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 Reports

Volumn 30, Issue 1, 2011, Pages 113-124

  Hiwasa Tanase, Kyoko ^a   Nyarubona, Mpanja ^a   Hirai, Tadayoshi ^a   Kato, Kazuhisa ^a   Ichikawa, Takanari ^b   Ezura, Hiroshi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

Author keywords

Codon optimization; Miraculin; Miraculin terminator; Read through; Transgenic tomato

Indexed keywords

CAULIFLOWER MOSAIC VIRUS; LYCOPERSICON ESCULENTUM;

EID: 78650754837     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-010-0949-y     Document Type: Article

References (43)

1. Batard Y, Hehn A, Nedelkina S, Schalk M, Pallett K, Schaller H, Werck-Reichhart D (2000) Increasing expression of P450 and P450-reductase proteins from monocots in heterologous systems. Arch Biochem Biophys 379: 161-169. doi: 10. 1006/abbi. 2000. 1867.
2. Chiba Y, Ishikawa M, Kijima F, Tyson RH, Kim J, Yamamoto A, Nambara E, Leustek T, Wallsgrove RM, Naito S (1999) Evidence for autoregulation of cystathionine γ-synthase mRNA stability in Arabidopsis. Science 286: 1371-1374. doi: 10. 1126/science. 286. 5443. 1371.
3. Chincinska IA, Liesche J, Krugel U, Michalska J, Geigenberger P, Grimm B, Khun C (2008) Sucrose transporter StSUT4 from potato affects flowering, tuberization, and shade avoidance response. Plant Physiol 146: 515-528. doi: 10. 1104/pp. 107. 112334.
4. Daniell H, Streatfield SJ, Wycoff K (2001) Medical molecular farming: production of antibodies, biopharmaceuticals and edible vaccines in plants. Trends Plant Sci 6: 219-226. doi: 10. 1016/S1360-1385(01)01922-7.
5. Deblaere R, Bytebier B, De Greve H, Deboeck F, Schell J, van Montagu M, Leemans J (1985) Efficient octopine Ti plasmid derived vectors for Agrobacterium-mediated gene transfer in plants. Nucleic Acids Res 13: 4777-4785.
6. 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.
7. Giddings G, Allison G, Brooks D, Carter A (2000) Transgenic plants as factories for biopharmaceuticals. Nat Biotechnol 18: 1151-1155. doi: 10. 1038/81132.
8. Gilmartin GM (2005) Eukaryotic mRNA 3′ processing: a common means to different ends. Genes Dev 19: 2517-2521. doi: 10. 1101/gad. 1378105.
9. 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.
10. Gutiérrez RA, Maclntosh GC, Green PJ (1999) Current perspectives on mRNA stability in plants: multiple levels and mechanisms of control. Trend Plant Sci 4: 429-438. doi: 10. 1016/S1360-1385(99)01484-3.
11. Hackel A, Schauer N, Carrari F, Fernie AR, Grimm B, Kuhn C (2006) Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant J 45: 180-192. doi: 10. 1111/j. 1365-313X. 2005. 02572. x.
12. Hirai T, Fukukawa G, Kakuta H, Fukuda N, Ezura H (2010) Production of recombinant miraculin using transgenic tomatoes in a closed cultivation system. J Agric Food Chem 58: 6096-6101. doi: 10. 1021/jf100414v.
13. Ingelbrecht ILW, Herman LMF, Dekeyser RA, van Montagu MC, Depicker AG (1989) Different 3′ end regions strongly influence the level of gene expression in plant cells. Plant Cell 1: 671-680. doi: 10. 1105/tpc. 1. 7. 671.
14. Ingelbrecht ILW, Breyne P, Vancompernolle K, Jacobs A, van Montagu MC, Depicker AG (1991) Transcriptional interference in transgenic plants. Gene 109: 239-243. doi: 10. 1016/0378-1119(91)90614-H.
15. Jackson RJ, Standart N (1990) Do the poly (A) tail and 3′ untranslated region control mRNA translation? Cell 62: 15-24. doi: 10. 1016/0092-8674(90)90235-7.
16. Jefferson RK, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907.
17. 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.
18. Kim YW, Kato K, Hirai T, Hiwasa-Tanase K, Ezura H (2010) Spatial and development profiling of miraculin accumulation in transgenic tomato fruits expressing the miraculin gene constitutively. J Agric Food Chem 58: 282-286. doi: 10. 1021/jf9030663.
19. 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.
20. Mason HS, Warzecha H, Mor T, Arntzen CJ (2002) Edible plant vaccines: application for prophylactic and molecular medicine. Trends Mol Med 8: 324-329. doi: 10. 1016/S1471-4914(02)02360-2.
21. Matsuura H, Shinmyo A, Kato K (2008) Preferential translation mediated by Hsp81-3 5′-UTR during heat shock involves ribosome entry at the 5′-end rather than an internal site in Arabidopsis suspention cells. J Biosci Bioeng 105: 39-47.
22. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15: 473-497. doi: 10. 1111/j. 1399-3054. 1962. tb08052. x.
23. Murray EE, Lotzer J, Eberle M (1989) Codon usage in plant genes. Nucleic Acids Res 17: 477-498.
24. 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: 328-332. doi: 10. 1093/pcp/pcp188.
25. 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 Rep 25: 124-132. doi: 10. 1007/s00299-005-0036-y.
26. 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.
27. 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.
28. Rang A, Linke B, Jansen B (2005) Detection of RNA variants transcribed from the transgene in Roundup Ready soybean. Eur Food Res Technol 220: 438-443. doi: 10. 1007/s00217-004-1064-5.
29. Rogers SO, Bendich AJ (1985) Extraction of DNA from milligram amounts of fresh, herbarium and mummified plant tissues. Plant Mol Biol 5: 69-76. doi: 10. 1007/BF00020088.
30. Rothnie HM, Reid J, Hohn T (1994) The contribution of AAUAAA and the upstream element UUUGUA to the efficiency of mRNA 3′-end formation in plants. EMBO J 13: 2200-2210.
31. Rouwendal GJ, Mendes O, Wolbert EJ, de 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.
32. Shen WJ, Forde BG (1989) Efficient transformation of Agrobacterium spp. by high voltage electroporation. Nucleic Acids Res 17: 8385.
33. Sugaya T, Yano M, Sun HJ, Hirai T, Ezura H (2008) Transgenic strawberry expressing a taste-modifying protein, miraculin. Plant Biotechnol 25: 329-333.
34. 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.
35. 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.
36. 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 Biotechnol J 5: 768-777. doi: 10. 1111/j. 1467-7652. 2007. 00283. x.
37. Suzuki A, Shirata Y, Ishida H, Chiba Y, Onouchi H, Naito S (2001) The first exon coding region of cystathionine γ-synthase gene is necessary and sufficient for downregulation of its own mRNA Accumulation in transgenic Arabidopsis thaliana. Plant Cell Physiol 42: 1174-1180.
38. Theerasilp S, Kurihara Y (1988) Complete purification and characterization of the taste-modifying protein, miraculin, from miracle fruit. J Biol Chem 263: 11536-11539.
39. 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.
40. Windels P, Taverniers I, Depicker A, van Bockstaele E, De Loose M (2001) Characterisation of the Roundup Ready soybean insert. Eur Food Res Technol 213: 107-112.
41. 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.
42. 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.
43. Zarudnaya MI, Kolomiets M, Potyahaylo AL, Hovorun DM (2003) Downstream elements of mammalian pre-mRNA polyadenylation signals: primary, secondary and higher-order structures. Nucleic Acids Res 31: 1375-1386.