Molecular insights into how a deficiency of amylose affects carbon allocation - carbohydrate and oil analyses and gene expression profiling in the seeds of a rice waxy mutant

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Zhang, Ming Zhou ^a   Fang, Jie Hong ^a   Yan, Xia ^b,c   Liu, Jun ^a   Bao, Jin Song ^d   Fransson, Gunnel ^b   Andersson, Roger ^b   Jansson, Christer ^e   Åman, Per ^b   Sun, Chuanxin ^b  

^a CHINA JILIANG UNIVERSITY   (China)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c Chinese Academy of Sciences   (China)

^d ZHEJIANG UNIVERSITY   (China)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

Carbon allocation; Gene expression; Quantitative polymerase chain reaction (qPCR); Rice (Oryza sativa); Suppression subtractive hybridization (SSH); Waxy seeds

Indexed keywords

ORYZA SATIVA;

AMYLOPECTIN; AMYLOSE; CARBON; STARCH SYNTHASE; VEGETABLE OIL; VEGETABLE PROTEIN; WAXY PROTEIN, PLANT;

ARTICLE; CARBOHYDRATE METABOLISM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; NUCLEIC ACID HYBRIDIZATION; PHENOTYPE; PLANT GENE; PLANT SEED; PROMOTER REGION; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE;

AMYLOPECTIN; AMYLOSE; CARBOHYDRATE METABOLISM; CARBON; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MUTATION; NUCLEIC ACID HYBRIDIZATION; ORYZA SATIVA; PHENOTYPE; PLANT OILS; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDS; STARCH SYNTHASE;

MLCS; MLOWN;

EID: 84870362239     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-230     Document Type: Article

References (78)

1. Charalampopoulos D, Wang R, Pandiella SS, Webb C. Application of cereals and cereal components in functional foods. Int J Food Microbiol 2002, 79:131-141.
2. Tharanathan RN. Food-derived carbohydrates-structural complexity and functional diversity. Crit Rev Biotechnol 2002, 22:65-84.
3. Banas A, Debski H, Banas W, Heneen WK, Dahlqvist A, Bafor M, Gummeson PO, Marttila S, Ekman A, Carlsson AS, Stymne S. Lipids in grain tissues of oat (Avena sativa): differences in content, time of deposition, and fatty acid composition. J Exp Bot 2007, 58:2463-2470.
4. Geigenberger P. Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 2011, 155:1566-1577.
5. Blennow A, Engelsen SB. Helix-breaking news: fighting crystalline starch energy deposits in the cell. Trends Plant Sci 2010, 15:236-240.
6. Kamal-Eldin A, Lærke HN, Knudsen KE, Lampi AM, Piironen V, Adlercreutz H, Katina K, Poutanen K, Åman P. Physical, microscopic and chemical characterisation of industrial rye and wheat brans from the Nordic countries. Food Nutr Res 2009,
7. Jones PJ. Dietary agents that target gastrointestinal and hepatic handling of bile acids and cholesterol. J Clin Lipidol 2008, 2:S4-10.
8. Andersson AA, Lampi AM, Nyström L, Piironen V, Li L, Ward JL, Gebruers K, Courtin CM, Delcour JA, Boros D, Fraś A, Dynkowska W, Rakszegi M, Bedo Z, Shewry PR, Åman P. Phytochemical and dietary fiber components in barley varieties in the HEALTHGRAIN Diversity Screen. J Agric Food Chem 2008, 56:9767-9776.
9. Hayden DM, Rolletschek H, Borisjuk L, Corwin J, Kliebenstein DJ, Grimberg A, Stymne S, Dehesh K. Cofactome analyses reveal enhanced flux of carbon into oil for potential biofuel production. Plant J 2011, 67:1018-1028.
10. Nalawade S, Nalawade S, Liu C, Jansson C, Sun C. Development of an efficient tissue culture after crossing (TCC) system for transgenic improvement of barley as a bioenergy crop. Appl Energy 2012, 91:405-411.
11. Pouvreau B, Baud S, Vernoud V, Morin V, Py C, Gendrot G, Pichon JP, Rouster J, Paul W, Rogowsky PM. Duplicate maize Wrinkled1 transcription factors activate target genes involved in seed oil biosynthesis. Plant Physiol 2011, 156:674-686.
12. Shen B, Allen WB, Zheng P, Li C, Glassman K, Ranch J, Nubel D, Tarczynski MC. Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 2010, 153:980-987.
13. Alonso AP, Val DL, Shachar-Hill Y. Central metabolic fluxes in the endosperm of developing maize seeds and their implications for metabolic engineering. Metab Eng 2011, 13:96-107.
14. Ayre BG. Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant 2011, 4:377-394.
15. Roitsch T. Source-sink regulation by sugar and stress. Curr Opin Plant Biol 1999, 2:198-206.
16. Emes MJ, Bowsher CG, Hedley C, Burrell MM, Scrase-Field ES, Tetlow IJ. Starch synthesis and carbon partitioning in developing endosperm. J Exp Bot 2003, 54:569-575.
17. Ekman A, Hayden DM, Dehesh K, Bülow L, Stymne S. Carbon partitioning between oil and carbohydrates in developing oat (Avena sativa L.) seeds. J Exp Bot 2008, 59:4247-4257.
18. Sanjaya, Durrett TP, Weise SE, Benning C. Increasing the energy density of vegetative tissues by diverting carbon from starch to oil biosynthesis in transgenic Arabidopsis. Plant Biotechnol J 2011, 9:874-883.
19. Gout E, Bligny R, Douce R, Boisson AM, Rivasseau C. Early response of plant cell to carbon deprivation: in vivo 31P-NMR spectroscopy shows a quasi-instantaneous disruption on cytosolic sugars, phosphorylated intermediates of energy metabolism, phosphate partitioning, and intracellular pHs. New Phytol 2011, 189:135-147.
20. Geigenberger P, Kolbe A, Tiessen A. Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 2005, 56:1469-1479.
21. Kühn C, Grof CP. Sucrose transporters of higher plants. Curr Opin Plant Biol 2010, 13:288-298.
22. Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS. Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 2010, 3:942-955.
23. Cho JI, Kim HB, Kim CY, Hahn TR, Jeon JS. Identification and characterization of the duplicate rice sucrose synthase genes OsSUS5 and OsSUS7 which are associated with the plasma membrane. Mol Cells 2011, 31:553-561.
24. Jansson C, Westerbergh A, Zhang J, Hu X, Sun C. Cassava, a potential biofuel crop in (the ) People's Republic of China. Appl Energy 2009, 86:S95-S99.
25. Halford NG, Paul MJ. Carbon metabolite sensing and signaling. Plant Biotechnol J 2003, 1:381-398.
26. Slewinski TL. Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: a physiological perspective. Mol Plant 2011, 4:641-662.
27. Comparot-Moss S, Denyer K. The evolution of the starch biosynthetic pathway in cereals and other grasses. J Exp Bot 2009, 60:2481-2492.
28. Kleczkowski LA, Geisler M, Fitzek E, Wilczynska M. A common structural blueprint for plant UDP-sugar-producing pyrophosphorylases. Biochem J 2011, 439:375-379.
29. Park JI, Ishimizu T, Suwabe K, Sudo K, Masuko H, Hakozaki H, Nou IS, Suzuki G, Watanabe M. UDP-glucose pyrophosphorylase is rate limiting in vegetative and reproductive phases in Arabidopsis thaliana. Plant Cell Physiol 2010, 51:981-996.
30. Ghillebert R, Swinnen E, Wen J, Vandesteene L, Ramon M, Norga K, Rolland F, Winderickx J. The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: structure, function and regulation. FEBS J 2011, 278:3978-3990.
31. Eastmond PJ, Graham IA. Trehalose metabolism: a regulatory role for trehalose-6-phosphate?. Curr Opin Plant Biol 2003, 6:231-235.
32. Weselake RJ, Taylor DC, Rahman MH, Shah S, Laroche A, McVetty PB, Harwood JL. Increasing the flow of carbon into seed oil. Biotechnol Adv 2009, 27:866-878.
33. Shi L, Katavic V, Yu Y, Kunst L, Haughn G. Arabidopsis glabra2 mutant seeds deficient in mucilage biosynthesis produce more oil. Plant J 2012, 69:37-46.
34. Sun C, Palmqvist S, Olsson H, Borén M, Ahlandsberg S, Jansson C. A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 2003, 15:2076-2092.
35. Sun C, Höglund AS, Olsson H, Mangelsen E, Jansson C. Antisense oligodeoxynucleotide inhibition as a potent strategy in plant biology: identification of SUSIBA2 as a transcriptional activator in plant sugar signalling. Plant J 2005, 44:128-138.
36. Bao JS, Corke H, Sun M. Genetic diversity in the physicochemical properties of waxy rice (Oryza sativa L.) starch. J Sci Food Agric 2004, 84:1299-1306.
37. Bao JS, Corke H, Sun M. Analysis of genetic diversity and relationship in Genetic diversity in waxy rice (Oryza sativa L.) using AFLP and ISSR markers. Genet Resour Crop Evol 2006a, 53:323-330.
38. Bao JS, Corke H, Sun M. 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 2006b, 113:1171-1183.
39. Terada R, Nakajima M, Isshiki M, Okagaki RJ, Wessler SR, Shimamoto K. Antisense waxy genes with highly active promoters effectively suppress waxy gene expression in transgenic rice. Plant Cell Physiol 2000, 41:881-888.
40. Nakamura T, Yamamori M, Hirano H, Hidaka S, Nagamine T. Production of waxy (amylose-free) wheats. Mol Gen Genet 1995, 248:253-259.
41. Vrinten PL, Nakamura T. Wheat granule-bound starch synthase I and II are encoded by separate genes that are expressed in different tissues. Plant Physiol 2000, 122:255-264.
42. Hirose T, Terao T. A comprehensive expression analysis of the starch synthase gene family in rice (Oryza sativa L.). Planta 2004, 220:9-16.
43. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. The COG database: an updated version includes eukaryotes. BMC Bioinforma 2003, 4:41.
44. Sun C, Sathish P, Ahlandsberg S, Jansson C. Analyses of isoamylase gene activity in wild-type barley indicate its involvement in starch synthesis. Plant Mol Biol 1999, 40:431-443.
45. Tian Z, Qian Q, Liu Q, Yan M, Liu X, Yan C, Liu G, Gao Z, Tang S, Zeng D, Wang Y, Yu J, Gu M, Li J. Allelic diversities in rice starch biosynthesis lead to a diverse array of rice eating and cooking qualities. Proc Natl Acad Sci USA 2009, 106:21760-21765.
46. Lü B, Guo Z, Liang J. Effects of the activities of key enzymes involved in starch biosynthesis on the fine structure of amylopectin in developing rice (Oryza sativa L.) endosperms. Sci China C Life Sci 2008, 51:863-871.
47. Itoh K, Ozaki H, Okada K, Hori H, Takeda Y, Mitsui T. Introduction of Wx transgene into rice wx mutants leads to both high- and low-amylose rice. Plant Cell Physiol 2003, 44:473-480.
48. Sato Y, Nishio T. Mutation detection in rice waxy mutants by PCR-RF-SSCP. Theor Appl Genet 2003, 107:560-567.
49. Patron NJ, Smith AM, Fahy BF, Hylton CM, Naldrett MJ, Rossnagel BG, Denyer K. The altered pattern of amylose accumulation in the endosperm of low-amylose barley cultivars is attributable to a single mutant allele of granule-bound starch synthase I with a deletion in the 5'-non-coding region. Plant Physiol 2002, 130:190-198.
50. Fujita N, Hasegawa H, Taira T. The isolation and characterization of a waxy mutant of diploid wheat (Triticum monococcum L.). Plant Sci 2001, 160:595-602.
51. Vrinten P, Nakamura T, Yamamori M. Molecular characterization of waxy mutations in wheat. Mol Gene Genet 1999, 261:463-471.
52. Okagaki RJ, Neuffer MG, Wessler SR. A deletion common to two independently derived waxy mutations of maize. Genetics 1991, 128:425-431.
53. Okagaki RJ, Wessler SR. Comparison of non-mutant and mutant waxy genes in rice and maize. Genetics 1988, 120:1137-1143.
54. Lee SK, Hwang SK, Han M, Eom JS, Kang HG, Han Y, Choi SB, Cho MH, Bhoo SH, An G, Hahn TR, Okita TW, Jeon JS. Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 2007, 65:531-546.
55. Kawagoe Y, Kubo A, Satoh H, Takaiwa F, Nakamura Y. Roles of isoamylase and ADP-glucose pyrophosphorylase in starch granule synthesis in rice endosperm. Plant J 2005, 42:164-174.
56. Ball S, Colleoni C, Cenci U, Raj WK, Tirtiaux C. The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J Exp Bot 2011, 62:1775-1801.
57. Zeeman SC, Kossmann J, Smith AM. Starch: its metabolism, evolution, and biotechnological modification in plants. Ann Rev Plant Biol 2010, 61:209-234.
58. Jeon JS, Ryoo N, Hahn TR, Walia H, Nakamura Y. Starch biosynthesis in cereal endosperm. Plant Physiol Biochem 2010, 48:383-392.
59. Hannah LC, James M. The complexities of starch biosynthesis in cereal endosperms. Curr Opin Biotechnol 2008, 19:160-165.
60. Ohdan T, Francisco PB, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y. Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot 2005, 56:3229-3244.
61. Hennen-Bierwagen TA, Lin Q, Grimaud F, Planchot V, Keeling PL, James MG, Myers AM. 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 2009, 149:1541-1559.
62. Angeles-Núñez JG, Tiessen A. Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds. Planta 2010, 232:701-718.
63. Grierson C, Du JS, de Torres Zabala M, Beggs K, Smith C, Holdsworth M, Bevan M. Separate cis sequences and trans factors direct metabolic and developmental regulation of a potato tuber storage protein gene. Plant J 1994, 5:815-826.
64. McCleary BV, Codd R. Measurement of (1→3), (1→4)-β-D-glucan in barley and oats: a streamlined enzymic procedure. J Sci Food Agric 1991, 55:303-312.
65. Sun C, Sathish P, Ahlandsberg S, Jansson C. The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. Plant Physiol 1998, 118:37-49.
66. Theander O, Aman P, Westerlund E, Andersson R, Pettersson D. Total dietary fiber determined as neutral sugar residues, uronic acid residues, and Klason lignin (the Uppsala method): collaborative study. J AOAC Int 1995, 78:1030-1044.
67. Rakha A, Åman P, Andersson R. Characterization of dietary fibre components in rye products. Food Chem 2010, 119:859-867.
68. Santacruz S, Koch K, Andersson R, Åman P. Characterization of potato leaf starch. J Agric Food Chem 2004, 52:1985-1989.
69. Chrastil J. Improved colorimetric determination of amylose in starches or flours. Carbohydr Res 1987, 159:154-158.
70. Bergmeyer HU, Bernt E, Schmidt F, Stork H. Methods of Enzymatic Analysis (Bergmeyer HU, ed.) 1974, 1196-1201. New York and London: Verlag Chemie, Weinheim/Academic Press, Inc, 3.
71. Bernt E, Bergmeyer HU. Methods of Enzymatic Analysis (Bergmeyer HU, ed.) 1974, 1304-1207. New York and London: Verlag Chemie, Weinheim/Academic Press, Inc, 3.
72. Anonymous Determination of crude oils and fat (Method B). Off J Eur Communities 1984, 15:29-30. Anonymous.
73. Mangelsen E, Wanke D, Kilian J, Sundberg E, Harter K, Jansson C. Significance of light, sugar, and amino acid supply for diurnal gene regulation in developing barley caryopses. Plant Physiol 2010, 153:14-33.
74. Jain M, Nijhawan A, Tyagi AK, Khurana JP. Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 2006, 345:646-651.
75. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 1996, 93:6025-6030.
76. Dai ZM, Zhu XJ, Yang WJ. Full-length normalization subtractive hybridization: a novel method for generating differentially expressed cDNAs. Mol Biotechnol 2009, 43:257-263.
77. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual 1989, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
78. Matz M, Shagin D, Bogdanova E, Britanova O, Lukyanov S, Diatchenko L, Chenchik A. Amplification of cDNA ends based on template-switching effect and step-out PCR. Nucleic Acids Res 1999, 27:1558-1560.