Changes in protein expression profiles between a low phytic acid rice (Oryza sativa L. Ssp. japonica) line and its parental line: A proteomic and bioinformatic approach

Journal of Agricultural and Food Chemistry

Volumn 58, Issue 11, 2010, Pages 6912-6922

  Emami, Kaveh ^a   Morris, Nicholas J ^b   Cockell, Simon J ^c   Golebiowska, Gabriela ^d   Shu, Qing Yao ^e   Gatehouse, Angharad M R ^a  

^a Institute for Research on Environment and Sustainability   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c THE FRANCISZEK GÓRSKI INSTITUTE OF PLANT PHYSIOLOGY   (Poland)

^d ZHEJIANG UNIVERSITY   (China)

^e Devonshire Building   (United Kingdom)

Author keywords

2 DE; Bioinformatics; MALDI; Mutagenesis; Myo inositol metabolism; Novel food; Oryza sativa; Phytic acid; Proteomics; SELDI; Unintended effects

Indexed keywords

PHYTIC ACID; VEGETABLE PROTEIN;

ARTICLE; BIOLOGY; CHEMISTRY; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; MASS SPECTROMETRY; METABOLISM; PROTEOMICS; RICE; TWO DIMENSIONAL GEL ELECTROPHORESIS;

COMPUTATIONAL BIOLOGY; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, PLANT; MASS SPECTROMETRY; ORYZA SATIVA; PHYTIC ACID; PLANT PROTEINS; PROTEOMICS;

JAPONICA; ORYZA SATIVA;

EID: 77953154379     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf904082b     Document Type: Article

References (72)

1. Raboy, V. Accumulation and storage of phosphate and minerals. In Cellular and Molecular Biology of Plant Seed Development; Larkins, B. A., Vasil, I. K., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1997; pp 441-447.
2. Liu, Z.; Cheng, F.; Zhang, G. Grain phytic acid content in japonica rice as affected by cultivar and environment and its relation to protein content Food Chem. 2005, 89, 49-52
3. Raboy, V. The ABCs of low-phytate crops Nat. Biotechnol. 2007, 25, 874-875
4. Saha, P. R.; Weaver, C. M.; Mason, A. C. Mineral bioavailability in rats from intrinsically labeled whole wheat flour of various phytate levels J. Agric. Food Chem. 1994, 42, 2531-2535
5. Gillooly, M.; Bothwell, T. H.; Torrance, J. D.; MacPhail, A. P.; Derman, D. P.; Bezwoda, W. R.; Mills, W.; Charlton, R. W.; Mayet, F. The effects of organic acids, phytates and polyphenols on the absorption of iron from vegetables Br. J. Nutr. 1983, 49, 331-342
6. Welch, R. M. Biotechnlogy, biofortfication, and global health Food Nutr. Bull. 2005, 26, 419-21
7. Jin, F.; Frohman, C.; Thannhauser, T. W.; Welch, R. M.; Glahn, R. P. Effects of ascorbic acid, phytic acid and tannic acid on iron bioavailability from reconstituted ferritin measured by an in vitro digestion-Caco-2 cell model Br. J. Nutr. 2009, 101, 972-981
8. Adams, C. L.; Hambidge, M.; Raboy, V.; Dorsch, J. A.; Lei, S.; Westcott, J. L.; Krebs, N. F. Zinc absorption from a low phytic acid maize Am. J. Clin. Nutr. 2002, 76, 1-4
9. Welch, R. M.; Graham, R. D. Breeding for micronutrients in staple food crops from a human nutrition perspective J. Exp. Bot. 2003, 55, 353-364
10. Sandberg, A. S.; Andersson, H.; Carlsson, N. G.; Sandstroem, B. Degradation products of bran phytate formed during digestion in the human small intestine: effect of extrusion cooking on digestibility J. Nutr. 1987, 117, 2061-2065
11. Larson, S. R.; Young, K. A.; Cook, A.; Blake, T. K.; Raboy, V. Linkage mapping of two mutations that reduce phytic acid content of barley grain Theor. Appl. Genet. 1998, 97, 141-146
12. Raboy, V.; Gerbasi, P. F.; Young, K. A.; Stoneberg, S. D.; Pickett, S. G.; Bauman, A. T.; Murthy, P. P. N.; Sheridan, W. F.; Ertl, D. S. Origin and seed phenotype of maize low phytic acid 1-1 and low phytic acid 2-1 Plant Physiol. 2000, 124, 355-368
13. Wilcox, J. R. Isolation of high seed inorganic P, low-phytate soybean mutants Crop Sci. 2000, 40, 1601-1605
14. Larson, S. R.; Rutger, J. N.; Young, K. A.; Raboy, V. Isolation and genetic mapping of a non-lethal rice (Oryza sativa L.) low phytic acid 1 mutation Crop Sci. 2000, 40, 1397-1405
15. Liu, Q. L.; Xu, X. H.; Ren, X. L.; Fu, H. W.; Wu, D. X.; Shu, Q. Y. Generation and characterization of low phytic acid germplasm in rice (Oryza sativa L.) Theor. Appl. Genet. 2007, 114, 803-814
16. Cellini, F.; Chesson, A.; Colquhoun, I.; Constable, A.; Davies, H. V.; Engel, K. H.; Gatehouse, A. M. R.; Kärenlampi, S.; Kok, E. J.; Leguay, J. J.; Lehesranta, S.; Noteborn, H. P. J.; Pedersen, M. J.; Smith, M. Unintended effects and their detection in genetically modified crops Food Chem. Toxicol. 2004, 42, 1089-1125
17. Ruebelt, M. C.; Leimgruber, N. K.; Lipp, M.; Reynolds, T. L.; Nemeth, M. A.; Astwood, J. D.; Engel, K. H.; Jany, K. D. Application of two-dimensional gel electrophoresis to interrogate alterations in the proteome of genetically modified crops. 1. Assessing analytical validation J. Agric. Food Chem. 2006, 54, 2154-2161
18. Ruebelt, M. C.; Lipp, M.; Reynolds, T. L.; Astwood, J. D.; Engel, K. L.; Jany, K. D. Application of two-dimensional gel electrophoresis to interrogate alterations in the proteome of genetically modified crops. 2. Assessing natural variability J. Agric. Food Chem. 2006, 54, 2162-2168
19. Ruebelt, M. C.; Lipp, M.; Reynolds, T. L.; Schmuke, J. J.; Astwood, J. D.; DellaPenna, D.; Engel, K. H.; Jany, K. D. Application of two-dimensional gel electrophoresis to interrogate alterations in the proteome of genetically modified crops. 3. Assessing unintended effects J. Agric. Food Chem. 2006, 54, 2169-77
20. Bowen, D. E.; Souza, E. J.; Guttieri, M. J.; Raboy, V.; Fu, J. A low phytic acid barley mutation alters seed gene expression Crop Sci. 2007, 47, S-149-S-159
21. Frank, T.; Meuleye, B. S.; Miller, A.; Shu, Q. Y.; Engel, K. H. Metabolite profiling of two low phytic acid (lpa) rice mutants J. Agric. Food Chem. 2007, 55, 11011-11019
22. Chen, P. S.; Toribara, T. Y.; Warner, H. Microdetermination of phosphorus Anal. Chem. 1956, 28, 1756-1758
23. Zang, X.; Komatsu, S. A proteomics approach for identifying osmotic-stress-related proteins in rice Phytochemistry 2007, 68, 426-437
24. Hashimoto, M.; Komatsu, S. Proteomic analysis of rice seedlings during cold stress Proteomics 2007, 7, 1293-1302
25. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteinâ dye binding Anal. Biochem. 1976, 72, 248-254
26. Khan, S.; Situ, G.; Decker, K.; Schmidt, C. GoFigure: Automated Gene Ontology annotation Bioinformatics 2003, 19, 2484-2485
27. Mao, X.; Cai, T.; Olyarchuk, J. G.; Wei, L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary Bioinformatics 2005, 21, 3787-3793
28. Shannon, P. Cytoscape: a softward environment for integrated models of biomolecular interaction networks Genome Res. 2003, 13, 2498-2504
29. Maere, S.; Heymans, K.; Kuiper, M. BiNGO: a Cytoscape plugin to assess over representation of gene ontology categories in biological networks Bioinformatics 2005, 21, 3448-3449
30. Badri, M. A.; Rivard, D.; Coenen, K.; Vaillancourt, L. P.; Goulet, C.; Michaud, D. A SELDI-TOF MS procedure for the detection, quantitation, and preliminary characterization of low-molecular-weight recombinant proteins expressed in transgenic plants Proteomics 2009, 2, 233-241
31. Komatsu, S. Rice proteome database: a step toward functional analysis of the rice genome Plant Mol. Biol. 2005, 59, 179-190
32. Breiteneder, H.; Radauer, C. A classification of plant food allergens J. Allergy Clin. Immunol. 2004, 113, 821-830
33. Breiteneder, H.; Mills, C. E. N. Plant food allergens-structural and functional aspects of allergenicity Biotechnol. Adv. 2005, 23, 395-399
34. Van Putten, M. C.; Frewer, L. J.; Gilissen, L. J. W. J.; Gremmen, B.; Peijnenburg, A. C. M.; Wicherse, H. J. Novel foods and food allergies: a review of the issues Trends Food Sci. Technol. 2006, 7, 289-299
35. Hammond, B.; Cockburn, A. The safety assessment of proteins introduced into crops developed through agricultural biotechnology: a consolidated approach to meet current and future needs. In Food Safety of Proteins in Agricultural Biotechnology; Hammond, B. G., Ed.; CRC Press: Bacon Raton, FL, 2008; Vol. 172, pp 259-288.
36. Kerim, T.; Imin, N.; Weinman, J. J.; Rolfe, B. G. Proteome analysis of male gametophyte development in rice anthers Proteomics 2003b, 3, 738-751
37. Weiss, W.; Vogelmeier, C.; Gorg, A. Electrophoretic characterization of wheat grain allergens from different cultivars involved in bakersâ asthma Electrophoresis 1993, 14, 805-816
38. Matsuda, T.; Nomura, R.; Sugiyama, M.; Nakamura, R. Immunochemical studies on rice allergenic proteins Agric. Biol. Chem. 1991, 55, 509-513
39. Izumi, H.; Adachi, T.; Fujii, N.; Matsuda, T.; Nakamura, R.; Tanaka, K.; Urisu, A.; Kurosawa, Y. Nucleotide sequence of a cDNA clone encoding a major allergenic protein in rice seeds. Homology of the deduced amino acid sequence with members of 7alpha;-amylase/trypsin inhibitor family FEBS Lett. 1992, 302, 213-216
40. Sander, I.; Flagge, A.; Merget, R.; Halder, T. M.; Meyer, H. E.; Baur, X. Identification of wheat flour allergens by means of 2-dimensional immunoblotting J. Allergy Clin. Immunol. 2001, 107, 907-913
41. Usui, Y.; Nakase, M.; Hotta, H.; Urisu, A.; Aoki, N.; Kitajima, K.; Matsuda, T. A 33-kDa allergen from rice (Oryza sativa L. japonica) J. Biol. Chem. 2001, 276, 11376-11381
42. Mannervik, B.; Ridderström, M. Catalytic and molecular properties of glyoxalase I Biochem. Soc. Trans. 1993, 21, 515-517
43. Frank, T.; Habernegg, R.; Yuan, F.-J.; Shu, Q.-Y.; Engel, K.-H. Assessment of the contents of phytic acid and divalent cations in lowphytic acid (lpa) mutants of rice and soybean J. Food Compos. Anal. 2009, 22, 278-284
44. Mills, E. N. C.; Jenkins, J. A.; Alcocer, M. J. C.; Shewry, P. R. Structural, biological, and evolutionary relationships of plant food allergens sensitizing via the gastrointestinal tract Crit. Rev. Food Sci. Nutr. 2004, 44 (5) 379-407
45. Ogawa, T.; Bando, N.; Tsuji, H.; Okajima, H.; Nishikawa, K.; Sasaoka, K. Investigation of the IgE-binding proteins in soybeans by immunoblotting with the sera of the soybean-sensitive patients with atopic dermatitis J. Nutr. Sci. Vitaminol. 1991, 37, 555-565
46. Rajendran, S.; Prakash, V. Kinetics and thermodynamics of the mechanism of interaction of sodium phytate with α-globulin Biochemistry 1993, 32 (13) 3474-3478
47. Franken, J.; Stephan, U.; Meyer, H. E.; Konig, W. Identification of α-amylase inhibitor as a major allergen of wheat flour Int. Arch. Allergy Immun. 1994, 104, 171-174
48. Soeria-Atmadja, D.; Lundell, T.; Gustafsson, M. G.; Hammerling, U. Computational detection of allergenic proteins attains a new level of accuracy with in silico variable-length peptide extraction and machine learning Nucleic Acids Res. 2006, 34, 3779-3793
49. Henikoff, S.; Henikoff, J. G. Protein family classification based on searching a database of blocks Genomics 1994, 19, 97-107
50. Verni, F.; Gandhi, R.; Goldberg, M. L.; Gatti, M. Genetic and molecular analysis of wings apart-like (wapl), a gene controlling heterochromatin organization in Drosophila melanogaster Genetics 2000, 154, 1693-1710
51. Raboy, V. The ABCs of low-phytate crops Nat. Biotechnol. 2007, 25, 874-875
52. Shi, J.; Wang, H.; Hazebroek, J.; Ertl, D. S.; Harp, T. The maize low-phytic acid 3 encodes a myo -inositol kinase that plays a role in phytic acid biosynthesis in developing seeds Plant J. 2005, 42, 708-719
53. Brearley, C. A.; Hanke, D. E. Metabolic evidence for the order of addition of individual phosphate esters to the myo -inositol moiety of inositol hexakisphosphate in the duckweed Spirodela polyrhiza L Biochem. J. 1996, 314, 227-233
54. Yoshida, K. T.; Wada, T.; Koyama, H.; Mizobuchi-Fukuoka, R.; Naito, S. Temporal and spatial patterns of accumulation of the transcript of myo -inositol-1-phosphate synthase and phytin-containing particles during seed development in rice Plant Physiol. 1999, 119, 65-72
55. Kim, I.; Andaya, C. B.; Newman, W.; Goyal, S. S.; Tai, T. H. Isolation and characterization of a low phytic acid rice mutant reveals a mutation in the rice orthologue of maize MIK Theor. Appl. Genet. 2008, 117, 1291-1301
56. Frank, T.; Habernegg, R.; Yuan, F. J.; Shu, Q. Y.; Engel, K. H. Assessment of the contents of phytic acid and divalent cations in lowphytic acid (lpa) mutants of rice and soybean J. Food Compos. Anal. 2009, 22, 278-284
57. Hazebroek, J.; Harp, T.; Shi, J.; Wang, H. Metabolomic analysis of low phytic acid maize kernels. In Concepts in Plant Metabolomics; Nikolau, B. J.; Wurtele, E. S., Eds.; Springer: Berlin, Germany, 2007; pp 221-238.
58. Raboy, V.; Young, K. A.; Dorsch, J. A.; Cook, A. Genetics and breeding of seed phosphorus and phytic acid J. Plant Physiol. 2001, 158, 489-497
59. Karner, U.; Peterbauer, T.; Raboy, V.; Jones, D. A.; Hedley, C. F.; Richter, A. Myo-inositol and sucrose concentrations affect the accumulation of raffinose family oligosaccharides in seeds J. Exp. Bot. 2004, 55, 1981-1987
60. Hitz, W. D.; Thomas, J. C.; Kerr, P. S.; Sebastian, S. A. Biochemical and molecular characterization of a mutation that confers a decreased raffinosccharide and phytic acid phenotype on soybean seeds Plant Physiol. 2002, 128, 650-660
61. Batista, R.; Saibo, N.; Lourenco, T.; Oliveira, M. M. Microarray analyses reveal that plant mutagenesis may induce more transcriptomic changes than transgene insertion Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 3640-3645
62. Till, B. J.; Cooper, J.; Tai, T. H.; Colowit, P.; Greene, E. A.; Henikoff, S.; Comai, L. Discovery of chemically induced mutations in rice by tilling BMC Plant Biol. 2007, 7, 19 (http://www.biomedcentral.com/1471-2229/7/ 19).
63. Fu, H. W.; Wang, C. X.; Shu, X. L.; Wu, D. X.; Shu, Q. Y. Microsatellite analysis for revealing parentage of gamma ray-induced mutants in rice (Oryza sativa L.) Isr. J. Plant Sci. 2007, 55, 201-206
64. Ahn, D. J.; Won, J. G.; Rico, C. M.; Lee, S. C. Influence of variety, location, growing year, and storage on the total phosphorus, phytate-phosphorus, and phytate-phosphorus to total phosphorus ratio in rice J. Agric. Food Chem. 2010, 58, 3008-3011
65. Yamasaki, T.; Deguchi, M.; Fujimoto, T.; Masumura, T.; Uno, T.; Kanamaru, K.; Yamagata, H. Rice bifunctional α-amylase/subtilisin inhibitor: cloning and characterization of the recombinant inhibitor expressed in Escherichia coli Biosci., Biotechnol., Biochem. 2006, 70, 1200-1209
66. Hoppe, S.; Steinhart, H.; Paschke, A. Identification of a 28 kDa lychee allergen as a triose-phosphate isomerase Food Agric. Immunol. 2006, 17, 9-19
67. Gatehouse, J. A. Plant resistance towards insect herbivores: a dynamic interaction New Phytol. 2002, 156, 145-169
68. Frickel, E. M.; Jemth, P.; Widersten, M.; Mannervik, B. Yeast glyoxalase I is a monomeric enzyme with two active sites J. Biol. Chem. 2001, 276, 1845-1849
69. Shewry, P. R.; Napier, J. A.; Tatham, A. S. Seed storage proteins: structures and Biosynthesis Plant Cell 1995, 7, 945-956
70. Ito, H.; Iwabuchi, M.; Ogawa, K. The sugar-metabolic enzymes aldolase and triose-phosphate isomerase are targets of glutathionylation in Arabidopsis thaliana: detection using biotinylated glutathione Plant Cell Physiol. 2003, 44, 655-660
71. Ohtsubo, K.; Richardson, M. The amino acid sequence of a 20 kDa bifunctional subtilisin/α-amylase inhibitor from bran of rice (Oryza sativa L.) seeds FEBS Lett. 1992, 309, 68-72
72. Migaud, M. E.; Frost, J. W. Elaboration of a general strategy for inhibition of myo -inositol 1-phosphate synthase: active site interactions of analogues possessing oxidized reaction centers J. Am. Chem. Soc. 1996, 118, 495-501