From miracle fruit to transgenic tomato: Mass production of the taste-modifying protein miraculin in transgenic plants

Plant Cell Reports

Volumn 31, Issue 3, 2012, Pages 513-525

  Hiwasa Tanase, Kyoko ^a   Hirai, Tadayoshi ^a   Kato, Kazuhisa ^a,b   Duhita, Narendra ^a   Ezura, Hiroshi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b IWATE UNIVERSITY   (Japan)

Author keywords

Commercialization; Cultivation; Expression host; Purification; Recombinant miraculin production; Safety assessment; Transgenic tomato

Indexed keywords

GLYCOPROTEIN; MIRACULIN PROTEIN, SYNSEPALUM DULCIFICUM; SWEETENING AGENT;

BIOSYNTHESIS; FOOD INDUSTRY; FOOD SAFETY; FRUIT; GENE EXPRESSION; GENETIC TRANSFORMATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; REVIEW; SYNSEPALUM; TASTE; TOMATO; TRANSGENIC PLANT;

FOOD INDUSTRY; FOOD SAFETY; FRUIT; GENE EXPRESSION; GLYCOPROTEINS; LYCOPERSICON ESCULENTUM; PLANTS, GENETICALLY MODIFIED; SWEETENING AGENTS; SYNSEPALUM; TASTE; TRANSFORMATION, GENETIC;

LYCOPERSICON ESCULENTUM;

EID: 84856961809     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-011-1197-5     Document Type: Review

References (80)

1. Almeida DPF, Huber DJ (1999) Apoplastic pH and inorganic ion levels in tomato fruit: a potential means for regulation of cell wall metabolism during ripening. Physiol Plant 105: 506-512. doi: 10. 1034/j. 1399-3054. 1999. 105316. x.
2. Armah GE, Achel DG, Acquaah RA, Belew M (1999) Purification of miraculin glycoprotein using tandem hydrophobic interaction chromatography. United States Patent #5886155.
3. Bartoszewski G, Niedziela A, Szwacka M, Niemirowicz-Szczytt K (2003) Modification of tomato taste in transgenic plants carrying a thaumatin gene from Thaumatococcus daniellii Benth. Plant Breed 122: 347-351. doi: 10. 1046/j. 1439-0523. 2003. 00864. x.
4. Brouwer JN, van Der Wei H, Francke A, Hemming G (1968) Miraculin, the sweetness inducing protein miracle fruit. Nature 220: 373-374. doi: 10. 1038/220373a0.
5. Daniell H (2006) Production of biopharmaceuticals and vaccines in plants via the chloroplast genome. Biotechnol J. 1: 1071-1079. doi: 10. 1002/biot. 200600145.
6. Deikman J, Fischer RL (1988) Interaction of a DNA binding factor with the 5′-flanking region of an ethylene-responsive fruit ripening gene from tomato. EMBO J 7: 3315-3320.
7. Desai PN, Shrivastava N, Padh H (2010) Production of heterologous proteins in plants: strategies for optimal expression. Biotechnol Adv 28: 427-435. doi: 10. 1016/j. biotechadv. 2010. 01. 005.
8. Doran PM (2006) Foreign protein degradation and instability in plants and plant tissue cultures. Trends Biotechnol 24: 426-432. doi: 10. 1016/j. tibtech. 2006. 06. 012.
9. Duhita N, Hiwasa-Tanase K, Yoshida S, Ezura H (2009) Single-step purification of native miraculin using immobilized metal affinity chromatography. J Agric Food Chem 57: 5148-5151. doi: 10. 1021/jf9004065.
10. Duhita N, Hiwasa-Tanase K, Yoshida S, Ezura H (2011) A simple method for purifying undenatured miraculin from transgenic tomato fruits. Plant Biotechnol 28: 281-286. doi: 10. 5511/plantbiotechnology. 11. 0207a.
11. Fluhr R, Kuhlemeier C, Nagy F, Chua NH (1986) Organ-specific and light-induced expression of plant genes. Science 232: 1106-1112. doi: 10. 1126/science. 232. 4754. 1106.
12. Gilmartin GM (2005) Eukaryotic mRNA 30 processing: a common means to different ends. Genes Dev 19: 2517-2521. doi: 10. 1101/gad. 1378105.
13. Giroux EL, Henkin RI (1974) Purification and some properties of miraculin, a glycoprotein from Synsepalum dulcificum which provokes sweetness and blocks sourness. J Agric Food Chem 22: 594-601. doi: 10. 1021/jf60194a033.
14. Gustafsson C, Govindarajan S, Minshull J (2004) Codon bias and heterologous protein expression. Trends Biotechnol 22: 346-353. doi: 10. 1016/j. tibtech. 2004. 04. 006.
15. Hirai T, Fukukawa G, Kakuta H, Fukuda N, Ezura H (2010a) Production of recombinant miraculin using transgenic tomato in a closed-cultivation system. J Agric Food Chem 58: 6096-6101. doi: 10. 1021/jf100414v.
16. Hirai T, Sato M, Toyooka K, Sun HJ, Yano M, Ezura H (2010b) Miraculin, a taste-modifying protein is secreted into intercellular spaces in plant cells. J Plant Physiol 167: 209-215. doi: 10. 1016/j. jplph. 2009. 08. 001.
17. Hirai T, Kim YW, Kato K, Hiwasa-Tanase K, Ezura H (2011a) Uniform accumulation of recombinant miraculin protein in transgenic tomato fruit using a fruit-ripening-specific E8 promoter. Transgenic Res. doi: 10. 1007/s11248-011-9495-9 (in press).
18. Hirai T, Kurokawa N, Duhita N, Hiwasa-Tanase K, Kato K, Kato K, Ezura H (2011b) The HSP terminator of Arabidopsis thaliana induces extremely high-level accumulation of miraculin protein in transgenic tomato. J Agric Food Chem 59: 9942-9949. doi: 10. 1021/jf202501e.
19. Hirai T, Shohael AM, Kim YW, Yano M, Ezura H (2011c) Ubiquitin promoter-terminator cassette promotes genetically stable expression of the taste-modifying protein miraculin in transgenic lettuce. Plant Cell Rep. doi: 10. 1007/s00299-011-1131-x (in press).
20. Hiwasa-Tanase K, Nyarubona M, Hirai T, Kato K, Ichikawa T, Ezura H (2011) High-level accumulation of recombinant miraculin protein in transgenic tomatoes expressing a synthetic miraculin gene with optimized codon usage terminated by the native miraculin terminator. Plant Cell Rep 30: 113-124. doi: 10. 1007/s00299-010-0949-y.
21. Hobbs SLA, Kpodar P, DeLong CMO (1990) The effect of T-DNA copy number, position and methylation on reporter gene expression in tobacco transformants. Plant Mol Biol 15: 851-864. doi: 10. 1007/BF00039425.
22. Igeta H, Tamura Y, Nakaya K, Nakamura Y, Kurihara Y (1991) Determination of disulfide array and subunit structure of taste-modifying protein, miraculin. Biochim Biophys Acta 1079: 303-307. doi: 10. 1016/0167-4838(91)90073-9.
23. Ingelbrecht ILW, Herman LMF, Dekeyser RA, van Montagu MC, Depicker AG (1989) Different 30 end regions strongly influence the level of gene expression in plant cells. Plant Cell 1: 671-680.
24. Ito K, Asakura T, Morita Y, Nakajima K, Koizumi A, Shimizu-Ibuka A, Masuda K, Ishiguro M, Terada T, Maruyama J, Kitamoto K, Misaka T, Abe K (2007) Microbial production of sensory-active miraculin. Biochem Biophys Res Commun 360: 407-411. doi: 10. 1016/j. bbrc. 2007. 06. 064.
25. Ito K, Sugawara T, Koizumi A, Nakajima K, Shimizu-Ibuka A, Shiroishi M, Asada H, Yurugi-Kobayashi T, Shimamura T, Asakura T, Masuda K, Ishiguro M, Misaka T, Iwata S, Kobayashi T, Abe K (2010) Bulky high-mannose-type N-glycan blocks the taste-modifying activity of miraculin. Biochim Biophys Acta 1800: 986-992. doi: 10. 1016/j. bbagen. 2010. 06. 003.
26. Jorgensen RA, Cluste PD, English J, Que Q, Napoli C (1996) Chalcone synthase cosuppression phenotypes in petunia flowers: comparison of sense vs. antisense constructs and single copy vs. complex T-DNA sequences. Plant Mol Biol 31: 957-973. doi: 10. 1007/BF00040715.
27. Kant R (2005) Sweet proteins-potential replacement for artificial low calorie sweeteners. Nutr J 4: 5. doi: 10. 1186/1475-2891-4-5.
28. Kato K, Yoshida R, Kikuzaki A, Hirai T, Kuroda H, Hiwasa-Tanase K, Takane K, Ezura H, Mizoguchi T (2010) Molecular breeding of tomato lines for mass production of miraculin in a plant factory. J Agric Food Chem 58: 9505-9510. doi: 10. 1021/jf101874b.
29. Kato K, Maruyama S, Hirai T, Hiwasa-Tanase K, Mizoguchi T, Goto E, Ezura H (2011) A trial of production of the plant-derived high-value recombinant protein in a plant factory: photosynthetic photon fluxes affect the accumulation of recombinant miraculin in transgenic tomato fruits. Plant Signal Behav 8: 1172-1179. doi: 10. 4161/psb. 6. 8. 16373.
30. Kaulen H, Schell J, Kreuzaler F (1986) Light-induced expression of the chimeric chalcone synthase-NPTII gene in tobacco cells. EMBO J 5: 1-8.
31. Kawabe A, Miyashita NT (2003) Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet Syst 78: 343-352. doi: 10. 1266/ggs. 78. 343.
32. Kim YW, Hirai T, Kato K, Hiwasa-Tanase K, Ezura H (2010a) Gene dosage and genetic background affect miraculin accumulation in transgenic tomato fruits. Plant Biotechnol 27: 333-338. doi: 10. 5511/plantbiotechnology. 27. 333.
33. Kim YW, Kato K, Hirai T, Hiwasa-Tanase K, Ezura H (2010b) Spatial and developmental profiling of miraculin accumulation in transgenic tomato fruits expressing the miraculin gene constitutively. J Agric Food Chem 58: 282-286. doi: 10. 1021/jf9030663.
34. Koizumi A, Tsuchiya A, Nakajima K, Ito K, Terada T, Shimizu-Ibuka A, Briand L, Asakura T, Misaka T, Abe K (2011) Human sweet taste receptor mediates acid-induced sweetness of miraculin. Proc Natl Acad Sci USA. doi: 10. 1073/pnas. 1016644108 (in press).
35. Kurihara Y (1994) Thaumatin. In: Witty M, Higginbotham JD (eds) Sweet proteins in general. CRC Press, Boca Raton, pp 1-18.
36. Kurihara K, Beidler LM (1968) Taste-modifying protein from miracle fruit. Science 161: 1241-1243. doi: 10. 1126/science. 161. 3847. 1241.
37. Kurihara K, Beidler LM (1969) Mechanism of the action of taste-modifying protein. Nature 222: 1176-1178. doi: 10. 1038/2221176a0.
38. Kurihara Y, Nirasawa S (1997) Structures and activities of sweetness-inducing substances (miraculin, curculin, strogin) and the heat-stable sweet protein, mabinlin. FFI J Jpn 174: 67-74.
39. Kusano M, Redestig H, Hirai T, Oikawa A, Matsuda F, Fukushima A, Arita M, Watanabe S, Yano M, Hiwasa-Tanase K, Ezura H, Saito K (2011) Covering the chemical diversity of genetically modified tomato using multi-platform metabolomics for an objective substantial equivalence assessment. PLoS ONE 6: e16989. doi: 10. 1371/journal. pone. 0016989.
40. Lamphear BJ, Barker DK, Brooks CA, Delaney DE, Lane JR, Beifuss K, Love R, Thompson K, Mayor J, Clough R, Harkey R, Poage M, Drees C, Horn ME, Streatfield SJ, Nikolov Z, Woodard SL, Hood EE, Jilka JM, Howard JA (2005) Expression of the sweet protein brazzein in maize for production of a new commercial sweetener. Plant Biotechnol J 3: 103-114. doi: 10. 1111/j. 1467-7652. 2004. 00105. x.
41. Lebedev VG, Taran SA, Shmatchenko VV, Dolgov SV (2002) Pear transformation with the gene for super-sweet protein thaumatin II. Acta Hortic 596: 199-202.
42. Leelavathi S, Reddy VS (2003) Cloroplast expression of His-tagged GUS-fusions: a general strategy to overproduce and purify foreign proteins using transplastomic plants as bioreactors. Mol Breed 11: 49-58. doi: 10. 1023/A: 1022114427971.
43. Lin HH, Huang LF, Su HC, Jeng ST (2009) Effect of the multiple polyadenylation signal AAUAAA on mRNA 3′-end formation and gene expression. Planta 230: 699-712. doi: 10. 1007/s00425-009-0977-4.
44. Lincoln JE, Fischer RL (1988a) Diverse mechanisms for the regulation of ethylene-inducible gene expression. Mol Gen Genet 212: 71-75. doi: 10. 1007/BF00322446.
45. Lincoln JE, Fischer RL (1988b) Regulation of gene expression by ethylene in wild-type and rin tomato (Lycopersicon esculentum) fruit. Plant Physiol 88: 370-374.
46. Liu Q, Xue Q (2005) Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species. J Genet 84: 55-62. doi: 10. 1007/BF02715890.
47. Maliga P (2003) Progress towards commercialization of plastid transformation technology. Trends Biotechnol 121: 20-28. doi: 10. 1016/S0167-7799(02)00007-0.
48. Masuda T, Kitabatake N (2006) Developments in biotechnological production of sweet proteins. J Biosci Bioeng 102: 375-389. doi: 10. 1263/jbb. 102. 375.
49. Masuda Y, Nirasawa S, Nakaya K, Kurihara Y (1995) Cloning and sequencing of a cDNA encoding a taste-modifying protein, miraculin. Gene 161: 175-177. doi: 10. 1016/0378-1119(95)00198-F.
50. Matsui T, Takita E, Sato T, Aizawa M, Ki M, Kadoyama Y, Hirano K, Kinjo S, Asao H, Kawamoto K, Kariya H, Makino S, Hamabata T, Sawada K, Kato K (2011) Production of double repeated B subunit of Shiga toxin 2e at high levels in transgenic lettuce plants as vaccine material for porcine edema disease. Transgenic Res 20: 735-748. doi: 10. 1007/s11248-010-9455-9.
51. Matsuyama T, Satoh M, Nakata R, Aoyama T, Inoue H (2009) Functional expression of miraculin, a taste-modifying protein in Escherichia coli. J Biochem 145: 445-450. doi: 10. 1093/jb/mvn184.
52. Meyer P (1996) Repeat-induced gene silencing: common mechanisms in plants and fungi. Biol Chem Hoppe Seyler 377: 87-95.
53. Meyers B, Zaltsman A, Lacroix B, Kozlovsky SV, Krichevsky A (2010) Nuclear and plastid genetic engineering of plants: comparison of opportunities and challenges. Biotechnol Adv 28: 747-756. doi: 10. 1016/j. biotechadv. 2010. 05. 022.
54. Morimoto T, Torii T, Hashimoto Y (1995) Optimal control of physiological processes of plants in a green plant factory. Control Eng Pract 3: 505-511. doi: 10. 1016/0967-0661(95)00022-M.
55. Murray EE, Lotzer J, Eberle M (1989) Codon usage in plant genes. Nucleic Acids Res 17: 477-498.
56. Nagaya S, Kawamura K, Shinmyo A, Kato K (2010) The HSP terminator of Arabidopsis thaliana increases gene expression in plant cells. Plant Cell Physiol 51: 328-532. doi: 10. 1093/pcp/pcp188.
57. Paladino A, Costantini S, Colonna G, Facchiano AM (2008) Molecular modeling of miraculin: structural analysis and functional hypothesis. Biochem Biophys Res Commun 367: 26-32. doi: 10. 1016/j. bbrc. 2007. 12. 102.
58. Paladino A, Colonna G, Facchiano AM, Constantini S (2010) Functional hypothesis on miraculin' sweetness by a molecular dynamics approach. Biochem Biophys Res Commun 396: 726-730. doi: 10. 1016/j. bbrc. 2010. 05. 002.
59. Peñarrubia L, Kim R, Giovannoni J, Kim SH, Fischer RL (1992) Production of the sweet protein monellin in transgenic plants. Nat Biotechnol 10: 561-564. doi: 10. 1038/nbt0592-561.
60. Peng RH, Yao QH, Xiong AS, Cheng ZM, Li Y (2006) Codon-modifications and an endoplasmic reticulum-targeting sequence additively enhance expression of an Aspergillus phytase gene in transgenic canola. Plant Cell Res 25: 124-132. doi: 10. 1007/s00299-005-0036-y.
61. Perlak FJ, Fuchs RL, Dean DA, McPherson SL, Fischhoff DA (1991) Modification of the coding sequence enhances plant expression of insect control protein genes. Proc Natl Acad Sci USA 88: 3324-3328.
62. Proudfoot N (2004) New perspectives on connecting messenger RNA 3′ end formation to transcription. Curr Opin Cell Biol 16: 272-278. doi: 10. 1016/j. ceb. 2004. 03. 007.
63. Rouwendal GJ, Mendes O, Wolbert EJH, Boer AD (1997) Enhanced expression in tobacco of the gene encoding green fluorescent protein by modification of its codon usage. Plant Mol Biol 33: 989-999. doi: 10. 1023/A: 1005740823703.
64. Schestibratov KA, Dolgov SV (2005) Transgenic strawberry plants expressing a thaumatin II gene from demonstrate enhanced resistance to Botrytis cinerea. Sci Hortic 106: 177-189. doi: 10. 1016/j. scienta. 2005. 03. 016.
65. Shimizu-Ibuka A, Morita Y, Terada T, Asakura T, Nakajima K, Iwata S, Misaka T, Sorimachi H, Arai S, Abe K (2006) Crystal structure of neoculin: insights into its sweetness and taste-modifying activity. J Mol Biol 359: 148-158. doi: 10. 1016/j. jmb. 2006. 03. 030.
66. Staub JM, Garcia B, Graves J, Hajdukiewicz PT, Hunter P, Nehra N, Paradkar V, Schlittler M, Carroll JA, Spatola L, Ward D, Ye G, Russell DA (2000) High-yield production of a human therapeutic protein in tobacco chloroplasts. Nat Biotechnol 18: 333-338. doi: 10. 1038/73796.
67. Stougaard J, Sandal NN, Gron A, Kuhle A, Marcker KA (1987) 5′ Analysis of the soybean leghaemoglobin lbc3 gene: regulatory elements required for promoter activity and organ specificity. EMBO J 6: 3565-3569.
68. Sugaya T, Yano M, Sun HJ, Hirai T, Ezura H (2008) Transgenic strawberry expressing a taste-modifying protein, miraculin. Plant Biotechnol 25: 329-333. doi: 10. 5511/plantbiotechnology. 25. 329.
69. Sun HJ, Cui ML, Ma B, Ezura H (2006a) Functional expression of the taste-modifying protein, miraculin, in transgenic lettuce. FEBS Lett 580: 620-626. doi: 10. 1016/j. febslet. 2005. 12. 080.
70. Sun HJ, Uchii S, Watanabe S, Ezura H (2006b) A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics. Plant Cell Physiol 47: 426-431. doi: 10. 1093/pcp/pci251.
71. Sun HJ, Kataoka H, Yano M, Ezura H (2007) Genetically stable expression of functional miraculin, a new type of alternative sweetener, in transgenic tomato plants. Plant Biotech J 5: 768-777. doi: 10. 1111/j. 1467-7652. 2007. 00283. x.
72. Szwacka M, Kryzymowska M, Osuch A, Kowalczyk ME, Malepszy S (2002) Variable properties of transgenic cucumber plants containing the thaumatin II gene from Thaumatococcus daniellii. Acta Physiol Plant 24: 173-185. doi: 10. 1007/s11738-002-0009-5.
73. Takagi K, Teshima R, Okunuki H, Sawada J (2003) Comparative study of in vitro digestibility of food proteins and effect of preheating on the digestion. Biol Pharm Bull 26: 969-973.
74. Theerasilp S, Kurihara Y (1988) Complete purification and characterization of the taste-modifying protein, miraculin, from miracle fruit. J Biol Chem 263: 11536-11539.
75. Theerasilp S, Hitotsuya H, Nakajo S, Nakaya K, Nakamura Y, Kurihara Y (1989) Complete amino acid sequence and structure characterization of the taste-modifying protein, miraculin. J Biol Chem 264: 6655-6659.
76. Twyman RM, Stoger E, Schillberg S, Christou P, Fischer R (2003) Molecular farming in plants: host systems and expression technology. Trends Biotechnol 21: 570-578. doi: 10. 1016/j. tibtech. 2003. 10. 002.
77. Williamson JD, Hirsch-Wyncott ME, Larkins BA, Gelvin SB (1989) Differential accumulation of a transcript driven by the CaMV 35S promoter in transgenic tobacco. Plant Physiol 90: 1570-1576. doi: 10. 1104/pp90. 4. 1570.
78. Witty M (1990) Preprothaumatin II is processed to biological activity in Solanum tuberosum. Biotechnol Lett 12: 131-136. doi: 10. 1007/BF01022429.
79. Xue GP, Patel M, Johnson JS, Smyth DJ, Vickers CE (2003) Selectable marker-free transgenic barley producing a high level of cellulose (1, 4-β-glucanase) in developing grains. Plant Cell Rep 21: 1088-1094. doi: 10. 1007/s00299-003-0627-4.
80. Yano M, Hirai T, Kato K, Hiwasa-Tanase K, Fukuda N, Ezura H (2010) Tomato is a suitable material for producing recombinant miraculin protein in genetically stable manner. Plant Sci 178: 469-473. doi: 10. 1016/j. plantsci. 2010. 02. 016.