|
|
|
|
|
| Effect of high temperature on the expressions of genes encoding starch synthesis enzymes in developing rice endosperms |
| CAO Zhen-zhen, PAN Gang, WANG Fu-biao, WEI Ke-su, LI Zhao-wei, SHI Chun-hai, GENG Wei, CHENG Fang-min |
| College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, P.R.China |
|
|
|
摘要 High temperature is the major environmental factor affecting grain starch properties of cooking rice cultivars. In this study, two non-waxy indica rice genotypes, cv. 9311 and its mutant with extremely high amylose phenotype (9311eha) were used to study the differential expressions of genes in starch synthesis and their responses to high temperature (HT). Significant increase in apparent amylose content and hot-water-soluble starch content in mutant 9311eha were genetically caused by a substitution from AGTTATA to AGGTATA at the leader intron 5´ splice site in Wx gene. This mutation resulted in different mRNA transcript levels, mRNA splicing efficiencies and protein levels of Wx between the two rice genotypes, which also lead to the genotype-dependent alteration in the temporal pattern of Wx transcription and granule-bound starch synthase (GBSS) activity in response to HT. However, changes in the activities of other starch synthesizing enzymes and their expressions of distinct isoform genes were not significant with the Wx gene mutation, thus only minor difference in the particle size of starch granule, chain-length distribution and gelatinization enthalpy were found between the two genotypes. The temporal- specific expression of multiple isoform genes responsive to different temperature regiments indicated that the reduction of GBSS transcript expression under HT was generally accompanied by the decreased expressions of SSSIIa, SSSIIIa and SBEIIb. Consequently, high temperature-ripened grains in 9311eha showed high proportion of intermediate and long B chains and somewhat lower level of short A chain compared to the wildtype. The temperature-dependent alteration of amylose content was not only attributed to the reduced expression of GBSS, but also associated with the complimentary effect of SSSIIa and SBEIIb.
Abstract High temperature is the major environmental factor affecting grain starch properties of cooking rice cultivars. In this study, two non-waxy indica rice genotypes, cv. 9311 and its mutant with extremely high amylose phenotype (9311eha) were used to study the differential expressions of genes in starch synthesis and their responses to high temperature (HT). Significant increase in apparent amylose content and hot-water-soluble starch content in mutant 9311eha were genetically caused by a substitution from AGTTATA to AGGTATA at the leader intron 5´ splice site in Wx gene. This mutation resulted in different mRNA transcript levels, mRNA splicing efficiencies and protein levels of Wx between the two rice genotypes, which also lead to the genotype-dependent alteration in the temporal pattern of Wx transcription and granule-bound starch synthase (GBSS) activity in response to HT. However, changes in the activities of other starch synthesizing enzymes and their expressions of distinct isoform genes were not significant with the Wx gene mutation, thus only minor difference in the particle size of starch granule, chain-length distribution and gelatinization enthalpy were found between the two genotypes. The temporal- specific expression of multiple isoform genes responsive to different temperature regiments indicated that the reduction of GBSS transcript expression under HT was generally accompanied by the decreased expressions of SSSIIa, SSSIIIa and SBEIIb. Consequently, high temperature-ripened grains in 9311eha showed high proportion of intermediate and long B chains and somewhat lower level of short A chain compared to the wildtype. The temperature-dependent alteration of amylose content was not only attributed to the reduced expression of GBSS, but also associated with the complimentary effect of SSSIIa and SBEIIb.
|
|
Received: 13 March 2013
Accepted:
|
| Fund: the National Natural Science Foundation of China (31071366 and 31271655) for its financial support to this research project. |
|
Corresponding Authors:
CHENG Fang-min, Tel: +86-571-86940446,E-mail: chengfm@zju.edu.cn
|
| About author: * These authors contributed equally to this study. |
Cite this article:
CAO Zhen-zhen, PAN Gang, WANG Fu-biao, WEI Ke-su, LI Zhao-wei, SHI Chun-hai, GENG Wei, CHENG Fang-min.
2015.
Effect of high temperature on the expressions of genes encoding starch synthesis enzymes in developing rice endosperms. Journal of Integrative Agriculture, 14(4): 642-659.
|
| Asaoka M, Okuno K, Fuwa H. 1985. Effect of environmental temperature at the milky stage on amylose content and fine structure of amylopectin of Waxy and Nonwaxy endosperm starches of rice (Oryza saliva L.). Agricultural and Biological Chemistry, 49, 373–379. Ayres N M, McClung A M, Larkin P D, Bligh H F J, Jones C A, Park W D. 1997. Microsatellites and a single-nucleotide polymorphism differentiate apparent amylose classes in an extended pedigree of US rice germ plasm. Theoretical and Applied Genetics, 94, 773–781. Blazek J, Copeland L. 2008. Pasting and swelling properties of wheat flour and starch in relation to amylose content. Carbohydrate Polymers, 71, 380–387. Brooks A, Jenner C F, Aspinall D. 1982. Effects of water deficit on endosperm starch granules and on grain physiology of wheat and barley. Australian Journal of Plant Physiology, 9, 423–436. Cai Y X, Wang W, Zhu Z W, Zhang Z J, Yang J C, Zhu Q S. 2006. The physiochemical characteristics of amylopectin and their relationships to pasting properties of rice flour in different varieties. Scientia Agricultura Sinica, 39, 1122–1129. (in Chinese) Crofts N, Abe K, Aihara S, Itoh R, Nakamura Y, Itoh K, Fujita N. 2012. Lack of starch synthase IIIa and high expression of granule-bound starch synthase I synergistically increase the apparent amylose content in rice endosperm. Plant Science, 193–194, 62–69. Fabian A, Jager K, Rakszegi M, Barnabas B. 2011. Embryo and endosperm development in wheat (Triticum aestivum L.) kernels subjected to drought stress. Plant Cell Reports, 30, 551–563. Fitzgerald M A, McCouch S R, Hall R D. 2009. Not just a grain of rice: The quest for quality. Trends in Plant Science, 14, 133–139. Fu F F, Xue H W. 2010. Coexpression analysis identifies rice starch regulator 1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiology, 154, 927–938. Fujita N, Kubo A, Suh D S, Wong K S, Jane J L, Ozawa K, Takaiwa F, Inaba Y, Nakamura Y. 2003. Antisense inhibition of isoamylase alters the structure of amylopectin and the physicochemical properties of starch in rice endosperm. Plant Cell Physiology, 44, 607–618. Fujita N, Yoshida M, Kondo T, Saito K, Utsumi Y, Tokunaga T, Nishi A, Satoh H, Park J H, Jane J L, Miyao A, Hirochika H, Nakamura Y. 2007. Characterization of SSIIIa-deficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm. Plant Physiology, 144, 2009–2023. Geigenberger P. 2011. Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiology, 155, 1566–1577. Hanashiro I, Itoh K, Kuratomi Y, Yamazaki M, Igarashi T, Takeda Y. 2008. Granule-bound starch synthase I is responsible for biosynthesis of extra-long unit chains of amylopectin in rice. Plant Cell Physiology, 49, 925–933. Hirose T, Terao T. 2004. A comprehensive expression analysis of the starch synthase gene family in rice (Oryza sativa L.). Planta, 220, 9–16. Jiang H, Dian W M, Wu P. 2003. Effect of high temperature on fine structure of amylopectin in rice endosperm by reducing the activity of the starch branching enzyme. Phytochemistry, 63, 53–59. Juliano B O. 1985. Rice Chemistry and Technology. 2nd ed. American Association of Cereal Chemists, Paul, MN. pp. 59–174. Kitahara K, Hamasuna K, Nozuma K, Otani M, Hamada T, Shimada T, Fujita K, Suganuma T. 2007. Physicochemical properties of amylose-free and high-amylose starches from transgenic sweetpotatoes modified by RNA interference. Carbohydrate Polymers, 69, 233–240. Larkin P D, Park W D. 1999. Transcript accumulation and utilization of alternate and non-consensus splice sites in rice granule-bound starch synthase are temperature-sentitive and controlled by a single-nucleotide polymorphism. Plant Molecular Biology, 40, 719–727. Lin C J, Li C Y, Lin S K, Yang F H, Huang J J, Liu Y H, Lur H S. 2010. Influence of high temperature during grain filling on the accumulation of storage proteins and grain quality in rice (Oryza sativa L.). Journal of Agricultural and Food Chemistry, 58, 10545–10555. Lin S K, Chang M C, Tsai Y G, Lur H S. 2005. Proteomic analysis of the expression of proteins related to rice quality during caryopsis development and the effect of high temperature on expression. Proteomics, 5, 2140–2156. Liu F, Makhmoudova A, Lee E A, Wait R, Emes M J, Tetlow I J. 2009. The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. Journal of Experimental Botany, 60, 4423–4440. Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods, 25, 402–408. Lu F H, Park Y J. 2012. An SNP downstream of the OsBEIIb gene is significantly associated with amylose content and viscosity properties in rice (Oryza sative L.). Journal of Cereal Science, 56, 706–712. Mizukami H, Takeda Y, Hizukuri S. 1999. The structure of the hot-water soluble components in the starch granules of new Japanese rice cultivars. Carbohydrate Polymers, 38, 329–335. Nakamura Y, Francisco P B, Hosaka Y, Sato A, Sawada T, Kubo A, Fujita N. 2005. Essential amino acids of starch synthase IIa differentiate amylopectin structure and starch quality between japonica and indica rice varieties. Plant Molecular Biology, 58, 213–227. Nakamura Y, Yuki K, Park S Y, Ohya T. 1989. Carbohydrate metabolism in the developing endosperm of rice grains. Plant and Cell Physiology, 30, 833–839. Nishi A, Nakamura Y, Tanaka N, Satoh H. 2001. Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiology, 127, 459–472. Ohdan T, Francisco Jr P B, Sawada T, Hirose T, Terao T, Satoh H, Nakaruma Y. 2005. Expression profiling of genes involved in starch synthesis in sink and source organs of rice. Journal of Experimental Botany, 56, 3229–3244. O’Shea M G, Samuel M S, Konik C M, Morell M K. 1998. Fluorophore-assisted carbohydrate electrophoresis (FACE) of oligosaccharides: Efficiency of labelling and high-resolution separation. Carbohydrate Research, 307, 1–12. Peng M, Gao M, Abdal-Aal E S M, Hucl P, Chibbar R N. 1999. Separation and characterization of A- and B-type starch granules in wheat endosperm. Cereal Chemistry, 76, 375–379. Reddy K R, Ali S Z, Bhattacharya K R. 1993. The fine structure of rice-starch amylopectin and its relation to the texture of cooked rice. Carbohydrate Polymers, 22, 267–275. Sidebottom C, Kirkland M, Strongitharm B, Jeffcoat R. 1998. Characterization of the difference of starch branching enzyme activities in normal and low-amylopectin maize during kernel development. Journal of Cereal Science, 27, 279–287. Tan Y F, Corke H. 2002. Factor analysis of physicochemical properties of 63 rice varieties. Journal of the Science of Food and Agriculture, 82, 745–752. Tetlow I J. 2011. Starch biosynthesis in developing seeds. Seed Science Research, 21, 5–32. Tian Z X, Qian Q, Liu M, Liu X, Yan C, Liu G, Gao Z, Tang S, Zeng D, Wang Y, Yu J, Gu M, Li J. 2009. Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proceedings of the National Academy of Sciences of the United States of America, 106, 21760–21765. Thitisaksakul M, Jiménez R C, Arias M C, Beckles D M. 2012. Effects of environmental factors on cereal starch biosynthesis and composition. Journal of Cereal Science, 56, 67–80. 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. Functional Plant Biology, 31, 671–684. Umemoto T, Terashima K, Nakamura Y, Satoh H. 1999. Differences in amylopectin structure between two rice varieties in relation to the effects of temperature during grain-filling. Food Chemistry, 51, 58–62. Vandeputte G E, Delcour J A. 2004. From sucrose to starch granule to starch physical behavior: A focus on rice starch. Carbohydrate Polymers, 58, 245–266. Yamakawa H, Hirose T, Kuroda M, Yamaguchi T. 2007. Comprehensive expression profiling of rice grain filling-related genes under high temperature using DNA microarray. Plant Physiology, 144, 258–277. Yamamoto H, Isozumi N, Sugitani T. 2005. A concavity property of the viscosity growth curve during alkali gelatinization of rice starch. Carbohydrate Polymers, 62, 379–386. Yoo S H, Jane J L. 2002. Structural and physical characteristics of waxy and other wheat starches. Carbohydrate Polymers, 49, 297–305. |
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
