Identification and characterization of the Arabidopsis gene encoding the tetrapyrrole biosynthesis enzyme uroporphyrinogen III synthase

Biochemical Journal

Volumn 410, Issue 2, 2008, Pages 291-299

  Tan, Fui Ching ^a   Cheng, Qi ^a   Saha, Kaushik ^a   Heinemann, Ilka U ^b   Jahn, Martina ^b   Jahn, Dieter ^b   Smith, Alison G ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

Author keywords

Chloroplast import in vitro; Deletion mutant; Functional complementation; Green fluorescent protein (GFP); Plastid location

Indexed keywords

BIOSYNTHESIS; CHLOROPHYLL; CONFOCAL MICROSCOPY; ENZYME ACTIVITY; ENZYME KINETICS; ESCHERICHIA COLI;

CHLOROPLASTS; DELETION MUTANT; FUNCTIONAL COMPLEMENTATION; GREEN FLUORESCENT PROTEIN (GFP); PLASTID LOCATION;

GENE ENCODING;

TETRAPYRROLE DERIVATIVE; UROPORPHYRINOGEN III SYNTHASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; CHLOROPLAST; CONFOCAL MICROSCOPY; CRYSTAL STRUCTURE; DNA LIBRARY; ESCHERICHIA COLI; EXPRESSION VECTOR; GENE; GENE CONSTRUCT; GENE DELETION; GENE IDENTIFICATION; GENE SEQUENCE; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; ORTHOLOGY; PLANT GENE; PLASMID; PRIORITY JOURNAL; PROTEIN DATABASE; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURAL HOMOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; CLONING, MOLECULAR; DNA PRIMERS; GENETIC COMPLEMENTATION TEST; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; TETRAPYRROLES; UROPORPHYRINOGEN III SYNTHETASE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 40449117381     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070770     Document Type: Article

References (43)

1. Warren, M. J. and Scott, A. I. (1990) Tetrapyrrole assembly and modification into the ligands of biologically functional cofactors. Trends Biochem. Sci. 15, 486-491
2. Battersby, A. R., Fookes, C. J. R., Gustafson-Potter, K. E., Matcham, G. W. J. and McDonald, E. (1979) Proof by synthesis that unrearranged hydroxymethylbilane is the product from deaminase and substrate for cosynthase in the biosynthesis of uroporphyrinogen III. J. Chem. Soc. Chem. Commun. 316-319
3. Desnick, R. J., Glass, I. A., Xu, W., Sous, C. and Astrin, K. H. (1998) Molecular genetics of congenital erythropoietic porphyria. Semin. Liver Dis. 18, 77-84
4. Kappas, A., Sassa, S., Galbraith, R. A. and Nordmann, Y. (1995) The Porphyrias, McGraw-Hill, New York
5. Sasarman, A., Nepveu, A., Echelard, Y., Dymetryszyn, J., Drolet, M. and Goyer, C. (1987) Molecular cloning and sequencing of the hemD gene of Escherichia coli K-12 and preliminary data on the Uro operon. J. Bacteriol. 169, 4257-4262
6. Tsai, S. F., Bishop, D. F. and Desnick, R. J. (1988) Human uroporphyrinogen III synthase: molecular cloning, nucleotide sequence, and expression of a full-length cDNA. Proc. Natl. Acad. Sci. U.S.A. 85, 7049-7053
7. Hansson, M., Rutberg, L., Schroder, I. and Hederstedt, L. (1991) The Bacillus subtilis hemAXCDBL gene cluster, which encodes enzymes of the biosynthetic pathway from glutamate to uroporphyrinogen III. J. Bacteriol. 173, 2590-2599
8. Mohr, C. D., Sonsteby, S. K. and Deretic, V. (1994) The Pseudomonas aeruginosa homologs of hemC and hemD are linked to the gene encoding the regulator of mucoidy AIgR. Mol. Gen. Genet. 242, 177-184
9. Jones, M. C., Jenkins, J. M., Smith, A. G. and Howe, C. J. (1994) Cloning and characterisation of genes for tetrapyrrole biosynthesis from the cyanobacterium Anacystis nidulans R2. Plant Mol. Biol. 24, 435-448
10. Bensidhoum, M., Ged, C. M., Poirier, C., Guenet, J. L. and de Verneuil, H. (1994) The cDNA sequence of mouse uroporphyrinogen III synthase and assignment to mouse chromosome 7. Mamm. Genome 5, 728-730
11. Amillet, J. M. and Labbe-Bois, R. (1995) Isolation of the gene HEM4 encoding uroporphyrinogen III synthase in Saccharomyces cerevisiae. Yeast 11, 419-424
12. Mathews, M. A., Schubert, H. L., Whitby, F. G., Alexander, K. J., Schadick, K., Bergonia, H. A., Phillips, J. D. and Hill, C. P. (2001) Crystal structure of human uroporphyrinogen III synthase. EMBO J. 20, 5832-5839
13. Murray, J. A. H. and Smith, A. G. (1996) Functional complementation in yeast and E. coli. In Plant Gene Isolation: Principles and Practice (Foster, G. D. and Twell, D., eds.), pp. 177-211, J. Wiley & Sons, Chichester
14. Minet, M., Dufour, M. E. and Lacroute, F. (1992) Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 2, 417-422
15. Wach, A., Brachat, A., Pohlmann, R. and Philippsen, P. (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808
16. Oka, A., Sugisaki, H. and Takanami, M. (1981) Nucleotide sequence of the kanamycin resistance transposon Tn903. J. Mol. Biol. 147, 217-226
17. Steiner, S. and Philippsen, P. (1994) Sequence and promoter analysis of the highly expressed TEF gene of the filamentous fungus Ashbya gossypii. Mol. Gen. Genet. 242, 263-271
18. Gietz, R. D. and Woods, R. A. (1994) High efficiency transformation of yeast with lithium acetate. In Molecular Genetics of Yeast: A Practical Approach (Johnston, J. R., ed.), pp. 121-143, Oxford University Press, Oxford
19. Rose, M. D., Winston, F. and Hieter, P. (1990) Methods in Yeast Genetics: A Laboratory Course Manual, Cold Spring Harbour Laboratory Press, New York
20. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680
21. Chartrand, P., Tardif, D. and Sasarman, A. (1979) Uroporphyrin- and coproporphyrin I-accumulating mutant of Escherichia coli K12. J. Gen. Microbiol. 110, 61-66
22. Raux, E., Leech, H. K., Beck, R., Schubert, H. L., Santander, P. J., Roessner, C. A., Scott, A. I., Martens, J. H., Jahn, D., Thermes, C. et al. (2003) Identification and functional analysis of enzymes required for precorrin-2 dehydrogenation and metal ion insertion in the biosynthesis of sirohaem and cobalamin in Bacillus megaterium. Biochem. J. 370, 505-516
23. Jordan, P. M. (1982) Uroporphyrinogen III cosynthetase: a direct assay method. Enzyme 28, 158-169
24. Alwan, A. F., Mgbeje, B. I. and Jordan, P. M. (1989) Purification and properties of uroporphyrinogen III synthase (co-synthase) from an overproducing recombinant strain of Escherichia coli K-12. Biochem. J. 264, 397-402
25. Cleary, S. P., Tan, F. C., Nakrieko, K. A., Thompson, S. J., Mullineaux, P. M., Creissen, G. P., von Stedingk, E., Glaser, E., Smith, A. G. and Robinson, C. (2002) Isolated plant mitochondria import chloroplast precursor proteins in vitro with the same efficiency as chloroplasts. J. Biol. Chem. 277, 5562-5569
26. Suzuki, T., Masuda, T., Singh, D. P., Tan, F. C., Tsuchiya, T., Shimada, H., Ohta, H., Smith, A. G. and Takamiya, K. (2002) Two types of ferrochelatase in photosynthetic and nonphotosynthetic tissues of cucumber: their difference in phylogeny, gene expression, and localization. J. Biol. Chem. 277, 4731-4737
27. Davis, S. J. and Vierstra, R. D. (1998) Soluble, highly fluorescent variants of green fluorescent protein (GFP) for use in higher plants. Plant Mol. Biol. 36, 521-528
28. Akashi, K., Grandjean, O. and Small, I. (1998) Potential dual targeting of an Arabidopsis archaebacterial-like histidyl-tRNA synthetase to mitochondria and chloroplasts. FEBS Lett. 431, 39-44
29. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
30. AGI (2000) Arabidopsis genome initiative: analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815
31. Frugoli, J. A., McPeek, M. A., Thomas, T. L. and McClung, C. R. (1998) Intron loss and gain during evolution of the catalase gene family in angiosperms. Genetics 149, 355-365
32. Chow, K.-S., Singh, D. P., Walker, A. R. and Smith, A. G. (1998) Two different genes encode ferrochelatase in Arabidopsis: mapping, expression and subcellular targeting of the precursor proteins. Plant J. 15, 531-541
33. Kohashi, M., Clement, R. P., Tse, J. and Piper, W. N. (1984) Rat hepatic uroporphyrinogen III co-synthase. Purification and evidence for a bound folate coenzyme participating in the biosynthesis of uroporphyrinogen III. Biochem. J. 220, 755-765
34. Hart, G. J. and Battersby, A. R. (1985) Purification and properties of uroporphyrinogen III synthase (co-synthetase) from Euglena gracilis. Biochem. J. 232, 151-160
35. Tsai, S. F., Bishop, D. F. and Desnick, R. J. (1987) Purification and properties of uroporphyrinogen III synthase from human erythrocytes. J. Biol. Chem. 262, 1268-1273
36. Shi, J., Blundell, T. L. and Mizuguchi, K. (2001) FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J. Mol. Biol. 310, 243-257
37. Witty, M., Jones, R. M., Robb, M. S., Jordan, P. M. and Smith, A. G. (1996) Subcellular location of the tetrapyrrole synthesis enzyme porphobilinogen deaminase in higher plants: an immunological investigation. Planta 199, 557-564
38. Smith, A. G., Marsh, O. and Elder, G. H. (1993) Investigation of the subcellular location of the tetrapyrrole-biosynthesis enzyme coproporphyrinogen oxidase in higher plants. Biochem. J. 292, 503-508
39. Santana, M. A., Tan, F. C. and Smith, A. G. (2002) Molecular characterisation of coproporphyrinogen oxidase from Glycine max and Arabidopsis thaliana. Plant Physiol. Biochem. 40, 289-298
40. Cornah, J. E., Roper, J. M., Singh, D. P. and Smith, A. G. (2002) Measurement of ferrochelatase activity using a novel assay suggests that plastids are the major site of haem biosynthesis in both photosynthetic and non-photosynthetic cells of pea (Pisum sativum L). Biochem. J. 362, 423-432
41. Jordan, P. M. (1991) The biosynthesis of 5-aminolaevulinic acid and its transformation into uroporphyrinogen III. In Biosynthesis of Tetrapyrroles (Jordan, P.M., ed.) pp. 1-35, Elsevier, Amsterdam
42. Schoenhaut, D. S. and Curtis, P. J. (1986) Nucleotide sequence of mouse 5-aminolevulinic acid synthase cDNA and expression of its gene in hepatic and erythroid tissue. Gene 48, 55-63
43. Zavgorodnyaya, A., Papenbrock, J. and Grimm, B. (1997) Yeast 5-aminolevulinate synthase provides additional chlorophyll precursor in transgenic tobacco. Plant J. 12, 169-178