Accumulation of sweet protein monellin is regulated by the psbA 5′UTR in tobacco chloroplasts

Journal of Plant Biology

Volumn 49, Issue 1, 2006, Pages 34-43

  Kyung, Hee Roh ^a   Shin, Kong Sik ^a   Lee, Yeon Hee ^a   Seo, Seok Cheol ^a   Park, Hyo Guen ^b   Daniell, Henry ^c   Lee, Seung Bum ^a  

^a National Institute of Animal Science   (South Korea)

^b Seoul National University   (South Korea)

^c UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

Chloroplast transformation; Endonucleolytic activation; Monellin; psbA 5 UTR; Sweet protein; Translation efficiency

Indexed keywords

NICOTIANA TABACUM;

EID: 33645470553     PISSN: 12269239     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF03030786     Document Type: Article

References (60)

1. Adams CC, Stern DB (1990) Control of mRNA stability in chloroplasts by 3′ inverted repeats: Effects of stem and loop mutations on degradation of psbA mRNA in vitro. Nucl Acids Res 18: 6003-6010
2. Agrawal GK, Kato H, Asayama M, Shirai M (2001) An AU-box motif upstream of the SD sequence of light-dependent psbA transcripts confers mRNA instability in darkness in cyanobacteria. Nucl Acids Res 29: 1835-1843
3. Alexander C, Faber N, Klaff P (1998) Characterization of protein-binding to the spinach chloroplast psbA mRNA 5′ untranslated region. Nucl Acids Res 26: 2265-2272
4. Arai Y, Shikanai T, Doi Y, Yoshida S, Yamaguchi I, Nakashita H (2004) Production of polyhydroxybutyrate by polycistronic expression of bacterial genes in tobacco plastid. Plant Cell Physiol 45: 1176-1184
5. Baginsky S, Gruissem W (2002) Endonucleolytic activation directs dark-induced chloroplast mRNA degradation. Nucl Acids Res 30: 4527-4533
6. Barkan A (1988) Proteins encoded by a complex chloroplast transcription unit are each translated from both monocistronic and polycistronic mRNAs. EMBO J 7: 2637-2644
7. Bock R (2000) Sense from nonsense: How the genetic information of chloroplasts is altered by RNA editing. Biochimie 82: 549-557
8. Bohak Z, Li SL (1976) The structure of monellin and its relation to the sweetness of the protein. Biochim Biophys Acta 427: 153-170
9. Bruick RK, Mayfield SP (1998) Processing of the psbA 5′ untranslated region in Chlamydomonas reinhardtii depends upon factors mediating ribosome association. J Cell Biol 143: 1145-1153
10. Chen HC, Stern D (1991) Specific ribonuclease activities in spinach chloroplasts promote mRNA maturation and degradation. J Biol Chem 266: 24205-24211
11. Chung HJ, Cho IS, Kim JH, In DS, Hur CG, Song JS, Woo SS, Choi DW, Liu JR (2003) Changes in gene expression during hairy root formation by Agrobacterium rhizogenes infection in ginseng. J Plant Biol 46: 187-198
12. Daniell H (2002) Molecular strategies for gene containment in transgenic crops. Nat Biotechnol 20: 581-586
13. Daniell H, Datta R, Varma S, Gray S, Lee SB (1998) Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nat Biotechnol 16: 345-348
14. DeCosa B, Moar W, Lee SB, Miller M, Daniell H (2001) Overexpression of the Bt cry2Aa2 operon in chloroplasts leads to formation of insecticidal crystals. Nat Biotechnol 19: 71-74
15. Dhingra A, Portis Jr AR, Daniell H (2004) Enhanced translation of a chloroplast-expressed RbcS gene restores small subunit levels and photosynthesis in nuclear RbcS antisense plants. Proc Natl Acad Sci USA 101: 6315-6320
16. Edens L, van der Wel H (1985) Microbial synthesis of the sweet tasting plant protein thaumatin. Trends Biotechnol 3: 61-64
17. Eibl C, Zou Z, Beck A, Kim M, Mullet J, Koop HU (1999) In vivo analysis of plastid psbA, rbcL and rpl32 UTR elements by chloroplast transformation: Tobacco plastid gene expression is controlled by modulation of transcript levels and translation efficiency. Plant J 19: 333-345
18. Faus I (2000) Recent developments in the characterization and biotechnological production of sweet-tasting proteins. Appl Microbiol Biotechnol 53: 145-151
19. Fernandez-San Millan A, Mingo-Castel A, Miller M, Daniell H (2003) A chloroplast transgenic approach to hyper express and purify human serum albumin, a protein highly susceptible to proteolytic degradation. Plant Biotechnol J 1: 71-79
20. Fujitani Y, Kobayashi I (2003) Asymmetric random walk in a reaction intermediate of homologous recombination. J Theor Biol 220: 359-370
21. Gumpel NJ, Rochaix JD, Purton S (1994) Studies on homologous recombination in the green alga Chlamydomonas reinhardtii. Curr Genet 26: 438-442
22. Higginbotham JD (1979) Protein sweeteners, In CAM Hough, KJ Parker, eds, Development in Sweeteners-1. Applied Science Publishers, London, pp 87-123
23. Hirose T, Sugiura M (1996) Cis-acting elements and transacting factors for accurate translation of chloroplast psbA mRNAs: Development of an in vitro translation system from tobacco chloroplasts. EMBO J 15: 1687-1695
24. Hirose T, Sugiura M (1997) Both RNA editing and RNA cleavage are required for translation of tobacco chloroplast ndhD mRNA: A possible regulatory mechanism for the expression of a chloroplast operon consisting of functionally unrelated genes. EMBO J 16: 6804-6811
25. Hirose T, Sugiura M (2004) Functional Shine-Dalgarno-like sequences for translational initiation of chloroplast mRNAs. Plant Cell Physiol 45: 114-117
26. Jirgensons B (1976) Conformational transitions of monellin, an intensely sweet protein. Biochim Biophys Acta 446: 255-261
27. Kavanagh TA, Thanh ND, Lao NT, McGrath N, Peter SO, Horvath EM, Dix PJ, Medgyesy P (1999) Homeologous plastid DNA transformation in tobacco is mediated by multiple recombination events. Genetics 152: 1111-1122
28. Kim IH, Lim KJ (1996) Large-scale purification of recombinant monellin from yeast. J Fermentat Bioengineer 82: 180-182
29. Kim J, Mayfield SP (2002) The active site of the thioredoxin-like domain of chloroplast protein disulfide isomerase, RB60, catalyzes the redox-regulated binding of chloroplast poly(A)-binding protein, RB47, to the 5′ untranslated region of psbA mRNA. Plant Cell Physiol 43: 1238-1243
30. Kim M, Christopher DA, Mullet JE (1993) Direct evidence for selective modulation of psbA, rpoA, rbcL and 16S rRNA stability during barley chloroplast development. Plant Mol Biol 22: 447-463
31. Kim SH, Kang CH, Kim R, Cho JM, Lee YB, Lee TK (1989) Redesigning a sweet protein: Increased stability and renaturability. Prot Engineer 2: 571-575
32. Klaff P (1995) mRNA decay in spinach chloroplasts: psbA mRNA degradation is initiated by endonucleolytic cleavages within the coding region. Nucl Acids Res 23: 4885-4892
33. Kohmura M, Nio N, Ariyoshi Y (1990) Complete amino acid sequence of the sweet protein monellin. Agric Biol Chem 54: 2219-2224
34. Kota M, Daniell H, Varma S, Garczynski SF, Gould F, Moar WJ (1999) Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. Proc Natl Acad Sci USA 96: 1840-1845
35. Kumar S, Daniell H (2004) Engineering the chloroplast genome for hyper-expression of human therapeutic proteins and vaccine antigens. Meth Mol Biol 267: 365-383
36. Lee MK, Kim HS, Kim SH, Park YD (2004) T-DNA integration patterns in transgenic tobacco plants. J Plant Biol 47: 179-186
37. Lee SB, Kwon HB, Kwon SJ, Park SC, Jeong MJ, Han SE, Byun MO, Daniell H (2003) Accumulation of trehalose within transgenic chloroplasts confers drought tolerance. Mol Breed 11: 1-13
38. Li HQ, Li MR (2004) RecQ helicase enhances homologous recombination in plants. FEBS Lett 574: 151-155
39. Maier RM, Zeltz P, Kössel H, Bonnard G, Gualberto JM, Grienenberger JM (1996) RNA editing in plant mitochondria and chloroplasts. Plant Mol Biol 32: 343-365
40. Maliga P (1993) Towards plastid transformation in higher plants. Trends Biotech 11: 101-107
41. Monde RA, Greene JC, Stern DB (2000) The sequence and secondary structure of the 3′ UTR affect 3′-end maturation, RNA accumulation, and translation in tobacco chloroplasts. Plant Mol Biol 4: 529-542
42. Morris JA, Cagan RH (1972) Purification of monellin, the sweet principal of Dioscoreophyllum cumminsii. Biochim Biophys Acta 261: 114-122
43. Ogata C, Hatada M, Tomlinson G, Shin WC, Kim SH (1987) Crystal structure of the intensively sweet protein monellin. Nature 328: 739-742
44. Park MC, Shin J, Kim N, Cho H, Park S, An K, Lee S, An G (2003) High-frequency Agrobacterium-mediated genetic transformation of Tongil rice varieties. J Plant Biol 46: 23-30
45. Penarrubia L, Kim R, Giovannoni J, Kim SH, Fischer RL (1992) Production of the sweet protein monellin in transgenic plants. Bio/Technol 10: 561-564
46. Ruf S, Zeltz P, Kssel H (1994) RNA editing of unspliced and dicistronic transcripts of the intron containing reading frame IRF170 from maize chloroplasts. Proc Natl Acad Sci USA 91: 2295-2299
47. Sexton TB, Christopher DA, Mullet JE (1990) Light-induced switch in barley psbD-psbC promoter utilization: A novel mechanism regulating chloroplast gene expression. EMBO J 9: 4485-4494
48. Shen Y, Danon A, Christopher DA (2001) RNA binding-proteins interact specifically with the Arabidopsis chloroplast psbA mRNA 5′ untranslated region in a redox-dependent manner. Plant Cell Physiol 42: 1071-1078
49. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohio C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: Its gene organization and expression. EMBO J 5: 2043-2049
50. Spadaccini R, Crescenzi O, Tancredi T, Casamassimi ND, Saviano G, Scognamiglio R, Donato AD, Temussi PA (2001) Solution structure of a sweet protein: NMR study of MNEI, a single chain monellin. J Mol Biol 305: 505-514
51. Srivastava S, Trivedi PK, Nath P (2004) Components involved in RNA-protein interaction at the 3′ untranslated region of rbcL mRNA of Populus deltoides. Plant Sci 167: 765-772
52. 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
53. Staub JM, Maliga P (1993) Accumulation of D1 polypeptide in tobacco plastids is regulated via the untranslated region of the psbA mRNA. EMBO J 12: 601-606
54. Staub JM, Maliga P (1995) Expression of a chimeric uidA gene indicates that polycistronic mRNAs are efficiently translated in tobacco plastids. Plant J 7: 845-848
55. Sugita M, Sugiura M (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol 32: 315-326
56. Wakasugi T, Sugita M, Tsudzuki T, Sugiura M (1998) Updated gene map of tobacco chloroplast DNA. Plant Mol Biol Rep 16: 231-241
57. Westhoff P, Herrmann RG (1988) Complex RNA maturation in chloroplasts: The psbB operon from spinach. Eur J Biochem 171: 551-564
58. Yohn CB, Cohen A, Rosch C, Kuchka MR, Mayfield SP (1998) Translation of the chloroplast psbA mRNA requires the nuclear-encoded poly(A)-binding protein, RB47. J Cell Biol 142: 435-442
59. Zerges W (2000) Translation in chloroplasts. Biochimie 82: 583-601
60. Zou Z, Eibl C, Koop HU (2003) The stem-loop region of the tobacco psbA 5′UTR is an important determinant of mRNA stability and translation efficiency. Mol Gen Genom 269: 340-349