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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

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The distribution of starch synthase I and starch branching enzyme IIb between the starch granule and amyloplast stroma plays an important role in determining endosperm amylose content of cereal grains.

Abstract

Starch synthase IIa (SSIIa) catalyses the polymerisation of intermediate length glucan chains of amylopectin in the endosperm of cereals. Mutations of SSIIa genes in barley and wheat and inactive SSIIa variant in rice induce similar effects on the starch structure and the amylose content, but the severity of the phenotypes is different. This study compared the levels of transcripts and partitioning of proteins of starch synthase I (SSI) and starch branching enzyme IIb (SBEIIb) inside and outside the starch granules in the developing endosperms of these ssIIa mutants and inactive SSIIa variant. Pleiotropic effects on starch granule-bound proteins suggested that the different effects of SSIIa mutations on endosperm amylose content of barley, wheat and rice are determined by the distribution of SSI and SBEIIb between the starch granule and amyloplast stroma in cereals. Regulation of starch synthesis in ssIIa mutants and inactive SSIIa variant may be at post-translational level or the altered amylopectin structure deprives the affinity of SSI and SBEIIb to amylopectin.

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References

  • Ahmed Z, Tetlow I, Ahmed R, Morell MK, Emes MJ (2015) 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 233:95–106

    Article  CAS  PubMed  Google Scholar 

  • Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54:207–233

    Article  CAS  PubMed  Google Scholar 

  • Ball S, Guan H-P, James M, Myers A, Keeling P, Mouille G, Buleon A, Colonna P, Preiss J (1996) From glycogen to amylopectin: a model explaining the biogenesis of the plant starch granule. Cell 86:349–352

    Article  CAS  PubMed  Google Scholar 

  • Bao JS, Corke H, Sun M (2006) Nucleotide diversity in starch synthase IIa and validation of single nucleotide polymorphisms in relation to starch gelatinization temperature and other physicochemical properties in rice (Oryza sativa L.). Theor Appl Genet 113:1171–1183

    Article  CAS  PubMed  Google Scholar 

  • Bao JS, Xiao P, Hiratsuka M, Sun M, Umemoto T (2009) Granule-bound SSIIa protein content and its relationship with amylopectin structure and gelatinization temperature of rice starch. Starch Starke 61:431–437

    Article  CAS  Google Scholar 

  • Butardo VM Jr, Daygon VD, Colgrave ML, Campbell PM, Resurreccion A, Cuevas RP, Jobling SA, Tetlow I, Rahman S, Morell MK, Fitzgerald M (2012) Biomolecular analyses of starch and starch granule proteins in the high-amylose rice mutant goami 2. J Agr Food Chem 60:11576–11585

    Article  CAS  Google Scholar 

  • Cao H, James MG, Myers AM (2000) Purification and characterization of soluble starch synthases from maize endosperm. Arch Biochem Biophys 373:135–146

    Article  CAS  PubMed  Google Scholar 

  • Castro JV, Ward RM, Gilbert RG, Fitzgerald MA (2005) Measurement of the molecular weight distribution of debranched starch. Biomacromolecules 6:2260–2270

    Article  CAS  PubMed  Google Scholar 

  • Cheng J, Khan MA, Qiu W-M, Li J, Zhou H, Zhang Q, Guo W, Zhu T, Peng J, Sun F, Li S, Korban SS, Han Y (2012) Diversification of genes encoding granule-bound starch synthase in monocots and dicots is marked by multiple genome-wide duplication events. PLoS One 7:e30088

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Colgrave ML, Goswami H, Howitt CA, Tanner GJ (2013) Proteomics as a tool to understand the complexity of beer. Food Res Int 54:1001–1012

    Article  CAS  Google Scholar 

  • Craig J, Lloyd J, Tomlinson K, Barber L, Edwards A, Wang TL, Martin C, Hedley C, Smith AM (1998) Mutations in the gene encoding starch synthase II profoundly alter amylopectin structure in pea embryos. Plant Cell 10:413–426

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cuevas RP, Daygon VD, Corpuz HM, Nora L, Reinke RF, Waters DLE, Fitzgerald MA (2010) Melting the secrets of gelatinisation temperature in rice. Funct Plant Biol 37:439–447

    Article  CAS  Google Scholar 

  • Delvalle D, Dumez S, Wattebled F, Roldan I, Planchot V, Berbezy P, Colonna P, Vyas D, Chatterjee M, Ball S, Merida A, D’Hulst C (2005) Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. Plant J 43:398–412

    Article  CAS  PubMed  Google Scholar 

  • Denyer K, Sidebottom C, Hylton CM, Smith AM (1993) Soluble isoforms of starch synthase and starch-branching enzyme also occur within starch granules in developing pea embryos. Plant J 4:191–198

    Article  CAS  PubMed  Google Scholar 

  • Denyer K, Hylton CM, Jenner CF, Smith AM (1995) Identification of multiple isoforms of soluble and granule-bound starch synthase in developing wheat endosperm. Planta 196:256–265

    Article  CAS  Google Scholar 

  • Denyer K, Clarke B, Hylton C, Tatge H, Smith A (1996) The elongation of amylase and amylopectin chains in isolated starch granules. Plant J 10:1135–1143

    Article  CAS  Google Scholar 

  • Fontaine T, Hulst CD, Maddelein ML, Routier F, Marianne-Pepin T, Decq A, Wieruszeski JM, Delrue B, Van Den Koornhuyse N, Bossu JP, Fournet B, Ball SG (1993) Toward an understanding of the biogenesis of the starch granule: evidence that Chlamydomonas soluble starch starch synthase II controls the synthesis of intermediate size glucans of amylopectin. J Biol Chem 268:16223–16230

    CAS  PubMed  Google Scholar 

  • Fujita N, Yoshida M, Asakura N, Ohdan T, Miyao A, Hirochika H, Nakamura Y (2006) Function and characterization of starch synthase I using mutants in rice. Plant Physiol 140:1070–1084

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fujita N, Satoh R, Hayashi A, Kodama M, Itoh R, Aihara S, Nakamura Y (2011) Starch biosynthesis in rice endosperm requires the presence of either starch synthase I or IIIa. J Exp Bot 62:4819–4831

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gao M, Fisher DK, Kim KN, Shannon JC, Guiltinan MJ (1996) Evolutionary conservation and expression patterns of maize starch branching enzyme I and IIb genes suggests isoform specialization. Plant Mol Biol 30:1223–1232

    Article  CAS  PubMed  Google Scholar 

  • Garwood DL, McArdle FJ, Vanderslice SF, Shannon JC (1976) Postharvest carbohydrate transformations and processed quality of high sugar maize in genotypes. J Am Society Hortic Sci 101:400–404

    CAS  Google Scholar 

  • Harn C, Knight M, Ramakrishnan A, Guan H, Keeling PL, Wasserman BP (1998) Isolation and characterization of the zSSIIa and zSSIIb starch synthase cDNA clones from maize endosperm. Plant Mol Biol 37:639–649

    Article  CAS  PubMed  Google Scholar 

  • Hennen-Bierwagen TA, Liu F, Marsh RS, Kim S, Gan Q, Tetlow IJ, Emes MJ, James MG, Myers AM (2008) Starch biosynthetic enzymes from developing maize endosperm associate in multisubunit complexes. Plant Physiol 146:1892–1908

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hennen-Bierwagen TA, Lin Q, Grimaud F, Planchot V, Keeling PL, James MG, Myers AM (2009) Proteins from multiple metabolic pathways associate with starch biosynthetic enzymes in high molecular weight complexes: a model for regulation of carbon allocation in maize amyloplasts. Plant Physiol 149:1541–1559

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hirose T, Terao T (2004) A comprehensive expression analysis of the starch synthase gene family in rice (Oryza sativa L.). Planta 220:9–26

    Article  CAS  PubMed  Google Scholar 

  • James MG, Denyer K, Myers AM (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6:215–222

    Article  CAS  PubMed  Google Scholar 

  • Jane JL, Chen YY, Lee LF, McPherson AE, Wong KS, Radosavljevic M, Kasemsuwan T (1999) Effects of amylopectin branch chain-length and amylose content on the gelatinization and pasting properties of starch. Cereal Chem 76:629–637

    Article  CAS  Google Scholar 

  • Konik-Rose C, Thistleton J, Chanvrier H, Tan I, Halley P, Gidley M, Kosar-Hashemi B, Wang H, Larroque O, Ikea J, McMaugh S, Regina A, Rahman S, Morell M, Li Z (2007) Effects of starch synthase IIa gene dosage on grain, protein and starch in endosperm of wheat. Theor Appl Genet 115:1053–1065

    Article  CAS  PubMed  Google Scholar 

  • Kossmann J, Lloyd J (2000) Understanding and influencing starch biochemistry. Crit Rev Plant Sci 19:171–226

    Article  CAS  Google Scholar 

  • Kramer H, Pfahler P, Whistler R (1958) Gene interactions in maize affecting endosperm properties. Agron J 50:207–210

    Article  Google Scholar 

  • Li Z, Chu XS, Mouille G, Yan LL, Kosar-Hashemi B, Hey S, Napier J, Shewry P, Clarke B, Appels R, Morell MK, Rahman S (1999) The localization and expression of the class II starch synthases of wheat. Plant Physiol 120:1147–1155

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li Z, Li D, Du X, Wang H, Larroque O, Jenkins CLD, Morell MK (2011) The barley amo1 locus is tightly linked to the starch synthase IIIa gene and negatively regulates expression of granule-bound starch synthetic genes. J Exp Bot 62:5217–5231

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lin Q, Huang B, Zhang M, Rivenbark JG, Zhang X, James MG, Myers AM, Hennen-Bierwagen AM (2011) Functional interactions between starch synthase III and isoamylase-type starch debranching enzyme in maize endosperm. Plant Physiol 158:679–692

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu F, Makhmoudova A, Lee EA, Wait R, Emes MJ, Tetlow IJ (2009) The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. J Exp Bot 60:4423–4440

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Ahmed Z, Lee EA, Donner E, Liu Q, Ahmed R, Morell MK, Emes MJ, Tetlow IJ (2012a) Allelic variants of the amylose extender mutation of maize demonstrate phenotypic variation in starch structure resulting from modified protein-protein interactions. J Exp Bot 63:1167–1183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu F, Romanova N, Lee EA, Ahmed R, Evans M, Gilbert EP, Morell MK, Emes MJ, Tetlow IJ (2012b) Glucan affinity of starch synthase IIa determines binding of starch synthase I and starch branching enzyme IIb to starch granules. Biochem J 448:373–387

    Article  CAS  PubMed  Google Scholar 

  • Luo J, Jobling SA, Millar A, Morell MK, Li Z (2015) Allelic effects on starch structure and properties of six starch biosynthetic genes in a rice recombinant inbred line population. Rice 8:15

    Article  PubMed Central  PubMed  Google Scholar 

  • Maddelein ML, Libessart N, Bellanger F, Delrue B, D’Hulst C, Van Den Koornhuyse N, Fontaine T, Wieruszeski JM, Decq A, Ball SG (1994) Toward an understanding of the biogenesis of the starch granule: determination of granule-bound and soluble starch synthase functions in amylopectin synthesis. J Biol Chem 269:25150–25157

    CAS  PubMed  Google Scholar 

  • Morell MK, Kosar-Hashemi B, Cmiel M, Samuel MS, Chandler P, Rahman S, Buleon A, Batey IL, Li Z (2003) Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties. Plant J 34:172–184

    Article  Google Scholar 

  • Nakamura Y, Francisco PB, Hosaka Y, Sato A, Sawada T, Kubo A, Fujita N (2005a) Essential amino acids of starch synthase IIa differentiate amylopectin structure and starch quality between japonica and indica rice varieties. Plant Mol Biol 58:213–227

    Article  CAS  PubMed  Google Scholar 

  • Nakamura T, Shimbata T, Vrinten P, Saito M, Yonemaru J, Seto Y, Yasuda H (2005b) Mutations in wheat starch synthase II genes and PCR-based selection of a SGP-1 null line. Theor Appl Genet 111:1072–1079

    Article  PubMed  Google Scholar 

  • Nishi A, Nakamura Y, Tanaka N, Satoh H (2001) Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiol 127:459–472

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • O’Shea MG, Morell MK (1996) High resolution slab gel electrophoresis of 8-amino-1,3,6-pyrenetrisulfonic acid (APTS) tagged oligosaccharides using a DNA sequencer. Electrophoresis 17:681–686

    Article  PubMed  Google Scholar 

  • Peng MS, Hucl P, Chibbar RN (2001) Isolation, characterization and expression analysis of starch synthase I from wheat (Triticum aestivum L.). Plant Sci 161:1055–1062

    Article  CAS  Google Scholar 

  • Rahman S, Kosarhashemi B, Samuel MS, Hill A, Abbott DC, Skerritt JH, Preiss J, Appels R, Morell MK (1995) The major proteins of wheat endosperm starch granules. Aust J Plant Physiol 22:793–803

    Article  CAS  Google Scholar 

  • Rahman S, Li Z, Batey I, Cochrane MP, Appels R, Morell MK (2000) Genetic alteration of starch functionality in wheat. J Cereal Sci 31:91–110

    Article  CAS  Google Scholar 

  • Regina A, Kosar-Hashemi B, Li Z, Pedler A, Mukai Y, Yamamoto M, Gale K, Sharp P, Morell MK, Rahman S (2005) 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 222:899–909

    Article  CAS  PubMed  Google Scholar 

  • Regina A, Bird A, Topping D, Bowden S, Freeman J, Barsby T, Kosar-Hashemi B, Li Z, Rahman S, Morell M (2006) High amylose wheat generated by RNA-interference improves indices of large bowel health in rats. PNAS 103:3546–3551

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Regina A, Kosar-Hashemi B, Ling S, Li Z, Rahman S, Morell MK (2010) Control of starch branching in barley defined through differential RNAi suppression of starch branching enzyme IIa and IIb. J Exp Bot 61:1469–1482

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roldan I, Wattebled F, Lucas MM, Delvalle D, Planchot V, Jimenez S, Perez R, Ball S, D’Hulst C, Merida A (2007) The phenotype of soluble starch synthase IV defective mutants of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant J 49:492–504

    Article  CAS  PubMed  Google Scholar 

  • Szydlowski N, Ragel P, Raynaud S, Lucas MM, Roldan I, Montero M, Munoz FJ, Ovecka M, Bahaji A, Planchot V, Pozueta-Romero J, D’Hulst C, Merida A (2009) Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 21:2443–2457

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tetlow IJ, Morell MK, Emes MJ (2004a) Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 55:2131–2145

    Article  CAS  PubMed  Google Scholar 

  • Tetlow IJ, Wait R, Lu Z, Akkasaeng R, Bowsher CG, Esposito S, Kosar-Hashemi B, Morell MK, Emes MJ (2004b) Protein phosphorylation in amyloplasts regulates starch branching enzyme activity and protein-protein interactions. Plant Cell 16:694–708

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tetlow IJ, Beisel KG, Cameron S, Makhmoudova A, Liu F, Bresolin NS, Wait R, Morell MK, Emes J (2008) Analysis of protein complexes in wheat amyloplasts reveals functional interactions among starch biosynthetic enzymes. Plant Physiol 146:1878–1891

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Toyota K, Tamura M, Ohdan T, Nakamura Y (2006) Expression profiling of starch metabolism-related plastidic translocator genes in rice. Planta 223:248–257

    Article  CAS  PubMed  Google Scholar 

  • Umemoto T, Aoki N (2005) Single-nucleotide polymorphisms in rice starch synthase IIa that alter starch gelatinisation and starch association of the enzyme. Func Plant Biol 32:763–768

    Article  CAS  Google Scholar 

  • Umemoto T, Yano M, Satoh H, Shomura A, Nakamura Y (2002) Mapping of a gene responsible for the difference in amylopectin structure between japonica-type and indica-type rice varieties. Theor Appl Genet 104:1–8

    Article  CAS  PubMed  Google Scholar 

  • Umemoto T, Aoki N, Lin H, Nakamura Y, Inouchi N, Sato Y, Yano M, Hirabayashi H, Maruyama S (2004) Natural variation in rice starch synthase IIa affects enzyme and starch properties. Func Plant Biol 31:671–684

    Article  CAS  Google Scholar 

  • Umemoto T, Horibata T, Aoki N, Hiratsuka M, Yano M, Inouchi N (2008) Effects of variations in starch synthase on starch properties and eating quality of rice. Plant Prod Sci 11:472–480

    Article  CAS  Google Scholar 

  • Waters DLE, Henry RJ, Reinke RF, Fitzgerald MA (2006) Gelatinization temperature of rice explained by polymorphisms in starch synthase. Plant Biotech J 4:115–122

    Article  CAS  Google Scholar 

  • Yamamori M, Fujita S, Hayakawa K, Matsuki J, Yasui T (2000) Genetic elimination of a starch granule protein, SGP-1, of wheat generates an altered starch with apparent high amylose. Theor Appl Genet 101:21–29

    Article  CAS  Google Scholar 

  • Yang Z, Wang Y, Xu S, Xu C, Yan C (2013) Molecular evolution and functional divergence of soluble starch synthase genes in Cassava (Manihot esculenta Crantz). Evol Bioinform 9:239–249

    Article  CAS  Google Scholar 

  • Zhang X, Colleoni C, Ratushna V, Sirghie-Colleoni M, James MG, Myers AM (2004) Molecular characterization demonstrates that the Zea mays gene sugary2 codes for the starch synthase isoform SSIIa. Plant Mol Biol 54:865–879

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Jixun Luo was supported by CSC Chinese Scholarship. This work was supported by CSIRO Food Future National Research Flagship. Hong Wang for analysis of starch synthetic enzymes using protein gels.

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The authors declare that they have no conflict of interest.

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Correspondence to Zhongyi Li.

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Communicated by X. Xia.

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Luo, J., Ahmed, R., Kosar-Hashemi, B. 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 128, 1407–1419 (2015). https://doi.org/10.1007/s00122-015-2515-z

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