A genetic strategy generating wheat with very high amylose content

Plant Biotechnology Journal

Volumn 13, Issue 9, 2015, Pages 1276-1286

  Regina, Ahmed ^a   Berbezy, Pierre ^b   Kosar Hashemi, Behjat ^a   Li, Suzhi ^a   Cmiel, Mark ^a   Larroque, Oscar ^a   Bird, Anthony R ^a   Swain, Steve M ^a   Cavanagh, Colin ^a   Jobling, Stephen A ^a   Li, Zhongyi ^a   Morell, Matthew ^a,c  

^a CSIRO   (Australia)

^b ZAC Les Portes de Riom ^*  (France)

^c INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

Author keywords

Amylopectin; Amylose; Resistant starch; Starch; Starch branching enzyme; Wheat

Indexed keywords

AMYLOSE; GENETIC MARKER;

ALLELE; BIOSYNTHESIS; CROSS BREEDING; GENETIC MARKER; GENETICS; METABOLISM; PLANT GENE; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSGENIC PLANT; WHEAT;

ALLELES; AMYLOSE; CROSSES, GENETIC; GENES, PLANT; GENETIC MARKERS; PLANTS, GENETICALLY MODIFIED; POLYMORPHISM, SINGLE NUCLEOTIDE; TRITICUM;

EID: 84955188362     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12345     Document Type: Article

References (61)

1. Andersson, L., Andersson, R., Andersson, R.E., Rydberg, U., Larsson, H. and Aman, P. (2002) Characterisation of the in vitro products of potato starch branching enzymes I and II. Carbohydr. Polym. 50, 249-257.
2. Belobrajdic, D.P., Bird, A.R., Conlon, M.A., Williams, B.A., Kang, S., McSweeney, C.S., Zhang, D., Bryden, W.L., Gidley, M.J. and Topping, D.L. (2012) An arabinoxylan-rich fraction from wheat enhances caecal fermentation and protects colonocyte DNA against diet-induced damage in pigs. Br. J. Nutr. 107, 1274-1282.
3. Bertoft, E., Piyachomkwan, K., Chatakanonda, P. and Sriroth, K. (2008) Internal unit chain composition in amylopectins. Carbohydr. Polym. 74, 527-543.
4. Blauth, S.L., Kim, K.N., Klucinec, J., Shannon, J.C., Thompson, D. and Guiltinan, M. (2002) Identification of Mutator insertional mutants of starch-branching enzyme 1 (sbe1) in Zea mays L. Plant Mol. Biol. 48, 287-297.
5. van Bussel, B.C.T., Soedamah-Muthu, S.S., Henry, R.M.A., Schalkwijk, C.G., Ferreira, I., Chaturvedi, N., Toeller, M., Fuller, J.H., Stehouwer, C.D.A. and Complications, E.P. (2013) Unhealthy dietary patterns associated with inflammation and endothelial dysfunction in type 1 diabetes: the EURODIAB study. Nutr. Metab. Cardiovasc. Dis. 23, 758-764.
6. 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. and Rahman, S. (2011) Impact of down-regulation of starch branching enzyme IIb in rice by artificial microRNA- and hairpin RNA-mediated RNA silencing. J. Exp. Bot. 62, 4927-4941.
7. Carciofi, M., Blennow, A., Jensen, S.L., Shaik, S.S., Henriksen, A., Buleon, A., Holm, P.B. and Hebelstrup, K.H. (2012) Concerted suppression of all starch branching enzyme genes in barley produces amylose-only starch granules. BMC Plant Biol. 12, 223.
8. Cavanagh, C., Morell, M., Mackay, I. and Powell, W. (2008) From mutations to MAGIC: resources for gene discovery, validation and delivery in crop plants. Curr. Opin. Plant Biol. 11, 215-221.
9. Chandler, P.M. and Harding, C.A. (2013) 'Overgrowth' mutants in barley and wheat: new alleles and phenotypes of the 'Green Revolution' Della gene. J. Exp. Bot. 64, 1603-1613.
10. Christiansen, C., Abou Hachem, M., Janecek, S., Vikso-Nielsen, A., Blennow, A. and Svensson, B. (2009) The carbohydrate-binding module family 20-diversity, structure, and function. FEBS J. 276, 5006-5029.
11. Conlon, M.A., Kerr, C.A., McSweeney, C.S., Dunne, R.A., Shaw, J.M., Kang, S., Bird, A.R., Morell, M.K., Lockett, T.J., Molloy, P.L., Regina, A., Toden, S., Clarke, J.M. and Topping, D.L. (2012) Resistant starches protect against colonic DNA damage and alter microbiota and gene expression in rats fed a western diet. J. Nutr. 142, 832-840.
12. Cunxu, W., Fengling, Q., Weidong, Z., Bin, X., Chong, C., Yifang, C., Youping, W., Minghong, G. and Qiaoquan, L. (2011) Comparison of the crystalline properties and structural changes of starches from high-amylose transgenic rice and its wild type during heating. Food Chem. 128, 645-652.
13. Drummond, G.S., Smith, E.E. and Whelan, W.J. (1972) Purification and properties of potato alpha-1, 4-glucan-alpha-1, 4-glucan 6-glycosyltransferase (Q-Enzyme). Eur. J. Biochem. 26, 168-176.
14. Flipse, E., Keetels, C., Jacobsen, E. and Visser, R.G.F. (1996) The dosage effect of the wildtype GBSS allele is linear for GBSS activity but not for amylose content: absence of amylose has a distinct influence on the physico-chemical properties of starch. Theor. Appl. Genet. 92, 121-127.
15. Gomand, S.V., Lamberts, L., Derde, L.J., Goesaert, H., Vandeputte, G.E., Goderis, B., Visser, R.G.F. and Delcour, J.A. (2010) Structural properties and gelatinisation characteristics of potato and cassava starches and mutants thereof. Food Hydrocoll. 24, 307-317.
16. Haralampu, S.G. (2000) Resistant starch - a review of the physical properties and biological impact of RS3. Carbohydr. Polym. 41, 285-292.
17. Hazard, B., Zhang, X., Colasuonno, P., Uauy, C., Beckles, D.M. and Dubcovsky, J. (2012) Induced mutations in the starch branching enzyme II (SBEII) genes increase amylose and resistant starch content in durum wheat. Crop Sci. 52, 1754-1766.
18. Xia, H., Yandeau-Nelson, M., Thompson, D.B. and Guiltinan, M.J. (2011) Deficiency of maize starch-branching enzyme i results in altered starch fine structure, decreased digestibility and reduced coleoptile growth during germination. BMC Plant Biol. 11, 13.
19. Huang, B.E., Cavanagh, C., Rampling, L., Kilian, A. and George, A.W. (2012) iDArTs: increasing the value of genomic resources at no cost. Mol. Breeding, 30, 927-938.
20. Imberty, A. and Perez, S. (1988) A revisit to the 3-dimensional structure of B-type starch. Biopolymers, 27, 1205-1221.
21. Itoh, K., Ozaki, H., Okada, K., Hori, H., Takeda, Y. and Mitsui, T. (2003) Introduction of Wx transgene into rice wx mutants leads to both high- and low-amylose rice. Plant Cell Physiol. 44, 473-480.
22. Jenkins, P.J. and Donald, A.M. (1995) The influence of amylose on starch granule structure. Int. J. Biol. Macromol. 17, 315-321.
23. Kumar, V., Sinha, A.K., Makkar, H.P.S., de Boeck, G. and Becker, K. (2012) Dietary roles of non-starch polysachharides in human nutrition: a review. Crit. Rev. Food Sci. Nutr. 52, 899-935.
24. Lee, J.-S., Ee, M.-L., Chung, K.-H. and Othman, Z. (2013) Formation of resistant corn starches induced by gamma-irradiation. Carbohydr. Polym. 97, 614-617.
25. Li, L., Jiang, H.X., Campbell, M., Blanco, M. and Jane, J.L. (2008) Characterization of maize amylose-extender (ae) mutant starches. Part I: relationship between resistant starch contents and molecular structures. Carbohydr. Polym. 74, 396-404.
26. Liu, F., Makhmoudova, A., Lee, E.A., Wait, R., Emes, M.J. and Tetlow, I.J. (2009) The amylose extender mutant of maize conditions novel protein-protein interactions between starch biosynthetic enzymes in amyloplasts. J. Exp. Bot. 60, 4423-4440.
27. Manners, D.J. (1989) Recent developments in our understanding of amylopectin structure. Carbohydr. Polym. 11, 87-112.
28. Mizuno, K., Kawasaki, T., Shimada, H., Satoh, H., Kobayashi, E., Okumura, S., Arai, Y. and Baba, T. (1993) Alteration of the structural-properties of starch components by the lack of an isoform of starch branching enzyme in rice seeds. J. Biol. Chem. 268, 19084-19091.
29. Morell, M.K., Kosar-Hashemi, B., Cmiel, M., Samuel, M.S., Chandler, P., Rahman, S., Buleon, A., Batey, I.L. and Li, Z. (2003) Barley sex6 mutants lack starch synthase IIa activity and contain a starch with novel properties. Plant J. 34, 173-185.
30. Morrison, W.R., Law, R.V. and Snape, C.E. (1993) Evidence for inclusion complexes of lipids with V-amylose in maize, rice and oat starches. J. Cereal Sci. 18, 107-109.
31. Ng, P.C. and Henikoff, S. (2003) SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res. 31, 3812-3814.
32. Nishi, A., Nakamura, Y., Tanaka, N. and Satoh, H. (2001) Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiol. 127, 459-472.
33. Rahman, S., Regina, A., Li, Z., Mukai, Y., Yamamoto, M., Kosar-Hashemi, B., Abrahams, S. and Morell, M.K. (2001) Comparison of starch-branching enzyme genes reveals evolutionary relationships among isoforms. Characterization of a gene for starch-branching enzyme IIa from the wheat D genome donor Aegilops tauschii. Plant Physiol. 125, 1314-1324.
34. Rahman, S., Bird, A., Regina, A., Li, Z., Ral, J.P., McMaugh, S., Topping, D. and Morell, M. (2007) Resistant starch in cereals: exploiting genetic engineering and genetic variation. J. Cereal Sci. 46, 251-260.
35. Rawat, N., Sehgal, S.K., Joshi, A., Rothe, N., Wilson, D.L., McGraw, N., Vadlani, P.V., Li, W. and Gill, B.S. (2012) A diploid wheat TILLING resource for wheat functional genomics. BMC Plant Biol. 12, 205.
36. Regina, A., Kosar-Hashemi, B., Li, Z.Y., Rampling, L., Cmiel, M., Gianibelli, M.C., Konik-Rose, C., Larroque, O., Rahman, S. and Morell, M.K. (2004) Multiple isoforms of starch branching enzyme-I in wheat: lack of the major SBE-I isoform does not alter starch phenotype. Funct. Plant Biol. 31, 591-601.
37. Regina, A., Kosar-Hashemi, B., Li, Z.Y., Pedler, A., Mukai, Y., Yamamoto, M., Gale, K., Sharp, P., Morell, M.K. and 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.
38. Regina, A., Bird, A., Topping, D., Bowden, S., Freeman, J., Barsby, T., Kosar-Hashemi, B., Li, Z.Y., Rahman, S. and Morell, M. (2006) High-amylose wheat generated by RNA interference improves indices of large-bowel health in rats. Proc. Natl Acad. Sci. USA, 103, 3546-3551.
39. Regina, A., Kosar-Hashemi, B., Ling, S., Li, Z.Y., Rahman, S. and Morell, M. (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.
40. Regina, A., Blazek, J., Gilbert, E., Flanagan, B.M., Gidley, M.J., Cavanagh, C., Ral, J.-P., Larroque, O., Bird, A.R., Li, Z. and Morell, M.K. (2012) Differential effects of genetically distinct mechanisms of elevating amylose on barley starch characteristics. Carbohydr. Polym. 89, 979-991.
41. Ryuto, H., Fukunishi, N., Hayashi, Y., Ichida, H., Abe, T., Kase, M. and Yano, Y. (2008) Heavy-ion beam irradiation facility for biological samples in RIKEN. Plant Biotechnol. 25, 119-122.
42. Satoh, H., Nishi, A., Yamashita, K., Takemoto, Y., Tanaka, Y., Hosaka, Y., Sakurai, A., Fujita, N. and Nakamura, Y. (2003) Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiol. 133, 1111-1121.
43. Schirmer, M., Hochstotter, A., Jekle, M., Arendt, E. and Becker, T. (2013) Physicochemical and morphological characterization of different starches with variable amylose/amylopectin ratio. Food Hydrocoll. 32, 52-63.
44. Sestili, F., Botticella, E., Proietti, G., Janni, M., D'Ovidio, R. and Lafiandra, D. (2012) Amylose content is not affected by overexpression of the Wx-B1 gene in durum wheat. Plant Breeding, 131, 700-706.
45. Sim, N.-L., Kumar, P., Hu, J., Henikoff, S., Schneider, G. and Ng, P.C. (2012) SIFT web server: predicting effects of amino acid substitutions on proteins. Nucleic Acids Res. 40, W452-W457.
46. Slade, A.J., McGuire, C., Loeffler, D., Mullenberg, J., Skinner, W., Fazio, G., Holm, A., Brandt, K.M., Steine, M.N., Goodstal, J.F. and Knauf, V.C. (2012) Development of high amylose wheat through TILLING. BMC Plant Biol. 12, 69.
47. Sorrells, M.E., La Rota, M., Bermudez-Kandianis, C.E., Greene, R.A., Kantety, R., Munkvold, J.D., Miftahudin, Mahmoud, A., Ma, X.F., Gustafson, P.J., Qi, L.L.L., Echalier, B., Gill, B.S., Matthews, D.E., Lazo, G.R., Chao, S.M., Anderson, O.D., Edwards, H., Linkiewicz, A.M., Dubcovsky, J., Akhunov, E.D., Dvorak, J., Zhang, D.S., Nguyen, H.T., Peng, J.H., Lapitan, N.L.V., Gonzalez-Hernandez, J.L., Anderson, J.A., Hossain, K., Kalavacharla, V., Kianian, S.F., Choi, D.W., Close, T.J., Dilbirligi, M., Gill, K.S., Steber, C., Walker-Simmons, M.K., McGuire, P.E. and Qualset, C.O. (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res. 13, 1818-1827.
48. Sun, C.X., Sathish, P., Ahlandsberg, S. and Jansson, C. (1998) The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. Plant Physiol. 118, 37-49.
49. Taylor, N.E. and Greene, E.A. (2003) PARSESNP: a tool for the analysis of nucleotide polymorphisms. Nucleic Acids Res. 31, 3808-3811.
50. Topping, D.L. and Clifton, P.M. (2001) Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol. Rev. 81, 1031-1064.
51. Topping, D.L., Segal, I., Regina, A., Conlon, M.A., Bajka, B.H., Toden, S., Clarke, J.M., Morell, M.K. and Bird, A.R. (2010) In: Dietary Fibre: New Frontiers for Food and Health. pp. 311-321. Wageningen Academic Publishers.
52. Tziotis, A., Seetharaman, K., Wong, K.S., Klucinec, J.D., Jane, J.L. and White, P.J. (2004) Structural properties of starch fractions isolated from normal and mutant corn genotypes using different methods. Cereal Chem. 81, 611-620.
53. Umemoto, T., Aoki, N., Lin, H.X., Nakamura, Y., Inouchi, N., Sato, Y., Yano, M., Hirabayashi, H. and Maruyama, S. (2004) Natural variation in rice starch synthase IIa affects enzyme and starch properties. Funct. Plant Biol. 31, 671-684.
54. Umemoto, T., Horibata, T., Aoki, N., Hiratsuka, M., Yano, M. and Inouchi, N. (2008) Effects of variations in starch synthase on starch properties and eating quality of rice. Plant Prod. Sci. 11, 472-480.
55. Wong, J.M.W., de Souza, R., Kendall, C.W.C., Emam, A. and Jenkins, D.J.A. (2006) Colonic health: fermentation and short chain fatty acids. J. Clin. Gastroenterol. 40, 235-243.
56. Wu, H.C.H. and Sarko, A. (1978) Packing analysis of carbohydrates and polysaccharides. 9. Double-helical molecular structure of crystalline A-Amylose. Carbohydr. Res. 61, 27-40.
57. Yamamori, M., Fujita, S., Hayakawa, K., Matsuki, J. and 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.
58. Yamamori, M., Kato, M., Yui, M. and Kawasaki, M. (2006) Resistant starch and starch pasting properties of a starch synthase IIa-deficient wheat with apparent high amylose. Aust. J. Agric. Res. 57, 531-535.
59. Yang, C.Z., Shu, X.L., Zhang, L.L., Wang, X.Y., Zhao, H.J., Ma, C.X. and Wu, D.X. (2006) Starch properties of mutant rice high in resistant starch. J. Agric. Food Chem. 54, 523-528.
60. Zhang, X.L., Colleoni, C., Ratushna, V., Sirghle-Colleoni, M., James, M.G. and Myers, A.M. (2004) Molecular characterization demonstrates that the Zea mays gene sugary2 codes for the starch synthase isoform SSIIa. Plant Mol. Biol. 54, 865-879.
61. Zhu, L., Gu, M., Meng, X., Cheung, S.C.K., Yu, H., Huang, J., Sun, Y., Shi, Y. and Liu, Q. (2012) High-amylose rice improves indices of animal health in normal and diabetic rats. Plant Biotechnol. J. 10, 353-362.