223420. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

38. Flügge UI, Häusler RE, Ludewig F, Gierth M. The role of transporters in supplying energy to plant plastids. J Exp Bot. 2011;62:2381–2392. doi: 10.1093/jxb/erq361. [PubMed] [CrossRef] [Google Scholar]

39. Fettke J, Malinova I, Albrecht T, Hejazi M, Steup M. Glucose-1-phosphate transport into protoplasts and chloroplasts from leaves of Arabidopsis. Plant Physiol. 2011;155:1723–1734. doi: 10.1104/pp.110.168716. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

40. Denyer K, Dunlap F, Thorbjørnsen T, Keeling P, Smith AM. The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol. 1996;112:779–785. doi: 10.1104/pp.112.2.779. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

41. Beckles DM, Smith AM, Rees T. A cytosolic ADP-glucose pyrophosphorylase is a feature of graminaceous endosperms, but not of other starch-storing organs. Plant Physiol. 2001;125:818–827. doi: 10.1104/pp.125.2.818. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

42. Kirchberger S, Leroch M, Huynen MA, Wahl M, Neuhaus HE, Tjaden J. Molecular and biochemical analysis of the plastidic ADP-glucose transporter (ZmBT1) from Zea mays. J Biol Chem. 2007;282:22481–22491. doi: 10.1074/jbc.M702484200. [PubMed] [CrossRef] [Google Scholar]

43. Kirchberger S, Tjaden J, Neuhaus HE. Characterization of the Arabidopsis Brittle1 transport protein and impact of reduced activity on plant metabolism. Plant J. 2008;56:51–63. doi: 10.1111/j.1365-313X.2008.03583.x. [PubMed] [CrossRef] [Google Scholar]

44. Geigenberger P. Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol. 2011;155:1566–1577. doi: 10.1104/pp.110.170399. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

45. Sowokinos JR, Preiss J. Pyrophosphorylases in Solanum tuberosum III. Purification, physical, and catalytic properties of ADPglucose pyrophosphorylase in potatoes. Plant Physiol. 1982;69:1459–1466. doi: 10.1104/pp.69.6.1459. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

46. Sikka VK, Choi SB, Kavakli IH, Sakulsingharoj C, Gupta S, Ito H, Okita TW. Subcellular compartmentation and allosteric regulation of the rice endosperm ADPglucose pyrophosphorylase. Plant Sci. 2001;161:461–468. doi: 10.1016/S0168-9452(01)00431-9. [CrossRef] [Google Scholar]

47. Fu Y, Ballicora MA, Leykam JF, Preiss J. Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. J Biol Chem. 1998;273:25045–25052. doi: 10.1074/jbc.273.39.25045. [PubMed] [CrossRef] [Google Scholar]

48. Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase. Plant Cell. 2002;14:2191–2213. doi: 10.1105/tpc.003640. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

49. Hädrich N, Hendriks JHM, Kötting O, Arrivault S, Feil R, Zeeman SC, Gibon Y, Schulze WX, Stitt M, Lunn JE. Mutagenesis of cysteine 81 prevents dimerization of the APS1 subunit of ADP-glucose pyrophosphorylase and alters diurnal starch turnover in Arabidopsis thaliana leaves. Plant J. 2012;70:231–242. doi: 10.1111/j.1365-313X.2011.04860.x. [PubMed] [CrossRef] [Google Scholar]

50. Stark DM, Timmerman KP, Barry GF, Preiss J, Kishore GM. Regulation of the amount of starch in plant tissues by ADP glucose pyrophosphorylase. Science. 1992;258:287–292. doi: 10.1126/science.258.5080.287. [PubMed] [CrossRef] [Google Scholar]

51. Sweetlove LJ, Burrell MM, Rees T. Starch metabolism in tubers of transgenic potato (Solanum tuberosum) with increased ADPglucose pyrophosphorylase. Biochem J. 1996;492:493–498. doi: 10.1042/bj3200493. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

52. Giroux MJ, Shaw J, Barry G, Cobb BG, Greene T, Okita T, Hannah LC. A single mutation that increases maize seed weight. Proc Natl Acad Sci. 1996;93:5824–5829. doi: 10.1073/pnas.93.12.5824. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

53. Smidansky ED, Clancy M, Meyer FD, Lanning SP, Blake NK, Talbert LE, Giroux MJ. Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield. Proc Natl Acad Sci. 2002;99:1724–1729. doi: 10.1073/pnas.022635299. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

54. Sakulsingharoj C, Choi SB, Hwang SK, Edwards GE, Bork J, Meyer CR, Preiss J, Okita TW. Engineering starch biosynthesis for increasing rice seed weight: the role of the cytoplasmic ADP-glucose pyrophosphorylase. Plant Sci. 2004;167:1323–1333. doi: 10.1016/j.plantsci.2004.06.028. [CrossRef] [Google Scholar]

55. Ihemere U, Arias-Garzon D, Lawrence S, Sayre R. Genetic modification of cassava for enhanced starch production. Plant Biotechnol J. 2006;4:453–465. doi: 10.1111/j.1467-7652.2006.00195.x. [PubMed] [CrossRef] [Google Scholar]

56. Wang Z, Chen X, Wang J, Liu T, Liu Y, Zhao L, Wang G. Increasing maize seed weight by enhancing the cytoplasmic ADP-glucose pyrophosphorylase activity in transgenic maize plants. Plant Cell Tissue Organ Cult. 2007;88:83–92. doi: 10.1007/s11240-006-9173-4. [CrossRef] [Google Scholar]

57. Kang G, Liu G, Peng X, Wei L, Wang C, Zhu Y, Ma Y, Jiang Y, Guo T. Increasing the starch content and grain weight of common wheat by overexpression of the cytosolic AGPase large subunit gene. Plant Physiol Biochem. 2013;73:93–98. doi: 10.1016/j.plaphy.2013.09.003. [PubMed] [CrossRef] [Google Scholar]

58. Tuncel A, Okita TW. Improving starch yield in cereals by over-expression of ADPglucose pyrophosphorylase: expectations and unanticipated outcomes. Plant Sci. 2013;211:52–60. doi: 10.1016/j.plantsci.2013.06.009. [PubMed] [CrossRef] [Google Scholar]

59. Lombard V, Ramulu HG, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:490–495. doi: 10.1093/nar/gkt1178. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

60. Liu H, Yu G, Wei B, Wang Y, Zhang J, Hu Y, Liu Y, Yu G, Zhang H, Huang Y. Identification and phylogenetic analysis of a novel starch synthase in maize. Front Plant Sci. 2015;6:1013. [PMC free article] [PubMed] [Google Scholar]

61. Leterrier M, Holappa LD, Broglie KE, Beckles DM. Cloning, characterisation and comparative analysis of a starch synthase IV gene in wheat: functional and evolutionary implications. BMC Plant Biol. 2008;8:98–119. doi: 10.1186/1471-2229-8-98. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

62. Buschiazzo A, Ugalde JE, Guerin ME, Shepard W, Ugalde RA, Alzari PM. Crystal structure of glycogen synthase: homologous enzymes catalyze glycogen synthesis and degradation. EMBO J. 2004;23:3196–3205. doi: 10.1038/sj.emboj.7600324. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

63. Sheng F, Jia X, Yep A, Preiss J, Geiger JH. The crystal structures of the open and catalytically competent closed conformation of Escherichia coli glycogen synthase. J Biol Chem. 2009;284:17796–17807. doi: 10.1074/jbc.M809804200. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

64. Momma M, Fujimoto Z. Interdomain disulfide bridge in the rice granule bound starch synthase I catalytic domain as elucidated by X-ray structure analysis. Biosci Biotechnol Biochem. 2012;76:1591–1595. doi: 10.1271/bbb.120305. [PubMed] [CrossRef] [Google Scholar]

65. Cuesta-Seijo JA, Nielsen MM, Marri L, Tanaka H, Beeren SR, Palcic MM. Structure of starch synthase I from barley: insight into regulatory mechanisms of starch synthase activity. Acta Crystallogr D. 2013;69:1013–1025. doi: 10.1107/S090744491300440X. [PubMed] [CrossRef] [Google Scholar]

66. Furukawa K, Tagaya M, Preiss J, Fukui T. Identification of lysine 15 at the active site in Escherichia coli glycogen synthase. J Biol Chem. 1990;265:2086–2090. [PubMed] [Google Scholar]

67. Furukawa K, Tagaya M, Tanizawa K, Fukui T. Role of the conserved Lys-X-Gly-Gly sequence at the ADP-glucose-binding site in Escherichia coli glycogen synthase. J Biol Chem. 1993;268:23837–23842. [PubMed] [Google Scholar]

68. Edwards A, Borthakur A, Bornemann S, Venail J, Denyer K, Waite D, Fulton D, Smith A, Martin C. Specificity of starch synthase isoforms from potato. Eur J Biochem. 1999;266:724–736. doi: 10.1046/j.1432-1327.1999.00861.x. [PubMed] [CrossRef] [Google Scholar]

69. Imparl-Radosevich JM, Keeling PL, Guan H. Essential arginine residues in maize starch synthase IIa are involved in both ADP-glucose and primer binding. FEBS Lett. 1999;457:357–362. doi: 10.1016/S0014-5793(99)01066-2. [PubMed] [CrossRef] [Google Scholar]

70. Nichols DJ, Keeling PL, Spalding M, Guan H. Involvement of conserved aspartate and glutamate residues in the catalysis and substrate binding of maize starch synthase. Biochemistry. 2000;39:7820–7825. doi: 10.1021/bi000407g. [PubMed] [CrossRef] [Google Scholar]

71. Yep A, Ballicora MA, Preiss J. The ADP-glucose binding site of the Escherichia coli glycogen synthase. Arch Biochem Biophys. 2006;453:188–196. doi: 10.1016/j.abb.2006.07.003. [PubMed] [CrossRef] [Google Scholar]

72. Busi MV, Palopoli N, Valdez HA, Fornasari MS, Wayllace NZ, Gomez-Casati DF, Parisi G, Ugalde RA. Functional and structural characterization of the catalytic domain of the starch synthase III from Arabidopsis thaliana. Proteins. 2008;70:31–40. doi: 10.1002/prot.21469. [PubMed] [CrossRef] [Google Scholar]

73. Hennen-Bierwagen TA, Liu F, Marsh RS, Kim S, Gan Q, Tetlow IJ, Emes MJ, James MG, Myers AM. Starch biosynthetic enzymes from developing maize endosperm associate in multisubunit complexes. Plant Physiol. 2008;146:1892–1908. doi: 10.1104/pp.108.116285. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

74. Hennen-Bierwagen TA, Lin Q, Grimaud F, Planchot V, Keeling PL, James MG, Myers AM. 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. 2009;149:1541–1559. doi: 10.1104/pp.109.135293. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

75. Gámez-Arjona FM, Raynaud S, Ragel P, Mérida A. Starch synthase 4 is located in the thylakoid membrane and interacts with plastoglobule-associated proteins in Arabidopsis. Plant J. 2014;80:305–316. doi: 10.1111/tpj.12633. [PubMed] [CrossRef] [Google Scholar]

76. Valdez HA, Busi MV, Wayllace NZ, Parisi G, Ugalde RA, Gomez-Casati DF. Role of the N-terminal starch-binding domains in the kinetic properties of starch synthase III from Arabidopsis thaliana. Biochemistry. 2008;47:3026–3032. doi: 10.1021/bi702418h. [PubMed] [CrossRef] [Google Scholar]

77. Wayllace NZ, Valdez HA, Ugalde RA, Busi MV, Gomez-Casati DF. The starch-binding capacity of the noncatalytic SBD2 region and the interaction between the N- and C-terminal domains are involved in the modulation of the activity of starch synthase III from Arabidopsis thaliana. FEBS J. 2010;277:428–440. doi: 10.1111/j.1742-4658.2009.07495.x. [PubMed] [CrossRef] [Google Scholar]

78. Yan HB, Pan XX, Jiang HW, Wu GJ. Comparison of the starch synthesis genes between maize and rice: copies, chromosome location and expression divergence. Theor Appl Genet. 2009;119:815–825. doi: 10.1007/s00122-009-1091-5. [PubMed] [CrossRef] [Google Scholar]

79. Ohdan T, Francisco PB, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y. Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot. 2005;56:3229–3244. doi: 10.1093/jxb/eri292. [PubMed] [CrossRef] [Google Scholar]

80. Zhang G, Cheng Z, Zhang X, Guo X, Su N, Jiang L. Double repression of soluble starch synthase genes SSIIa and SSIIIa in rice (Oryza sativa L.) uncovers interactive effects on the physicochemical properties of starch. Genome. 2011;54(459):448–459. doi: 10.1139/g11-010. [PubMed] [CrossRef] [Google Scholar]

81. Jiang H, Dian W, Liu F, Wu P. Molecular cloning and expression analysis of three genes encoding starch synthase II in rice. Planta. 2004;218:1062–1070. doi: 10.1007/s00425-003-1189-y. [PubMed] [CrossRef] [Google Scholar]

82. Cheng J, Khan MA, Qiu W-M, Li J, Zhou H, Zhang Q, Guo W, et al. Diversification of genes encoding granule-bound starch synthase in monocots and dicots is marked by multiple genome-wide duplication events. PLoS One. 2012;7:e30088. doi: 10.1371/journal.pone.0030088. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

83. Vrinten PL, Nakamura T. Wheat granule-bound starch synthase I and II are encoded by separate genes that are expressed in different tissues. Plant Physiol. 2000;122:255–264. doi: 10.1104/pp.122.1.255. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

84. Edwards A, Vincken J-P, Suurs LCJM, Visser RGF, Zeeman S, Smith A, Martin C. Discrete forms of amylose are synthesized by isoforms of GBSSI in pea. Plant Cell. 2002;14:1767–1785. doi: 10.1105/tpc.002907. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

85. Sprague GF, Brimhall B, Hixon RM. Some effects of the waxy gene in corn on properties of the endosperm starch. Agron J. 1943;35:817–823. doi: 10.2134/agronj1943.00021962003500090008x. [CrossRef] [Google Scholar]

86. Shure M, Wessler S, Fedoroff N. Molecular identification and isolation of the Waxy locus in maize. Cell. 1983;35:225–233. doi: 10.1016/0092-8674(83)90225-8. [PubMed] [CrossRef] [Google Scholar]

87. Sano Y. Differential regulation of waxy gene expression in rice endosperm. Theor Appl Genet. 1984;68:467–473. doi: 10.1007/BF00254822. [PubMed] [CrossRef] [Google Scholar]

88. Wang Z-Y, Zheng F-Q, Shen G-Z, Gao J-P, Snustad DP, Li M-G, Zhang J-L, Hong M-M. The amylose content in rice endosperm is related to the post-transcriptional regulation of the waxy gene. Plant J. 1995;7:613–622. doi: 10.1046/j.1365-313X.1995.7040613.x. [PubMed] [CrossRef] [Google Scholar]

89. Nakamura T, Yamamori M, Hirano H, Hidaka S, Nagamine T. Production of waxy (amylose-free) wheats. Mol Gen Genet. 1995;248:253–259. doi: 10.1007/BF02191591. [PubMed] [CrossRef] [Google Scholar]

90. Patron NJ, Smith AM, Fahy BF, Hylton CM, Naldrett MJ, Rossnagel BG, Denyer K. The altered pattern of amylose accumulation in the endosperm of low-amylose barley cultivars is attributable to a single mutant allele of granule-bound starch synthase I with a deletion in the 5′-non-coding region. Plant Physiol. 2002;130:190–198. doi: 10.1104/pp.005454. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

91. Konishi Y, Nojima H, Okuno K, Asaoka M, Fuwa H. Characterization of starch granules from waxy, nonwaxy, and hybrid seeds of Amaranthus hypochondriacus L. Agric Biol Chem. 1985;49:1965–1971. doi: 10.1080/00021369.1985.10867018. [CrossRef] [Google Scholar]

92. Hovenkamp-Hermelink JHM, Jacobsen E, Ponstein AS, Visser RGF, Vos-Scheperkeuter GH, Bijmolt EW, de Vries JN, Witholt B, Feenstra WJ. Isolation of an amylose-free starch mutant of the potato (Solanum tuberosum L.) Theor Appl Genet. 1987;75:217–221. doi: 10.1007/BF00249167. [CrossRef] [Google Scholar]

93. Jacobsen E, Hovenkamp-Hermelink JHM, Krijgsheld HT, Nijdam H, Pijnacker LP, Witholt B, Feenstra WJ. Phenotypic and genotypic characterization of an amylose-free starch mutant of the potato. Euphytica. 1989;44:43–48. doi: 10.1007/BF00022597. [CrossRef] [Google Scholar]

94. Denyer K, Baber LM, Burton R, Hedley CL, Hylton CM, Johnson S, Jones DA, et al. The isolation and characterization of novel low-amylose mutants of Pisum sativum L. Plant Cell Environ. 1995;18:1019–1026. doi: 10.1111/j.1365-3040.1995.tb00612.x. [CrossRef] [Google Scholar]

95. Seung D, Soyk S, Coiro M, Maier BA, Eicke S, Zeeman SC. PROTEIN TARGETING TO STARCH is required for localising GRANULE-BOUND STARCH SYNTHASE to starch granules and for normal amylose synthesis in Arabidopsis. PLoS Biol. 2015;13:e1002080. doi: 10.1371/journal.pbio.1002080. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

96. Delrue B, Fontaine T, Routier F, Decq A, Wieruszeski JM, Van Den Koornhuyse N, Maddelein ML, Fournet B, Ball S. Waxy Chlamydomonas reinhardtii: monocellular algal mutants defective in amylose biosynthesis and granule-bound starch synthase activity accumulate a structurally modified amylopectin. J Bacteriol. 1992;174:3612–3620. [PMC free article] [PubMed] [Google Scholar]

97. Ral J-P, Colleoni C, Wattebled F, Dauvillée D, Nempont C, Deschamps P, Li Z, et al. Circadian clock regulation of starch metabolism establishes GBSSI as a major contributor to amylopectin synthesis in Chlamydomonas reinhardtii. Plant Physiol. 2006;142:305–317. doi: 10.1104/pp.106.081885. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

98. Tatge H, Marshall J, Martin C, Edwards EA, Smith AM. Evidence that amylose synthesis occurs within the matrix of the starch granule in potato tubers. Plant Cell Environ. 1999;22:543–550. doi: 10.1046/j.1365-3040.1999.00437.x. [CrossRef] [Google Scholar]

99. Denyer K, Waite D, Motawia S, Møller BL, Smith AM. Granule-bound starch synthase I in isolated starch granules elongates malto-oligosaccharides processively. Biochem J. 1999;340:183–191. doi: 10.1042/bj3400183. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

100. Van Wal M, De D’Hulst C, Vincken JP, Buléon A, Visser R, Ball S. Amylose is synthesized in vitro by extension of and cleavage from amylopectin. J Biol Chem. 1998;273:22232–22240. doi: 10.1074/jbc.273.35.22232. [PubMed] [CrossRef] [Google Scholar]

101. Zeeman SC, Smith SM, Smith AM. The priming of amylose synthesis in Arabidopsis leaves. Plant Physiol. 2002;128:1069–1076. doi: 10.1104/pp.010640. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

102. Denyer K, Clarke B, Hylton C, Tatge H, Smith AM. The elongation of amylose and amylopectin chains in isolated starch granules. Plant J. 1996;10:1135–1143. doi: 10.1046/j.1365-313X.1996.10061135.x. [CrossRef] [Google Scholar]

103. Denyer K, Sidebottom C, Hylton CM, Smith AM. Soluble isoforms of starch synthase and starch branching enzyme also occur within starch granules in developing pea embryos. Plant J. 1993;4:191–198. doi: 10.1046/j.1365-313X.1993.04010191.x. [PubMed] [CrossRef] [Google Scholar]

104. Lohmeier-Vogel EM, Kerk D, Nimick M, Wrobel S, Vickerman L, Muench DG, Moorhead GBG. Arabidopsis At5g39790 encodes a chloroplast-localized, carbohydrate-binding, coiled-coil domain-containing putative scaffold protein. BMC Plant Biol. 2008;8:120. doi: 10.1186/1471-2229-8-120. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

105. Yeh JY, Garwood DL, Shannon JC. Characterization of starch from maize endosperm mutants. Starch/Stärke. 1981;33:222–230. doi: 10.1002/star.19810330703. [CrossRef] [Google Scholar]

106. Klucinec JD, Thompson DB. Structure of amylopectins from ae-containing maize starches. Cereal Chem. 2002;79:19–23. doi: 10.1094/CCHEM.2002.79.1.19. [CrossRef] [Google Scholar]

107. Reddy KR, Ali SZ, Bhattacharya KR. The fine structure of rice-starch amylopectin and its relation to the texture of cooked rice. Carbohydr Polym. 1993;22:267–275. doi: 10.1016/0144-8617(93)90130-V. [CrossRef] [Google Scholar]

108. Ahuja G, Jaiswal S, Hucl P, Chibbar RN. Wheat genome specific granule-bound starch synthase I differentially influence grain starch synthesis. Carbohydr Polym. 2014;114:87–94. doi: 10.1016/j.carbpol.2014.08.004. [PubMed] [CrossRef] [Google Scholar]

109. Inouchi N, Glover DV, Fuwa H. Chain length distribution of amylopectins of several single mutants and the normal counterpart, and sugary-1 phytoglycogen in maize (Zea mays L.) Starch/Stärke. 1987;39:259–266. doi: 10.1002/star.19870390802. [CrossRef] [Google Scholar]

110. Bertoft E, Piyachomkwan K, Chatakanonda P, Sriroth K. Internal unit chain composition in amylopectins. Carbohydr Polym. 2008;74:527–543. doi: 10.1016/j.carbpol.2008.04.011. [CrossRef] [Google Scholar]

111. Crofts N, Abe K, Aihara S, Itoh R, Nakamura Y, Itoh K, Fujita N. Lack of starch synthase IIIa and high expression of granule-bound starch synthase I synergistically increase the apparent amylose content in rice endosperm. Plant Sci. 2012;193–194:62–69. doi: 10.1016/j.plantsci.2012.05.006. [PubMed] [CrossRef] [Google Scholar]

112. Wattebled F, Buléon A, Bouchet B, Ral JP, Liénard L, Delvallé D, Binderup K, Dauvillée D, Ball S, D’Hulst C. Granule-bound starch synthase I: a major enzyme involved in the biogenesis of B-crystallites in starch granules. Eur J Biochem. 2002;269:3810–3820. doi: 10.1046/j.1432-1033.2002.03072.x. [PubMed] [CrossRef] [Google Scholar]

113. Maddelein M-L, Libessarts N, Bellanger F, Delrue B, Hulst CD, Van Den Koornhuyse N, Fontaine T, Wieruszeski J-M, Decq A, Ball S. Toward an understanding of the biogenesis of the starch granule. J Biol Chem. 1994;269:25150–25157. [PubMed] [Google Scholar]

114. Fulton DC, Edwards A, Pilling E, Robinson HL, Fahy B, Seale R, Kato L, et al. Role of granule-bound starch synthase in determination of amylopectin structure and starch granule morphology in potato. J Biol Chem. 2002;277:10834–10841. doi: 10.1074/jbc.M111579200. [PubMed] [CrossRef] [Google Scholar]

115. Tetlow IJ, Emes MJ. Starch biosynthesis in higher plants: the enzymes of starch synthesis. In: Murray M-Y, editor. Comprehensive biotechnology. 2. Amsterdam: Elsevier; 2011. pp. 47–65. [Google Scholar]

116. Roldán I, Wattebled F, Lucas MM, Delvallé D, Planchot V, Jiménez S, Pérez R, Ball S, D’Hulst C, Mérida A. 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. 2007;49:492–504. doi: 10.1111/j.1365-313X.2006.02968.x. [PubMed] [CrossRef] [Google Scholar]

117. Szydlowski N, Ragel P, Raynaud S, Lucas MM, Roldán I, Montero M, Muñoz FJ, et al. Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell. 2009;21:2443–2457. doi: 10.1105/tpc.109.066522. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

118. Crumpton-Taylor M, Pike M, Lu K-J, Hylton CM, Feil R, Eicke S, Lunn JE, Zeeman SC, Smith AM. Starch synthase 4 is essential for coordination of starch granule formation with chloroplast division during Arabidopsis leaf expansion. New Phytol. 2013;200:1064–1075. doi: 10.1111/nph.12455. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

119. Zhang X, Szydlowski N, Delvallé D, D’Hulst C, James MG, Myers AM. Overlapping functions of the starch synthases SSII and SSIII in amylopectin biosynthesis in Arabidopsis. BMC Plant Biol. 2008;8:96. doi: 10.1186/1471-2229-8-96. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

120. Delatte T, Trevisan M, Parker ML, Zeeman SC. 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. doi: 10.1111/j.1365-313X.2005.02348.x. [PubMed] [CrossRef] [Google Scholar]

121. Streb S, Delatte T, Umhang M, Eicke S, Schorderet M, Reinhardt D, Zeeman SC. Starch granule biosynthesis in Arabidopsis is abolished by removal of all debranching enzymes but restored by the subsequent removal of an endoamylase. Plant Cell. 2008;20:3448–3466. doi: 10.1105/tpc.108.063487. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

122. Pfister B, Lu K-J, Eicke S, Feil R, Lunn JE, Streb S, Zeeman SC. Genetic evidence that chain length and branch point distributions are linked determinants of starch granule formation in Arabidopsis. Plant Physiol. 2014;165:1457–1474. doi: 10.1104/pp.114.241455. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

123. Tetlow IJ, Wait R, Lu Z, Akkasaeng R, Bowsher CG, Esposito S, Kosar-Hashemi B, Morell MK, Emes MJ. Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein–protein interactions. Plant Cell. 2004;16:694–708. doi: 10.1105/tpc.017400. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

124. Tetlow IJ, Beisel KG, Cameron S, Makhmoudova A, Liu F, Bresolin NS, Wait R, Morell MK, Emes MJ. Analysis of protein complexes in wheat amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiol. 2008;146:1878–1891. doi: 10.1104/pp.108.116244. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

125. Liu F, Makhmoudova A, Lee EA, Wait R, Emes MJ, Tetlow IJ. The amylose extender mutant of maize conditions novel protein–protein interactions between starch biosynthetic enzymes in amyloplasts. J Exp Bot. 2009;60:4423–4440. doi: 10.1093/jxb/erp297. [PubMed] [CrossRef] [Google Scholar]

126. Ahmed Z, Tetlow IJ, Ahmed R, Morell MK, Emes MJ. Protein–protein interactions among enzymes of starch biosynthesis in high-amylose barley genotypes reveal differential roles of heteromeric enzyme complexes in the synthesis of A and B granules. Plant Sci. 2015;233:95–106. doi: 10.1016/j.plantsci.2014.12.016. [PubMed] [CrossRef] [Google Scholar]

127. Crofts N, Abe N, Oitome NF, Matsushima R, Hayashi M, Tetlow IJ, Emes MJ, Nakamura Y, Fujita N. Amylopectin biosynthetic enzymes from developing rice seed form enzymatically active protein complexes. J Exp Bot. 2015;66:4469–4482. doi: 10.1093/jxb/erv212. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

128. Cao H, Imparl-Radosevich J, Guan H, Keeling PL, James MG, Myers AM. Identification of the soluble starch synthase activities of maize endosperm. Plant Physiol. 1999;120:205–215. doi: 10.1104/pp.120.1.205. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

129. Knight ME, Harn C, Lilley CER, Guan H, Singletary GW, Mu-Forster C, Wasserman BP, Keeling PL. Molecular cloning of starch synthase I from maize (W64) endosperm and expression in Escherichia coli. Plant J. 1998;14:613–622. doi: 10.1046/j.1365-313X.1998.00150.x. [PubMed] [CrossRef] [Google Scholar]

130. Abel GJW, Springer F, Willmitzer L, Kossmann J. Cloning and functional analysis of a cDNA encoding a novel 139 kDa starch synthase from potato (Solanum tuberosum L.) Plant J. 1996;10:981–991. doi: 10.1046/j.1365-313X.1996.10060981.x. [PubMed] [CrossRef] [Google Scholar]

131. Marshall J, Sidebottom C, Debet M, Martin C, Smith AM, Edwards A. Identification of the major starch synthase in the soluble fraction of potato tubers. Plant Cell. 1996;8:1121–1135. doi: 10.1105/tpc.8.7.1121. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

132. Tomlinson K, Craig J, Smith AM. Major differences in isoform composition of starch synthase between leaves and embryos of pea (Pisum sativum L.) Planta. 1998;204:86–92. doi: 10.1007/s004250050233. [CrossRef] [Google Scholar]

133. Kossmann J, Abel GJ, Springer F, Lloyd JR, Willmitzer L. Cloning and functional analysis of a cDNA encoding a starch synthase from potato (Solanum tuberosum L.) that is predominantly expressed in leaf tissue. Planta. 1999;208:503–511. doi: 10.1007/s004250050587. [PubMed] [CrossRef] [Google Scholar]

134. Szydlowski N, Ragel P, Hennen-Bierwagen TA, Planchot V, Myers AM, Mérida A, D’Hulst C, Wattebled F. Integrated functions among multiple starch synthases determine both amylopectin chain length and branch linkage location in Arabidopsis leaf starch. J Exp Bot. 2011;62:4547–4559. doi: 10.1093/jxb/err172. [PubMed] [CrossRef] [Google Scholar]

135. Smith SM, Fulton DC, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman SC, Smith AM. 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. 2004;136:2687–2699. doi: 10.1104/pp.104.044347. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

136. Fujita N, Yoshida M, Asakura N, Ohdan T, Miyao A, Hirochika H, Nakamura Y. Function and characterization of starch synthase I using mutants in rice. Plant Physiol. 2006;140:1070–1084. doi: 10.1104/pp.105.071845. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

137. McMaugh SJ, Thistleton JL, Anschaw E, Luo J, Konik-Rose C, Wang H, Huang M, et al. Suppression of starch synthase I expression affects the granule morphology and granule size and fine structure of starch in wheat endosperm. J Exp Bot. 2014;65:2189–2201. doi: 10.1093/jxb/eru095. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

138. Delvallé D, Dumez S, Wattebled F, Roldán I, Planchot V, Berbezy P, Colonna P, et al. Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. Plant J. 2005;43:398–412. doi: 10.1111/j.1365-313X.2005.02462.x. [PubMed] [CrossRef] [Google Scholar]

139. Commuri PD, Keeling PL. Chain-length specificities of maize starch synthase I enzyme: studies of glucan affinity and catalytic properties. Plant J. 2001;25:475–486. doi: 10.1046/j.1365-313x.2001.00955.x. [PubMed] [CrossRef] [Google Scholar]

140. Senoura T, Isono N, Yoshikawa M, Asao A, Hamada S, Watanabe K, Ito H, Matsui H. Characterization of starch synthase I and II expressed in early developing seeds of kidney bean (Phaseolus vulgaris L.) Biosci Biotechnol Biochem. 2004;68:1949–1960. doi: 10.1271/bbb.68.1949. [PubMed] [CrossRef] [Google Scholar]

141. Mu-Forster C, Huang R, Powers JR, Harriman RW, Knight M, Singletary GW, Keeling PL, Wasserman BP. Physical association of starch biosynthetic enzymes with starch granules of maize endosperm. Granule-associated forms of starch synthase I and starch branching enzyme II. Plant Physiol. 1996;111:821–829. doi: 10.1104/pp.111.3.821. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

142. Brust H, Orzechowski S, Fettke J, Steup M. Starch synthesizing reactions and paths: in vitro and in vivo studies. J Appl Glycosci. 2013;60:3–20. doi: 10.5458/jag.jag.JAG-2012_018. [CrossRef] [Google Scholar]

143. Brust H, Lehmann T, D’Hulst C, Fettke J. 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. 2014;9:e102364. doi: 10.1371/journal.pone.0102364. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

144. Cuesta-Seijo JA, Nielsen MM, Ruzanski C, Krucewicz K, Beeren SR, Rydhal MG, Yoshimura Y, et al. In vitro biochemical characterization of all barley endosperm starch synthases. Front Plant Sci. 2016;6:1–17. doi: 10.3389/fpls.2015.01265. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

145. Glaring MA, Skryhan K, Kötting O, Zeeman SC, Blennow A. Comprehensive survey of redox sensitive starch metabolising enzymes in Arabidopsis thaliana. Plant Physiol Biochem. 2012;58:89–97. doi: 10.1016/j.plaphy.2012.06.017. [PubMed] [CrossRef] [Google Scholar]

146. Edwards A, Marshall J, Sidebottom C, Visser RGF, Smith AM, Martin C. Biochemical and molecular characterization of a novel starch synthase from potato tubers. Plant J. 1995;8:283–294. doi: 10.1046/j.1365-313X.1995.08020283.x. [PubMed] [CrossRef] [Google Scholar]

147. Edwards A, Fulton DC, Hylton CM, Jobling SA, Gidley M, Ro U, Martin C, Smith AM. A combined reduction in activity of starch synthases II and III of potato has novel effects on the starch of tubers. Plant J. 1999;17:251–261. doi: 10.1046/j.1365-313X.1999.00371.x. [CrossRef] [Google Scholar]

148. Lloyd JR, Landschütze V, Kossmann J. Simultaneous antisense inhibition of two starch-synthase isoforms in potato tubers leads to accumulation of grossly modified amylopectin. Biochem J. 1999;338:515–521. doi: 10.1042/bj3380515. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

149. Craig J, Lloyd JR, Tomlinson K, Barber L, Edwards A, Wang TL, Martin C, Hedley CL, Smith AM. Mutations in the gene encoding starch synthase II profoundly alter amylopectin structure in pea embryos. Plant Cell. 1998;10:413–426. [PMC free article] [PubMed] [Google Scholar]

150. Yamamori M, Fujita S, Hayakawa K, Matsuki J, Yasui T. Genetic elimination of a starch granule protein, SGP-1, of wheat generates an altered starch with apparent high amylose. Theor Appl Genet. 2000;101:21–29. doi: 10.1007/s001220051444. [CrossRef] [Google Scholar]

151. Morell MK, Kosar-Hashemi B, Cmiel M, Samuel MS, Chandler P, Rahman S, Buleon A, Batey IL, Li Z. Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties. Plant J. 2003;34:173–185. doi: 10.1046/j.1365-313X.2003.01712.x. [PubMed] [CrossRef] [Google Scholar]

152. Umemoto T, Nakamura Y, Satoh H, Terashima K. Differences in amylopectin structure between two rice varieties in relation to the effects of temperature. Starch/Stärke. 1999;2–3:58–62. doi: 10.1002/(SICI)1521-379X(199903)51:2<58::AID-STAR58>3.0.CO;2-J. [CrossRef] [Google Scholar]

153. Umemoto T, Yano M, Satoh H, Shomura A, Nakamura Y. Mapping of a gene responsible for the difference in amylopectin structure between japonica-type and indica-type rice varieties. Theor Appl Genet. 2002;104:1–8. doi: 10.1007/s001220200000. [PubMed] [CrossRef] [Google Scholar]

154. Zhang X, Colleoni C, Ratushna V, Sirghie-Colleoni M, James MG, Myers AM. Molecular characterization demonstrates that the Zea mays gene sugary2 codes for the starch synthase isoform SSIIa. Plant Mol Biol. 2004;54:865–879. doi: 10.1007/s11103-004-0312-1. [PubMed] [CrossRef] [Google Scholar]

155. Nakamura Y, Francisco PB, Hosaka Y, Sato A, Sawada T, Kubo A, Fujita N. Essential amino acids of starch synthase IIa differentiate amylopectin structure and starch quality between japonica and indica rice varieties. Plant Mol Biol. 2005;58:213–227. doi: 10.1007/s11103-005-6507-2. [PubMed] [CrossRef] [Google Scholar]

156. Wang Y-J, White P, Pollak L, Jane J. Characterization of starch structures of 17 maize endosperm mutant genotypes with Oh43 inbred line background. Cereal Chem. 1993;70:171–179. [Google Scholar]

157. Fujita N, Yoshida M, Kondo T, Saito K, Utsumi Y, Tokunaga T, Nishi A, et al. Characterization of SSIIIa-deficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm. Plant Physiol. 2007;144:2009–2023. doi: 10.1104/pp.107.102533. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

158. Zhang X, Myers AM, James MG. Mutations affecting starch synthase III in Arabidopsis alter leaf starch structure and increase the rate of starch synthesis. Plant Physiol. 2005;138:663–674. doi: 10.1104/pp.105.060319. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

159. Li Z, Li D, Du X, Wang H, Larroque O, Jenkins CLD, Jobling SA, Morell MK. 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. 2011;62:5217–5231. doi: 10.1093/jxb/err239. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

160. Lin Q, Huang B, Zhang M, Zhang X, Rivenbark J, Lappe RL, James MG, Myers AM, Hennen-Bierwagen TA. Functional interactions between starch synthase III and isoamylase-type starch-debranching enzyme in maize endosperm. Plant Physiol. 2012;158:679–692. doi: 10.1104/pp.111.189704. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

161. Jobling SA, Westcott RJ, Tayal A, Jeffcoat R, Schwall GP. Production of a freeze-thaw-stable potato starch by antisense inhibition of three starch synthase genes. Nat Biotechnol. 2002;20:295–299. doi: 10.1038/nbt0302-295. [PubMed] [CrossRef] [Google Scholar]

162. Boyer CD, Preiss J. Evidence for independent genetic control of the multiple forms of maize endosperm branching enzymes and starch synthases. Plant Physiol. 1981;67:1141–1145. doi: 10.1104/pp.67.6.1141. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

163. Toyosawa Y, Kawagoe Y, Matsushima R, Crofts N, Ogawa M, Fukuda M, Kumamaru T, et al. Deficiency of starch synthase IIIa and IVb alters starch granule morphology from polyhedral to spherical in rice endosperm. Plant Physiol. 2016;170:1255–1270. [PMC free article] [PubMed] [Google Scholar]

164. Crumpton-Taylor M, Grandison S, Png KMY, Bushby AJ, Smith AM. Control of starch granule numbers in Arabidopsis chloroplasts. Plant Physiol. 2012;158:905–916. doi: 10.1104/pp.111.186957. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

165. Gámez-Arjona FM, Li J, Raynaud S, Baroja-Fernández E, Muñoz FJ, Ovecka M, Ragel P, Bahaji A, Pozueta-Romero J, Mérida Á. Enhancing the expression of starch synthase class IV results in increased levels of both transitory and long-term storage starch. Plant Biotechnol J. 2011;9:1049–1060. doi: 10.1111/j.1467-7652.2011.00626.x. [PubMed] [CrossRef] [Google Scholar]

166. Myers AM, James MG, Lin Q, Yi G, Stinard PS, Hennen-Bierwagen TA, Becraft PW. Maize opaque5 encodes monogalactosyldiacylglycerol synthase and specifically affects galactolipids necessary for amyloplast and chloroplast function. Plant Cell. 2011;23:2331–2347. doi: 10.1105/tpc.111.087205. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

167. Kawagoe Y. The characteristic polyhedral, sharp-edged shape of compound-type starch granules in rice endosperm is achieved via the septum-like structure of the amyloplast. J Appl Glycosci. 2013;60:29–36. doi: 10.5458/jag.jag.JAG-2012_013. [CrossRef] [Google Scholar]

168. Ugalde JE, Parodi AJ, Ugalde RA. De novo synthesis of bacterial glycogen: Agrobacterium tumefaciens glycogen synthase is involved in glucan initiation and elongation. Proc Natl Acad Sci. 2003;100:10659–10663. doi: 10.1073/pnas.1534787100. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

169. Lomako J, Lomako WM, Whelan WJ. A self-glucosylating rabbit protein glycogen is the primer for rabbit muscle glycogen biosynthesis. FASEB J. 1988;2:3097–3103. [PubMed] [Google Scholar]

170. Pitcher J, Smythe C, Cohen P. Glycogenin is the priming glucosyltransferase required for the initiation of glycogen biogenesis in rabbit skeletal muscle. Eur J Biochem. 1988;176:391–395. doi: 10.1111/j.1432-1033.1988.tb14294.x. [PubMed] [CrossRef] [Google Scholar]

171. Linden JC, Schilling N, Brackenhofer H, Kandler O. Asymmetric labelling of maltose during photosynthesis in 14CO2. Zeitschrift für Pflanzenphysiologie. 1975;76:176–181. doi: 10.1016/S0044-328X(75)80035-3. [CrossRef] [Google Scholar]

172. Szecowka M, Heise R, Tohge T, Nunes-Nesi A, Vosloh D, Huege J, Feil R, et al. Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell. 2013;25:694–714. doi: 10.1105/tpc.112.106989. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

173. Rothschild A, Tandecarz JS. UDP-glucose:protein transglucosylase in developing maize endosperm. Plant Sci. 1994;98:119–127. doi: 10.1016/0168-9452(94)90048-5. [CrossRef] [Google Scholar]

174. Singh D, Lomako J, Lomako W, Whealan W, Meyer H, Serwe M, Metzger J. Βeta-glucosylarginine—a new glucose protein bond in a self-glucosylating protein from sweet corn. FEBS Lett. 1995;376:61–64. doi: 10.1016/0014-5793(95)01247-6. [PubMed] [CrossRef] [Google Scholar]

175. Langeveld SMJ, Vennik M, Kottenhagen M, Van Wijk R, Buijk A, Kijne JW, de Pater S. Glucosylation activity and complex formation of two classes of reversibly glycosylated polypeptides. Plant Physiol. 2002;129:278–289. doi: 10.1104/pp.010720. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

176. Drakakaki G, Zabotina O, Delgado I, Robert S, Keegstra K, Raikhel N. Arabidopsis reversibly glycosylated polypeptides 1 and 2 are essential for pollen development. Plant Physiol. 2006;142:1480–1492. doi: 10.1104/pp.106.086363. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

177. Chatterjee M, Berbezy P, Vyas D, Coates S, Barsby T. Reduced expression of a protein homologous to glycogenin leads to reduction of starch content in Arabidopsis leaves. Plant Sci. 2005;168:501–509. doi: 10.1016/j.plantsci.2004.09.015. [CrossRef] [Google Scholar]

178. Tetlow IJ, Emes MJ. A review of starch-branching enzymes and their role in amylopectin biosynthesis. IUBMB Life. 2014;66:546–558. doi: 10.1002/iub.1297. [PubMed] [CrossRef] [Google Scholar]

179. Dumez S, Wattebled F, Dauvillee D, Delvalle D, Planchot V, Ball SG, D’Hulst C. Mutants of Arabidopsis lacking starch branching enzyme II substitute plastidial starch synthesis by cytoplasmic maltose accumulation. Plant Cell. 2006;18:2694–2709. doi: 10.1105/tpc.105.037671. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

180. Gao M, Fisher DK, Kim K-N, Shannon JC, Guiltinan MJ. Evolutionary conservation and expression patterns of maize starch branching enzyme I and IIb genes suggests isoform specialization. Plant Mol Biol. 1996;30:1223–1232. doi: 10.1007/BF00019554. [PubMed] [CrossRef] [Google Scholar]

181. Gao M, Fisher DK, Kim K-N, Shannon JC, Guiltinan MJ. lndependent genetic control of maize starch-branching enzymes IIa and llb. Plant Physiol. 1997;114:69–78. doi: 10.1104/pp.114.1.69. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

182. Yamanouchi H, Nakamura Y. Organ specificity of isoforms of starch branching enzyme (Q-enzyme) in rice. Plant Cell Physiol. 1992;33:985–991. [Google Scholar]

183. Sun C, Sathish P, Ahlandsberg S, Jansson C. The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. Plant Physiol. 1998;118:37–49. doi: 10.1104/pp.118.1.37. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

184. Han Y, Sun FJ, Rosales-Mendoza S, Korban SS. Three orthologs in rice, Arabidopsis, and Populus encoding starch branching enzymes (SBEs) are different from other SBE gene families in plants. Gene. 2007;401:123–130. doi: 10.1016/j.gene.2007.06.026. [PubMed] [CrossRef] [Google Scholar]

185. Wang X, Xue L, Sun J, Zuo J. The Arabidopsis BE1 gene, encoding a putative glycoside hydrolase localized in plastids, plays crucial roles during embryogenesis and carbohydrate metabolism. J Integr Plant Biol. 2010;52:273–288. doi: 10.1111/j.1744-7909.2010.00930.x. [PubMed] [CrossRef] [Google Scholar]

186. Takeda Y, Guan HP, Preiss J. Branching of amylose by the branching isoenzymes of maize endosperm. Carbohydr Res. 1993;240:253–263. doi: 10.1016/0008-6215(93)84188-C. [CrossRef] [Google Scholar]

187. Guan HP, Preiss J. Differentiation of the properties of the branching isozymes from maize (Zea mays) Plant Physiol. 1993;102:1269–1273. [PMC free article] [PubMed] [Google Scholar]

188. Guan H, Li P, Imparl-Radosevich J, Preiss J, Keeling P. Comparing the properties of Escherichia coli branching enzyme and maize branching enzyme. Arch Biochem Biophys. 1997;342:92–98. doi: 10.1006/abbi.1997.0115. [PubMed] [CrossRef] [Google Scholar]

189. Rydberg U, Andersson L, Andersson R, Åman P, Larsson H. Comparison of starch branching enzyme I and II from potato. Eur J Biochem. 2001;268:6140–6145. doi: 10.1046/j.0014-2956.2001.02568.x. [PubMed] [CrossRef] [Google Scholar]

190. Nakamura Y, Utsumi Y, Sawada T, Aihara S, Utsumi C, Yoshida M, Kitamura S. Characterization of the reactions of starch branching enzymes from rice endosperm. Plant Cell Physiol. 2010;51:776–794. doi: 10.1093/pcp/pcq035. [PubMed] [CrossRef] [Google Scholar]

191. Sawada T, Nakamura Y, Ohdan T, Saitoh A, Francisco PB, Suzuki E, Fujita N, et al. Diversity of reaction characteristics of glucan branching enzymes and the fine structure of α-glucan from various sources. Arch Biochem Biophys. 2014;562:9–21. doi: 10.1016/j.abb.2014.07.032. [PubMed] [CrossRef] [Google Scholar]

192. Lu K-J, Streb S, Meier F, Pfister B, Zeeman SC. Molecular genetic analysis of glucan branching enzymes from plants and bacteria in Arabidopsis reveals marked differences in their functions and capacity to mediate starch granule formation. Plant Physiol. 2015;169:1638–1655. doi: 10.1104/pp.15.00921. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

193. Boyer L, Roussel X, Courseaux A, Ndjindji OM, Lancelon-Pin C, Putaux J-L, Tetlow I, et al. Expression of E. coli glycogen branching enzyme in an Arabidopsis mutant devoid of endogenous starch branching enzymes induces the synthesis of starch-like polyglucans. Plant Cell. 2015 [PubMed] [Google Scholar]

194. Blauth SL, Kim KN, Klucinec J, Shannon JC, Thompson D, Guiltinan M. Identification of mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays L. Plant Mol Biol. 2002;48:287–297. doi: 10.1023/A:1013335217744. [PubMed] [CrossRef] [Google Scholar]

195. Xia H, Yandeau-Nelson M, Thompson DB, Guiltinan MJ. Deficiency of maize starch-branching enzyme I results in altered starch fine structure, decreased digestibility and reduced coleoptile growth during germination. BMC Plant Biol. 2011;11:95. doi: 10.1186/1471-2229-11-95. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

196. Satoh H, Nishi A, Yamashita K, Takemoto Y, Tanaka Y, Hosaka Y, Sakurai A, Fujita N, Nakamura Y. Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiol. 2003;133:1111–1121. doi: 10.1104/pp.103.021527. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

197. Regina A, Kosar-Hashemi B, Li Z, Rampling L, Cmiel M, Gianibelli MC, Konik-Rose C, Larroque O, Rahman S, Morell MK. Multiple isoforms of starch branching enzyme-I in wheat: lack of the major SBE-I isoform does not alter starch phenotype. Funct Plant Biol. 2004;31:591–601. doi: 10.1071/FP03193. [CrossRef] [Google Scholar]

198. Safford R, Jobling SA, Sidebottom CM, Westcott RJ, Cooke D, Tober KJ, Strongitharm BH, Russell AL, Gidley MJ. Consequences of antisense RNA inhibition of starch branching enzyme activity on properties of potato starch. Carbohydr Polym. 1998;35:155–168. doi: 10.1016/S0144-8617(97)00249-X. [CrossRef] [Google Scholar]

199. Hedman KD, Boyer CD. Gene dosage at the amylose-extender locus of maize: effects on the levels of starch branching enzymes. Biochem Genet. 1982;20:483–492. doi: 10.1007/BF00484699. [PubMed] [CrossRef] [Google Scholar]

200. Mizuno K, Kawasaki T, Shimada H, Satoh H, Kobayashi E, Okumura S, Arai Y, Baba T. Alteration of the structural properties of starch components by the lack of an isoform of starch branching enzyme in rice seeds. J Biol Chem. 1993;268:19084–19091. [PubMed] [Google Scholar]

201. Sestili F, Janni M, Doherty A, Botticella E, D’Ovidio R, Masci S, Jones HD, Lafiandra D. Increasing the amylose content of durum wheat through silencing of the SBEIIa genes. BMC Plant Biol. 2010;10:144. doi: 10.1186/1471-2229-10-144. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

202. Boyer CD, Damewood PA, Matters GL. Effect of gene dosage at high amylose loci on the properties of the amylopectin fractions of the starches. Starch/Stärke. 1980;7:217–222. doi: 10.1002/star.19800320702. [CrossRef] [Google Scholar]

203. Bhattacharyya MK, Smith AM, Ellis THN, Hedley C, Martin C. The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme. Cell. 1990;60:115–122. doi: 10.1016/0092-8674(90)90721-P. [PubMed] [CrossRef] [Google Scholar]

204. Regina A, Bird A, Topping D, Bowden S, Freeman J, Barsby T, Kosar-Hashemi B, Li Z, Rahman S, Morell M. High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats. Proc Natl Acad Sci. 2006;103:3546–3551. doi: 10.1073/pnas.0510737103. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

205. Regina A, Kosar-Hashemi B, Ling S, Li Z, Rahman S, Morell M. Control of starch branching in barley defined through differential RNAi suppression of starch branching enzyme IIa and IIb. J Exp Bot. 2010;61:1469–1482. doi: 10.1093/jxb/erq011. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

206. Nishi A, Nakamura Y, Tanaka N, Satoh H. Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiol. 2001;127:459–472. doi: 10.1104/pp.010127. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

207. Butardo VM, Fitzgerald MA, Bird AR, Gidley MJ, Flanagan BM, Larroque O, Resurreccion AP, et al. Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA- and hairpin RNA-mediated RNA silencing. J Exp Bot. 2011;62:4927–4941. doi: 10.1093/jxb/err188. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

208. Asai H, Abe N, Matsushima R, Crofts N, Oitome NF, Nakamura Y, Fujita N. Deficiencies in both starch synthase IIIa and branching enzyme IIb lead to a significant increase in amylose in SSIIa-inactive japonica rice seeds. J Exp Bot. 2014;65:5497–5507. doi: 10.1093/jxb/eru310. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

209. Tanaka N, Fujita N, Nishi A, Satoh H, Hosaka Y, Ugaki M, Kawasaki S, Nakamura Y. The structure of starch can be manipulated by changing the expression levels of starch branching enzyme IIb in rice endosperm. Plant Biotechnol J. 2004;2:507–516. doi: 10.1111/j.1467-7652.2004.00097.x. [PubMed] [CrossRef] [Google Scholar]

210. Jobling SA, Schwall GP, Westcott RJ, Sidebottom CM, Debet M, Gidley MJ, Jeffcoat R, Safford R. A minor form of starch branching enzyme in potato (Solanum tuberosum L.) tubers has a major effect on starch structure: cloning and characterisation of multiple forms of SBE A. Plant J. 1999;18:163–171. doi: 10.1046/j.1365-313X.1999.00441.x. [PubMed] [CrossRef] [Google Scholar]

211. Schwall GP, Safford R, Westcott RJ, Jeffcoat R, Tayal A, Shi YC, Gidley MJ, Jobling SA. Production of very-high-amylose potato starch by inhibition of SBE A and B. Nat Biotechnol. 2000;18:551–554. doi: 10.1038/75427. [PubMed] [CrossRef] [Google Scholar]

212. Brummell DA, Watson LM, Zhou J, McKenzie MJ, Hallett IC, Simmons L, Carpenter M, Timmerman-Vaughan GM. Overexpression of STARCH BRANCHING ENZYME II increases short-chain branching of amylopectin and alters the physicochemical properties of starch from potato tuber. BMC Biotechnol. 2015;15:28. doi: 10.1186/s12896-015-0143-y. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

213. Blauth SL, Yao Y, Klucinec JD, Shannon JC, Thompson DB, Guilitinan MJ. Identification of mutator insertional mutants of starch-branching enzyme 2a in corn. Plant Physiol. 2001;125:1396–1405. doi: 10.1104/pp.125.3.1396. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

214. Yandeau-Nelson MD, Laurens L, Shi Z, Xia H, Smith AM, Guiltinan MJ. Starch-branching enzyme IIa is required for proper diurnal cycling of starch in leaves of maize. Plant Physiol. 2011;156:479–490. doi: 10.1104/pp.111.174094. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

215. Zeeman SC, Kossmann J, Smith AM. Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol. 2010;61:209–234. doi: 10.1146/annurev-arplant-042809-112301. [PubMed] [CrossRef] [Google Scholar]

216. Hizukuri S, Abe J, Hanashiro I. Starch: analytical aspects. In: Eliasson A-C, editor. Carbohydrates in food. Boca Raton: CRC Press; 2006. pp. 305–390. [Google Scholar]

217. Dinges JR, Colleoni C, James MG, Myers AM. Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism. Plant Cell. 2003;15:666–680. doi: 10.1105/tpc.007575. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

218. Wattebled F, Dong Y, Dumez S, Delvallé D, Planchot V, Berbezy P, Vyas D, et al. Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin. Plant Physiol. 2005;138:184–195. doi: 10.1104/pp.105.059295. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

219. Delatte T, Umhang M, Trevisan M, Eicke S, Thorneycroft D, Smith SM, Zeeman SC. Evidence for distinct mechanisms of starch granule breakdown in plants. J Biol Chem. 2006;281:12050–12059. doi: 10.1074/jbc.M513661200. [PubMed] [CrossRef] [Google Scholar]

220. Yun MS, Umemoto T, Kawagoe Y. Rice debranching enzyme Isoamylase3 facilitates starch metabolism and affects plastid morphogenesis. Plant Cell Physiol. 2011;52:1068–1082. doi: 10.1093/pcp/pcr058. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

221. Kubo A, Fujita N, Harada K, Matsuda T, Satoh H, Nakamura Y. The starch-debranching enzymes isoamylase and pullulanase are both involved in amylopectin biosynthesis in rice endosperm. Plant Physiol. 1999;121:399–410. doi: 10.1104/pp.121.2.399. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

222. Fujita N, Toyosawa Y, Utsumi Y, Higuchi T, Hanashiro I, Ikegami A, Akuzawa S, et al. 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. 2009;60:1009–1023. doi: 10.1093/jxb/ern349. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

223. Wattebled F, Planchot V, Dong Y, Szydlowski N, Pontoire B, Devin A, Ball S, D’Hulst C. 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. 2008;148:1309–1323. doi: 10.1104/pp.108.129379. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

224. Pan D, Nelson OE. A debranching enzyme deficiency in endosperms of the sugary-1 mutants of maize. Plant Physiol. 1984;74:324–328. doi: 10.1104/pp.74.2.324. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

225. James MG, Robertson DS, Myers AM. Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell. 1995;7:417–429. doi: 10.1105/tpc.7.4.417. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

226. Nakamura Y, Umemoto T, Takahata Y, Komae K, Amano E, Satoh H. Changes in structure of starch and enzyme activities affected by sugary mutations in developing rice endosperm. Possible role of starch debranching enzyme (R-enzyme) in amylopectin biosynthesis. Physiol Plant. 1996;97:491–498. doi: 10.1111/j.1399-3054.1996.tb00508.x. [CrossRef] [Google Scholar]

227. Burton RA, Jenner H, Carrangis L, Fahy B, Fincher GB, Hylton C, Laurie DA, et al. Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. Plant J. 2002;31:97–112. doi: 10.1046/j.1365-313X.2002.01339.x. [PubMed] [CrossRef] [Google Scholar]

228. Bustos R, Fahy B, Hylton CM, Seale R, Nebane NM, Edwards A, Martin C, Smith AM. Starch granule initiation is controlled by a heteromultimeric isoamylase in potato tubers. Proc Natl Acad Sci. 2004;101:2215–2220. doi: 10.1073/pnas.0305920101. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

229. Mouille G, Maddelein ML, Libessart N, Talaga P, Decq A, Delrue B, Ball S. Preamylopectin processing: a mandatory step for starch biosynthesis in plants. Plant Cell. 1996;8:1353–1366. doi: 10.1105/tpc.8.8.1353. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

230. Sumner J, Somers G. The water-soluble polysaccharides of sweet corn. Arch Biochem. 1944;4:7–9. [Google Scholar]

231. Fujita N, Hanashiro I, Suzuki S, Higuchi T, Toyosawa Y, Utsumi Y, Itoh R, Aihara S, Nakamura Y. Elongated phytoglycogen chain length in transgenic rice endosperm expressing active starch synthase IIa affects the altered solubility and crystallinity of the storage α-glucan. J Exp Bot. 2012;63:5859–5872. doi: 10.1093/jxb/ers235. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

232. Ball S, Guan HP, James M, Myers A, Keeling P, Mouille G, Buléon A, Colonna P, Preiss J. From glycogen to amylopectin: a model for the biogenesis of the plant starch granule. Cell. 1996;86:349–352. doi: 10.1016/S0092-8674(00)80107-5. [PubMed] [CrossRef] [Google Scholar]

233. Zeeman SC, Umemoto T, Lue WL, Au-Yeung P, Martin C, Smith AM, Chen J. A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell. 1998;10:1699–1712. doi: 10.1105/tpc.10.10.1699. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

234. Lin Q, Facon M, Putaux JL, Dinges JR, Wattebled F, D’Hulst C, Hennen-Bierwagen TA, Myers AM. Function of isoamylase-type starch debranching enzymes ISA1 and ISA2 in the Zea mays leaf. New Phytol. 2013;200:1009–1021. doi: 10.1111/nph.12446. [PubMed] [CrossRef] [Google Scholar]

235. Sundberg M, Pfister B, Fulton D, Bischof S, Delatte T, Eicke S, Stettler M, Smith SM, Streb S, Zeeman SC. The heteromultimeric debranching enzyme involved in starch synthesis in Arabidopsis requires both Isoamylase1 and Isoamylase2 subunits for complex stability and activity. PLoS One. 2013;8:e75223. doi: 10.1371/journal.pone.0075223. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

236. Zeeman SC, Northrop F, Smith AM, Rees T. A starch-accumulating mutant of Arabidopsis thaliana deficient in a chloroplastic starch-hydrolysing enzyme. Plant J. 1998;15:357–365. doi: 10.1046/j.1365-313X.1998.00213.x. [PubMed] [CrossRef] [Google Scholar]

237. Facon M, Lin Q, Azzaz AM, Hennen-Bierwagen TA, Myers AM, Putaux J-L, Roussel X, D’Hulst C, Wattebled F. Distinct functional properties of isoamylase-type starch debranching enzymes in monocot and dicot leaves. Plant Physiol. 2013;163:1363–1375. doi: 10.1104/pp.113.225565. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

238. Hussain H, Mant A, Seale R, Zeeman S, Hinchliffe E, Edwards A, Hylton C, et al. Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans. Plant Cell. 2003;15:133–149. doi: 10.1105/tpc.006635. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

239. Deschamps P, Moreau H, Worden AZ, Dauvillée D, Ball SG. Early gene duplication within chloroplastida and its correspondence with relocation of starch metabolism to chloroplasts. Genetics. 2008;178:2373–2387. doi: 10.1534/genetics.108.087205. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

240. Utsumi Y, Nakamura Y. Structural and enzymatic characterization of the Isoamylase1 homo-oligomer and the Isoamylase1-Isoamylase2 hetero-oligomer from rice endosperm. Planta. 2006;225:75–87. doi: 10.1007/s00425-006-0331-z. [PubMed] [CrossRef] [Google Scholar]

241. Kubo A, Colleoni C, Dinges JR, Lin Q, Lappe RR, Rivenbark JG, Meyer AJ, et al. Functions of heteromeric and homomeric isoamylase-type starch-debranching enzymes in developing maize endosperm. Plant Physiol. 2010;153:956–969. doi: 10.1104/pp.110.155259. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

242. Sim L, Beeren SR, Findinier J, Dauville D, Ball SG, Henriksen A, Palcic MM. Crystal structure of the Chlamydomonas starch debranching enzyme isoamylase ISA1 reveals insights into the mechanism of branch trimming and complex assembly. J Biol Chem. 2014;289:22991–23003. doi: 10.1074/jbc.M114.565044. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

243. Utsumi Y, Utsumi C, Sawada T, Fujita N, Nakamura Y. Functional diversity of isoamylase oligomers: the ISA1 homo-oligomer is essential for amylopectin biosynthesis in rice endosperm. Plant Physiol. 2011;156:61–77. doi: 10.1104/pp.111.173435. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

244. Luo J, Ahmed R, Kosar-Hashemi B, Larroque O, Butardo VM, Tanner GJ, Colgrave ML, et al. The different effects of starch synthase IIa mutations or variation on endosperm amylose content of barley, wheat and rice are determined by the distribution of starch synthase I and starch branching enzyme IIb between the starch granule and amyloplast stroma. Theor Appl Genet. 2015;128:1407–1419. doi: 10.1007/s00122-015-2515-z. [PubMed] [CrossRef] [Google Scholar]

245. Liu F, Romanova N, Lee EA, Ahmed R, Evans M, Gilbert EP, Morell MK, Emes MJ, Tetlow I. Glucan affinity of starch synthase IIa determines binding of starch synthase I and starch branching enzyme IIb to starch granules. Biochem J. 2012;448:373–387. doi: 10.1042/BJ20120573. [PubMed] [CrossRef] [Google Scholar]

246. Liu F, Ahmed Z, Lee EA, Donner E, Liu Q, Ahmed R, Morell MK, Emes MJ, Tetlow IJ. Allelic variants of the amylose extender mutation of maize demonstrate phenotypic variation in starch structure resulting from modified protein–protein interactions. J Exp Bot. 2012;63:1167–1183. doi: 10.1093/jxb/err341. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

247. Makhmoudova A, Williams D, Brewer D, Massey S, Patterson J, Silva A, Vassall KA, et al. Identification of multiple phosphorylation sites on maize endosperm starch branching enzyme IIb, a key enzyme in amylopectin biosynthesis. J Biol Chem. 2014;289:9233–9246. doi: 10.1074/jbc.M114.551093. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

248. Kötting O, Pusch K, Tiessen A, Geigenberger P, Steup M, Ritte G. Identification of a novel enzyme required for starch metabolism in Arabidopsis leaves. The phosphoglucan, water dikinase. Plant Physiol. 2005;137:242–252. doi: 10.1104/pp.104.055954. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

249. Ritte G, Heydenreich M, Mahlow S, Haebel S, Kötting O, Steup M. Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinases. FEBS Lett. 2006;580:4872–4876. doi: 10.1016/j.febslet.2006.07.085. [PubMed] [CrossRef] [Google Scholar]

250. Edner C, Li J, Albrecht T, Mahlow S, Hejazi M, Hussain H, Kaplan F, et al. Glucan, water dikinase activity stimulates breakdown of starch granules by plastidial beta-amylases. Plant Physiol. 2007;145:17–28. doi: 10.1104/pp.107.104224. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

251. Kötting O, Santelia D, Edner C, Eicke S, Marthaler T, Gentry MS, Comparot-Moss S, et al. STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell. 2009;21:334–346. doi: 10.1105/tpc.108.064360. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

252. Santelia D, Kötting O, Seung D, Schubert M, Thalmann M, Bischof S, Meekins DA, et al. The phosphoglucan phosphatase Like Sex Four2 dephosphorylates starch at the C3-position in Arabidopsis. Plant Cell. 2011;23:4096–4111. doi: 10.1105/tpc.111.092155. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

253. Silver DM, Kötting O, Moorhead GBG. Phosphoglucan phosphatase function sheds light on starch degradation. Trends Plant Sci. 2014;19:471–478. doi: 10.1016/j.tplants.2014.01.008. [PubMed] [CrossRef] [Google Scholar]

254. Hejazi M, Mahlow S, Fettke J. The glucan phosphorylation mediated by α-glucan, water dikinase (GWD) is also essential in the light phase for a functional transitory starch turn-over. Plant Signal Behav. 2014;9:e28892. doi: 10.4161/psb.28892. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

255. Nielsen TH, Wischmann B, Enevoldsen K, Moller BL. Starch phosphorylation in potato tubers proceeds concurrently with de novo biosynthesis of starch. Plant Physiol. 1994;105:111–117. [PMC free article] [PubMed] [Google Scholar]

256. Mahlow S, Hejazi M, Kuhnert F, Garz A, Brust H, Baumann O, Fettke J. Phosphorylation of transitory starch by α-glucan, water dikinase during starch turnover affects the surface properties and morphology of starch granules. New Phytol. 2014;203:495–507. doi: 10.1111/nph.12801. [PubMed] [CrossRef] [Google Scholar]

257. Skeffington AW, Graf A, Duxbury Z, Gruissem W, Smith AM. Glucan, water dikinase exerts little control over starch degradation in Arabidopsis leaves at night. Plant Physiol. 2014;165:866–879. doi: 10.1104/pp.114.237016. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

258. Shimoura S, Nagai M, Fukui T. Comparative glucan specificities of two types of spinach leaf phosphorylase. J Biochem. 1982;91:703–717. [PubMed] [Google Scholar]

259. Yu Y, Mu HH, Wasserman BP, Carman GM. Identification of the maize amyloplast stromal 112-kD protein as a plastidic starch phosphorylase. Plant Physiol. 2001;125:351–359. doi: 10.1104/pp.125.1.351. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

260. Tiessen A, Nerlich A, Faix B, Hümmer C, Fox S, Trafford K, Weber H, Weschke W, Geigenberger P. Subcellular analysis of starch metabolism in developing barley seeds using a non-aqueous fractionation method. J Exp Bot. 2012;63:2071–2087. doi: 10.1093/jxb/err408. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

261. Satoh H, Shibahara K, Tokunaga T, Nishi A, Tasaki M, Hwang S-K, Okita TW, et al. Mutation of the plastidial alpha-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. Plant Cell. 2008;20:1833–1849. doi: 10.1105/tpc.107.054007. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

262. Hwang S-K, Nishi A, Satoh H, Okita TW. Rice endosperm-specific plastidial alpha-glucan phosphorylase is important for synthesis of short-chain malto-oligosaccharides. Arch Biochem Biophys. 2010;495:82–92. doi: 10.1016/j.abb.2009.12.023. [PubMed] [CrossRef] [Google Scholar]

263. Higgins JE, Kosar-Hashemi B, Li Z, Howitt CA, Larroque O, Flanagan B, Morell MK, Rahman S. Characterization of starch phosphorylases in barley grains. J Sci Food Agric. 2013;93:2137–2145. doi: 10.1002/jsfa.6019. [PubMed] [CrossRef] [Google Scholar]

264. Kossmann J, Visser RGF, Müller-Röber BT, Willmitzer L, Sonnewald U. Cloning and expression analysis of a potato cDNA that encodes branching enzyme: evidence for co-expression of starch biosynthetic genes. Mol Gen Genet. 1991;230:39–44. doi: 10.1007/BF00290648. [PubMed] [CrossRef] [Google Scholar]

265. Ozbun JL, Hawker JS, Greenberg E, Lammel C, Preiss J. Starch synthetase, phosphorylase, ADPglucose pyrophosphorylase, and UDPglucose pyrophosphorylase in developing maize kernels. Plant Physiol. 1973;51:1–5. doi: 10.1104/pp.51.1.1. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

266. Schupp N, Ziegler P. The relation of starch phosphorylases to starch metabolism in wheat. Plant Cell Physiol. 2004;45:1471–1484. doi: 10.1093/pcp/pch270. [PubMed] [CrossRef] [Google Scholar]

267. Dauvillée D, Chochois V, Steup M, Haebel S, Eckermann N, Ritte G, Ral JP, et al. Plastidial phosphorylase is required for normal starch synthesis in Chlamydomonas reinhardtii. Plant J. 2006;48:274–285. doi: 10.1111/j.1365-313X.2006.02870.x. [PubMed] [CrossRef] [Google Scholar]

268. Subasinghe RM, Liu F, Polack UC, Lee EA, Emes MJ, Tetlow IJ. Multimeric states of starch phosphorylase determine protein–protein interactions with starch biosynthetic enzymes in amyloplasts. Plant Physiol Biochem. 2014;83:168–179. doi: 10.1016/j.plaphy.2014.07.016. [PubMed] [CrossRef] [Google Scholar]

269. Sonnewald U, Basner A, Greve B, Steup M. A second L-type isozyme of potato glucan phosphorylase: cloning, antisense inhibition and expression analysis. Plant Mol Biol. 1995;27:567–576. doi: 10.1007/BF00019322. [PubMed] [CrossRef] [Google Scholar]

270. Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H, Haldimann P, Bechtold N, Smith AM, Smith SM. 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. 2004;135:849–858. doi: 10.1104/pp.103.032631. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

271. Devin A (2010) Etablissement de l’implication des α- et β-amylases et des α-glucanes phosphorylases au cours de la dégradation de l’amidon dans la feuille d’Arabidopsis thaliana. Dissertation, Université des Sciences et Technologies de Lille

272. Malinova I, Mahlow S, Alseekh S, Orawetz T, Fernie AR, Baumann O, Steup M, Fettke J. Double knockout mutants of Arabidopsis grown under normal conditions reveal that the plastidial phosphorylase isozyme participates in transitory starch metabolism. Plant Physiol. 2013;164:907–921. doi: 10.1104/pp.113.227843. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

273. Weise SE, Schrader SM, Kleinbeck KR, Sharkey TD. Carbon balance and circadian regulation of hydrolytic and phosphorolytic breakdown of transitory starch. Plant Physiol. 2006;141:879–886. doi: 10.1104/pp.106.081174. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

274. Peng C, Wang Y, Liu F, Ren Y, Zhou K, Lv J, Zheng M, et al. FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. Plant J. 2014;77:917–930. doi: 10.1111/tpj.12444. [PubMed] [CrossRef] [Google Scholar]

275. Feike D, Seung D, Graf A, Bischof S, Ellick T, Coiro M, Soyk S, Eicke S, Mettler T, Lu KJ, Trick M, Zeeman SC, Smith AM (2016) A novel starch-granule-associated protein required for the control of starch degradation in Arabidopsis thaliana leaves. Plant Cell (accepted) [PMC free article] [PubMed]

276. Han X, Wang Y, Liu X, Jiang L, Ren Y, Liu F, Peng C, et al. The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice. J Exp Bot. 2012;63:121–130. doi: 10.1093/jxb/err262. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

277. Wang Y, Ren Y, Liu X, Jiang L, Chen L, Han X, Jin M, et al. OsRab5a regulates endomembrane organization and storage protein trafficking in rice endosperm cells. Plant J. 2010;64:812–824. doi: 10.1111/j.1365-313X.2010.04370.x. [PubMed] [CrossRef] [Google Scholar]

278. Matsushima R, Maekawa M, Kusano M, Kondo H, Fujita N, Kawagoe Y, Sakamoto W. Amyloplast-localized SUBSTANDARD STARCH GRAIN4 protein influences the size of starch grains in rice endosperm. Plant Physiol. 2013;164:623–636. doi: 10.1104/pp.113.229591. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

279. Matsushima R, Maekawa M, Fujita N, Sakamoto W. A rapid, direct observation method to isolate mutants with defects in starch grain morphology in rice. Plant Cell Physiol. 2010;51:728–741. doi: 10.1093/pcp/pcq040. [PubMed] [CrossRef] [Google Scholar]

280. Zhang L, Ren Y, Lu B, Yang C, Feng Z, Liu Z, Chen J, et al. FLOURY ENDOSPERM7 encodes a regulator of starch synthesis and amyloplast development essential for peripheral endosperm development in rice. J Exp Bot. 2015 [PMC free article] [PubMed] [Google Scholar]

281. Wang JC, Xu H, Zhu Y, Liu QQ, Cai XL. OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. J Exp Bot. 2013;64:3453–3466. doi: 10.1093/jxb/ert187. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

282. Fu F-F, Xue H-W. Coexpression analysis identifies Rice Starch Regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol. 2010;154:927–938. doi: 10.1104/pp.110.159517. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

283. She K-C, Kusano H, Koizumi K, Yamakawa H, Hakata M, Imamura T, Fukuda M, et al. A novel factor FLOURY ENDOSPERM2 is involved in regulation of rice grain size and starch quality. Plant Cell. 2010;22:3280–3294. doi: 10.1105/tpc.109.070821. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

284. Streb S, Zeeman SC (2012) Starch metabolism in Arabidopsis. In: The Arabidopsis Book, Number 9. The American Society of Plant Biologists. doi:10.1199/tab.0160

285. Emanuelsson O, Nielsen H, von Heijne G. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 1999;8:978–984. doi: 10.1110/ps.8.5.978. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

286. McDonnell AV, Jiang T, Keating AE, Berger B. Paircoil2: improved prediction of coiled coils from sequence. Bioinformatics. 2006;22:356–358. doi: 10.1093/bioinformatics/bti797. [PubMed] [CrossRef] [Google Scholar]

287. Letunic I, Doerks T, Bork P. SMART: recent updates, new developments and status in 2015. Nucleic Acids Res. 2014;43:D257–D260. doi: 10.1093/nar/gku949. [PMC free article] [PubMed] [CrossRef] [Google Scholar]

How are starch molecules adapted for their function in plant cells?

Starch can be straight or branched and is used as energy storage for plants because it can form compact structures and is easily broken down. In cellulose, molecules are connected in opposite orientations. Cellulose is found in cell walls and gives plant cells protection and structure.

Why is starch good for storage in plants?

Plants store energy in the form of starch, instead of glucose, because starch is insoluble. This means that starch will not effect the water concentration inside cells and also it will not move away from the storage areas within the plant.

What are two features of starch that make it a good storage molecule?

Starch is an ideal storage molecule because: it is insoluble and therefore doesn't affect the water potential of the cell. it is large and therefore cannot diffuse from the cell. it is compact and therefore much can be stored in a small space.

What is a feature of starch?

Starch is a soft, white, tasteless powder that is insoluble in cold water, alcohol, or other solvents. The basic chemical formula of the starch molecule is (C6H10O5)n. Starch is a polysaccharide comprising glucose monomers joined in α 1,4 linkages.