Phytobilin biosynthesis: Cloning and expression of a gene encoding soluble ferredoxin-dependent heme oxygenase from Synechocystis sp. PCC 6803

Plant Journal

Volumn 15, Issue 1, 1998, Pages 99-107

  Cornejo, Juan ^a   Willows, Robert D ^a   Beale, Samuel I ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BILIVERDIN; BIOSYNTHESIS; CATALYSIS; CENTRIFUGATION; CHROMATOPHORE; CLONING; ESCHERICHIA COLI; FERREDOXIN; GENE EXPRESSION; HEME OXYGENASE; HEME; INCUBATION; OPEN READING FRAME; PHYCOBILIPROTEIN; PHYTOBILIN; PHYTOCHROME; POLYPEPTIDE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SPECTROMETRY;

BACTERIAL PROTEINS; BILIVERDINE; CLONING, MOLECULAR; CYANOBACTERIA; ESCHERICHIA COLI; FERREDOXINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HEME OXYGENASE (DECYCLIZING); HEMIN; LIGHT-HARVESTING PROTEIN COMPLEXES; MOLECULAR WEIGHT; PLANT PROTEINS; RNA, BACTERIAL; RNA, MESSENGER;

ANIMALIA; ESCHERICHIA COLI; SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 0032127571     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.1998.00186.x     Document Type: Article

References (51)

1. Beale, S.I. (1994) Biosynthesis of cyanobacterial tetrapyrrole pigments: hemes, chlorophylls, phycobilins. In The Molecular Biology of Cyanobacteria (Bryant, D.A., ed.). Dordrecht: Kluwer Academic Publishers, pp. 519-558.
2. Beale, S.I. and Cornejo, J. (1983) Biosynthesis of phycocyanobilin from exogenous labeled biliverdin in Cyanidium caldarium. Arch. Biochem. Biophys. 227, 279-286.
3. Beale, S.I. and Cornejo, J. (1984a) Enzymic transformation of biliverdin to phycocyanobilin by extracts of the unicellular red alga, Cyanidium caldarium. Plant Physiol. 76, 7-15.
4. Beale, S.I. and Cornejo, J. (1984b) Enzymatic heme oxygenase activity in soluble extracts of the unicellular red alga, Cyanidium caldarium. Arch. Biochem. Biophys. 235, 371-384.
5. Beale, S.I. and Cornejo, J. (1991a) Biosynthesis of phycobilins. Ferredoxin-mediated reduction of biliverdin catalyzed by extracts of Cyanidium caldarium. J. Biol. Chem. 266, 22328-22332.
6. Beale, S.I. and Cornejo, J. (1991b) Biosynthesis of phycobilins. 3(Z)-Phycoerythrobilin and 3(2)-phycocyanobilin are intermediates in the formation of 3(E)-phycocyanobilin from biliverdin IXα. J. Biol. Chem. 266, 22333-22340.
7. Beale, S.I. and Cornejo, J. (1991c) Biosynthesis of phycobilins. 15,16-Dihydrobiliverdin IXα is a partially reduced intermediate in the formation of phycobilins from biliverdin IXα. J. Biol. Chem. 266, 22341-22345.
8. Chory, J., Peto, C.A., Ashbaugh, M., Saganich, R., Pratt, L.H. and Ausubel, F.M. (1989) Different roles for phytochrome in etiolated and green plants deduced from characterization of Arabidopsis thaliana mutants. Plant Cell, 1, 867-880.
9. Cornejo, J. and Beale, S.I. (1988) Algal heme oxygenase from Cyanidium caldarium. Partial purification and fractionation into three required protein components. J. Biol. Chem. 26, 11915-11921.
10. Cornejo, J. and Beale, S.I. (1997) Phycobilin biosynthetic reactions in extracts of cyanobacteria. Photosynth. Res. 51, 223-230.
11. Cornejo, J., Beale, S.I., Terry, M.J. and Lagarias, J.C. (1992) Phytochrome assembly. The structure and biological activity of 2(R),3(E)-phytochromobilin derived from phycobiliproteins. J. Biol. Chem. 267, 14790-14798.
12. Cornejo, J., Willows, R.W. and Beale, S.I. (1997) Cloning and expression of a Synechocystis sp. PCC 6803 gene for heme oxygenase (abstract no. 744). Plant Physiol. 111, 155.
13. Evans, C.-O., Healey, J.F., Greene, Y. and Bonkovsky, H.L. (1991) Cloning, sequencing and expression of cDNA for chick liver haem oxygenase. Comparison of avian and mammalian cDNAs as deduced proteins. Biochem. J. 273, 659-666.
14. Hughes, J., Lamparter, T., Mittmann, F., Hartmann, E., Gärtner, W., Wilde, A. and Börner, T. (1997) A prokaryotic phytochrome. Nature, 386, 663.
15. Ishikawa, K. Sato, M. Ito, M. and Yoshida, T. (1992) Importance of histidine residue 25 of rat heme oxygenase for its catalytic activity. Biochem. Biophys. Res. Commun. 182, 981-986.
16. Ishikawa, K. Sato, M. and Yoshida, T. (1991) Expression of rat heme oxygenase in Escherichia coli as a catalytically active, full-length form that binds to bacterial membranes. Eur. J. Biochem. 202, 161-165.
17. Kaneko, T. Sato, S. Kotani, H. et al. (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3, 109-136.
18. Koornneef, M., Cone, J.W., Dekens, R.G., O'Herne-Robers, E.G., Spruitt, C.J.P. and Kendrick, R.E. (1985) Photomorphogenic responses of long-hypocotyl mutants of tomato. J. Plant Physiol. 120, 153-165.
19. Koornneef, M., Rolff, E. and Spruitt, C.J.P. (1980) Genetic control, of light-inhibited hypocotyl elongation in Arabidopsis thaliana L. Heynh. Z. Pflanzenphysiol. 100, 147-160.
20. Lagarias, D.M., Wu, S.H. and Lagarias, J.C. (1995) Atypical phytochrome gene structure in the green alga Mesotaenium caldariorum. Plant Mol. Biol. 29, 1127-1142.
21. Matera, K.M., Zhou, H., Migata, C.T., Hobert, S.E., Ishikawa, K., Katakura, K., Maeshima, H., Yoshida, T. and Ikeda-Saito, M. (1997) Histidine-132 does not stabilize a distal water ligand and is not an important residue for the enzyme activity in heme oxygenase-1. Biochemistry, 36, 4909-4915.
22. McCoubrey, W.K. Jr, Ewing, J.F. and Maines, M.D. (1992) Human heme oxygenase-2. Characterization and expression of a full-length cDNA and evidence suggesting that the two HO-2 transcripts may differ by choice of polyadenylation signal. Arch. Biochem. Biophys. 295, 13-20.
23. McCoubrey, W.K. Jr, Huang, T.J. and Maines, M.D. (1997) Heme oxygenase-1 is a hemoprotein and binds heme through heme regulatory motifs that are not involved in heme catalysis. J. Biol. Chem. 272, 12568-12574.
24. 14C]biliverdin by using 2,3-dichloro-5, 6-dicyanobenzoquinone. Biochem. J. 189, 193-208.
25. Parks, B.M. and Quail, P.H. (1991) Phytochrome-deficient hy1 and hy2 long hypocotyl mutants of Arabidopsis are defective in phytochrome chromophore biosynthesis. Plant Cell, 3, 1177-1186.
26. Reith, M.E. and Munholland, J. (1995) Complete nucleotide sequence of the Porphyra purpurea chloroplast genome. Plant Mol. Biol. Rep. 13, 333-335.
27. Rhie, G. and Beale, S.I. (1992) Biosynthesis of phycobilins. Ferredoxin-supported, NADPH-independent heme oxygenase and phycobilin-forming activities from Cyanidium caldarium. J. Biol. Chem. 67, 16088-16093.
28. Rhie, G. and Beale, S.I. (1994) Regulation of heme oxygenase activity in Cyanidium caldarium by light, glucose, and phycobilin precursors. J. Biol. Chem. 269, 9620-9626.
29. Rhie, G. and Beale, S.I. (1995) Phycobilin biosynthesis. Reductant requirements and product identification for heme oxygenase from Cyanidium caldarium. Arch. Biochem. Biophys. 320, 182-194.
30. Richaud, C. and Zabulon, G. (1997) The heme oxygenase gene (pbsA) in the red alga Rhodella violacea is discontinuous and transcriptionally activated during iron limitation. Proc. Natl Acad. Sci. USA, 94, 11736-11741.
31. Rippka, R., Desrulles, J., Waterbury, J.B., Herdman, M. and Stanier, R.Y. (1979) Genetic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111, 1-61.
32. Rotenberg, M.O. and Maines, M.D. (1990) Isolation, characterization, and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J. Biol. Chem. 265, 7501-7506.
33. Rotenberg, M.O. and Maines, M.D. (1991) Characterization of a cDNA-encoding rabbit brain heme oxygenase-2 and identification of a conserved domain among mammalian heme oxygenase isozymes. Possible heme-binding site? Arch. Biochem. Biophys. 229, 336-344.
34. Salih, G.F. and Jansson, C. (1997) Activation of the silent psbA1 gene in the cyanobacterium Synechocystis sp strain 6083 produces a novel and functional D1 protein. Plant Cell, 9, 869-878.
35. Schmitt, M.P. (1997) Utilization of host iron sources by Corynebacterium diphtheriae. Identification of a gene whose product is homologous to eukaryotic heme oxygenases and is required for acquisition of iron from heme and hemoglobin. J. Bacteriol. 179, 838-845.
36. Straus, N.A. (1994) Iron deprivation: physiology and gene regulation. In The Molecular Biology of Cyanobacteria (Bryant, D.A., ed.). Dordrecht: Kluwer Academic Publishers, pp. 731-750.
37. Sun, J., Loehr, T.M., Wilks, A. and Ortiz de Montellano, P.R. (1994) Identification of histidine 25 as the heme ligand in human liver heme oxygenase. Biochemistry, 33, 13734-13740.
38. Tenhunen, R., Marver, H.S. and Schmid, R. (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc. Natl Acad. Sci. USA, 61, 748-755.
39. Terry, M.J. and Kendrick, R.E. (1996) The aurea and yellow-green-2 mutants of tomato are deficient in phytochrome chromophore synthesis. J. Biol. Chem. 271, 21681-21686.
40. Terry, M.J., McDowell, M.D. and Lagarias, J.C. (1995) 3Z- and 3E-phytochromobilin are intermediates in the biosynthesis of the phytochrome chromophore. J. Biol. Chem. 270, 11111-11118.
41. Weller, J.L., Terry, M.J., Rameau, C., Reid, J.B. and Kendrick, R.E. (1996) The phytochrome-deficient pcd1 mutant of pea is unable to convert heme to biliverdin IXα. Plant Cell, 8, 55-67.
42. Weller, J.L., Terry, M.J., Reid, J.B. and Kendrick, R.E. (1997) The phytochrome-deficient pcd2 mutant of pea is unable to convert biliverdin IXα to 3 (Z) -phytochromobilin. Plant J. 11, 1177-1186.
43. Wilde, A., Yuri, C., Schubert, H. and Börner, T. (1997) Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. FEBS Lett. 406, 89-92.
44. Wilks, A., Black, S.M., Miller, W.L. and Ortiz de Montellano, P.R. (1995) Expression and characterization of truncated human heme oxygenase (hHO-1) and a fusion protein of hHO-1 with human cytochrome P450 reductase. Biochemistry, 34, 4421-4427.
45. Wilks, A. and Ortiz de Montellano, P.R. (1993) Rat liver heme oxygenase. High-level expression of a truncated soluble form and nature of the meso-hydroxylating species. J. Biol. Chem. 268, 22357-22362.
46. Wilks, A., Ortiz de Montellano, P.R., Sun, J. and Loehr, T.M. (1996) Heme oxygenase (HO-1). His-132 stabilizes a distal water ligand and assists catalysis. Biochemistry, 35, 930-936.
47. Wilks, A. and Schmitt, M.P. (1998) Expression and characterization of a heme oxygenase (HmuO) from Corynebacterium diphtheriae. Iron acquisition requires oxidative cleavage of the heme macrocycle. J. Biol. Chem. 273, 837-841.
48. Wu, S., Lu, Q. and Kriz, A.L. (1995) Multiple-sandwich, one-stop hybridization of northern and Southern blots. BioTechniques, 18, 585-586.
49. Yoshida, T., Biro, P., Cohen, T., Müller, R.M. and Shibahara, S. (1988) Human heme oxygenase cDNA and induction of its mRNA by hemin. Eur. J. Biochem. 171, 457-461.
50. Yoshida, T., Ishikawa, K. and Sato, M. (1991) Degradation of heme by a soluble peptide of heme oxygenase obtained from rat liver microsomes by mild trypsinization. Eur. J. Biochem. 199, 729-733.
51. Yoshinaga, T., Sassa, S. and Kappas, A. (1982) The occurrence of molecular interactions among NADPH-cytochrome c reductase, heme oxygenase, and biliverdin reductase in heme degradation. J. Biol. Chem. 257, 7786-7793.