Skip to content
BY-NC-ND 4.0 license Open Access Published by De Gruyter Open Access October 28, 2017

Recent progress toward understanding the role of starch biosynthetic enzymes in the cereal endosperm

  • Cheng Li , Prudence O. Powell and Robert G. Gilbert EMAIL logo
From the journal Amylase

Abstract

Starch from cereal endosperm is a major energy source for many mammals. The synthesis of this starch involves a number of different enzymes whose mode of action is still not completely understood. ADPglucose pyrophosphorylase is involved in the synthesis of starch monomer (ADP-glucose), a process, which almost exclusively takes place in the cytosol. ADPglucose is then transported into the amyloplast and incorporated into starch granules by starch synthase, starch-branching enzyme and debranching enzyme. Additional enzymes, including starch phosphorylase and disproportionating enzyme, may be also involved in the formation of starch granules, although their exact functions are still obscure. Interactions between these enzymes in the form of functional complexes have been proposed and investigated, resulting more complicated starch biosynthetic pathways. An overall picture and recent advances in understanding of the functions of these enzymes is summarized in this review to provide insights into how starch granules are synthesized in cereal endosperm.

References

[1] Gilbert R.G., Size-separation characterization of starch and glycogen for biosynthesis-structure-property relationships, Anal. Bioanal. Chem., 2011, 399, 1425-1438.10.1007/s00216-010-4435-8Search in Google Scholar

[2] Bertoft E., On the building block and backbone concepts of amylopectin structure, Cereal Chem., 2013, 90, 294-311.10.1094/CCHEM-01-13-0004-FISearch in Google Scholar

[3] Takeda Y., Shitaozono T., Hizukuri S., Structures of sub-fractions of corn amylose, Carbohydr. Res., 1990, 199, 207-214.10.1016/0008-6215(90)84262-SSearch in Google Scholar

[4] Li C., Gilbert R.G., Progress in controlling starch structure by modifying starch-branching enzymes, Planta, 2016, 243, 13-22.10.1007/s00425-015-2421-2Search in Google Scholar PubMed

[5] Blennow A., Jensen S.L., Shaik S.S., Skryhan K., Carciofi M., Holm P.B., et al., Future cereal starch bioengineering: cereal ancestors encounter gene technology and designer enzymes, Cereal Chem., 2013, 90, 274-287.10.1094/CCHEM-01-13-0010-FISearch in Google Scholar

[6] Tetlow I.J., Starch biosynthesis in developing seeds, Seed Sci. Res., 2010, 21, 5-32.10.1017/S0960258510000292Search in Google Scholar

[7] Pontis H.G., Babio J.R., Salerno G., Reversible unidirectional inhibition of sucrose synthase activity by disulfides, Proc. Natl. Acad. Sci. USA, 1981, 78, 6667-6669.10.1073/pnas.78.11.6667Search in Google Scholar PubMed PubMed Central

[8] Li J., Baroja-Fernandez E., Bahaji A., Munoz F.J., Ovecka M., Montero M., et al., Enhancing sucrose synthase activity results in increased levels of starch and ADP-glucose in maize (Zea mays L.) seed endosperms, Plant Cell Physiol., 2013, 54, 282-294.10.1093/pcp/pcs180Search in Google Scholar PubMed

[9] Baroja-Fernandez E., Munoz F.J., Montero M., Etxeberria E., Sesma M.T., Ovecka M., et al., Enhancing sucrose synthase activity in transgenic potato (Solanum tuberosum L.) tubers results in increased levels of starch, ADPglucose and UDPglucose and total yield, Plant Cell Physiol., 2009, 50, 1651-1662. 10.1093/pcp/pcp108Search in Google Scholar PubMed

[10] Thevenot C., Simond-Cote E., Reyss A., Manicacci D., Trouverie J., Le Guilloux M., et al., QTLs for enzyme activities and soluble carbohydrates involved in starch accumulation during grain filling in maize, J. Exp. Bot., 2005, 56, 945-958. 10.1093/jxb/eri087Search in Google Scholar PubMed

[11] Nagai Y.S., Sakulsingharoj C., Edwards G.E., Satoh H., Greene T.W., Blakeslee B., et al., Control of starch synthesis in cereals: metabolite analysis of transgenic rice expressing an up-regulated cytoplasmic ADP-glucose pyrophosphorylase in developing seeds, Plant Cell Physiol., 2009, 50, 635-643. 10.1093/pcp/pcp021Search in Google Scholar PubMed

[12] Baroja-Fernandez E., Munoz F.J., Li J., Bahaji A., Almagro G., Montero M., et al., Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production, Proc. Natl. Acad. Sci. USA, 2012, 109, 321-326. 10.1073/pnas.1117099109Search in Google Scholar PubMed PubMed Central

[13] Cumino A.C., Marcozzi C., Barreiro R., Salerno G.L., Carbon cycling in Anabaena sp. PCC 7120. Sucrose synthesis in the heterocysts and possible role in nitrogen fixation, Plant Physiol., 2007, 143, 1385-1397. 10.1104/pp.106.091736Search in Google Scholar PubMed PubMed Central

[14] Baroja-Fernandez E., Munoz F.J., Saikusa T., Rodriguez-Lopez M., Akazawa T., Pozueta-Romero J., Sucrose synthase catalyzes the de novo production of ADPglucose linked to starch biosynthesis in heterotrophic tissues of plants, Plant Cell Physiol., 2003, 44, 500-509. 10.1093/pcp/pcg062Search in Google Scholar PubMed

[15] Kirchberger S., Leroch M., Huynen M.A., Wahl M., Neuhaus H.E., Tjaden J., Molecular and biochemical analysis of the plastidic ADP-glucose transporter (ZmBT1) from Zea mays, J. Biol. Chem., 2007, 282, 22481-22491. 10.1074/jbc.M702484200Search in Google Scholar PubMed

[16] Shannon J.C., Pien F.M., Liu K.C., Nucleotides and nucleotide sugars in developing maize endosperms (synthesis of ADP-glucose in brittle-1), Plant Physiol., 1996, 110, 835-843. 10.1104/pp.110.3.835Search in Google Scholar PubMed PubMed Central

[17] Sullivan T.D., Strelow L.I., Illingworth C.A., Phillips R.L., Nelson Jr. O.E., Analysis of maize brittle-1 alleles and a defective suppressor-mutator-induced mutable allele, Plant Cell, 1991, 3, 1337-1348. 10.1105/tpc.3.12.1337Search in Google Scholar PubMed PubMed Central

[18] Weber A.P., Schwacke R., Flugge U.I., Solute transporters of the plastid envelope membrane, Annu. Rev. Plant Biol., 2005, 56, 133-164.10.1146/annurev.arplant.56.032604.144228Search in Google Scholar PubMed

[19] Jiang Y., Guo W., Zhu H., Ruan Y.L., Zhang T., Overexpression of GhSusA1 increases plant biomass and improves cotton fiber yield and quality, Plant Biotechnol. J., 2012, 10, 301-312. 10.1111/j.1467-7652.2011.00662.xSearch in Google Scholar PubMed

[20] Xu S.M., Brill E., Llewellyn D.J., Furbank R.T., Ruan Y.L., Overexpression of a potato sucrose synthase gene in cotton accelerates leaf expansion, reduces seed abortion, and enhances fiber production, Mol. Plant, 2012, 5, 430-441. 10.1093/mp/ssr090Search in Google Scholar PubMed

[21] Chourey P.S., Nelson O.E., The enzymatic deficiency conditioned by the shrunken-1 mutations in maize, Biochem. Genet., 1976, 14, 1041-1055. 10.1007/BF00485135Search in Google Scholar PubMed

[22] Asano T., Kunieda N., Omura Y., Ibe H., Kawasaki T., Takano M., 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. 10.1105/tpc.010454Search in Google Scholar PubMed PubMed Central

[23] Ballicora M.A., Dubay J.R., Devillers C.H., Preiss J., Resurrecting the ancestral enzymatic role of a modulatory subunit, J. Biol. Chem., 2005, 280, 10189-10195. 10.1074/jbc.M413540200Search in Google Scholar PubMed

[24] Geigenberger P., Kolbe A., Tiessen A., Redox regulation of carbon storage and partitioning in response to light and sugars, J. Exp. Bot., 2005, 56, 1469-1479. 10.1093/jxb/eri178Search in Google Scholar PubMed

[25] Tetlow I.J., Morell M.K., Emes M.J., Recent developments in understanding the regulation of starch metabolism in higher plants, J. Exp. Bot., 2004, 55, 2131-2145. 10.1093/jxb/erh248Search in Google Scholar PubMed

[26] Beckles D.M., Smith A.M., ap 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. 10.1104/pp.125.2.818Search in Google Scholar PubMed PubMed Central

[27] Beckles D.M., Craig J., Smith A.M., ADP-glucose pyrophosphorylase is located in the plastid in developing tomato fruit, Plant Physiol., 2001, 126, 261-266. 10.1104/pp.126.1.261Search in Google Scholar PubMed PubMed Central

[28] Giroux M.J., Hannah L.C., ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize, Mol. Gen. Genet., 1994, 243, 400-408. 10.1007/BF00280470Search in Google Scholar PubMed

[29] Denyer K., Dunlap F., Thorbjornsen T., Keeling P., Smith A.M., The major form of ADP-glucose pyrophosphorylase in maize endosperm is extra-plastidial, Plant Physiol., 1996, 112, 779-785. 10.1104/pp.112.2.779Search in Google Scholar PubMed PubMed Central

[30] Thorbjornsen T., Villand P., Kleczkowski L.A., Olsen O.A., A single gene encodes two different transcripts for the ADP-glucose pyrophosphorylase small subunit from barley (Hordeum vulgare), Biochem. J., 1996, 313, 149-154. 10.1042/bj3130149Search in Google Scholar PubMed PubMed Central

[31] Choi S.B., Kim K.H., Kavakli I.H., Lee S.K., Okita T.W., Transcriptional expression characteristics and subcellular localization of ADP-glucose pyrophosphorylase in the oil plant Perilla frutescens, Plant Cell Physiol., 2001, 42, 146-153. 10.1093/pcp/pce019Search in Google Scholar PubMed

[32] Bhave M.R., Lawrence S., Barton C., Hannah L.C., Identification and molecular characterization of shrunken-2 cDNA clones of maize, Plant Cell, 1990, 2, 581-588. 10.1105/tpc.2.6.581Search in Google Scholar PubMed PubMed Central

[33] Hannah L.C., Shaw J.R., Giroux M.J., Reyss A., Prioul J.L., Bae J.M., et al., Maize genes encoding the small subunit of ADP-glucose pyrophosphorylase, Plant Physiol., 2001, 127, 173-183. 10.1104/pp.127.1.173Search in Google Scholar PubMed PubMed Central

[34] Patron N.J., Greber B., Fahy B.F., Laurie D.A., Parker M.L., Denyer K., The lys5 mutations of barley reveal the nature and importance of plastidial ADP-Glc transporters for starch synthesis in cereal endosperm, Plant Physiol., 2004, 135, 2088-2097. 10.1104/pp.104.045203Search in Google Scholar PubMed PubMed Central

[35] Comparot-Moss S., Denyer K., The evolution of the starch biosynthetic pathway in cereals and other grasses, J. Exp. Bot., 2009, 60, 2481-2492. 10.1093/jxb/erp141Search in Google Scholar PubMed

[36] Preiss J., Biochemistry and molecular biology of glycogen synthesis in bacteria and mammals and starch synthesis in plants. Comprehensive Natural Products II, Oxford, Elsevier, 2010. 10.1016/B978-008045382-8.00644-4Search in Google Scholar

[37] Gross P., Ap Rees T., Alkaline inorganic pyrophosphatase and starch synthesis in amyloplasts, Planta, 1986, 167, 140-145. 10.1007/BF00446381Search in Google Scholar PubMed

[38] Hendriks J.H.M., Kolbe A., Gibon Y., Stitt M., Geigenberger P., ADP-glucose pyrophosphorylase is activated by posttranslational redox-modification in response to light and to sugars in leaves of Arabidopsis and other plant species, Plant Physiol., 2003, 133, 838-849. 10.1104/pp.103.024513Search in Google Scholar PubMed PubMed Central

[39] Sakulsingharoj C., Choi S.-B., Hwang S.-K., Edwards G.E., Bork J., Meyer C.R., et al., Engineering starch biosynthesis for increasing seed weight: the role of the cytoplasmic ADP-glucose pyrophosphorylase, Plant Sci., 2004, 167, 1323-1333. 10.1016/j.plantsci.2004.06.028Search in Google Scholar

[40] Smidansky E.D., Clancy M., Meyer F.D., Lanning S.P., Blake N.K., Talbert L.E., et al., Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield, Proc. Natl. Acad. Sci. USA, 2002, 99, 1724-1729. 10.1073/pnas.022635299Search in Google Scholar PubMed PubMed Central

[41] Smidansky E.D., Martin J.M., Hannah L.C., Fischer A.M., Giroux M.J., Seed yield and plant biomass increases in rice are conferred by deregulation of endosperm ADP-glucose pyrophosphorylase, Planta, 2003, 216, 656-664. 10.1007/s00425-002-0897-zSearch in Google Scholar

[42] Ball S., Guan H.P., James M., Myers A., Keeling P., Mouille G., et al., From glycogen to amylopectin: a model for the biogenesis of the plant starch granule, Cell, 1996, 86, 349-352. 10.1016/S0092-8674(00)80107-5Search in Google Scholar

[43] Nichols D.J., Keeling P.L., 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. 10.1021/bi000407gSearch in Google Scholar

[44] Gao Z., Keeling P., Shibles R., Guan H., Involvement of lysine-193 of the conserved “K-T-G-G” motif in the catalysis of maize starch synthase IIa, Arch. Biochem. Biophys., 2004, 427, 1-7. 10.1016/j.abb.2004.01.010Search in Google Scholar

[45] Jeon J.S., Ryoo N., Hahn T.R., Walia H., Nakamura Y., Starch biosynthesis in cereal endosperm, Plant Physiol. Biochem., 2010, 48, 383-392. 10.1016/j.plaphy.2010.03.006Search in Google Scholar

[46] Yoon J.W., Jung J.Y., Chung H.J., Kim M.R., Kim C.W., Lim S.T., Identification of botanical origin of starches by SDS-PAGE analysis of starch granule-associated proteins, J. Cereal Sci., 2010, 52, 321-326. 10.1016/j.jcs.2010.06.015Search in Google Scholar

[47] Ball S.G., van de Wal M.H.B.J., Visser R.G.F., Progress in understanding the biosynthesis of amylose, Trends Plant Sci., 1998, 3, 462-467. 10.1016/S1360-1385(98)01342-9Search in Google Scholar

[48] Seung D., Soyk S., Coiro M., Maier B.A., Eicke S., Zeeman S.C., 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. 10.1371/journal.pbio.1002080Search in Google Scholar PubMed PubMed Central

[49] Keeling P.L., Myers A.M., Biochemistry and genetics of starch synthesis, Annu. Rev. Food Sci. Technol., 2010, 1, 271-303. 10.1146/annurev.food.102308.124214Search in Google Scholar PubMed

[50] Denyer K., Waite D., Motawia S., Moller B.L., Smith A.M., Granule-bound starch synthase I in isolated starch granules elongates malto-oligosaccharides processively, Biochem. J., 1999, 340, 183-191. 10.1042/bj3400183Search in Google Scholar

[51] Fujita N., Kubo A., Suh D.S., Wong K.S., Jane J.L., Ozawa K., et al., Antisense inhibition of isoamylase alters the structure of amylopectin and the physicochemical properties of starch in rice endosperm, Plant Cell Physiol., 2003, 44, 607-618. 10.1093/pcp/pcg079Search in Google Scholar PubMed

[52] Delvalle D., Dumez S., Wattebled F., Roldan I., Planchot V., Berbezy 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. 10.1111/j.1365-313X.2005.02462.xSearch in Google Scholar PubMed

[53] Commuri P.D., Keeling P.L., Chain-length specificities of maize starch synthase I enzyme: studies of glucan affinity and catalytic properties, Plant J., 2001, 25, 475-486. 10.1046/j.1365-313x.2001.00955.xSearch in Google Scholar PubMed

[54] Fujita N., Yoshida M., Asakura N., Ohdan T., Miyao A., Hirochika H., et al., Function and characterization of starch synthase I using mutants in rice, Plant Physiol., 2006, 140, 1070-1084. 10.1104/pp.105.071845Search in Google Scholar PubMed PubMed Central

[55] Wang K., Henry R.J., Gilbert R.G., Causal relations among starch biosynthesis, structure, and properties, Springer Science Reviews, 2014, 2, 15-33. 10.1007/s40362-014-0016-0Search in Google Scholar

[56] Morell M.K., Kosar-Hashemi B., Cmiel M., Samuel M.S., Chandler P., Rahman S., et al., Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties, Plant J., 2003, 34, 173-185. 10.1046/j.1365-313X.2003.01712.xSearch in Google Scholar

[57] Mu-Forster C., Huang R., Powers J.R., Harriman R.W., Knight M., Singletary G.W., et al., 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. 10.1104/pp.111.3.821Search in Google Scholar PubMed PubMed Central

[58] Umemoto T., Aoki N., Single-nucleotide polymorphisms in rice starch synthase IIa that alter starch gelatinisation and starch association of the enzyme, Funct. Plant Biol., 2005, 32, 763-768. 10.1071/FP04214Search in Google Scholar PubMed

[59] Ryoo N., Yu C., Park C.S., Baik M.Y., Park I.M., Cho M.H., et al., Knockout of a starch synthase gene OsSSIIIa/Flo5 causes white-core floury endosperm in rice (Oryza sativa L.), Plant Cell Rep., 2007, 26, 1083-1095. 10.1007/s00299-007-0309-8Search in Google Scholar PubMed

[60] Fujita N., Yoshida M., Kondo T., Saito K., Utsumi Y., Tokunaga T., 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. 10.1104/pp.107.102533Search in Google Scholar PubMed PubMed Central

[61] Dian W.M., Jiang H.W., Wu P., Evolution and expression analysis of starch synthase III and IV in rice, J. Exp. Bot., 2005, 56, 623-632. 10.1093/jxb/eri065Search in Google Scholar PubMed

[62] Zeeman S.C., Kossmann J., Smith A.M., Starch: its metabolism, evolution, and biotechnological modification in plants, Annu. Rev. Plant Biol., 2010, 61, 209-234. 10.1146/annurev-arplant-042809-112301Search in Google Scholar PubMed

[63] Roldan I., Wattebled F., Mercedes Lucas M., Delvalle D., Planchot V., Jimenez S., et al., 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. 10.1111/j.1365-313X.2006.02968.xSearch in Google Scholar PubMed

[64] Crumpton-Taylor M., Pike M., Lu K.J., Hylton C.M., Feil R., Eicke S., et al., Starch synthase 4 is essential for coordination of starch granule formation with chloroplast division during Arabidopsis leaf expansion, New Phytol., 2013, 200, 1064-1075. 10.1111/nph.12455Search in Google Scholar PubMed PubMed Central

[65] Nielsen T.H., 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. 10.1074/jbc.M201866200Search in Google Scholar PubMed

[66] 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. 10.1006/abbi.1997.0115Search in Google Scholar PubMed

[67] Nakamura Y., Utsumi Y., Sawada T., Aihara S., Utsumi C., Yoshida M., et al., Characterization of the reactions of starch branching enzymes from rice endosperm, Plant Cell Physiol., 2010, 51, 776-794. 10.1093/pcp/pcq035Search in Google Scholar PubMed

[68] Wu A.C., Gilbert R.G., Molecular weight distributions of starch branches reveal genetic constraints on biosynthesis, Biomacromolecules, 2010, 11, 3539-3547.10.1021/bm1010189Search in Google Scholar PubMed

[69] Li C., Wu A.C., Go R.M., Malouf J., Turner M.S., Malde A.K., et al., The characterization of modified starch branching enzymes: toward the control of starch chain-length distributions, PLoS One, 2015, 10, e0125507. 10.1371/journal.pone.0125507Search in Google Scholar PubMed PubMed Central

[70] Liu Y., Li C., Gu Z., Xin C., Cheng L., Hong Y., et al., Alanine 310 is important for the activity of 1,4-α-glucan branching enzyme from Geobacillus thermoglucosidans STB02, Int. J. Biol. Macromol., 2017, 97, 156-163. 10.1016/j.ijbiomac.2017.01.028Search in Google Scholar PubMed

[71] Tetlow I.J., Wait R., Lu Z., Akkasaeng R., Bowsher C.G., Esposito S., et al., Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions, Plant Cell, 2004, 16, 694-708. 10.1105/tpc.017400Search in Google Scholar PubMed PubMed Central

[72] Morell M.K., Blennow A., Kosar-Hashemi B., Samuel M.S., Differential expression and properties of starch branching enzyme isoforms in developing wheat endosperm, Plant Physiol., 1997, 113, 201-208. 10.1104/pp.113.1.201Search in Google Scholar PubMed PubMed Central

[73] Regina A., Kosar-Hashemi B., Li Z., Pedler A., Mukai Y., Yamamoto M., et al., Starch branching enzyme IIb in wheat is expressed at low levels in the endosperm compared to other cereals and encoded at a non-syntenic locus, Planta, 2005, 222, 899-909. 10.1007/s00425-005-0032-zSearch in Google Scholar PubMed

[74] Gao M., Fisher D.K., Kim K.N., Shannon J.C., Guiltinan M.J., Independent genetic control of maize starch-branching enzymes IIa and IIb. Isolation and characterization of a Sbe2a cDNA, Plant Physiol., 1997, 114, 69-78. 10.1104/pp.114.1.69Search in Google Scholar PubMed PubMed Central

[75] Mizuno K., Kobayashi E., Tachibana M., Kawasaki T., Fujimura T., Funane K., et al., Characterization of an isoform of rice starch branching enzyme, RBE4, in developing seeds, Plant Cell Physiol., 2001, 42, 349-357. 10.1093/pcp/pce042Search in Google Scholar PubMed

[76] Rahman S., Regina A., Li Z., Mukai Y., Yamamoto M., Kosar- Hashemi B., et al., 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. 10.1104/pp.125.3.1314Search in Google Scholar PubMed PubMed Central

[77] Yao Y., Thompson D.B., Guiltinan M.J., Maize starch-branching enzyme isoforms and amylopectin structure. In the absence of starch-branching enzyme IIb, the further absence of starchbranching enzyme Ia leads to increased branching, Plant Physiol., 2004, 136, 3515-3523. 10.1104/pp.104.043315Search in Google Scholar PubMed PubMed Central

[78] Blauth S.L., Kim K.N., Klucinec J., Shannon J.C., 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. 10.1023/A:1013335217744Search in Google Scholar

[79] Satoh H., Nishi A., Yamashita K., Takemoto Y., Tanaka Y., Hosaka Y., et al., Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm, Plant Physiol., 2003, 133, 1111-1121. 10.1104/pp.103.021527Search in Google Scholar PubMed PubMed Central

[80] 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. 10.1104/pp.010127Search in Google Scholar

[81] Blauth S.L., Yao Y., Klucinec J.D., Shannon J.C., Thompson D.B., Guilitinan M.J., Identification of Mutator insertional mutants of starch-branching enzyme 2a in corn, Plant Physiol., 2001, 125, 1396-1405. 10.1104/pp.125.3.1396Search in Google Scholar

[82] 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. 10.1093/pcp/pcf091Search in Google Scholar

[83] Yun S.H., Matheson N.K., Structures of the amylopectins of waxy, normal, amylose-extender, and wx:Ae genotypes and of the phytoglycogen of maize, Carbohydr. Res., 1993, 243, 307-321. 10.1016/0008-6215(93)87035-QSearch in Google Scholar

[84] Evans A., Thompson D.B., Resistance to α-amylase digestion in four native high-amylose maize starches, Cereal Chem., 2004, 81, 31-37. 10.1094/CCHEM.2004.81.1.31Search in Google Scholar

[85] Klucinec J.D., Thompson D.B., Structure of amylopectins from ae-containing maize starches, Cereal Chem., 2002, 79, 19-23. 10.1094/CCHEM.2002.79.1.19Search in Google Scholar

[86] Sawada T., Francisco Jr. P.B., Aihara S., Utsumi Y., Yoshida M., Oyama Y., et al., Chlorella starch branching enzyme II (BEII) can complement the function of BEIIb in rice endosperm, Plant Cell Physiol., 2009, 50, 1062-1074. 10.1093/pcp/pcp058Search in Google Scholar PubMed

[87] Tanaka N., Fujita N., Nishi A., Satoh H., Hosaka Y., Ugaki M., et al., 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. 10.1111/j.1467-7652.2004.00097.xSearch in Google Scholar PubMed

[88] Streb S., Zeeman S.C., Replacement of the endogenous starch debranching enzymes ISA1 and ISA2 of Arabidopsis with the rice orthologs reveals a degree of functional conservation during starch synthesis, PLoS One, 2014, 9, 1-9. 10.1371/journal.pone.0092174Search in Google Scholar PubMed PubMed Central

[89] Wattebled F., Planchot V., Dong Y., Szydlowski N., Pontoire B., Devin A., et al., 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. 10.1104/pp.108.129379Search in Google Scholar PubMed PubMed Central

[90] Cenci U., Nitschke F., Steup M., Minassian B.A., Colleoni C., Ball S.G., Transition from glycogen to starch metabolism in archaeplastida, Trends Plant Sci., 2014, 19, 18-28. 10.1016/j.tplants.2013.08.004Search in Google Scholar PubMed

[91] Dinges J.R., Colleoni C., Myers A.M., James M.G., Molecular structure of three mutations at the maize sugary1 locus and their allele-specific phenotypic effects, Plant Physiol., 2001, 125, 1406-1418. 10.1104/pp.125.3.1406Search in Google Scholar PubMed PubMed Central

[92] Wong K.S., Kubo A., Jane J.L., Harada K., Satoh H., Nakamura Y., Structures and properties of amylopectin and phytoglycogen in the endosperm of sugary-1 mutants of rice, J. Cereal Sci., 2003, 37, 139-149. 10.1006/jcrs.2002.0485Search in Google Scholar

[93] Burton R.A., Jenner H., Carrangis L., Fahy B., Fincher G.B., Hylton C., et al., Starch granule initiation and growth are altered in barley mutants that lack isoamylase activity, Plant J., 2002, 31, 97-112. 10.1046/j.1365-313X.2002.01339.xSearch in Google Scholar PubMed

[94] Rahman A., Wong K.S., Jane J.L., Myers A.M., James M.G., Characterization of SU1 isoamylase, a determinant of storage starch structure in maize, Plant Physiol., 1998, 117, 425-435. 10.1104/pp.117.2.425Search in Google Scholar PubMed PubMed Central

[95] Inouchi N., Glover D.V., Takaya T., Fuwa H., Development changes in fine-structure of starches of several endosperm mutants of maize, Starch-Starke, 1983, 35, 371-376. 10.1002/star.19830351102Search in Google Scholar

[96] Inouchi N., Glover D.V., Fuwa H., Chain-length distribution of amylopectins of several single mutants and the normal counterpart, and sugary-1 phytoglycogen in maize, Starch-Starke, 1987, 39, 259-266. 10.1002/star.19870390802Search in Google Scholar

[97] Zeeman S.C., Umemoto T., Lue W.L., Au-yeung P., Martin C., Smith A.M., et al., A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglocogen, Plant Cell, 1998, 10, 1699-1711. 10.1105/tpc.10.10.1699Search in Google Scholar PubMed PubMed Central

[98] Delatte T., Trevisan M., Parker M.L., Zeeman S.C., 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. 10.1111/j.1365-313X.2005.02348.xSearch in Google Scholar PubMed

[99] Wattebled F., Dong Y., Dumez S., Delvalle D., Planchot V., Berbezy P., et al., Mutants of Arabidopsis lacking a chloroplastic isoamylase accumulate phytoglycogen and an abnormal form of amylopectin, Plant Physiol., 2005, 138, 184-195. 10.1104/pp.105.059295Search in Google Scholar PubMed PubMed Central

[100] Kubo A., Rahman S., Utsumi Y., Li Z., Mukai Y., Yamamoto M., et al., Complementation of sugary-1 phenotype in rice endosperm with the wheat isoamylase1 gene supports a direct role for isoamylase1 in amylopectin biosynthesis, Plant Physiol., 2005, 137, 43-56. 10.1104/pp.104.051359Search in Google Scholar PubMed PubMed Central

[101] Lin Q., Facon M., Putaux J.L., Dinges J.R., Wattebled F., D’Hulst C., et al., Function of isoamylase-type starch debranching enzymes ISA1 and ISA2 in the Zea mays leaf, New Phytol., 2013, 200, 1009-1021. 10.1111/nph.12446Search in Google Scholar

[102] Hussain H., Mant A., Seale R., Zeeman S., Hinchliffe E., Edwards A., et al., Three isoforms of isoamylase contribute different catalytic properties for the debranching of potato glucans, Plant Cell, 2003, 15, 133-149. 10.1105/tpc.006635Search in Google Scholar

[103] Kubo A., Colleoni C., Dinges J.R., Lin Q., Lappe R.R., Rivenbark J.G., et al., Functions of heteromeric and homomeric isoamylase-type starch-debranching enzymes in developing maize endosperm, Plant Physiol., 2010, 153, 956-969. 10.1104/pp.110.155259Search in Google Scholar

[104] 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. 10.1007/s00425-006-0331-zSearch in Google Scholar

[105] 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. 10.1104/pp.111.173435Search in Google Scholar

[106] Beatty M.K., Rahman A., Cao H., Woodman W., Lee M., Myers A.M., et al., Purification and molecular genetic characterization of ZPU1, a pullulanase-type starch-debranching enzyme from maize, Plant Physiol., 1999, 119, 255-266. 10.1104/pp.119.1.255Search in Google Scholar

[107] Nakamura Y., Umemoto T., Ogata N., Kuboki Y., Yano M., Sasaki T., Starch debranching enzyme (R-enzyme or pullulanase) from developing rice endosperm: purification, cDNA and chromosomal localization of the gene, Planta, 1996, 199, 209-218. 10.1007/BF00196561Search in Google Scholar

[108] Li Q.F., Zhang G.Y., Dong Z.W., Yu H.X., Gu M.H., Sun S.S., et al., Characterization of expression of the OsPUL gene encoding a pullulanase-type debranching enzyme during seed development and germination in rice, Plant Physiol. Biochem., 2009, 47, 351-358. 10.1016/j.plaphy.2009.02.001Search in Google Scholar

[109] Dinges J.R., Colleoni C., James M.G., Myers A.M., Mutational analysis of the pullulanase-type debranching enzyme of maize indicates multiple functions in starch metabolism, Plant Cell, 2003, 15, 666-680. 10.1105/tpc.007575Search in Google Scholar

[110] Wu C., Colleoni C., Myers A.M., James M.G., Enzymatic properties and regulation of ZPU1, the maize pullulanase-type starch debranching enzyme, Arch. Biochem. Biophys., 2002, 406, 21-32. 10.1016/S0003-9861(02)00412-5Search in Google Scholar

[111] Myers A.M., Morell M.K., James M.G., Ball S.G., Recent progress towards understanding biosynthesis of the amylopectin crystal, Plant Physiol., 2000, 122, 989-997. 10.1104/pp.122.4.989Search in Google Scholar PubMed PubMed Central

[112] Zeeman S.C., Smith S.M., Smith A.M., The diurnal metabolism of leaf starch, Biochem. J., 2007, 401, 13-28. 10.1042/BJ20061393Search in Google Scholar PubMed

[113] Fujita N., Toyosawa Y., Utsumi Y., Higuchi T., Hanashiro I., Ikegami A., 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. 10.1093/jxb/ern349Search in Google Scholar PubMed PubMed Central

[114] Lin T.P., Preiss J., Characterization of D-enzyme (4-α-glucanotransferase) in Arabidopsis leaf, Plant Physiol., 1988, 86, 260-265. 10.1104/pp.86.1.260Search in Google Scholar PubMed PubMed Central

[115] Takaha T., Yanase M., Okada S., Smith S.M., Disproportionating enzyme (4-α-glucanotransferase; EC 2.4.1.25) of potato. Purification, molecular cloning, and potential role in starch metabolism, J. Biol. Chem., 1993, 268, 1391-1396. Search in Google Scholar

[116] Ball S.G., Morell M.K., From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule, Annu. Rev. Plant Biol., 2003, 54, 207-233. 10.1146/annurev.arplant.54.031902.134927Search in Google Scholar PubMed

[117] Colleoni C., Dauvill e D., Mouille G., Morell M., Samuel M., Slomiany M.C., et al., Biochemical characterization of the Chlamydomonas reinhardtii α-1,4 glucanotransferase supports a direct function in amylopectin biosynthesis, Plant Physiol., 1999, 120, 1005-1014. 10.1104/pp.120.4.1005Search in Google Scholar PubMed PubMed Central

[118] Colleoni C., Dauvill e D., Mouille G., Bul on A., Gallant D., Bouchet B., et al., Genetic and biochemical evidence for the involvement of α-1,4 glucanotransferases in amylopectin synthesis, Plant Physiol., 1999, 120, 993-1004. 10.1104/pp.120.4.993Search in Google Scholar PubMed PubMed Central

[119] Bresolin N.S., Li Z., Kosar-Hashemi B., Tetlow I.J., Chatterjee M., Rahman S., et al., Characterisation of disproportionating enzyme from wheat endosperm, Planta, 2006, 224, 20-31. 10.1007/s00425-005-0187-7Search in Google Scholar PubMed

[120] Takaha T., Critchley J., Okada S., Smith S.M., Normal starch content and composition in tubers of antisense potato plants lacking D-enzyme (4-α-glucanotransferase), Planta, 1998, 205, 445-451. 10.1007/s004250050342Search in Google Scholar

[121] Boos W., Shuman H., Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation, Microbiol. Mol. Biol. Rev., 1998, 62, 204-229. 10.1128/MMBR.62.1.204-229.1998Search in Google Scholar PubMed PubMed Central

[122] Yu Y., Mu H.H., Wasserman B.P., Carman G.M., Identification of the maize amyloplast stromal 112-kD protein as a plastidic starch phosphorylase, Plant Physiol., 2001, 125, 351-359. 10.1104/pp.125.1.351Search in Google Scholar PubMed PubMed Central

[123] Tickle P., Burrell M.M., Coates S.A., Emes M.J., Tetlow I.J., Bowsher C.G., Characterization of plastidial starch phosphorylase in Triticum aestivum l. Endosperm, J. Plant Physiol., 2009, 166, 1465-1478. 10.1016/j.jplph.2009.05.004Search in Google Scholar PubMed

[124] Satoh H., Shibahara K., Tokunaga T., Nishi A., Tasaki M., Hwang S.K., et al., Mutation of the plastidial α-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm, Plant Cell, 2008, 20, 1833-1849. 10.1105/tpc.107.054007Search in Google Scholar PubMed PubMed Central

[125] Hennen-Bierwagen T.A., Liu F., Marsh R.S., Kim S., Gan Q., Tetlow I.J., et al., Starch biosynthetic enzymes from developing maize endosperm associate in multisubunit complexes, Plant Physiol., 2008, 146, 1892-1908. 10.1104/pp.108.116285Search in Google Scholar PubMed PubMed Central

[126] Tetlow I.J., Beisel K.G., Cameron S., Makhmoudova A., Liu F., Bresolin N.S., et al., Analysis of protein complexes in wheat amyloplasts reveals functional interactions among starch biosynthetic enzymes, Plant Physiol., 2008, 146, 1878-1891. 10.1104/pp.108.116244Search in Google Scholar PubMed PubMed Central

[127] Liu F., Makhmoudova A., Lee E.A., Wait R., Emes M.J., Tetlow I.J., The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts, J. Exp. Bot., 2009, 60, 4423-4440. 10.1093/jxb/erp297Search in Google Scholar PubMed

[128] Makhmoudova A., Williams D., Brewer D., Massey S., Patterson J., Silva A., 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. 10.1074/jbc.M114.551093Search in Google Scholar PubMed PubMed Central

[129] Liu F., Romanova N., Lee E.A., Ahmed R., Evans M., Gilbert E.P., et al., 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. 10.1042/BJ20120573Search in Google Scholar PubMed

[130] Crofts N., Nakamura Y., Fujita N., Critical and speculative review of the roles of multi-protein complexes in starch biosynthesis in cereals, Plant Sci., 2017, 262, 1-8. 10.1016/j.plantsci.2017.05.007Search in Google Scholar PubMed

[131] Crofts N., Abe N., Oitome N.F., Matsushima R., Hayashi M., Tetlow I.J., et al., Amylopectin biosynthetic enzymes from developing rice seed form enzymatically active protein complexes, J. Exp. Bot., 2015, 66, 4469-4482. 10.1093/jxb/erv212Search in Google Scholar PubMed PubMed Central

[132] Ahmed Z., Tetlow I.J., Ahmed R., Morell M.K., Emes M.J., 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. 10.1016/j.plantsci.2014.12.016Search in Google Scholar PubMed

[133] Nakamura Y., Ono M., Utsumi C., Steup M., Functional interaction between plastidial starch phosphorylase and starch branching enzymes from rice during the synthesis of branched maltodextrins, Plant Cell Physiol., 2012, 53, 869-878. 10.1093/pcp/pcs030Search in Google Scholar PubMed

[134] Hwang S.K., Koper K., Satoh H.,Okita T.W., Rice endosperm starch phosphorylase (Pho1) assembles with disproportionating enzyme (Dpe1) to form a protein complex that enhances synthesis of malto-oligosaccharides, J. Biol. Chem., 2016, 291, 19994-20007. 10.1074/jbc.M116.735449Search in Google Scholar PubMed PubMed Central

[135] Hennen-Bierwagen T.A., Lin Q., Grimaud F., Planchot V., Keeling P.L., James M.G., et al., 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.[136] Liu F., Ahmed Z., Lee E.A., Donner E., Liu Q., Ahmed R., et al., 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. 10.1104/pp.109.135293Search in Google Scholar PubMed PubMed Central

[137] Bustos R., Fahy B., Hylton C.M., Seale R., Nebane N.M., Edwards A., et al., Starch granule initiation is controlled by a heteromultimeric isoamylase in potato tubers, Proc. Natl. Acad. Sci. USA, 2004, 101, 2215-2220. 10.1073/pnas.0305920101Search in Google Scholar PubMed PubMed Central

[138] Streb S., Delatte T., Umhang M., Eicke S., Schorderet M., Reinhardt D., et al., 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. 10.1105/tpc.108.063487Search in Google Scholar PubMed PubMed Central

[139] Sim L., Beeren S.R., Findinier J., Dauvillee D., Ball S.G., Henriksen A., et al., 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. 10.1074/jbc.M114.565044Search in Google Scholar PubMed PubMed Central

[140] Hwang S.K., Nishi A., Satoh H., Okita T.W., Rice endospermspecific plastidial α-glucan phosphorylase is important for synthesis of short-chain malto-oligosaccharides, Arch. Biochem. Biophys., 2010, 495, 82-92.10.1016/j.abb.2009.12.023Search in Google Scholar PubMed

Received: 2017-7-31
Accepted: 2017-9-22
Published Online: 2017-10-28
Published in Print: 2017-10-26

© 2017

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

Downloaded on 25.4.2024 from https://www.degruyter.com/document/doi/10.1515/amylase-2017-0006/html
Scroll to top button