Protochlorophyllide photoreduction

Photosynthesis Research

Volumn 58, Issue 1, 1998, Pages 5-23

  Lebedev, Nikolai ^a   Timko, Michael P ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Chlorophyll biosynthesis; Chloroplast development gene expression; Light regulation; Plant enzymes

Indexed keywords

EID: 0032418272     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006082119102     Document Type: Short Survey

References (159)

1. Adamson HY, Hiler RG and Walmsley J (1997) Protochlorophyllide reduction and greening in angiosperms: An evolutionary perspective. J Photochem Photobiol B Biol 41: 201-221
2. Apel K (1981) The protochlorophyllide holochrome of barley (Hordeum vulgare L.). Phytochrome-induced decrease of translatable mRNA coding for the NADPH: Protochlorophyllide oxidoreductase. Eur J Biochem 120: 89-93
3. Apel K, Gollmer I and Batschauer A (1983) The light-dependent control of chloroplast development in barley (Hordeum vulgare L). J Cell Biochem 23: 181-189
4. Apel K, Santel HJ, Redlinger TE and Falk H (1980) The protochlorophyllide holochrome of barley (Hordeum vulgare L.). Isolation and characterization of the NADPH:protochlorophyllide oxidoreductase. Eur J Biochem 111:251-258
5. Argyroudi-Akoyunoglou JH and Prombona A (1996) Light-independent endogenous circadian rhythm in the capacity for chlorophyll formation. J Photochem Photobiol B Biol 36: 271-277
6. Armstrong GA, Runge S, Frick G, Sperling U and 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
7. Artus NN, Ryberg M, Lindsten A, Ryberg H and Sundqvist C (1992) The shibata shift and the transformation of etioplasts to chloroplasts in wheat with clomazone (FMC 57020) and amiprophos-methyl (Tokunol M). Plant Physiol 98: 253-263
8. Baker ME (1994) Protochlorophyllide reductase is homologous to human carbonyl reductase and pig 20 beta-hydroxysteroid dehydrogenase. Biochem J 300: 605-607
9. Barnes SA, Nishizawa NK, Quaggio RB, Whitelam GC and Chua NH (1996) Far-red light blocks greening of Arabidopsis seedlings via a phytochrome A-mediated change in plastid development. Plant Cell 8: 601-615
10. Batschauer A and Apel K (1984) An inverse control by phytochrome of the expression of two nuclear genes in barley (Hordeum vulgare L.). Eur J Biochem 143: 593-597
11. Bauer CE, Bollivar DW and Suzuki JY (1993) Genetic analyses of photopigment biosynthesis in eubacteria: A guiding light for algae and plants. J Bacteriol 175: 3919-3925
12. Bauer CE Buggy JJ Yang Z and Marrs BL (1991) The superoperonal organization of genes for pigment biosynthesis and reaction center proteins is a conserved feature in Rhodobacter sphaeroides: Analysis of overlapping bchB and puhA transcripts. Mol Gen Genet 228: 433-444
13. Beer NS and Griffiths WT (1981) Purification of the enzyme NADPH: protochlorophyllide oxidoreductase. Biochem J 195: 83-92
14. Begley TP and Young H (1988) Protochlorophyllide reductase. 1. Determination of the regiochemistry and the stereochemistry of the reduction of protochlorophyllide to chlorophyllide. J Am Chem Soc 111:3095-3096
15. Belanger FC and Rebeiz CA (1980) Chloroplasts biogenesis: detection of divinylprotochlorophyllide ester in higher plants. Biochemistry 19: 4875-4883
16. Belanger FC, Duggan JX and Rebeiz CA (1982) Chloroplast biogenesis. Identification of chlorophyllide a (E458F674) as a divinyl chlorophyllide a. J Biol Chem 257: 4849-4858
17. Belyaeva OB and Litvin FF (1980) New intermediate reactions in the process of protochlorophyllide photoreduction Biofizika 25: 617-623
18. Benli M, Schulz R and Apel K (1991) Effect of light on the NADPH-protochlorophyllide oxidoreductase of Ambidopsis thaliana. Plant Mol Biol 16: 615-625
19. Birve SJ, Selstam E and Johansson LBA (1996) Secondary structure of NADPH: protochlorophyllide oxidoreductase examined by circular dichroism and prediction methods. Biochem J 317: 549-555
20. Boddi B, Soos J and Lang F (1980) Protochlorophyll forms with different molecular arrangements. Biochim Biophys Acta 593: 158-165
21. Boddi B, Evertsson I Ryberg M and Sundqvist C (1996) Protochlorophyllide transformations and chlorophyll accumulation in epicotyls of pea (Pisum sativum). Physiol Planta 96: 706-713
22. Boddi B, Ryberg M and Sundqvist C (1991) The formation of a short-wavelength chlorophyllide form at partial phototransformation of protochlorophyllide in etioplast inner membranes. Photochem Photobiol 53: 667-674
23. Boddi B, Ryberg M and Sundqvist C (1993) Analysis of the 77 K fluorescence emission and excitation spectra of isolated etioplast inner membranes. J Photochem Photobiol B Biol 21: 125-133
24. Boddi B, Ryberg M and Sundqvist C (1992) Identification of four universal protochlorophyllide forms in dark-grown leaves by analyses of the 77 K fluorescence emission spectra. J Photochem Photobiol B Biol 12: 389-401
25. Bogorad L (1950) Faktors associated with the synthesis of chlorophyll in the dark in seedlings of Pinus jeffreyi. Bot Gaz 111: 221-241
26. Burke DH, Alberti M and Hearst JE (1993a) bchFNBH Bacteriochlorophyll synthesis genes of Rhodobacter sphaeroides and identification of the third subunit of light-independent protochlorophyllide reductase in bacteria and plants. J Bacteriol 175: 2414-2422
27. Burke DH, Hearst JE and Sidow A (1993b) Early evolution of photosynthesis: Clues from nitrogenase and chlorophyll iron proteins. Proc Natl Acad Sci USA 90: 7134-7138
28. Chereskin BM, Castelfranco PA, Dallas JL and Straub KM (1983) Mg-2,4-divinyl pheoporphyrin a5: The product of a reaction catalyzed in vitro by developing chloroplasts. Arch Biochem Biophys 226: 10-18
29. Coomber SA, Chaudhri M, Connor A, Britton G and Hunter CN (1990) Localised transposon TnS mutagenesis of the photosynthetic gene claster of Rhodobacter sphaeroides. Mol Microbiol 4: 977-989
30. Dahlin C, Sundqvist C and Timko MP (1995) The in vitro assembly of the NADPH-protochlorophyllide oxidoreductase in pea chloroplasts. Plant Mol Biol 29: 317-330
31. Darrah PM, Kay SA, Teakle GR and Griffiths WT (1990) Cloning and sequencing of protochlorophyllide reductase. Biochem J 265: 789-798
32. Denev ID and Minkov IN (1997) Use of fluorescence probes 1-aniline-8-naphthalene sulfonate and pyrene for studying the localisation of proteins in inner membranes from wheat etioplasts. Photosynthetica 33: 303-312
33. Durchan M and Lebedev NN (1995) Changes in the near UV fluorescence excitation spectrum during protochlorophyllide photoreduction in etiolated cucumber cotyledons. Photosynthetica 31:599-611
34. Eichacker LA, Soll J, Lauterbach P, Rudiger W, Klein RR and Mullet JE (1990) In vitro synthesis of chlorophyll a in the dark triggers accumulation of chlorophyll a apoproteins in barley etioplasts. J Biol Chem 265: 13566-13571
35. Eullaffroy P and Popovic R (1997) Effect of heat treatment on protochlorophyllide phototransformation initiated by different light intensities. J Plant Physiol 151: 293-298
36. Forreiter C and 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
37. Forreiter C, Van Cleve B, Schmidt A and Apel K (1991) Evidence for a general light-dependent negative control of NADPH-protochlorophyllide oxidoreductase in angiosperms. Planta 183: 126-132
38. Fradkin LI, Domanskaya IN, Radyuk MS, Domanskii VP and Kolyago VM (1993) Effect of benzyladenine and irradiance on energy transfer from precursor to chlorophyll in greening barley leaves. Photosynthetica 29: 227-234
39. Franck F and Strzalka K (1992) Detection of the photoactive protochlorophyllide-protein complex in the light during the greening of barley. FEBS Lett 309: 73-77
40. Franck F, Barthelemy X and Strzalka K (1993) Spectroscopic characterization of protochlorophyllide photoreduction in the greening leaf. Photosynthetica 29: 185-194
41. Fujita Y (1996) Protochlorophyllide reduction: A key step in the greening of plants. Plant Cell Physiol 37: 411-421
42. Fujita Y, Takahashi Y, Shonai F, Ogura Y and Matsubara H (1991) Cloning, nucleotide sequences and diffirential expression of the nifH and nifH-like (frxC) genes from the filamentous nitrogen-fixing bacterium Plectonema boryanum. Plant Cell Physiol 32: 1093-1106
43. Gassman ML (1973) Absorbance and fluorescence properties of protochlorophyllide in etiolated bean leaves. Biochem Biophys Res Commun 53: 693-702
44. Griffiths WT (1975) Characterization of the terminal stages of chlorophyll (ide) synthesis in etioplast membrane preparations. Biochem J 152: 623-655
45. Griffiths WT (1978) Reconstitution of chlorophyllide formation by isolated etioplast membranes. Biochem J 174: 681-692
46. Griffiths WT (1980) Substrate-specificity studies on protochlorophyllide reductase in barley (Hordeum vulgare) etioplast membranes. Biochem J 186: 267-278
47. Griffiths WT (1991) Protochlorophyllide photoreduction. In: Scheer H (ed) Chlorophylls, pp 433-449. CRC Press, Boca Raton, FL
48. Griffiths WT, McHugh T and Blankenship RE (1996) The light intensity dependence of protochlorophyllide photoconversion and its significance to the catalytic mechanism of protochlorophyllide reductase. FEBS Lett 398: 235-238
49. Hauser I, Dehesh K and Apel K (1984) The proteolytic degradation in vitro of the NADPH-protochlorophyllide oxidoreductase of barley (Hordeum vulgare L.). Arch Biochem Biophys 228: 577-586
50. He ZH, Li J, Sundqvist C and Timko MP (1994) Leaf developmental age controls expression of genes encoding enzymes of chlorophyll and heme biosynthesis in pea (Pisum sativum L.). Plant Physiol 106: 537-546
51. Helfrich M, Schoch S, Schafer W, Ryberg M and Rudiger W (1996) Absolute configuration of protochlorophyllide a and substrate specificity of NADPH-protochlorophyllide oxidoreductase. J Am Chem Soc 118: 2606-2611
52. Hinterstoisser B, Cichna M, Kuntner O and Peschek GA (1993) Cooperation of plasma and thylakoid membranes for the biosynthesis of chlorophyll in cyanobacteria: The role of the thylakoid centers. J Plant Physiol 142: 407-413
53. Holtorf H and Apel K (1996a) Transcripts of the two NADPH protochlorophyllide oxidereductase genes PorA and PorB are differentially degraded in etiolated barley seedlings. Plant Mol Biol 31: 387-392
54. Holtorf H and Apel K (1996b) The regulation of NADPH-protochlorophyllide oxidoreductases a and b in green barley plants kept under a diural light dark cycle. Planta 199: 289-295
55. Holtorf H, Reinbothe S, Reinbothe C, Bereza B and 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
56. Honda T, Tanaka A and Tsuji H (1994) Proteolytic activity in intact barley etioplasts: Endoproteolysis of NADPH-protochlorophyllide oxidoreductase protein. Plant Sci 97: 129-135
57. Ignatov NV and Litvin FF (1981) Energy migration in a pigmented protochlorophyllide complex. Biofizika 26: 664-668
58. Ignatov NV and Litvin FF (1995a) Light-regulated pigment interconversion in pheophytin/chlorophyll-containing complexes formed during plant leaves greening. Photosynth Res 46: 445-453
59. Ignatov NV and Litvin FF (1995b) Biosynthesis of Photosystem I core chlorophyll in a greening mutant of Chlorella vulgaris. Biochemistry-Russia 60: 1429-1438
60. 2O) on reactions of chlorophyll biosynthesis in greening plant leaves. Biochemistry-Russia 62: 312-320
61. Ignatov NV and Litvin FF (1994) Photoinduced formation of pheophytin/chlorophyll-containing complexes during the greening of plant leaves. Photosynth Res 42: 27-35
62. Ignatov NV, Belayeva OB and Litvin FF (1993a) Low temperature phototransformations of protochlorophyll(ide) in etiolated leaves. Photosynth Res 38: 117-124
63. Ignatov NV, Belyaeva OB and Litvin FF (1993b) Possible role of flavin components of protochlorophyllide-protein complexes in primary processes of protochlorophyllide photoreduction in etiolated plant leaves. Photosynthetica 29: 235-241
64. Joyard J, Block M, Pineau B, Albrieux C and Douce R (1990) Envelope membranes from mature spinach chloroplasts contain a NADPH:protochlorophyllide reductase on the cytosolic side of the outer membrane. J Biol Chem 265: 21820-21827
65. Kahn A, Boardman NK and Thorne SW (1970) Energy transfer between protochlorophyllide molecules: Evidence for multiple chromophores in the photoactive protochlorophyllide-protein complex in vivo and in vitro. J Mol Biol 48: 85-101
66. Klein RR (1991) Regulation of light-induced chloroplast transcription and translation in eight-day-old dark-grown barley seedlings. Plant Physiol 97: 335-342
67. Klein RR and Mullet JE (1986) Regulation of chloroplast-encoded chlorophyll-binding protein translation during higher plant chloroplast biogenesis. J Biol Chem 261: 11138-11145
68. Knaust R and Senger H (1994) Monovinyl and divinyl protochlorophyll in different stages of esterification isolated from mutant C-2A' of the unicellular green alga Scenedesmus obliquus. Physiol Planta 90: 490-496
69. Knaust R, Seyfried B, Schmidt L, Schulz R and Senger H (1993) Phototransformation of monovinyl and divinyl protochlorophyllide by NADPH:protochlorophyllide oxidoreductase of barley expressed in Escherichia coli. J Photochem Photobiol B Biol 20: 161-166
70. Kohchi T, Shirai H, Fukuzawa H, Sano T, Komano T, Umesono K, Inokuchi H, Ozeki H and Ohyama K (1988) Structure and organization of the Marchantia polymorpha chloroplast genome. IV. Inverted repeat and single copy regions. J Mol Biol 203: 353-372
71. Kuroda H, Masuda T, Ohta H, Shioi Y and Takamiya K (1995) Light-enhanced gene expression of NADPH-protochlorophyllide oxidoreductase in cucumber. Biochem Biophys Res Commun 210: 310-316
72. Kuroda H, Masuda T, Ohta H, Shioi Y and Takamiya K (1996) Effects of light, developmental age and phytohormones on the expression of the gene encoding NADPH-protochlorophyllide oxidoreductase in cucumis sativus. Plant Physiol Biochem 34: 17-22
73. Labesse G, Vidal-Cros A, Chomilier J, Gaudry M and 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 (the 'RED' family). Biochem J 304: 95-99
74. Lebedev N (1996) Fluorescence analysis of protochlorophyll(ide) to chlorophyll(ide) conversion in the green alga Chlamydomonas reinhardtii mutants. Photosynthetica 32: 569-585
75. Lebedev NN and Barskaya IV (1989) Fluorescence of the reaction center of Photosystem II in cells of green alga Chlamydomonas reinhardtii. FEBS Lett 255: 248-252
76. Lebedev NN and Dujardin E (1993) Energy transfer from NADPH to protochlorophyllide in isolated protochlorophyllide holochrome as determined by fluorescence excitation spectropy Z Naturforsch 48c: 402-405
77. Lebedev NN and Dzhelepova ID (1991) Chemical control of monomeric pigment fluorescence in Chlamydomonas reinhardtii cells. Biokhimiya 56: 1495-1502
78. Lebedev NN, Siffel P and Krasnovskii AA (1985) Detection of protocholorphyllide forms in irradiated green leaves and chloroplasts by difference fluorescence spectroscopy at 77K. Photosynthetica 19: 183-187
79. Lebedev NN, Pakshina EV, Bolychevtseva YuB and Karapetyan NV (1988) Fluorescence characterization of chlorophyll-proteins in barley seedlings grown with the herbicide - norflurazon under low irradiance. Photosynthetica 22: 371-376
80. Lebedev NN, Ni CV and Krasnovskii AA (1989) Reversible reorganization of the chlorophyll-protein complexes of Photosystem II in cyanobactrium cells in the dark. FEBS Lett 247: 97-100
81. Lebedev NN, Nozdrina VN and Filippovich II (1990) Location of chlorophyll alpha and beta synthesis in etiochloroplast membrane. Photosynthetica 24: 563-571
82. Lebedev NN, Dzhelepova ID and Krasnovskii AA (1991a) Fluorescence of protochlorophyllide in the cells of green alga Chlamydomonas reinhardtii. Biofizika 36: 1022-1029
83. Lebedev NN, Krasnovsky AA Jr. and Litvin FF (1991b) Phosphorescence of protochlorophyll(ide) and chlorophyll(ide) in etiolated and greening bean leaves: Assignment of spectral bands. Photosynth Res 30: 7-14
84. Lebedev N, VanCleve B, Armstrong G and Apel K (1995) Chlorophyll synthesis in a deetiolated-(DET340) mutant of Arabidopsis without NADPH-protochlorophyllide (PChlide) oxidoreductase (POR) a and photoactive PChlide-F655. Plant Cell 7: 2081-2090
85. Li J and Timko MP ( 1996) The pc-1 phenotype of Chlamydomonas reinhardtii results from a deletion mutation in the nuclear gene for NADPH:protochlorophyllide oxidoreductase. Plant Mol Biol 30: 15-37
86. Li J, Goldschmidt-Clermont M and Timko MP (1993) Chloroplast encoded chlB is required for light-independent protochlorophyllide reductase activity in Chlamydomonas reinhardtii. Plant Cell 5:1817-1829
87. Lidholm J and Gustafsson P (1991) Homologues of the green algal gidA gene and the liverwort frxC gene are present in the chloroplast genomes of conifers. Plant Mol Biol 17: 787-798
88. Litvin FF and Belyaeva OB (1971) Sequence of photochemical and dark reactions in the terminal stage of chlorophyll biosynthesis. Photosynthetica 5: 200-209
89. Litvin FF and Krasnovskii AA (1957) Anlysis of intermediate steps for chlorophyll formation in etiolated leaves by fluorescence spectrocopy. Doklady AN SSSR 117: 106-109
90. Lutz C, Roper U, Beer NS and Griffiths T (1981) Sub-etioplast localization of the enzyme NADPH:protochlorophyllide oxidoreductase. Eur J Biochem 118: 347-353
91. Mapleston RE and Griffiths WT (1980) Light modulation of the activity of protochlorophyllide reductase. Biochem J 189: 125-133
92. Marrison JL, Schunmann PHD, Ougham HJ and Leech RM (1996) Subcellular visualization of gene transcripts encoding key proteins of the chlorophyll accumulation process in developing chloroplasts. Plant Physiol 110: 1089-1096
93. Martin GEM Timko MP and Wilks HM (1997) Purification and kinetic analysis of pea (Pisum sativum L.) NADPH-protochlorophyllide oxidoreductase expressed as a fusion with maltose-binding protein in Escherichia coli. Biochem J 325: 139-145
94. Mathis P and Sauer K (1972) Circular dichroism studies on the structure and the photochemistry of protochlorophyllide and chlorophyllide holochrome. Biochim Biophys Acta 267: 498-511
95. McCormac DJ, Marwood CA, Bruce D and Greenberg BM (1996) Assembly of Photosystem I and II during the early phases of light-induced development of chloroplasts from proplastids in Spirodela oligorrhiza. Photochem Photobiol 63: 837-845
96. McEwen B, Seyyedi M, Younis S and Sundqvist C (1996) Formation of short-wavelength chlorophyll(ide) after brief irradiation is correlated with the occurrence of protochlorophyll(ide)(636-642) in dark-grown epi- and hypocotyls of bean (Phaseolus vulgaris). Physiol Planta 96: 51-58
97. Minkov I and Denev I (1992) Changes in the microviscosity of the lipid bilayer of internal etioplast membranes accompanying light-induced reduction of the protochlorophyllide. Fiziologiya Na Rasteniyata 18: 13-17
98. Mosinger E, Batschauer A, Schafer E and Apel K (1985) Phytochrome control of in vitro transcription of specific genes in isolated nuclei from barley (Hordeum vulgare). Eur J Biochem 147: 137-142
99. Nayar P and Begley TP (1996) Protochlorophyllide reductase. Ill: Synthesis of a protochlorophyllide-dihydroflavin complex. Photochem Photobiol 63: 100-105
100. OgawaM and Konishi M (1979) Kinetics of photoconversion of protochlorophyllide 649 to chlorophyllide 676 at low temperature in etiolated cotyledons of Pharbitis nil. Biochim Biophys Acta 548: 119-127
101. Oliver RP and Griffiths WT (1980) Identification of the polypeptides of NADPH-protochlorophyllide oxidoreductase. Biochem J 191: 277-280
102. Oliver RP and Griffiths WT (1981) Covalent labelling of the NADPH: protochlorophyllide oxidoreductase from etioplast membranes with (3H)N-phenylmaleimide. Biochem J 195: 93-101
103. Parham R and Rebeiz CA (1992) Chloroplast biogenesis: (4-Vinyl)chlorophyllide a reductase is a divinyl chlorophyllide a-specific, NADPH-dependent enzyme. Biochemistry 31: 8460-8464
104. Pineau B, Dubertret G, Joyard J and Douce R (1986) Fluorescence properties of the envelope membranes from spinach chloroplasts. Detection of protochlorophyllide. J Biol Chem 261: 9210-9215
105. Pineau B, Gerard-Hirne C, Douce R and Joyard J (1993) Identification of the main species of tetrapyrrolic pigments in envelope membranes from spinach chloroplasts. Plant Physiol 102: 821-828
106. Porra RJ (1997) Recent progress in porphyrin and chlorophyll biosynthesis. Photochem Photobiol 65: 492-516
107. Raskin VI (1977) Energy transfer among pigment molecules in the course of protochlorophyllide reduction. Dokl Akad Nauk BSSR 21: 272-275
108. Reinbothe C, Apel K and Reinbothe S (1995) A light-induced protease from barley plastids degrades NADPH:protochlorophyllide oxidoreductase complexed with chlorophyllide. Mol Cell Biol 15: 6206-6212
109. Reinbothe C, Lebedev N, Apel K and Reinbothe S (1997) Regulation of chlorophyll protein import through a protochlorophyllide responsive transit peptide. Proc Natl Acad Sci 94: 8890-8894
110. Reinbothe S and Reinbothe C (1996a) The regulation of enzymes involved in chlorophyll biosynthesis. Eur J Biochem 237: 323-343
111. Reinbothe S and Reinbothe C (1996b) Regulation of chlorophyll biosynthesis in angiosperms. Plant Physiol 111: 1-7
112. Reinbothe S, Reinbothe C, Runge S and Apel K (1995a) Enzymatic product formation impairs both the chloroplast receptor-binding function as well as translocation competence of the NADPH:protochlorophyllide oxidoreductase, a nuclear-encoded plastid precursor protein. J Cell Biol 129: 299-308
113. Reinbothe S, Runge S, Reinbothe C, Van Cleve B and Apel K (1995b) Substrate-dependent transport of the NADPH:protochlorophyllide oxidoreductase into isolated plastids. Plant Cell 7: 161-172
114. Reinbothe S, Reinbothe C, Holtorf H and Apel K (1995c) Two nadph-protochlorophyllide oxidoreductases in barley - evidence for the selective disappearance of PORa during the light-induced greening of etiolated seedlings. Plant Cell 7: 1933-1940
115. Reinbothe S, Reinbothe C, Lebedev N and Apel K (1996a) PORa and PORb, two light-dependent protochlorophyllide-reducing enzymes of angiosperm chlorophyll biosynthesis. Plant Cell 8: 763-769
116. Reinbothe S, Reinbothe C, Neumann D and Apel K (1996b) A plastid enzyme arrested in the step of precursor translocation in vivo. Proc Natl Acad Sci USA 93: 12026-12030
117. Reinbothe S, Reinbothe C, Apel K and Lebedev N (1996c) Evolution of chlorophyll biosynthesis - the challenge to survive photooxydation. Cell 86: 703-705
118. Reith M and Munholland J (1993) A high-resolution gene map of the chloroplast genome of the red alga Porphyra purpurea. Plant Cell 5: 465-475
119. Rowe JD and Griffiths WT (1995) Protochlorophyllide reductase in photosynthetic prokaryotes and its role in chlorophyll synthesis. Biochem J 311: 417-424
120. Rudiger W (1997) Chlorophyll metabolism: from outer space down to the molecular level. Phytochemistry 46: 1151-1167
121. Runge S, Sperling U, Frick G, Apel K and Armstrong GA (1996) Distinct roles for light-dependent NADPH:protochlorophyllide oxidoreductases (POR) A and B during greening in higher plants. Plant J 9: 513-523
122. Ryberg M and Sundqvist C (1991) Structural and functional significance of pigment protein complexes of chlorophyll precursors. In: Scheer H (ed) Chlorophylls, pp 587-612. CRC Press, Boca Raton, FL
123. Santel HJ and Apel K (1981) The protochlorophyllide holochrome of barley (Hordeum vulgare L.). The effect of light on the NADPH:protochlorophyllide oxidoreductase. Eur J Biochem 120: 95-103
124. Satinier RY and Cohen-Bazire G (1977) Photosynthetic procariotes: The cyanobacteria. Ann Rev Microbiol 31: 225-247
125. Schoch S, Helfrich M, Wiktorsson B, Sundqvist C, Rudiger W and Ryberg M (1995) Photoreduction of zinc protopheophorbide b with NADPH-protochlorophyllide oxidoreductase from etiolated wheat (Triticum aestivum L.). Eur J Biochem 229: 291-298
126. Schoefs B and Franck F (1993) Photoreduction of protochlorophyllide to chlorophyllide in 2-d-old dark-brown bean (Phaseolus vulgaris cv. Commodore) leaves: Comparison with 10-d-old dark-grown (etiolated) leaves. J Exp Bot 44: 1053-1057
127. Schulz R, Steinmuller K, Klaas M, Forreiter C, Rasmussen S, Hiller C and Apel K (1989) Nucleotide sequence of a cDNA coding for the NADPH-protochlorophyllide oxidoreductase (PCR) of barley (Hordeum vulgare L.) and its expression in Escherichia coli. Mol Gen Genet 217: 355-361
128. Schunmann PH and Ougham HJ (1996) Identification of three cDNA clones expressed in the leaf extension zone and with altered patterns of expression in the slender mutant of barley: A tonoplast intrinsic protein, a putative structural protein and protochlorophyllide oxidoreductase. Plant Mol Biol 31: 529-537
129. Seliskar CJ and Ke B (1968) Protochlorophyllide aggregation in solution and associated spectral changes. Biochim Biophys Acta 153: 685-691
130. Shibata K (1957) Spectroscopic studies on chlorophyll formation in intact leaves. J Biochem 44: 147-173
131. Shioi Y and Takamiya KI (1992) Monovinyl and divinyl protochlorophyllide pools in etiolated tissues of higher plants. Plant Physiol 100: 1291-1295
132. Siffel P, Lebedev NN and Krasnovskii AA (1987) Detection of short-wavelength chlorophyll a emission in green leaves. Photosynthetica 21: 23-28
133. Spano AJ, He Z, Michel H, Hunt DF and Timko MP (1992a) Molecular cloning, nuclear gene structure, and developmental expression of NADPH: protochlorophyllide oxidoreductase in pea (Pisum sativum L.). Plant Mol Biol 18: 967-972
134. Spano AJ, He Z and Timko MP (1992b) NADPH: protochlorophyllide oxidoreductases in white pine (Pinus strobus) and loblolly pine (P. taeda). Evidence for light and developmental regulation of expression and conservation in gene organization and protein structure between angiosperms and gymnos. Mol Gen Genet 236: 86-95
135. Sperling U, Frank F, vanCleve B, Frick G, Apel K and Armstrong G (1998) Etioplast differentiation in Arabidopsis: Both PORa and PORb restore the prolamellar body and photoactive protochlorophyllide - F655 to the copl photomorphogenetic mutant. Plant Cell 10: 283-296
136. Sperling U, vanCleve B, Frick G, Apel K and Armstrong G (1997) Overexpression of light-dependent PORA or PORB in plants depleted of endogenous POR by far-red light enhances seedling survival in white light and protects against photooxidative damage. Plant J 12: 649-658
137. Sundqvist C and Dahlin C (1997) With chlorophyll pigments from prolamellar bodies to light-harvesting complexes. Physiol Planta 100: 748-759
138. Suzuki JY and Bauer CE (1995) A prokaryotic origin for light-dependent chlorophyll biosynthesis of plants. Proc Natl Acad Sci USA 92: 3749-3753
139. Teakle GR and Griffiths WT (1993) Cloning, characterization and import studies on protochlorophyllide reductase from wheat (Triticum aestivum). Biochem J 296: 225-230
140. Thomas H (1997) Chlorophyll: A symptom and a regulator of plastid development. New Physiologist 136: 163-181
141. Thorne SW and Boardman NK (1972) The kinetics of photoconversion of protochlorophyllide in etiolated bean leaves. Biochim Biophys Acta 267: 104-110
142. Timko MP (1998) Pigment biosynthesis: Chlorophylls, heme, and carotenoids. In: Rochaix J-D Goldschmidt-Clermont M and Merchant S (eds) Molecular Biology of Chlamydomonas: Chloroplasts and Mitochondria. Kluwer Academic Publishers, Dordrecht, The Netherlands
143. Townley HE, Griffiths WT and Nugent JP (1998) A reappraisal of the mechanism of the photoenzyme protochlorophyllide reductase based on studies with the heterologously expressed protein. FEBS Lett 422: 19-22
144. Tripathy BC and Rebeiz CA (1986) Chloroplast biogenesis. Demonstration of the monovinyl and divinyl monocarboxylic routes of chlorophyll biosynthesis in higher plants. J Biol Chem 261: 13556-13564
145. Valera V, Fung M, Wessler AN and Richards WR (1987) Synthesis of 4R- and 4S-tritium labeled NADPH for the determination of the coenzyme stereospecificity of NADPH:protochlorophyllide oxidoreductase. Biochem Biophys Res Commun 148: 515-520
146. Vaughan GD and Sauer K (1974) Energy transfer from protochlorophyllide to chlorophyllide during photoconversion of etiolated bean holochrome. Biochim Biophys Acta 347: 383-394
147. VonWettstein D, Gough S and Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7: 1039-1057
148. Walker CJ and Griffiths WT (1988) Protochlorophyllide reductase: A flavoprotein? FEBS Lett 239: 259-262
149. Whyte BJ and Griffiths WT (1993) 8-Vinyl reduction and chlorophyll a biosynthesis in higher plants. Biochem J 291: 939-944
150. Wiktorsson B, Ryberg M, Gough S and Sundqvist C (1992) Isoelectric focusing of pigment-protein complexes solubilized from non-irradiated and irradiated prolamellar bodies. Physiol Planta 85: 659-669
151. Wiktorsson B, Engdahl S, Zhong LB, Boddi B, Ryberg M and Sundquvist C (1993) The effect of cross-linking of the subunits on NADPH-protochlorophyllide oxidoreductase on the aggregational state of protochlorophyllide. Photosynthetica 29: 205-218
152. Wiktorsson B, Ryberg M and Sundqvist C (1996) Aggregation of NADPH-protochlorophyllide oxidoreductase-pigment complexes is favoured by protein phosphorylation. Plant Physiol Biochem 34: 23-34
153. Wilks HM and Timko MP (1995) A light-dependent complementation system for analysis of NADPH:protochlorophyllide oxidoreductase: Identification and mutagenesis of two conserved residues that are essential for activity. Proc Natl Acad Sci USA 92: 724-728
154. Williams WP, Selstam E and Brain T (1998) X-ray diffraction studies of the structural organisation of prolamellar bodies isolated from Zea mays. FEBS Lett 422: 252-254
155. Wu Q and Vermaas WF (1995) Light-dependent chlorophyll a biosynthesis upon chlL deletion in wild-type and Photosystem I-less strains of the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 29: 933-945
156. Yamada K, Matsuda M, Fujita Y, Matsubara H and Sugai M (1992) A frxC homolog exists in the chloroplast DNAs from various pteridophytes and in gymnosprms. Plant Cell Physiol 33: 325-327
157. Yang Z and Bauer CE (1990) Rhodobacter capsulatus genes involved in the early steps of the bacteriochlorophyll biosynthetic pathway. J Bacteriol 172: 5001-5010
158. Younis S, Ryberg M and Sundqvist C (1995) Plastid development in germinating wheat (Triticum aestivum) is enhanced by gibberellic acid and delayed by gabaculine. Physiol Planta 95: 336-346
159. Zsebo KM and Hearst JE (1984) Genetic -physical mapping of a photosynthetic gene claster from R. capsulatus. Cell 37: 937-947