Investigating the production of foreign membrane proteins in tobacco chloroplasts: Expression of an algal plastid terminal oxidase

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Ahmad, Niaz ^a,b   Michoux, Franck ^a   Nixon, Peter J ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NATIONAL INSTITUTE FOR BIOTECHNOLOGY AND GENETIC ENGINEERING NIBGE   (Pakistan)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; PLASTID TERMINAL OXIDASE 1; PLASTOQUINONE; RNA 16S; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; BACTERIOPHAGE T7; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL FLUORESCENCE; CHLOROPLAST GENOME; CODON; DNA SEQUENCE; ENZYME ACTIVE SITE; GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION STATE; PHOTOSENSITIVITY; PLANT GROWTH; PLANT LEAF; PLANT REGENERATION; PLASTID TERMINAL OXIDASE 1 GENE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROMOTER REGION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE ALIGNMENT; TOBACCO; WESTERN BLOTTING;

AMINO ACID SEQUENCE; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; GENE EXPRESSION; GENETIC ENGINEERING; GENETIC VECTORS; LIGHT; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHYLOGENY; PLANT LEAVES; PLASTOQUINONE; PROTEIN TRANSPORT; STRESS, PHYSIOLOGICAL; TOBACCO; TRANSFORMATION, GENETIC;

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; NICOTIANA TABACUM;

EID: 84864370850     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041722     Document Type: Article

References (49)

1. Sprenger RR, Jensen ON, (2010) Proteomics and the dynamic plasma membrane: Quo Vadis? Proteomics 10: 3997-4011.
2. Wallin E, Heijne GV, (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 7: 1029-1038.
3. Bakheet TM, Doig AJ, (2009) Properties and identification of human protein drug targets. Bioinformatics 25: 451-457.
4. Carpenter EP, Beis K, Cameron AD, Iwata S, (2008) Overcoming the challenges of membrane protein crystallography. Curr Opin Struct Biol 18: 581-586.
5. Lössl AG, Waheed MT, (2011) Chloroplast-derived vaccines against human diseases: achievements, challenges and scopes. Plant Biotechnol J 9: 527-539.
6. Verma D, Samson NP, Koya V, Daniell H, (2008) A protocol for expression of foreign genes in chloroplasts. Nat Protoc 3: 739-758.
7. Singh ND, Li M, Lee S-B, Schnell D, Daniell H, (2008) Arabidopsis Tic40 expression in tobacco chloroplasts results in massive proliferation of the inner envelope membrane and upregulation of associated proteins. Plant Cell 20: 3405-3417.
8. Cournac L, Josse EM, Joët T, Rumeau D, Redding K, et al. (2000) Flexibility in photosynthetic electron transport: a newly identified chloroplast oxidase involved in chlororespiration. Philos Trans R Soc Lond B Biol Sci 355: 1447-1454.
9. Joët T, Genty B, Josse EM, Kuntz M, Cournac L, et al. (2002) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J Biol Chem 277: 31623-31630.
10. Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson L, et al. (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol 142: 574-585.
11. Berthold DA, Stenmark P, (2003) Membrane-bound diiron carboxylate proteins. Ann Rev Plant Biol 54: 497-517.
12. Lennon AM, Prommeenate P, Nixon PJ, (2003) Location, expression and orientation of the putative chlororespiratory enzymes, Ndh and IMMUTANS, in higher-plant plastids. Planta 218: 254-260.
13. Carol P, Kuntz M, (2001) A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trends Plant Sci 6: 31-36.
14. Shahbazi M, Gilbert M, Laboure AM, Kuntz M, (2007) Dual role of the plastid terminal oxidase in tomato. Plant Physiol 145: 691-702.
15. Stepien P, Johnson GN, (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol 149: 1154-1165.
16. Houille-Vernes L, Rappaport F, Wollman F-A, Alric J, Johnson X, (2011) Plastid Terminal Oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc Nati Acad Sci USA 108: 20820-20825.
17. Berthold DA, Andersson ME, Nordlund P, (2000) New insight into the structure and function of the alternative oxidase. Biochim Biophys Acta 1460: 241-254.
18. Fu A, Park S, Rodermel S, (2005) Sequences required for the activity of PTOX (IMMUTANS), a plastid terminal oxidase. J Bio Chem 280: 42489-42496.
19. McDonald AE, Amirsadeghi S, Vanlerberghe GC, (2003) Prokaryotic orthologues of mitochondrial alternative oxidase and plastid terminal oxidase. Plant Mol Biol 53: 865-876.
20. Emanuelsson O, Nielsen H, Heijne GV, (1999) ChloroP, a neural network based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8: 978-984.
21. Emanuelsson O, Nielsen H, Brunak S, von Heijne G, (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005-1016.
22. Kuroda H, Maliga P, (2001) Complementarity of the 16S rRNA penultimate stem with sequences downstream of the AUG destabilizes the plastid mRNAs. Nucl Acids Res 29: 970-975.
23. Svab Z, Maliga P, (1993) High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. Proc Natl Acad Sci USA 90: 913-917.
24. Krause G, Weis E, (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Biol 42: 313-349.
25. Mano J, Miyake C, Schreiber U, Asada K, (1995) Photoactivation of the electron flow from NADPH to plastoquinone in spinach chloroplasts. Plant Cell Physiol 36: 1589-1598.
26. Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ, (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17: 868-876.
27. Maxwell K, Johnson GN, (2000) Chlorophyll fluorescence-a practical guide. J Exp Bot 51: 659-668.
28. Barber J, Andersson B, (1992) Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci 17: 61-66.
29. Bjökman O, Demmig B, (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170: 489-504.
30. Heyno E, Gross CM, Laureau C, Culcasi M, Pietri S, et al. (2009) Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J Bio Chem 284: 31174-31180.
31. Umbach AL, Siedow JN, (1993) Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher plant mitochondria and their relationship to enzyme activity. Plant Physiol 103: 845-854.
32. Kuntz M, (2004) Plastid terminal oxidase and its biological significance. Planta 218: 896-899.
33. Ye GN, Hajdukiewicz PTJ, Broyles D, Rodriguez D, Xu CW, et al. (2001) Plastid-expressed 5-enolpyruvylshikimate-3-phosphate synthase genes provide high level glyphosate tolerance in tobacco. Plant J 25: 261-270.
34. Zhang Y, Ding S, Lu Q, Yang Z, Wen X, et al. (2011) Characterization of photosystem II in transgenic tobacco plants with decreased iron superoxide dismutase. Biochim Biophys Acta 1807: 391-403.
35. Bowler C, Montagu MV, Inze D, (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43: 83-116.
36. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F, (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9: 490-498.
37. Takahashi S, Badger MR, (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16: 53-60.
38. Murashige T, Skoog F, (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol 79: 197-205.
39. Ahmad N, Michoux F, McCarthy J, Nixon PJ, (2012) Expression of the affinity tags, glutathione-S-transferase and maltose-binding protein, in tobacco chloroplasts. Planta 235: 863-871.
40. Larkin M, Blackshields G, Brown N, Chenna R, McGettigan P, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
41. Huson D, Richter D, Rausch C, Dezulian T, Franz M, et al. (2007) Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics 8: 460-467.
42. Michoux F, Ahmad N, McCarthy J, Nixon PJ, (2011) Contained and high-level production of recombinant proteins in plant chloroplasts using a temporary immersion bioreactor. Plant Biotechnol J 9: 575-584.
43. Cho K, Torres N, Subramanyam S, Deepak S, Sardesai N, et al. (2006) Protein extraction/solubilization protocol for monocot and dicot plant gel-based proteomics. Plant Biol 49: 413-420.
44. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
45. Suorsa M, Regel RE, Paakkarinen V, Battchikova N, Herrmann RG, et al. (2004) Protein assembly of photosystem II and accumulation of subcomplexes in the absence of low molecular mass subunits PsbL and PsbJ. Eur J Biochem 271: 96-107.
46. Boehm M, Nield J, Zhang P, Aro EM, Komenda J, et al. (2009) Structural and mutational analysis of band 7 proteins in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 191: 6425-6435.
47. Oey M, Lohse M, Kreikemeyer B, Bock R, (2009) Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J 57: 436-445.
48. Klughammer C, Schreiber U, (1994) An improved method, using saturating light pulses, for the determination of photosystem I quantum yield via P700+-absorbance changes at 830 nm. Planta 192: 261-268.
49. Mussgnug JH, Wobbe L, Elles I, Claus C, Hamilton M, et al. (2005) NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii. Plant Cell 17: 3409-3421.