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Plant function and evolutionary biology
RESEARCH ARTICLE

Natural variation in rice starch synthase IIa affects enzyme and starch properties

Takayuki Umemoto A H , Noriaki Aoki A , Hongxuan Lin B C , Yasunori Nakamura D , Naoyoshi Inouchi E , Youichiro Sato F , Masahiro Yano B , Hideyuki Hirabayashi A and Sachio Maruyama A G
+ Author Affiliations
- Author Affiliations

A National Institute of Crop Science, Tsukuba, Ibaraki 305-8518, Japan.

B National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan.

C Current address; Shanghai Institute of Plant Physiology and Ecology, The Chinese Academy of Science, National Laboratory of Plant Molecular Genetics, 300 Fenglin Road, Shanghai 200032, P.R. China.

D Akita Prefectural University and CREST, Akita, Akita 010-0195, Japan.

E Fukuyama University, Gakuen-cho, Fukuyama, Hiroshima 729-0292, Japan.

F Research Institute for Humanity and Nature, Kamigyo-ku, Kyoto 602-0878, Japan.

G Current address; University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan.

H Corresponding author; email: ume@affrc.go.jp

Functional Plant Biology 31(7) 671-684 https://doi.org/10.1071/FP04009
Submitted: 13 January 2004  Accepted: 30 March 2004   Published: 22 July 2004

Abstract

The natural variation in starch synthase IIa (SSIIa) of rice (Oryza sativa L.) was characterised using near-isogenic lines (NILs). SSIIa is a candidate for the alk gene regulating the alkali disintegration of rice grains, since both genes are genetically mapped at the same position on chromosome 6 and related to starch properties. In this study, we report that the alkali-susceptible cultivar Nipponbare lacked SSIIa activity in endosperm. However, the activity was detected with NILs having the alk allele of alkali-tolerant Kasalath. SSIIa protein was present even in Nipponbare endosperm, but it was not associated with starch granules at the milky stage of endosperm. Three single-nucleotide polymorphisms (SNPs) predicting amino acid substitutions existed between the cDNA sequences of SSIIa of Nipponbare and Kasalath were genotyped with 65 rice cultivars and four wild relatives of cultivated rice. The results obtained explain the potential importance of two of the amino acid residues for starch association of rice SSIIa. An analysis of the chain-length distribution of β-limit dextrin of amylopectin showed that without SSIIa activity, the relative number of A-chains (the short chains without branches) increased and that of B1-chains (the short chains with branches) decreased. This suggests that, given the SSIIa defect, short A-chains could not reach a sufficient length for branching enzymes to act on them to produce B1-chains.

Keywords: alk, alkali disintegration, amylopectin, rice, starch synthase.


Acknowledgments

We thank Dr Yanfeng Ding and Kazuyuki Okamoto for their gifts of rice seeds, Yuko Hosaka for cDNA sequencing, and Yoshinori Utsumi for DSC measurement. We also thank Hiroaki Yamanouchi for his helpful discussions, and Dr Kiyoaki Maruyama for his encouragement during this work. This work was supported mainly by funds from the Ministry of Agriculture, Forestry, and Fisheries of Japan.


References


Aggarwal RK, Brar DS, Nandi S, Huang N, Khush GS (1999) Phylogenetic relationships among Oryza species revealed by AFLP markers. Theoretical and Applied Genetics 98, 1320–1328.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ayres NM, McClung AM, Larkin PD, Bligh HFJ, Jones CA, Park WD (1997) Microsatellites and a single-nucleotide polymorphism differentiate apparent amylose classes in an extended pedigree of US rice germplasm. Theoretical and Applied Genetics 94, 773–781.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bhattacharya M, Zee SY, Corke H (1999) Physicochemical properties related to quality of rice noodles. Cereal Chemistry 76, 861–867. open url image1

Cai X, Wang Z, Xing Y, Zhang J, Hong M (1998) Aberrant splicing of intron 1 leads to the heterogeneous 5′ UTR and decreased expression of waxy gene in rice cultivars of intermediate amylose content. The Plant Journal 14, 459–465.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Commuri PD, Keeling PL (2001) Chain-length specificities of maize starch synthase I enzyme: studies of glucan affinity and catalytic properties. The Plant Journal 25, 475–486.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cooke D, Gidley MJ (1992) Loss of crystalline and molecular order during starch gelatinisation: origin of the enthalpic transition. Carbohydrate Research 227, 103–112.
Crossref | GoogleScholarGoogle Scholar | open url image1

Craig J, Lloyd JR, Tomlinson K, Barber L, Edwards A, Wang TL, Martin C, Hedley CL, Smith AM (1998) Mutations in the gene encoding starch synthase II profoundly alter amylopectin structure in pea embryos. The Plant Cell 10, 413–426.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. The Plant Journal 4, 191–198.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. open url image1

Doehlert DC, Kuo TM (1993) Characteristics of carbohydrate metabolism in sweet corn (sugary-1) endosperms. Journal of American Society of Hortical Science 118, 661–666. open url image1

Domon E, Fujita M, Ishikawa N (2002) The insertion / deletion polymorphisms in the waxy gene of barley genetic resources from East Asia. Theoretical and Applied Genetics 104, 132–138.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Edwards A, Fulton DC, Hylton CM, Jobling SA, Gidley M, Rossner U, Martin C, Smith AM (1999) combined reduction in activity of starch synthase II and III of potato has novel effects on the starch of tubers. The Plant Journal 17, 251–261.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gidley M, Bulpin PV (1987) Crystallisation of malto-oligosaccharides as models of the crystalline forms of starch: minimum chain-length requirement for the formation of double helices. Carbohydrate Research 161, 291–300.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hanashiro I, Abe J, Hizukuri S (1996) A periodic distribution of the chain length of amylopectin as revealed by high-performance anion-exchange chromatography. Carbohydrate Research 283, 151–159.
Crossref | GoogleScholarGoogle Scholar | open url image1

Harushima Y, Yano M, Shomura A, Sato M, Shimano T , et al . (1998) A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148, 479–494.
PubMed |
open url image1

Hirano HY, Eiguchi M, Sano Y (1998) A single base change altered the regulation of the waxy gene at the posttranscriptional level during the domestication of rice. Molecular Biology and Evolution 15, 978–987.
PubMed |
open url image1

Imparl-Radosevich JM, Keeling PL, Guan H (1999) Essential arginine residues in maize starch synthase IIa are involved in both ADP-glucose and primer binding. FEBS Letters 457, 357–362.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Inouchi N, Glover DV, Sugimoto Y, Fuwa H (1991a) DSC characteristics of gelatinization of starches of single-, double-, and triple-mutants and their normal counterpart in the inbred Oh43 maize (Zea mays L.) background. Starch 43, 468–472. open url image1

Inouchi N, Glover DV, Sugimoto Y, Fuwa H (1991b) DSC characteristics of retrograded starches of single-, double-, and triple-mutants and their normal counterpart in the inbred Oh43 maize (Zea mays L.) background. Starch 43, 473–477. open url image1

Isshiki M, Morino K, Nakajima M, Okagaki RJ, Wessler SR, Izawa T, Shimamoto K (1998) A naturally occurring functional allele of the rice waxy locus has a GT to TT mutation at the 5′ splice site of the first intron. The Plant Journal 15, 133–138.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

James MG, Robertson DS, Myers AM (1995) Characterization of the maize gene sugary1, a determinant of starch composition in kernels. The Plant Cell 7, 417–429.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jane J, Chen YY, Lee LF, Mcpherson AE, Wong KS, Radosavljevic M, Kasemsuwan T (1999) Effects of amylopectin branch chain length and amylose content on the gelatinazation and pasting properties of starch. Cereal Chemistry 76, 629–637. open url image1

Jobling SA, Westcott RJ, Tayal A, Jeffcoat R, Schwall GP (2002) Production of a freeze–thaw-stable potato starch by antisense inhibition of three starch synthase genes. Nature Biotechnology 20, 295–299.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Juliano BO (1998) Varietal inpact on rice quality. Cereal Foods World 43, 207–222. open url image1

Kudo M (1968) Genetical and thremmatological studies of characters, physiological or ecological, in the hybrids between ecological rice groups. Bulletin of National Institute of Agricultural Science. 19, 1–84. open url image1

Li Z, Chu X, Mouille G, Yan L, Kosar-Hashemi B , et al . (1999) The localization and expression of the class II starch synthases of wheat. Plant Physiology 120, 1147–1156.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Little RR, Hilder GB, Dawson EH (1958) Differential effect of dilute alkali on 25 varieties of milled white rice. Cereal Chemistry 35, 111–126. open url image1

Moates KL, Noel TR, Parker R, Ring SG (1997) The effect of chain length and solvent interactions on the dissolution of the B-type crystalline polymorph of amylose in water. Carbohydrate Research 298, 327–333.
Crossref | GoogleScholarGoogle Scholar | open url image1

Monna L, Lin HX, Kojima S, Sasaki T, Yano M (2002) Genetic dissection of a genomic region for a quantitative trait locus, Hd3, into two loci, Hd3a and Hd3b, controlling heading date in rice. Theoretical and Applied Genetics 104, 772–778.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. The Plant Journal 34, 173–185.
PubMed |
open url image1

Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4325.
PubMed |
open url image1

Nakamura Y (2002) Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant and Cell Physiology 43, 718–725.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nakamura T, Yamamori M, Hirano H, Hidaka S, Nagamine T (1995) Production of waxy (amylose-free) wheats. Molecular and General Genetics 248, 253–259.
PubMed |
open url image1

Nakamura Y, Nagamura Y, Kurata N, Minobe Y (1994) Linkage localization of the starch branching enzyme I (Q-enzyme I) gene in rice. Theoretical and Applied Genetics 89, 859–860. open url image1

Nakamura Y, Kubo A, Shimamune T, Matsuda T, Harada K, Satoh H (1997) Correlation between activities of starch debranching enzyme and α polyglucan structure in endosperm of sugary-1 mutants of rice. The Plant Journal 12, 143–153.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nakamura Y, Sakurai A, Inaba Y, Kimura K, Iwasawa N, Nagamine T (2002) The fine structure of amylopectin in endosperm from Asian cultivated rice can be largely classified into two classes. Starch 54, 117–131.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nichols DJ, Keeling PL, Spalding M, Guan H (2000) Involvement of conserved aspartate and glutamate residues in the catalysis and substrate binding of maize starch synthase. Biochemistry 39, 7820–7825.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Okagaki RJ, Wessler SR (1988) Comparison of non-mutant and mutant waxy genes in rice and maize. Genetics 120, 1137–1143.
PubMed |
open url image1

Okamoto K, Kobayashi K, Hirasawa H, Umemoto T (2002) Structural differences in amylopectin affect waxy rice processing. Plant Production Science 5, 45–50. open url image1

Patron NJ, Smith AM, Fahy BF, Hylton CM, Naldrett MJ, Rossnagel BG, Denyer K (2002) The altered pattern of amylose accumulation in the endosperm of low-amylose barley cultivars in attributable to a single mutant allele of granule-bound starch synthase I with a deletion in the 5′-non-coding region. Plant Physiology 130, 190–198.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rahman S, Kosar-Hashemi B, Samuel M, Hill A, Abbott DC, Skerritt JH, Preiss J, Appels R, Morell M (1995) The major proteins of wheat endosperm starch granules. Australian Journal of Plant Physiology 22, 793–803. open url image1

Richardson PH, Jeffcoat R, Shi YC (2000) High-amylose starches: from biosynthesis to their use as food ingredients. Materials Research Society Bulletin 25, 20–24. open url image1

Stinard PS, Robertson DS, Schnable PS (1993) Genetic isolation, cloning, and analysis of a mutator-induced, dominant antimorph of the maize amylose extender1 locus. The Plant Cell 5, 1555–1566.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Takagi K, Nagano H, Kishima Y, Sano Y (2003) MITE-transposon display efficiently detects polymorphisms among the Oryza AA-genome species. Breeding Science 53, 125–132.
Crossref | GoogleScholarGoogle Scholar | open url image1

Takaoka M, Watanabe S, Sassa H, Yamamori M, Nakamura T, Sasakuma T, Hirano H (1997) Structural characterisation of high-molecular-weight starch granule-bound proteins in wheat (Triticum aestivum L.). Journal of Agricultural and Food Chemistry 45, 2929–2934.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tanaka K, Ohnishi S, Kishimoto N, Kawasaki T, Baba T (1995) Structure, organization, and chromosomal location of the gene encoding a form of rice soluble starch synthase. Plant Physiology 108, 677–683.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Umemoto T, Terashima K (2002) Activity of granule-bound starch synthase is an important determinant of amylose content in rice endosperm. Functional Plant Biology 29, 1121–1124.
Crossref | GoogleScholarGoogle Scholar | open url image1

Umemoto T, Nakamura Y, Satoh H, Terashima K (1999) Differences in amylopectin structure between two rice varieties in relation to the effects of temperature during grain-filling. Starch 51, 58–62.
Crossref | GoogleScholarGoogle Scholar | open url image1

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. Theoretical and Applied Genetics 104, 1–8.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Umemoto T, Yano M, Satoh H, Shomura A, Okamoto K, Kobayashi K, Nakamura Y (in press) The alk locus controls amylopectin structure and a starch synthase activity. ‘Rice gentics IV. Supplementary volume’. (Eds GS Khush, DS Brar, B Hardy) (International Rice Research Institute: Los Banos, Phillipines)

Warth FJ, Darabsett DB (1914) Disintegration of rice grains by means of alkali. Bulletin of Agricultural Research Institute, Pasa 38, 1–9. open url image1

Webb BD (1991) Rice quality and grades. ‘Rice. Vol. 2. Utilization (2nd edn)’. (Ed. BS Luh) pp. 89–119. (Van Nostrand Reinhold: New York, NY)

Yamamori M, Fujita M, 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. Theoretical and Applied Genetics 101, 21–29.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L , et al . (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. The Plant Cell 12, 2473–2483.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1