Starch synthesis in the cereal endosperm

Current Opinion in Plant Biology

Volumn 6, Issue 3, 2003, Pages 215-222

  James, Martha G ^a   Denyer, Kay ^b   Myers, Alan M ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0038810286     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(03)00042-6     Document Type: Review

References (64)

1. Smith AM: The biosynthesis of starch granules. Biomacromolecules 2001, 2:335-341.
2. Myers AM, Morell MK, James MG, Ball SG: Recent progress toward understanding the amylopectin crystal. Plant Physiol 2000, 122:989-997.
3. Imberty A, Buleon A, Tran V, Perez S: Recent advances in knowledge of starch structure. Starch/Staerke 1991, 43:375-384.
4. Gallant DJ, Bouchet B, Baldwin PM: Microscopy of starch: evidence of a new level of granule organization. Carbohydrate Polymers 1997, 32:177-191.
5. Nakamura Y: Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant Cell Physiol 2002, 43:718-725. This review examines the contribution of each starch biosynthetic enzyme isoform toward determining the fine structure of amylopectin in rice. A model is presented that describes amylopectin synthesis in the endosperm as a two-step process. Branches are introduced and chains are elongated in the amorphous region to form a core for each new cluster, then branch formation and chain elongation proceeds in the crystalline region. As in the glucan-trimming model, ill-placed branches are cleared by DBEs.
6. Thorbjornsen T, Villand P, Kleczkowski LA, Olsen OA: A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare). Biochem J 1996, 313:149-154.
7. Shannon JC, Pien FM, Liu KC: Nucleotides and nucleotide sugars in developing maize endosperms (synthesis of ADP-glucose in brittle-1). Plant Physiol 1996, 110:835-843.
8. Giroux MJ, Hannah LC: ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Mol Gen Genet 1994, 243:400-408.
9. Denyer K, Dunlap F, Thorbjornsen T, Keeling P, Smith AM: The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial. Plant Physiol 1996, 112:779-785.
10. 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. A rapid screening method involving measurement of the ADPG to UDP-glucose ratio was used to infer the intracellular location of AGP. This study provides evidence that ADPG is synthesized primarily in the cytosol in the endosperms of all grasses, and in the plastids in the starch-storing organs of other plant species.
11. Beckles DM, Craig J, Smith AM: ADP-glucose pyrophosphorylase is located in the plastid in developing tomato fruit. Plant Physiol 2001, 126:261-266.
12. Burton RA, Johnson PE, Beckles DM, Fincher GB, Jenner H, Naldrett MJ, Denyer K: Characterization of the genes encoding the cytosolic and plastidial forms of ADP-glucose pyrophosphorylase in wheat endosperm. Plant Physiol 2002, 130:1464-1475. The authors show that cytosolic AGP accounts for most of the AGP activity in wheat endosperm. In wheat, as in barley, a gene that encodes the cytosolic AGP small subunit also produces a larger second transcript that is predicted to encode a transit peptide. The amino-acid sequence of the plastidial AGP small subunit does not, however, match that deduced for this second gene product. Thus, the gene encoding the plastidial AGP small subunit has not yet been identified.
13. Hannah LC, Shaw JR, Giroux MJ, Reyss A, Prioul JL, Bae JM, Lee JY: Maize genes encoding the small subunit of ADP-glucose pyrophosphorylase. Plant Physiol 2001, 127:173-183. Sequence comparison of the AGP small subunit genes from eudicots and monocots is used to infer how these genes evolved. Exon 1 sequences that include subcellular-targeting information are particularly diverse among species, even within the monocots, suggesting they have independent and relatively recent origins. This is a thorough and insightful study, limited only by the lack of sequence information for species and organs other than the storage organs of the major crops.
14. Sullivan TD: The maize brittle1 gene encodes amyloplast membrane polypeptides. Planta 1995, 196:477-484.
15. Shannon JC, Pein FM, Cao HP, Liu KC: Brittle-1, an adenylate translocator, facilitates transfer of extraplastidial synthesized ADP-glucose into amyloplasts of maize endosperms. Plant Physiol 1998, 117:1235-1252.
16. Mohlmann T, Tjaden J, Henrichs G, Quick WP, Hausler R, Neuhaus HE: ADP-glucose drives starch synthesis in isolated maize endosperm amyloplasts: characterization of starch synthesis and transport properties across the amyloplast envelope. Biochem J 1997, 324:503-509.
17. Emes MJ, Bowsher CG, Hedley C, Burrell MM, Scrase-Field ES, Tetlow IJ: Starch synthesis and carbon partitioning in developing endosperm. J Exp Bot 2003, 54:569-575.
18. Hannah LC: Starch synthesis in the maize endosperm. In Advances in Cellular and Molecular Biology of Plants, vol 4. Edited by Larkins BA, Vasil IK. Dordrecht, The Netherlands: Kluwer Academic Publishers; 1997:375-405.
19. 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 USA 2002, 99:1724-1729.
20. Gomez-Casati D, Iglesias AA: ADP-glucose pyrophosphorylase from wheat endosperm. Purification and characterization of an enzyme with novel regulatory properties. Planta 2002, 214:428-434.
21. Ballicora MA, Frueauf JB, Fu YB, Schurmann P, Preiss J: Activation of the potato tuber ADP-glucose pyrophosphorylase by thioredoxin. J Biol Chem 2000, 275:1315-1320.
22. Tiesen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farre EM, Geigenberger P: Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophorylase: a novel regulatory mechanism linking starch synthesis to sucrose supply. Plant Cell 2002, 14:2191-2213.
23. Cao H, James MG, Myers AM: Purification and characterization of soluble starch synthases from maize endosperm. Arch Biochem Biophys 2000, 373:135-146.
24. Nelson OE, Rines HW: The enzymatic deficiency in the waxy mutant of maize. Biochem Biophys Res Commun 1962, 9:297-300.
25. Shure M, Wessler S, Federoff N: Molecular identification and isolation of the Waxy locus in maize. Cell 1983, 35:225-233.
26. Tsai CY: The function of the waxy locus in starch synthesis in maize endosperm. Biochem Genet 1974, 11:83-96.
27. Fujita N, Hasegawa H, Taira T: The isolation and characterization of a waxy mutant of diploid wheat (Triticum monococcum L.). Plant Sci 2001, 160:595-602.
28. Denyer K, Johnson P, Zeeman S, Smith AM: The control of amylose synthesis. J Plant Physiol 2001, 158:479-487.
29. 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. Sequencing of the gene encoding a mutant form of GBSSI in several barley cultivars suggests that most waxy barleys carry the same mutation in GBSSI. This mutation likely arose in China in the 16th century. The mutation does not entirely eliminate the expression of GBSSI, but causes the expression of this enzyme to be restricted to the outer endosperm cells late in endosperm development.
30. 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. Investigation of the chain-length specificities of maize endosperm SSI shows that its preferred substrates are the shortest amylopectin chains. SSI tightly binds longer amylopectin chains, whereupon its catalytic activity diminishes or is lost. Thus, longer amylopectin chains are probably extended by isoforms other than SSI. This work strongly supports the idea that different SS isoforms perform specific roles in amylopectin synthesis.
31. Wang Y-J, White P, Pollack L, Jane J-L: Characterization of starch structures of 17 maize endosperm mutant genotypes with Oh43 inbred line background. Cereal Chem 1993, 70:171-179.
32. Gao M, Wanat J, Stinard PS, James MG, Myers AM: Characterization of dull1, a maize gene coding for a novel starch synthase. Plant Cell 1998, 10:399-412.
33. Harn C, Knight M, Ramakrishnan A, Guan H, Keeling PL, Wasserman BP: Isolation and characterization of the zSSIIa and zSSIIb starch synthase cDNA clones from maize endosperm. Plant Mol Biol 1998, 37:639-649.
34. 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. Analysis of the biochemical and genetic differences between japonica and indica varieties of rice, and the physico-chemical properties of their starch granules, reveals the role of SSIIa in elongating short- to intermediate-size chains in amylopectin. The strength of this study lies in the breadth of techniques brought to bear on a clearly defined question.
35. Takeda Y, Guan H-P, Preiss J: Branching of amylose by the branching isoenzymes of maize endosperm. Carbohydr Res 1993, 240:253-263.
36. Guan H, Preiss J: Differentiation of the properties of the branching isozymes from maize (Zea mays). Plant Physiol 1993, 102:1269-1273.
37. Mizuno K, Kobayashi E, Tachibana M, Kawasaki T, Fujimura T, Funane K, Kobayashi M, Baba T: Characterization of an isoform of rice starch branching enzyme, RBE4, in developing seeds. Plant Cell Physiol 2001, 42:349-357. A BEIIa homologue (RBE4) that has been characterized in rice is expressed earlier than either BEIIb (RBE3) or BEI (RBE1) in the developing endosperm. Comparisons of the lengths of branch chains transferred by recombinant rice BEs showed that the two BEII forms are similar, primarily transferring chains of DP6, whereas BEI branch products are DP6-11. BEIIb also transfers shorter chains after extended incubation but BEIIa does not.
38. Rahman S, Regina A, Li Z, Mukai Y, Yamamoto M, Kosar-Hashemi B, Abrahams S, Morell MK: Comparison of starch-branching enzyme genes reveals evolutionary relationships among isoforms. Characterization of a gene for starch-branching enzyme IIa from the wheat genome donor Aegilops tauschii. Plant Physiol 2001, 125:1314-1324.
39. Blauth SL, Kim KN, Klucinec J, Shannon JC, Thompson D, Guilitinan M: Identification of Mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays L. Plant Mol Biol 2002, 48:287-297.
40. 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. Analysis of a rice double mutant that is deficient in BEIIb and GBSSI (and consequently lacks the amylose component of starch) reveals the role of BEIIb in amylopectin synthesis. The function of BEIIb in the transfer of short chains within amylopectin is not complemented by BEIIa or BEI, suggesting that each BE isoform has a specific role.
41. 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.
42. Seo BS, Kim S, Scott MP, Singletary GW, Wong KS, James MG, Myers AM: Functional interactions between heterologously expressed starch-branching enzymes of maize and the glycogen synthases of Brewer's yeast. Plant Physiol 2002, 128:1189-1199. Heterologous expression of all three maize BEs in yeast, singly and in combination, shows that BEI functions only when expressed with both BEIIa and BEIIb. The activity of all three BEs produces a glucan that has significantly more branches than that produced when only BEIIa and BEIIb are functional. The authors predict that the BEs may act sequentially during glucan polymer construction, with the BEII isoforms producing precursor molecules that are suitable substrates for BEI activity.
43. 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.
44. Pan D, Nelson OE: A debranching enzyme deficiency in endosperms of the sugary-1 mutants of maize. Plant Physiol 1984, 74:324-328.
45. 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.
46. Burton RA, Jenner H, Carrangis L, Fahy B, Fincher GB, Hylton C, Laurie DA, Parker M, Waite D, van Wegen S et al.: Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity. Plant J 2002, 31:97-112. The authors of this paper suggest a new model for the role of the isoamylase-type DBE in the initiation of starch granules. Their model is based on the effects of barley isa-1 mutations on the numbers of starch granules in endosperm plastids. The emphasis is shifted away from a role for isoamylase in polymer synthesis during granule assembly to a role in the early events of granule formation. According to this model, phytoglycogen accumulation is relegated to a possible, but not an inevitable, consequence of isoamylase deficiency.
47. Dinges JR, Colleoni C, Myers AM, James MG: Molecular structure of three mutations at the maize sugary1 locus and their allele-specific phenotypic effects. Plant Physiol 2001, 125:1406-1418. Phenotypic differences among three alleles of su1 in maize reveal allele-specific pleiotropic effects on enzymes other than the SU1 protein, and suggest that there are specific interactions between the SU1 protein and other components of the starch-biosynthetic machinery. This paper, and other work from the same laboratory, highlights the potential importance of protein-protein interactions in starch biosynthesis.
48. Genschel U, Abel G, Lorz H, Lutticke S: The sugary-type isoamylase in wheat: tissue distribution and subcellular localisation. Planta 2002, 214:813-820.
49. Dinges JR, Colleoni C, James MG, Myers AM: Mutational analysis of the pullulanase-type debranching enzyme in maize indicates multiple functions in starch metabolism. Plant Cell 2003, 15:666-680.
50. Wu C, Colleoni C, Myers AM, James MG: Enzymatic properties and regulation of ZPU1, the maize pullulanase-type starch debranching enzyme. Arch Biochem Biophys 2002, 406:21-32. This biochemical characterization of the maize pullulanase-type DBE shows the enzyme to be endo-acting, to hydrolyze only very short chains, and to be subject to potential regulation by changes in redox status and sugar concentration in the endosperm.
51. Nielsen TH, Baunsgaard L, Blennow A: Intermediary glucan structures formed during starch granule biosynthesis are enriched in short side chains, a dynamic pulse labeling approach. J Biol Chem 2002, 277:20249-20255. In a new approach to the study of starch synthesis in vivo, this group used pulse labeling to reveal an intermediary starch form that is enriched in short chains of DP6-11 on the granule surface. The excessive branching is consistent with a role for DBEs in starch synthesis, but does not provide direct support for a particular model.
52. 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.
53. Asano T, Kunieda N, Omura Y, Ibe H, Kawasaki T, Takano M, Sato M, Furuhashi H, Mujin T, Takaiwa F et al.: Rice SPK, a calmodulin-like domain protein kinase, is required for storage product accumulation during seed development: phosphorylation of sucrose synthase is a possible factor. Plant Cell 2002, 14:619-628. Activation of sucrose synthase via phosphorylation is required for storage product synthesis in rice seeds. Absence of the protein kinase SPK, which is responsible for sucrose synthase phosphorylation, results in watery inviable seeds and represses the activity of several enzymes, including BEI.
54. Chung HJ, Sehnke PC, Ferl RJ: The 14-3-3 proteins: cellular regulators of plant metabolism. Trends Plant Sci 1999, 4:367-371.
55. Sehnke PC, Chung HJ, Wu K, Ferl RJ: Regulation of starch accumulation by granule-associated plant 14-3-3 proteins. Proc Natl Acad Sci USA 2001, 98:765-770.
56. Shannon JC, Garwood DL: Genetics and physiology of starch development. In Starch; Chemistry and Technology. Edited by Whistler RL, BeMiller JN, Paschall EF. Orlando, FL: Academic Press; 1984:25-68.
57. Barry GF: The use of the Monsanto draft rice genome sequence in research. Plant Physiol 2001, 125:1164-1165.
58. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H et al.: A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 2002, 296:92-100. This paper reports the draft sequence of the genome of the japonica subspecies of rice. This milestone event represents the first near-compete sequence of a cereal genome, and thus provides a foundation for acquiring important sequence information for other cereal crops that will facilitate our understanding of starch biosynthesis.
59. Yuan Q, Quackenbush J, Sultana R, Pertea M, Salzberg SL, Buell CR: Rice bioinformatics. Analysis of rice sequence data and leveraging the data to other plant species. Plant Physiol 2001, 125:1166-1174.
60. Koller A, Washburn MP, Lange BM, Andon NL, Deciu C, Haynes PA, Hays L, Schieltz D, Ulaszek R, Wei J et al.: Proteomic survey of metabolic pathways in rice. Proc Natl Acad Sci USA 2002, 99:11969-11974. This group undertook the most complete proteomics analysis of rice to date. As part of this study, the tissue-specific expression of proteins that function in starch metabolism was examined, and new information was provided regarding tissue-specific forms of AGP.
61. Hunter BG, Beatty MK, Singletary GW, Hamaker BR, Dilkes BP, Larkins BA, Jung R: Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 2002, 14:2591-2612.
62. Beatty MK, Rahman A, Cao H, Woodman W, Lee M, Myers AM, James MG: Purification and molecular genetic characterization of ZPU1, a pullulanase-type starch debranching enzyme from maize. Plant Physiol 1999, 119:255-266.
63. Olsen KM, Purugganan MD: Molecular evidence on the origin and evolution of glutinous rice. Genetics 2002, 162:941-950.
64. Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES: Genetic diversity and selection in the maize starch pathway. Proc Natl Acad Sci USA 2002, 99:12959-12962. This study of nucleotide-sequence diversity in maize showed that genes in the starch biosynthetic pathway have dramatically lower diversity compared with random loci. This suggests that the starch pathway was critically important in maize evolution, exerting selective pressure for yield and/or grain quality.