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Allelic variations in the soluble starch synthase II gene family result in changes of grain quality and starch properties in rice (Oryza sativa L.)

Published online by Cambridge University Press:  03 June 2016

X. Y. FAN ,
M. GUO ,
R. D. LI ,
Y. H. YANG ,
M. LIU ,
Q. ZHU ,
S. Z. TANG ,
M. H. GU ,
R. G. XU  and
C. J. YAN
X. Y. FAN
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
M. GUO
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
R. D. LI
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
Y. H. YANG
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
M. LIU
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
Q. ZHU
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
S. Z. TANG
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
M. H. GU
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
R. G. XU*
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
C. J. YAN*
Affiliation:
Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, China
*
*To whom all correspondence should be addressed. Email: [email protected] and [email protected]
*To whom all correspondence should be addressed. Email: [email protected] and [email protected]
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Summary

Soluble starch synthase II (SSII) plays an important role in the biosynthesis of starch and in rice it consists of three isoforms encoded by SSII-1, SSII-2 and SSII-3. However, the genetic effects of various SSII alleles on grain quality have not been systematically characterized. In the present study, the japonica alleles on SSII-1, SSII-2 and SSII-3 (SSIIa) loci from a japonica cultivar, Suyunuo, were respectively introgressed by molecular marker-assisted selection into a typical indica cultivar, Guichao2, through successive backcrossing, generating three sets of near-isogenic lines (NILs). Grain quality and starch property analysis showed that NIL-SSII-3j exhibited significant decreases in the following parameters: amylose content, average granule size, and setback viscosity and consistency; but increases in peak viscosity, hot paste viscosity, gelatinization temperature and relative crystallinity. Moreover, the proportion of short amylopectin chains and branching degree also increased when compared with those of NIL-SSII-3i (Guochao2). Similar effects were observed in NIL-SSII-1j , and certain alterations in the fine structure of starch (granule size) were revealed. However, NIL-SSII-2j did not exert significant effect on grain quality and starch properties. In brief, among the SSII gene family, the functional diversity occurred on SSII-1 and SSII-3, and not on SSII-2. Therefore, it appears that more attention should be directed to SSII-1 and SSII-3 loci for improving the eating and cooking quality of rice.

Type
Crops and Soils Research Papers
Information
The Journal of Agricultural Science , Volume 155 , Issue 1 , January 2017 , pp. 129 - 140
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Copyright
Copyright © Cambridge University Press 2016 

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References

American Association of Cereal Chemists (2000). Approved Methods for the AACC, 10th edn, St. Paul, MN, USA: AACC.Google Scholar
Bao, J. S., He, P., Xia, Y. W., Chen, Y. & Zhu, L. H. (1999). Starch RVA profile parameters of rice are mainly controlled by Wx gene. Chinese Science Bulletin 44, 2047–2051.Google Scholar
Bao, J. S., 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.). Theoretical and Applied Genetics 113, 1171–1183.CrossRefGoogle ScholarPubMed
Butardo, V. M., Fitzgerald, M. A., Bird, A. R., Gidley, M. J., Flanagan, B. M., Larroque, O., Resurreccion, A. P., Laidlaw, H. K. C., Jobling, S. A., Morell, M. K. & Rahman, S. (2011). Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA- and hairpin RNA-mediated RNA silencing. Journal of Experimental Botany 62, 4927–4941.Google Scholar
Cagampang, G. B., Perez, C. M. & Juliano, B. O. (1973). A gel consistency test for eating quality of rice. Journal of the Science of Food and Agriculture 24, 1589–1594.Google Scholar
Cai, L. M., Shi, Y. C., Rong, L. & Hsiao, B. S. (2010). Debranching and crystallization of waxy maize starch in relation to enzyme digestibility. Carbohydrate Polymers 81, 385–393.Google Scholar
Cheetham, N. W. H. & Tao, L. (1998). Variation in crystalline type with amylose content in maize starch granules: an X-ray powder diffraction study. Carbohydrate Polymers 36, 277–284.Google Scholar
Chun, A., Lee, H. J., Hamaker, B. R. & Janaswamy, S. (2015). Effects of ripening temperature on starch structure and gelatinization, pasting, and cooking properties in rice (Oryza sativa). Journal of Agricultural and Food Chemistry 63, 3085–3093.Google Scholar
Gao, Z. Y., Zeng, D. L., Cui, X., Zhou, Y., Yan, M., Huang, D., Li, J. & Qian, Q. (2003). Map-based cloning of the ALK gene, which controls the gelatinization temperature of rice. Science in China C: Life Sciences 46, 661–668.Google Scholar
Gidley, M. J. & Bulpin, P. V. (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.Google Scholar
Han, Y. P., Xu, M. L., Liu, X. Y., Yan, C. J., Korban, S. S., Chen, X. L. & Gu, M. H. (2004). Genes coding for starch branching enzymes are major contributors to starch viscosity characteristics in waxy rice (Oryza sativa L.). Plant Science 166, 357–364.Google Scholar
Hoover, R. & Ratnayake, W. S. (2002). Starch characteristics of black bean, chick pea, lentil, navy bean and pinto bean cultivars grown in Canada. Food Chemistry 78, 489–498.Google Scholar
Jane, J., Chen, Y. Y., Lee, L. F., McPherson, A. E., Wong, K. S., Radosavljevic, M. & Kasemsuwan, T. (1999). Effects of amylopectin branch chain length and amylose content on the gelatinization and pasting properties of starch. Cereal Chemistry 76, 629–637.Google Scholar
Jeon, J. S., Ryoo, N., Hahn, T. R., Walia, H. & Nakamura, Y. (2010). Starch biosynthesis in cereal endosperm. Plant Physiology and Biochemistry 48, 383–392.Google Scholar
Jiang, H. W., Dian, W. M., Liu, F. Y. & Wu, P. (2004). Molecular cloning and expression analysis of three genes encoding starch synthase II in rice. Planta 218, 1062–1070.CrossRefGoogle ScholarPubMed
Juliano, B. O. (1985). Criteria and test for rice grain quality. In Rice Chemistry and Technology (Ed. Juliano, B. O.), pp. 443–513. St. Paul, MN, USA: American Association of Cereal Chemists Inc.Google Scholar
Larkin, P. D., McClung, A. M., Ayres, N. M. & Park, W. D. (2003). The effect of the Waxy locus (granule bound starch synthase) on pasting curve characteristics in specialty rices (Oryza sativa L.). Euphytica 131, 243–253.Google Scholar
Little, R. R., Hilder, G. B. & Dawson, E. H. (1958). Differential effect of dilute alkali on 25 varieties of milled white rice. Cereal Chemistry 35, 111–126.Google Scholar
Li, E., Hasjim, J., Dhital, S., Godwin, R. D. & Gilbert, R. G. (2011). Effect of a gibberellin-biosynthesis inhibitor treatment on the physicochemical properties of sorghum starch. Journal of Cereal Science 53, 328–334.Google Scholar
Luo, J., Jobling, S. A., Millar, A., Morell, M. K. & 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. doi: 10.1186/s12284-015-0046-5 Google Scholar
McKenzie, K. S. & Rutger, J. N. (1983). Genetic analysis of amylose content, alkali spreading score, and grain dimensions in rice. Crop Science 23, 306–311.Google Scholar
Mikami, I., Uwatoko, N., Ikeda, Y., Yamaguchi, J., Hirano, H. Y., Suzuki, Y. & Sano, Y. (2008). Allelic diversification at the wx locus in landraces of Asian rice. Theoretical and Applied Genetics 116, 979–989.Google Scholar
Moates, G. K., Noel, T. R., Parker, R. & Ring, S. G. (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.Google Scholar
Myers, A. M., Morell, M. K., James, M. G. & Ball, S. G. (2000). Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiology 122, 989–997.Google Scholar
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.Google Scholar
Nakamura, Y., Francisco, P. B., Hosaka, Y., Sato, A., Sawada, T., Kubo, A. & Fujita, N. (2005). Essential amino acids of starch IIa differentiate amylopectin structure and starch quality between japonica and indica rice varieties. Plant Molecular Biology 58, 213–227.Google Scholar
Noda, T., Takahata, Y., Sato, T., Suda, I., Morishita, T., Ishiguro, K. & Yamakawa, O. (1998). Relationships between chain length distribution of amylopectin and gelatinization properties within the same botanical origin for sweet potato and buckwheat. Carbohydrate Polymers 37, 153–158.Google Scholar
Ohdan, T., Francisco, P. B., Sawada, T., Hirose, T., Terao, T., Satoh, H. & Nakamura, Y. (2005). Expression profiling of genes involved in starch synthesis in sink and source organs of rice. Journal of Experimental Botany 56, 3229–3244.Google Scholar
Park, I. M., Ibanez, A. M., Zhong, F. & Shoemaker, C. F. (2007). Gelatinization and pasting properties of waxy and non-waxy rice starches. Starch/Staerke 59, 388–396.CrossRefGoogle Scholar
Ramesh, M., Zakiuddin Ali, S. & Bhattacharya, K. R. (1999). Structure of rice starch and its relation to cooked-rice texture. Carbohydrate Polymers 38, 337–347.Google Scholar
Sevenou, O., Hill, S. E., Farhat, I. A. & Mitchell, J. R. (2002). Organisation of the external region of the starch granule as determined by infrared spectroscopy. International Journal of Biological Macromolecules 31, 79–85.Google Scholar
Song, Y. & Jane, J. (2000). Characterization of barley starches of waxy, normal, and high amylose varieties. Carbohydrate Polymers 41, 365–377.Google Scholar
Takeda, Y., Hizukuri, S. & Juliano, B. O. (1989). Structures and amounts of branched molecules in rice amyloses. Carbohydrate Research 186, 163–166.Google Scholar
Tan, Y. F., Li, J. X., Yu, S. B., Xing, Y. Z., Xu, C. G. & Zhang, Q. F. (1999). The three important traits for cooking and eating quality of rice grains are controlled by a single locus in an elite rice hybrid, Shanyou 63. Theoretical and Applied Genetics 99, 642–648.Google Scholar
Tian, Z. X., Qian, Q., Liu, Q. Q., Yan, M. X., Liu, X. F., Yan, C. J., Liu, G. F., Gao, Z. Y., Tang, S. Z., Zeng, D. L., Wang, Y. H., Yu, J. M., Gu, M. H. & Li, J. Y. (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.Google Scholar
Tian, Z. X., Yan, C. J., Qian, Q., Yan, S., Xie, H. L., Wang, F., Xu, J. F., Liu, G. F., Wang, Y. H., Liu, Q. Q., Tang, S. Z., Li, J. Y. & Gu, M. H. (2010). Development of gene-tagged molecular markers for starch synthesis-related genes in rice. Chinese Science Bulletin 55, 3768–3777.Google Scholar
Tran, T. T. B., Shelat, K. J., Tang, D., Li, E., Gilbert, R. G. & Hasjim, J. (2011). The degradation on three structural levels of starch in rice flour can be independently controlled during grinding. Journal of Agricultural and Food Chemistry 59, 3964–3973.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. Theoretical and Applied Genetics 104, 1–8.Google Scholar
Vandeputte, G. E. & Delcour, J. A. (2004). From sucrose to starch granule to starch physical behaviour: a focus on rice starch. Carbohydrate Polymers 58, 245–266.Google Scholar
Wang, K., Hasjim, J., Wu, A. C., Henry, R. J. & Gilbert, R. G. (2014). Variation in amylose fine structure of starches from different botanical sources. Journal of Agricultural and Food Chemistry 62, 4443–4453.Google Scholar
Wang, Y. J., White, P., Pollack, L. & Jane, J. (1993). Characterization of starch structures of 17 maize endosperm mutant genotypes with Oh43 inbred line background. Cereal Chemistry 70, 171–179.Google Scholar
Wang, Z. Y., Zheng, F. Q., Shen, G. Z., Gao, J. P., Snustad, D. P., Li, M. G., Zhang, J. L. & Hong, M. M. (1995). The amylose content in rice endosperm is related to the post-transcriptional regulation of the waxy gene. Plant Journal 7, 613–622.Google Scholar
Warren, F. J., Royall, P. G., Gaisford, S., Butterworth, P. J. & Ellis, P. R. (2011). Binding interactions of α-amylase with starch granules: the influence of supramolecular structure and surface area. Carbohydrate Polymers 86, 1038–1047.CrossRefGoogle Scholar
Waters, D. L., Henry, R. J., Reinke, R. F. & Fitzgerald, M. A. (2006). Gelatinization temperature of rice explained by polymorphisms in starch synthase. Plant Biotechnology Journal 4, 115–122.CrossRefGoogle ScholarPubMed
Wei, C. X., Qin, F. L., Zhou, W. D., Yu, H. G., Xu, B., Chen, C., Zhu, L. J., Wang, Y. P., Gu, M. H. & Liu, Q. Q. (2010 a). Granule structure and distribution of allomorphs in C-type high-amylose rice starch granule modified by antisense RNA inhibition of starch branching enzyme. Journal of Agricultural and Food Chemistry 58, 11946–11954.Google Scholar
Wei, C. X., Xu, B., Qin, F. L., Yu, H. G., Chen, C., Meng, X. L., Zhu, L. J., Wang, Y. P., Gu, M. H. & Liu, Q. Q. (2010 b). C-type starch from high-amylose rice resistant starch granules modified by antisense RNA inhibition of starch branching enzyme. Journal of Agricultural and Food Chemistry 58, 7383–7388.Google Scholar
Wei, C. X., Qin, F. L., Zhou, W. D., Xu, B., Chen, C., Chen, Y. F., Wang, Y. P., Gu, M. H. & Liu, Q. Q. (2011). Comparison of the crystalline properties and structural changes of starches from high-amylose transgenic rice and its wild type during heating. Food Chemistry 128, 645–652.Google Scholar
Wu, H. K., Liang, G. H., Gu, Y. J., Shan, L. L., Wang, F., Han, Y. P. & Gu, M. H. (2006). The effect of the starch-synthesizing genes on RVA profile characteristics in rice (Oryza sativa L.). Acta Agronomica Sinica 32, 1597–1603.Google Scholar
Yan, C. J., Fang, Y. W., Li, M., Peng, J. C., Liu, Q. Q., Tang, S. Z. & Gu, M. H. (2010). Genetic effect of PUL allelic variation on rice cooking and eating qualities. Acta Agronomica Sinica 36, 728–735.Google Scholar
Yan, C. J., Tian, Z. X., Fang, Y. W., Yang, Y. C., Li, J., Zeng, S. Y., Gu, S. L., Xu, C. W., Tang, S. Z. & Gu, M. H. (2011). Genetic analysis of starch paste viscosity parameters in glutinous rice (Oryza sativa L.). Theoretical and Applied Genetics 122, 63–76.Google Scholar
Yu, G., Olsen, K. M. & Schaal, B. A. (2011). Association between nonsynonymous mutations of starch synthase IIa and starch quality in rice (Oryza sativa). New Phytologist 189, 593–601.Google Scholar
Zhang, Z. J., Li, M., Fang, Y. W., Liu, F. C., Lu, Y., Meng, Q. C., Peng, J. C., Yi, X. H., Gu, M. H. & Yan, C. J. (2012). Diversification of the Waxy gene is closely related to variations in rice eating and cooking quality. Plant Molecular Biology Reporter 30, 462–469.Google Scholar
Zhu, L. J., Liu, Q. Q., Sang, Y. J., Gu, M. H. & Shi, Y. C. (2010). Underlying reasons for waxy rice flours having different pasting properties. Food Chemistry 120, 94–100.Google Scholar