Differential operation of dual protochlorophyllide reductases for chlorophyll biosynthesis in response to environmental oxygen levels in the cyanobacterium Leptolyngbya boryana

Plant Physiology

Volumn 142, Issue 3, 2006, Pages 911-922

  Yamazaki, Shoji ^a   Nomata, Jiro ^a   Fujita, Yuichi ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOSYNTHESIS;

ANAEROBIC ENVIRONMENTS; MUTANT CELLS; PHOTOSYNTHETIC CELLS;

ENZYMES;

ANAEROBIC PROCESS; BACTERIA; BIOSYNTHESIS; ENZYMES;

CYANOBACTERIA; LEPTOLYNGBYA BORYANA; PLECTONEMA;

EID: 33751079088     PISSN: 00320889     EISSN: None     Source Type: Journal    
DOI: 10.1104/pp.106.086090     Document Type: Article

References (72)

1. Armstrong GA (1998) Greening in the dark: light-independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms. J Photochem Photobiol B 36: 87-10 0
2. Armstrong GA, Runge S, Frick G, Sperling U, Apel K (1995) Identification of NADPH: protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol 108: 1505-1517
3. Baker ME (1994) Protochlorophyllide reductase is homologous to human carbonyl reductase and pig 20β-hydroxysteroid dehydrogenase. Biochem J 300: 605-607
4. 2 fixation by non-heterocystous cyanobacteria. FEMS Microbiol Rev 19: 139-185
5. Berkner LV, Marshall LC (1965) On the origin and rise of oxygen concentration in the Earth's atmosphere. J Atmos Sci 22:225-261
6. Blankenship R (2001) Molecular evidence for the evolution of photosynthesis. Trends Plant Sci 6: 4-6
7. Bulen WA, Burns RC, LeComte JR (1965) Nitrogen fixation: hydrosulfite as electron donor with cell-free preparations of Azotobacter vinelandii and Rhodospirillum rubrum. Proc Natl Acad Sci USA 53: 532-539
8. Burke DH, Hearst JE, Sidow A (1993) Early evolution of photosynthesis: clues from nitrogenase and chlorophyll iron proteins. Proc Natl Acad Sci USA 90: 7134-7138
9. Cahoon AB, Timko MP (2000) yellow-in-the-dark mutants of Chlamydomonas lack the CHLL subunit of light-independent protochlorophyllide reductase. Plant Cell 12: 559-568
10. Cahoon AB, Timko MP (2003) Biochemistry and regulation of chlorophyll biosynthesis. In AW Larkum, SE Douglas JA Raven, eds, Photosynthesis in Algae. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 95-131
11. Christiansen J, Dean DR, Seeleldt LC (2001) Mechanistic features of the Mo-containing nitrogenase. Annu Rev Plant Physiol Plant Mol Biol 52: 269-295
12. Forreiter C, Apel K (1993) Light-independent and light-dependent protochlorophyllide-reducing activities and two distinct NADPH- protochlorophyllide oxidoreductase polypeptides in mountain pine (Pinus mugo). Planta 190: 536-545
13. Fujita Y (1996) Protochlorophyllide reduction: a key step in the greening of plants. Plant Cell Physiol 37: 411-421
14. Fujita Y (2002) Chlorophylls. In Encyclopedia of Life Sciences, Vol 4. Macmillan Publishers Ltd, Nature Publishing Group, London, pp 324-335
15. Fujita Y, Bauer CE (2000) Reconstitution of light-independent protochlorophyllide reductase from purified BchL and BchN-BchB subunits. In vitro confirmation of nitrogenase-like features of a bacteriochlorophyll biosynthesis enzyme. J Biol Chem 275: 23583-23588
16. Fujita Y, Bauer CE (2003) The light-independent protochlorophyilide reductase: a nitrogenase-like enzyme catalyzing a key reaction for greening in the dark. In KM Kadish, KM Smith, R Guilard, eds, Porphyrin Handbook, Vol 13, Chlorophylls and Bilins: Biosynthesis, Synthesis, and Degradation. Academic Press, San Diego, pp 109-156
17. Fujita Y, Takagi H, Hase T (1996) Identification of the chlB gene and the gene product essential for the light-independent chlorophyll biosynthesis in the cyanobacterium Plectonema boryanum. Plant Cell Physiol 37: 313-323
18. Fujita Y, Takagi H, Hase T (1998) Cloning of the gene encoding a protochlorophyllide reductase: the physiological significance of the co-existence of light-dependent and -independent protochlorophyllide reduction systems in the cyanobacterium Plectonema boryanum. Plant Cell Physiol 39: 177-185
19. Fujita Y, Takahashi Y, Kohchi T, Ozeki H, Ohyama K, Matsubara H (1989) Identification of a novel nifH-like (frxC) protein in chloroplasts of the liverwort Marchantia polymorpha. Plant Mol Biol 13: 551-561
20. Fujita Y, Takahashi Y, Shonai F, Ogura Y, Matsubara H (1991) Cloning, nucleotide sequences and differential expression of the nifH and nifH-like (fnxC) genes from the filamentous nitrogen-fixing cyanobacterium Plectonema boryanum. Plant Cell Physiol 32: 1093-1106
21. Fusada N, Masuda T, Kuroda H, Shiraishi T, Shimada H, Ohta H, Takamiya K (2000) NADPH-protochlorophyllide oxidoreductase in cucumber is encoded by a single gene and its expression is transcriptionally enhanced by illumination. Photosynth Res 64: 147-154
22. 2. New Phytol 122: 571-609
23. Galperin MY, Walker DR, Koonin EV (1998) Analogous enzymes: independent inventions in enzyme evolution. Genome Res 8: 779-790
24. Gardner PR (1997) Superoxide-driven aconitase Fe-S center cycling. Biosci Rep 17: 33-42
25. Gill SC, von Hippel PH (1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182: 319-326
26. Griffiths WT (1991) Protochlorophyllide photoreduction. In H Scheer, ed, Chlorophylls. CRC Press, Boca Raton, FL, pp 433-449
27. Grula JW (2005) Evolution of photosynthesis and biospheric oxygenation contingent upon nitrogen fixation? Int J Astrobiol 4: 251-257
28. Heyes DJ, Ruban AV, Hunter CN (2003) Protochlorophyllide oxidoreductase: 'dark' reactions of a light-driven enzyme. Biochemistry 42: 523-528
29. Hill S (1988) How is nitrogenase regulated by oxygen? FEMS Microbiol Rev 34: 111-130
30. Holtorf H, Reinbothe S, Reinbothe C, Bereza B, Apel K (1995) Two routes of chlorophyllide synthesis that are differentially regulated by light in barley (Hordeum vulgare L.). Proc Natl Acad Sci USA 92: 3254-3258
31. Igarashi RY, Seefeldt LC (2003) Nitrogen fixation: the mechanism of the Mo-dependent nitrogenase. Crit Rev Biochem Mol Biol 38: 351-381
32. Jergensen BB, Revsbech NP, Blackburn H, Cohen Y (1979) Diurnal cycle of oxygen and sulfide microgradients and microbial photosynthesis in a cyanobacterial mat sediment. Appl Environ Microbiol 38: 46-58
33. Jörnvall H, Persson B, Krook M, Atrian S, González-Duarte R, Jeffery J, Ghosh D (1999) Short-chain dehydrogenases/reductases (SDR). Biochemistry 34: 6003-6013
34. Kada S, Koike H, Satoh K, Hase T, Fujita Y (2003) Arrest of chlorophyll synthesis and differential decrease of photosystems I and II in a cyanobacterial mutant lacking light-independent protochlorophyllide reductase. Plant Mol Biol 51: 225-235
35. Kasting JF (1987) Theoretical constraints on oxygen and carbon dioxide concentrations in the Precambrian atmosphere. Precambrian Res 34: 205-229
36. Kasting JF (1992) Models relating to Proterozoic atmosphere and ocean chemistry. In JM Schopf, C Klein, eds, The Proterozoic Biosphere: A Multidisciplinary Study. Cambridge University Press, New York, pp 1185-1187
37. Keeley JE (1988) Photosynthesis in Quillworts, or why are some aquatic plants similar to cacti? Plants Today 1: 127-132
38. 4-photosynthetic-cell-specific ferredoxins. EMBO J19: 5041-5050
39. Knoll AH (2003) The geological consequences of evolution. Geobiology 1: 3-14
40. Labesse G, Vidal-Cros A, Chomilier J, Gaudry M, Mornon JP (1994) Structural comparisons lead to the definition of a new superfamily of NAD(P)(H)-accepting oxidoreductases: the single-domain reductases/epimerases/ dehydrogenases. Biochem J 304: 95-99
41. Layer G, Heinz DW, Jahn D, Schubert WD (2004) Structure and function of radical SAM enzymes. Curr Opin Chem Biol 8: 468-476
42. Lebedev N, Timko MP (1999) Protochlorophyllide oxidoreductase B-catalyzed protochlorophyllide photoreduction in vitro: insight into the mechanism of chlorophyll formation in light-adapted plants. Proc Natl Acad Sci USA 96: 9954-9959
43. Masuda T, Takamiya K (2004) Novel insight into the enzymology, regulation and physiological functions of light-dependent protochlorophyllide oxidoreductase in angiosperms. Photosynth Res 81: 1-29
44. Misra HS, Khairnar NP, Mahajan SK (2003) An alternate photosynthetic electron donor system for PSI supports light dependent nitrogen fixation in a non-heterocystous cyanobacterium, Plectonema boryanum. J Plant Physiol 160: 33-39
45. Misra HS, Tuli TS (2000) Differential expression of photosynthesis and nitrogen fixation genes in the cyanobacterium Plectonema boryanum. Plant Physiol 122: 731-736
46. Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, Tsuchiya T, Sasamoto S, Watanabe A, Kawashima K, Kishida Y, et al (2003) Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Res 10:137-145
47. Nomata J, Kitashima M, Inoue K, Fujita Y (2006a) Nitrogenase Fe protein-like Fe-S cluster is conserved in L-protein (BchL) of dark-operative protochlorophyllide reductase from Rhodobacter capsulatus. FEBS Lett (in press)
48. Nomata J, Mizoguchi T, Tamiaki H, Fujita Y (2006b) A second nitrogenase-like enzyme for bacteriochlorophyll biosynthesis: reconstitution of chlorophyllide α reductase with purified X-protein (BchX) and YZ-protein (BchY-BchZ) from Rhodobacter capsulatus. J Biol Chem 281:15021-15028
49. Nomata J, Swem LR, Bauer CE, Fujita Y (2005) Overexpression and characterization of dark-operative protochlorophyllide reductase from Rhodobacter capsulatus. Biochim Biophys Acta 1708: 229-237
50. Oelze J (2000) Respiratory protection of nitrogenase in Azotobacter species: Is a widely held hypothesis unequivocally supported by experimental evidence? FEMS Microbiol Rev 24: 321-333
51. Oosawa N, Masuda T, Awai K, Fusada N, Shimada H, Ohta H, Takamiya K (2000) Identification and light-induced expression of a novel gene of NADPH: protochlorophyllide oxidoreductase isoform in Arabidopsis thaliana. FEBS Lett 474: 133-136
52. Ouchane S, Steunou AS, Picaud M, Astier C (2004) Aerobic and anaerobic Mg-protoporphyrin monomethyl ester cyclases in purple bacteria. J Biol Chem 279: 6385-6394
53. Peschek GA, Hinterstoisser B, Pineau B, Missbichler A (1989a) Light independent NADPH-protochlorophyllide oxidoreductase activity in purified plasma membrane from the cyanobacterium Anacystis nidulans. Biochem Biophys Res Commun 162: 71-78
54. Peschek GA, Hinterstoisser B, Wastyn M, Kuntner O, Pineau B, Missbichler A, Lang J (1989b) Chlorophyll precursors in the plasma membrane of a cyanobacterium, Anacystis nidulans. Characterization of protochlorophyllide and chlorophyllide by spectrophotometry, spectrofluorimetry, solvent partition, and high performance liquid chromatography. J Biol Chem 264: 11827-11832
55. Porta RJ (1991) Recent progress in porphyrin and chlorophyll biosynthesis. In H Scheer, ed, Chlorophylls. CRC Press, Boca Raton, FL, pp 587-612
56. Rai AN, Borthakur M, Bergman B (1992) Nitrogenase derepression, its regulation and metabolic changes associated with diazotrophy in the non-heterocystous cyanobacterium Plectonema boryanum PCC 73110. J Gen Microbiol 138: 481-491
57. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21: 541-554
58. Rees DC, Howard JB (2000) Nitrogenase: standing at the crossroad. Curr Opin Chem Biol 4: 559-566
59. Reinbothe S, Reinbothe C, Apel K, Lebedev N (1996) Evolution of chlorophyll biosynthesis-the challenge to survive photooxidation. Cell 86: 703-705
60. Rüdiger W (2003) The last steps of chlorophyll synthesis. In KM Kadish, KM Smith, R Guilard, eds, Porphyrin Handbook, Vol 13, Chlorophylls and Bilins: Biosynthesis, Synthesis, and Degradation. Academic Press, San Diego, pp 71-108
61. Runnegar B (1991) Precambrian oxygen levels estimated from the biochemistry and physiology of early eukaryotes. Palaeogeogr Palaeoclimatol Palaeoecol 97: 97-111
62. Rye B, Holland HD (1998) Paleosols and the evolution of atmospheric oxygen: a critical review. Am J Sci 298: 621-672
63. Sganga MW, Bauer CE (1992) Regulatory factors controlling photosynthetic reaction center and light-harvesting gene expression in Rhodobacter capsulatus. Cell 68: 945-54
64. Sundqvist C, Dahlin C (1997) With chlorophyll from prolamellar bodies to light-harvesting complexes. Physiol Plant 100: 748-759
65. Tomitani A, Knoll AH, Cavanaugh CM, Ohno T (2006) The evolutionary diversification of cyanobacteria: molecular-phylogenetic and paleontological perspectives. Proc Natl Acad Sci USA 103: 5442-5447
66. von Wettstein D, Gough S, Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7: 1039-1057
67. Varghese S, Tang Y, Imlay JA (2003) Contrasting sensitivity of Escherichia coli aconitases A and B to oxidation and iron depletion. J Bacteriol 185: 221-230
68. Weare NM, Benemann JR (1974) Nitrogenase activity and photosynthesis in Plectonema boryanum. J Bacteriol 119: 258-265
69. Whitton BA, Potts M (2000) Introduction to the cyanobacteria. In BA Whitton, M Potts, eds, The Ecology of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 1-11
70. Wolk CP (2000) Heterocyst formation in Anabaena. In YV Brun, LJ Shimkets, eds, Prokaryotic Development. American Society of Microbiology, Washington, DC, pp 83-104
71. Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724r-1730
72. Yang J, Cheng Q (2004) Origin and evolution of the light-dependent protochlorophyllide oxidoreductase (LPOR) genes. Plant Biol 6:537-544