Analysis of heterologous regulatory and coding regions in algal chloroplasts

Applied Microbiology and Biotechnology

Volumn 97, Issue 10, 2013, Pages 4499-4510

  Gimpel, Javier A ^a   Mayfield, Stephen P ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Chlamydomonas reinhardtii; Chloroplast transcription; Chloroplast translation; D1; Heterologous gene; psbA

Indexed keywords

CHLAMYDOMONAS REINHARDTII; CHLOROPLAST TRANSLATION; D1; HETEROLOGOUS GENES; PSBA;

ALGAE; AMINO ACIDS; BIOLOGY; GENES; PROTEINS; RNA;

TRANSCRIPTION;

ALGAL PROTEIN; D1 PROTEIN OF PHOTOSYSTEM II; MESSENGER RNA; UNCLASSIFIED DRUG;

AMINO ACID; CHLOROPLAST; CYANOBACTERIUM; GREEN ALGA; PHOTOSYNTHESIS; PROTEIN;

5' UNTRANSLATED REGION; ARTICLE; ATPA GENE; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CONTROLLED STUDY; GENE; GENETIC CODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOSYNTHESIS; PHOTOSYSTEM II; PROMOTER REGION; PROTEIN EXPRESSION; PSBD GENE; TUFA GENE;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; CHLOROPLASTS; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; SEAWEED; SEQUENCE HOMOLOGY, NUCLEIC ACID;

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; CYANOBACTERIA; EMBRYOPHYTA;

EID: 84877725350     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-012-4580-4     Document Type: Article

References (61)

1. Alexander C, Faber N, Klaff P (1998) Characterization of protein-binding to the spinach chloroplast psbA mRNA 5′ untranslated region. Nucleic Acids Res 26:2265-2272 (Pubitemid 28297323)
2. Barnes D, Cohen A, Bruick RK, Kantardjieff K, Fowler S, Efuet E, Mayfield SP (2004) Identification and characterization of a novel RNA binding protein that associates with the 5′-untranslated region of the chloroplast psbA mRNA. Biochem 43:8541-8550 (Pubitemid 38902532)
3. Barnes D, Franklin S, Schultz J, Henry R, Brown E, Coragliotti MSP (2005) Contribution of 5′- and 3′-untranslated regions of plastid mRNAs to the expression of Chlamydomonas reinhardtii chloroplast genes. Mol Genet Genomics 274:625-636 (Pubitemid 41746829)
4. Bateman JM, Purton S (2000) Tools for chloroplast transformation in Chlamydomonas: expression vectors and a new dominant selectable marker. Mol Gen Genet 263:404-410
5. Bohne AV, Irihimovitch V, Weihe A, Stern DB (2006) Chlamydomonas reinhardtii encodes a single sigma 70-like factor which likely functions in chloroplast transcription. Curr Genet 49:333-340 (Pubitemid 43880485)
6. Bohne AV, Ruf S, Börner T, Bock R (2007) Faithful transcription initiation from a mitochondrial promoter in transgenic plastids. Nucleic Acids Res 35:7256-7266
7. Bruick RK, Mayfield SP (1998) Processing of the psbA 5′ untranslated region in Chlamydomonas reinhardtii depends upon factors mediating ribosome association. J Cell Biol 143:1145-1154 (Pubitemid 28559818)
8. Chen R, Gyokusen M, Nakazawa Y, Gyokusen K (2010) Selection of housekeeping genes for transgene expression analysis in Eucommia ulmoides Oliver using real-time RT-PCR. J Bot 2010:1-7
9. Choquet Y, Wollman FA (2002) Translational regulations as specific traits of chloroplast gene expression. FEBS Lett 529:39-42 (Pubitemid 35283909)
10. Danon A, Mayfield SP (1991) Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J 10:3993-4001 (Pubitemid 21905428)
11. Danon A, Mayfield SP (1994) Light-regulated translation of chloroplast messenger RNAs through redox potential. Science 266:1717-1719
12. Eberhard S, Drapier D, Wollman FA (2002) Searching limiting steps in the expression of chloroplast-encoded proteins: relations between gene copy number, transcription, transcript abundance and translation rate in the chloroplast of Chlamydomonas reinhardtii. Plant J 31:149-160 (Pubitemid 34829628)
13. Erickson JM, Rahire M, Rochaix JD (1984) Chlamydomonas reinhardtii gene for the 32,000 mol. wt. protein of photosystem II contains four large introns and is located entirely within the chloroplast inverted repeat. EMBO J 3:2753-2762
14. Franklin S, Ngo B, Efuet E, Mayfield SP (2002) Development of a GFP reporter gene for Chlamydomonas reinhardtii chloroplast. Plant J 30:733-744 (Pubitemid 34696065)
15. Gisby MF, Mellors P, Madesis P, Ellin M, Laverty H, O'Kane S, Ferguson MWJ, Day A (2011) A synthetic gene increases TGFβ3 accumulation by 75-fold in tobacco chloroplasts enabling rapid purification and folding into a biologically active molecule. Plant Biotechnol J 9:618-628
16. Golden SS, Brusslan J, Haselkorn R (1986) Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5:2789-2798
17. Gorman D, Levine R (1965) Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci USA 54:1665-1669
18. Hibberd JM, Linley PJ, Khan MS, Gray JC (1998) Transient expression of green fluorescent protein in various plastid types following microprojectile bombardment. Plant J 16:627-632 (Pubitemid 29032487)
19. Johanningmeier U, Heiss S (1993) Construction of a Chlamydomonas reinhardtii mutant with an intronless psbA gene. Plant Mol Biol 22:91-99
20. Kato K, Ishikura K, Kasai S, Shinmyo A (2006) Efficient translation destabilizes transcripts in chloroplasts of Chlamydomonas reinhardtii. J Biosci Bioeng 101:471-477 (Pubitemid 44354429)
21. Keller A, Schleicher T, Förster F, Ruderisch B, Dandekar T, Müller T, Wolf M (2008) ITS2 data corroborate a monophyletic chlorophycean DO-group (Sphaeropleales). BMC Evol Biol 8:218
22. Klein U, De Camp JD, Bogorad L (1992) Two types of chloroplast gene promoters in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 89:3453-3457
23. Krammer EM, Sebban P, Ullmann GM (2009) Profile hidden Markov models for analyzing similarities and dissimilarities in the bacterial reaction center and photosystem II. Biochem 48:1230-1243
24. Kramzar LM, Mueller T, Erickson B, Higgs DC (2006) Regulatory sequences of orthologous petD chloroplast mRNAs are highly specific among Chlamydomonas species. Plant Mol Biol 60:405-422 (Pubitemid 43327577)
25. Kuroda H, Maliga P (2001) Complementarity of the 16S rRNA penultimate stem with sequences downstream of the AUG destabilizes the plastid mRNAs. Nucleic Acids Res 29:970-975 (Pubitemid 32162266)
26. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948 (Pubitemid 350162903)
27. Li R, Golden SS (1993) Enhancer activity of light-responsive regulatory elements in the untranslated leader regions of cyanobacterial psbA genes. Proc Natl Acad Sci USA 90:11678-11682 (Pubitemid 24008702)
28. Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW (2005) Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438:86-89 (Pubitemid 41599824)
29. Lindell D, Jaffe JD, Coleman ML, Futschik ME, Axmann IM, Rector T, Kettler G, Sullivan MB, Steen R, Hess WR (2007) Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449:83-86 (Pubitemid 47373778)
30. Lyubetsky VA, Rubanov LI, Seliverstov AV (2010) Lack of conservation of bacterial type promoters in plastids of Streptophyta. Biol Direct 5:34
31. Manuell AL, Beligni MV, Elder JH, Siefker DT, Tran M, Weber A, McDonald TL, Mayfield SP (2007) Robust expression of a bioactive mammalian protein in Chlamydomonas chloroplast. Plant Biotechnol J 5:402-412 (Pubitemid 46558325)
32. Marín-Navarro J, Manuell AL, Wu J, Mayfield SP (2007) Chloroplast translation regulation. Photosynthesis Res 94:359-374 (Pubitemid 350229094)
33. Mayfield SP, Cohen A, Danon A, Yohn CB (1994) Translation of the psbA mRNA of Chlamydomonas reinhardtii requires a structured RNA element contained within the 5′ untranslated region. J Cell Biol 127:1537-1545 (Pubitemid 24380894)
34. Mayfield SP, Schultz J (2004) Development of a luciferase reporter gene, luxCt, for Chlamydomonas reinhardtii chloroplast. Plant J 37:449-458 (Pubitemid 38192970)
35. Mayfield SP, Manuell AL, Chen S, Wu J, Tran M, Siefker D, Muto M, Marín-Navarro J (2007) Chlamydomonas reinhardtii chloroplasts as protein factories. Curr Opin Biotechnol 18:126-133 (Pubitemid 46575227)
36. Memon AR, Meng B, Mullet JE (1996) RNA-binding proteins of 37/38 kDa bind specifically to the barley chloroplast psbA 3′-end untranslated RNA. Plant Mol Biol 30:1195-1205 (Pubitemid 26310790)
37. Minai L, Wostrikoff K, Wollman FA, Choquet Y (2006) Chloroplast biogenesis of photosystem II cores involves a series of assembly-controlled steps that regulate translation. Plant Cell 18:159-175 (Pubitemid 43951322)
38. Mulo P, Sakurai I, Aro EM (2012) Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochim Biophys Acta Bioenergetics 1817:247-257
39. Newell CA, Birch-Machin I, Hibberd JM, Gray JC (2003) Expression of green fluorescent protein from bacterial and plastid promoters in tobacco chloroplasts. Transgenic Res 12:631-634 (Pubitemid 37292450)
40. Nickelsen J (1999) Transcripts containing the 5′ untranslated regions of the plastid genes psbA and psbB from higher plants are unstable in Chlamydomonas reinhardtii chloroplasts. Mol Gen Genet 262:768-771 (Pubitemid 30018819)
41. Nixon PJ, Rogner M, Diner BA (1991) Expression of a higher plant psbA gene in Synechocystis 6803 yields a functional hybrid photosystem II reaction center complex. Plant Cell 3:383-395 (Pubitemid 21913705)
42. Ossenbuhl F, Hartmann K, Nickelsen J (2002) A chloroplast RNA binding protein from stromal thylakoid membranes specifically binds to the 5′ untranslated region of the psbA mRNA. Eur J Biochem 269:3912-3919 (Pubitemid 34994886)
43. Pinto FL, Lindblad P (2010) A guide for in-house design of template-switch-based 5′ rapid amplification of cDNA ends systems. Anal Biochem 397:227-232
44. Puigbo P, Bravo I, Garcia-Vallve S (2008) CAIcal: a combined set of tools to assess codon usage adaptation. Biol Direct 3:38
45. Rasala BA, Muto M, Lee PA, Jager M, Cardoso RMF, Behnke CA, Kirk P, Hokanson CA, Crea R, Mendez M (2010) Production of therapeutic proteins in algae, analysis of expression of seven human proteins in the chloroplast of Chlamydomonas reinhardtii. Plant Biotechnol J 8:719-733
46. Rasala BA, Muto M, Sullivan J, Mayfield SP (2011) Improved heterologous protein expression in the chloroplast of Chlamydomonas reinhardtii through promoter and 5′ untranslated region optimization. Plant Biotechnol J 9:674-683
47. Ruhlman T, Verma D, Samson N, Daniell H (2010) The role of heterologous chloroplast sequence elements in transgene integration and expression. Plant Physiol 152:2088-2104
48. Schult K, Meierhoff K, Paradies S, Töller T, Wolff P, Westhoff P (2007) The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19:1329-1346 (Pubitemid 46941657)
49. Sharp PM, Li WH (1987) The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281-1295
50. 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 (Pubitemid 33037875)
51. Shi T, Bibby TS, Jiang L, Irwin AJ, Falkowski PG (2005) Protein interactions limit the rate of evolution of photosynthetic genes in cyanobacteria. Mol Biol Evol 22:2179-2189 (Pubitemid 41437799)
52. Smith DR, Lee RW (2009) The mitochondrial and plastid genomes of Volvox carteri: bloated molecules rich in repetitive DNA. BMC Genomics 10:132
53. Sriraman P, Silhavy D, Maliga P (1998) Transcription from heterologous rRNA operon promoters in chloroplasts reveals requirement for specific activating factors. Plant Physiol 117:1495-1499 (Pubitemid 128652921)
54. Stern DB, Radwanski ER, Kindle KL (1991) A 3′ stem/loop structure of the Chlamydomonas chloroplast atpB gene regulates mRNA accumulation in vivo. Plant Cell 3:285-297 (Pubitemid 21913696)
55. Sueoka N (1960) Mitotic replication of deoxyribonucleic acid in Chlamydomonas reinhardi. Proc Natl Acad Sci USA 46:83-91
56. 2 and high light conditions. Mol Microbiol 52:837-845 (Pubitemid 38621752)
57. Verma D, Daniell H (2007) Chloroplast vector systems for biotechnology applications. Plant Physiol 145:1129-1143 (Pubitemid 350276732)
58. Weiss C, Bertalan I, Johanningmeier U (2012) Effects of rare codon clusters on the expression of a high-turnover chloroplast protein in Chlamydomonas reinhardtii. J Biotech 160:105-111
59. Zhang L, Aro EM (2002) Synthesis, membrane insertion and assembly of the chloroplast-encoded D1 protein into photosystem II. FEBS Lett 512:13-18 (Pubitemid 34164442)
60. Zicker AA, Kadakia CS, Herrin DL (2007) Distinct roles for the 5′ and 3′ untranslated regions in the degradation and accumulation of chloroplast tufA mRNA: identification of an early intermediate in the in vivo degradation pathway. Plant Mol Biol 63:689-702
61. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406-3415 (Pubitemid 37442169)