Protochlorophyllide reduction: Mechanisms and evolution

[en] Protochlorophyllide (Pchlide) reductases are key enzymes in the process of chlorophyll biosynthesis. In this review, current knowledge on the molecular organization, substrate specificity and assembly of the light-dependent reduced nicotinamide adenine dinucleotide phosphate:Pchlide oxidoreductases are discussed. Characteristics of light-independent enzymes are also described briefly, and the possible reasons for the selection of light-dependent enzymes during the course of evolution are discussed.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Schoefs, B.

Franck, Fabrice ; Université de Liège - ULiège > Département des sciences de la vie > Biochimie végétale

Language :

English

Title :

Protochlorophyllide reduction: Mechanisms and evolution

Publication date :

December 2003

Journal title :

Photochemistry and Photobiology

ISSN :

0031-8655

Publisher :

Amer Soc Photobiology, Augusta, United States - Georgia

Volume :

Issue :

Pages :

543-557

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 17 May 2010

Statistics

Number of views

69 (2 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

123

Scopus citations^®
without self-citations

115

OpenCitations

Bibliography

Begley, T. P. (1994) Photoenzymes: a novel class of biological catalysts. Acc. Chem. Res. 27, 394-401.
Morren, E. (1858) Dissertation sur les feuilles vertes et colorées envisagées du point de vue des rapports de la chlorophylle et de l'érythrophylle. University of Gand, Gand, Belgium.
Suzuki, J. Y. and C. E. Bauer (1992) Light-independent chlorophyll biosynthesis: involvement of the chloroplast gene chlL (frxC). Plant Cell 4, 929-940.
Liu, X. Q., H. Xu and C. Huang (1993) Chloroplast chlB gene is required for light-independent chlorophyll accumulation in Chlamydomonas reinhardtii. Plant Mol. Biol. 23, 297-308.
Richard, M., C. Trembley and G. Bellamare (1994) Chloroplastic genomes of Ginkgo biloba and Chlamydomonas moewusii contains a chlB gene coding one subunit of a light-independent protochlorophyllide oxidase. Curr. Genet. 26, 159-165.
Xiong, J., K. Inoue and C. E. Bauer (1998) Tracking molecular evolution of photosynthesis by characterization of a major gene cluster from Heliobacter mobilis. Proc. Natl. Acad. Sci. USA 95, 14851-14856.
Armstrong, G. A., S. Runge, G. Frick, U. Sperling and K. Apel (1995) Identification of NADPH:protochlorophyllide oxidoreductases A and B branched pathway for light-dependent chlorophyll synthesis in Arabidopsis thaliana. Plant Physiol. 108, 1505-1517.
Boardman, N. K. and J. M. Anderson (1964) Studies of greening of dark-grown plants. I. Formation of chloroplasts from proplastids. Aust. J. Biol. Sci., 17, 86-92.
Leyon, H. (1953) The structure of chloroplasts. II. The first differentiation structure of Vallota and Taraxacum studied by means of electron miscroscopy. Exp. Cell. Res. 5, 520-529.
Von Wettstein, D. (1959) Developmental changes in chloroplast and their genetic control. In Developmental Cytology (Edited by D. Rudnick), pp. 123-160. The Ronald Press Company, New York.
Ryberg, M. and C. Sundqvist (1982a) Characterization of prolamellar bodies and prothylakoids fractionated from wheat. Physiol. Plant. 56, 125-132.
Ryberg, M. and C. Sundqvist (1982b) Spectral forms of protochlorophyllide in prolamellar bodies and prothylakoids fractionated from wheat etioplasts. Physiol. Plant. 56, 133-138.
Lindsten, A., M. Ryberg and C. Sundqvist (1988) The polypeptide composition of highly purified prolamellar bodies and prothylakoids from wheat (Triticum aestivum) as revealed by silver staining. Physiol. Plant. 72, 167-176.
Shaw, P., J. Henwood, R. Oliver and W. T. Griffiths (1985) Immunogold localization of protochlorophyllide oxidoreductase in barley etioplasts. Eur. J. Cell Biol. 39, 50-55.
Ryberg, M. and K. Dehesh (1986) Localization of NADPH: protochlorophyllide oxidoreductase in dark-grown wheat (Triticum aestivum) by immuno-electron microscopy before and after transformation of the prolamellar bodies. Physiol. Plant. 66, 616-624.
Sundqvist, C. and M. Ryberg (1989) The distribution and structural role of NADPH-protochlorophyllide oxidoreductase in isolated etioplast inner membranes. Photosynthetica 23, 427-438.
Selstam, E. and A. Widell-Wigge (1989) Hydrophobicity of protochlorophyllide reductase, characterized by means of Triton X-114 partitioning of isolated etioplast membrane fractions. Physiol. Plant. 77, 401-406.
Widell-Wigge, A. and E. Selstam (1990) Effects of salt-wash on the structure of the prolamellar body membrane and the membrane binding of NADPH-protochlorophyllide oxidoreductase. Physiol. Plant. 78, 315-323.
Schulz, R., K. Steinmuller, M. Klaas, C. Forreiter, S. Rasmussen, C. Hiller and K. Apel (1989) Nucleotide sequence of 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.
Dahlin, C., C. Sundqvist and M. P. Timko (1995) The in vitro assembly of the NADPH-protochlorophyllide oxidoreductase in pea chloroplasts. Plant Mol. Biol. 29, 317-330.
Rowe, J. D. and W. T. Griffiths (1995) Protochlorophyllide reductase in photosynthetic prokaryotes and its role in chlorophyll synthesis. Biochem. J. 311, 417-424.
Selstam, E. and A. Widell (1986) Characterization of prolamellar bodies from dark-grown seedlings of Scots pine, containing light- and NADPH-dependent protochlorophyllide oxidoreductase. Physiol. Plant. 67, 345-352.
Selstam, E., A. Widell and L. B. Johansson (1987) A comparison of prolamellar bodies from wheat, Scots pine and Jeffrey pine. Pigment spectra and properties of protochlorophyllide oxidoreductase. Physiol. Plant. 70, 209-214.
Krasnovsky, A. A. and L. M. Kosobutskaya (1952) Spectral investigations of chlorophyll during its formation in plants and in colloidal solutions of material from etiolated leaves. Dokl. Akad. Nauk. SSSR 85, 177-180.
Smith, J. H. C. and A. Benitez (1953) The protochlorophyllchlorophyll transformation: the nature of protochlorophyll in leaves, Camegie Inst. Wash. Year Book 52, 151-153.
Griffiths, W. T. (1978) Reconstitution of chlorophyllide formation by isolated membranes. Biochem. J. 174, 681-692.
Franck, F., M. Ouazzani, E. Dujardin and R. Popovic (1993) Optical multichannel analysis of the protochlorophyllide phototransformation in detergent-solubilized etioplast membranes of wheat, Z. Naturforsch. 49c, 125-131.
Ouazzani Chahdi, M. A., B. Schoefs and F. Franck (1998) Isolation and characterization of photoactive complexes of NADPH:protochlorophyllie oxidoreductase from wheat. Planta 206, 673-680.
Boardman, N. K. (1966) Protochlorophyll. In The Chlorophylls (Edited by L. P. Vernon and G. R. Seely), pp. 437-479. Academic Press, New York.
Schopfer, P. and H. W. Siegleman (1968) Purification of protochlorophyllide holochrome. Plant Physiol. 43, 990-996.
Henningsen, K. W. and A. Kahn (1971) Photoactive protochlorophyllide subunits of protochlorophyll(ide) holochrome. Plant Physiol. 47, 685-690.
Canaani, O. D. and K. Sauer (1977) Analysis of the subunit structure of protochlorophyllide holochrome by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Plant Physiol. 60, 422-529.
Dujardin, E., M. Bertrand, A. Radunz and G. H. Schmid (1987) Immunological evidence for the presence of proteins of the photosynthetic membrane in etiolated leaves of Phaseolus vulgaris. J. Plant Physiol. 128, 95-107.
Oliver, R. P. and W. T. Griffiths (1980) Identification of the polypeptides of NADPH:protochlorophyllide oxidoreductase. Biochem. J. 191, 277-280.
Birve, S. J., E. Selstam and L. B. A. Johansson (1996) Secondary structure of NADPH:protochlorophyllide oxidoreductase examined by circular dichroism and prediction methods. Biochem. J. 317, 549-555.
Klement, H., M. Helfrich, U. Oster, S. Schoch and W. Rüdiger (1999) Pigment free NADPH:protochlorophyllide oxidoreductase from Avena sativa L. Purification and substrate specificity. Eur. J. Biochem. 265, 862-875.
Apel, K., H. J. Santel, T. E. Redlinger and H. Falk (1980) The protochlorophyllide holochrome of barley (Hordeum vulgare). Isolation and characterization of the NADPH: protochlorophyllide oxidoreductase. Eur. J. Biochem. 111, 251-258.
Oliver, R. P. and W. T. Griffiths (1981) Covalent binding of the NADPH:protochlorophyllide oxidoreductase from etioplast membranes with (3H)N-phenylmaleimide. Biochem. J. 195, 93-101.
Grebanier, A. E., K. Steinback and L. Bogorad (1979) Comparison of the molecular weights of proteins synthesized by isolated chloroplasts with those which appear during greening in Zea mays. Plant Physiol. 63, 436-439.
Griffiths, W. T. and N. S. Beer (1982) Site of synthesis of NADPH-protochlorophyllide oxidoreductase in rye (Secale cereale). Plant Physiol. 70, 1014-1018.
Ikeuchi, M. and S. Murakami (1982) Membranes of squash etioplasts during greening. Plant Cell Physiol. 23, 575-583.
Röper, U., H. Prinz and C. Lütz (1987) Amino acid composition of the enzyme NADPH:protochlorophyllide oxidoreductase. Plant Sci. Lett. 52, 15-19.
Holtorf, H., S. Reinbothe, R. Reinbothe, B. Bereza and K. Apel (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.
Forreiter, C. and K. Apel (1993) Light-independent and light-dependent protochlorophyllide-reducing activities and two distinct NADPH-protochlorophyllide oxidoreductase polypeptides in moutain pine (Pinus mungo). Planta 190, 536-545.
Skinner, J. S. and M. P. Timko (1998) Loblolly pine (Pinus taeda L.) contains multiple expressed gene encoding light-dependent NADPH:-protochlorophyllide oxidoreductase (POR). Plant Cell Physiol. 39, 795-806.
Oosawa, N., T. Masuda, K. Awai, N. Fusada, H. Shimada, H. Ohta and K. Takamiya (2000) Identification and light-induced expression of a novel gene of NADPH-protochlorophyllide oxidoreductase isoform in Arabidopsis thaliana. FEBS Lett. 474, 133-136.
Kaneko, T., S. Sato, H. Kotani, A. Tanaka, E. Asamizu, Y. Nakamura, N. Miyajima, M. Hirosawa, M. Sugiura, S. Sasamoto, T. Kimura, T. Hosouchi, A. Matsuno, A. Muraki, N. Nakazaki, K. Naruo, S. Okamura, S. Shimpo, C. Takeuchi, T. Wada, A. Watanabe, M. Yamada, M. Ysaduda and S. Tabata (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6903. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3, 109-136.
Heyes, D. J., G. E. M. Martin, R. T. Reid, C. N. Hunter and H. M. Wilks (2000) NADPH:protochlorophyllide oxidoreductase from Synechocystis: overexpression, purification and preliminary characterization. FEBS Lett. 483, 47-51.
Li, J. and M. P. Timko (1996) The pc-1 phenotype of Chlamydomonas reinhardtii results from a deletion mutation in the nuclear region for NADPH: protochlorophyllide oxidoreductase. Plant Mol. Biol. 30, 15-37.
Kuroda, H., T. Masuda, N. Fusada, H. Ohta and K. Takamiya (2000) Expression of NADPH-protochlorophyllide oxidoreductase gene in fully green leaves of cucumber. Plant Cell Physiol. 41, 226-229.
Spano, A. J., Z. He, H. Michel, D. F. Hunt and M. P. Timko (1992a) Molecular cloning, nuclear gene structure, and developmental expression of NADPH:protochlorophyllide oxidoreductase in pea (Pisum sativum L.). Plant Mol. Biol. 18, 967-972.
He, Z. H., J. Li, C. Sundqvist and M. P. Timko (1994) Leaf developmental age controls expression of genes encoding enzymes of chlorophyll and haem biosynthesis in pea (Pisum sativum L). Plant Physiol. 106, 537-546.
Kuroda, H., T. Masuda, H. Ohta, Y. Shioi and A. K. Takamiy (1995) Light-enhanced gene expression of NADPH-protochlorophyllide oxidoreductase in cucumber. Biochem. Biophys. Res. Commun. 210, 310-316.
Yoshida, K., R. M. Chen, A. Tanaka, H. Teramoto, R. Tanaka, M. P. Timko and H. Tsuji (1995) Correlated changes in the activity, amount of protein, and abundance of transcript of NADPH:protochlorophyllide oxidoreductase and chlorophyll accumulation during greening of cucumber cotyledons. Plant Physiol. 109, 231-238.
Schoefs, B. (1999) Light-dependent and light-independent protochlorophyllide reduction. Photosynthetica 36, 481-496.
Lebedev, N. and M. P. Timko (1998) Protochlorophyllide photoreduction. Photosynth. Res. 58, 5-23.
Von Armin, A. and X.-W. Deng (1996) Light control of seedlings development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 215-243.
Sperling, U., F. Franck, B. Van Cleve, G. Frick, K. Apel and G. A. Armstrong (1998) Etiopalst differentiation in Arabidopsis: both PORA and PORB restore the prolamellar body and photoactive Pchlide-F655 to the cop1 photomorphogenic mutant. Plant Cell 10, 283-296.
Franck, F., U. Sperling, G. Frick, B. Pochert, B. Van Cleve, K. Apel and G. A. Armstrong (2000) Regulation of etioplast pigment-protein complexes, inner membrane architecture, and protochlorophyllide a chemical heterogeneity by light-dependent NADPH:protochlorophyllide oxidoreductases A and B. Plant Physiol. 124, 1678-1696.
Lebedev, N. and M. P. Timko (1999) Protochlorophyllide oxidoreductase B-catalyzed protochlorophyllide reduction in vitro: insight into the mechanism of chlorophyll formation in light-adapted plants. Proc. Natl. Acad. Sci. USA 96, 17954-17959.
Su, Q., G. Frick, G. A. Armstrong and K. Apel (2001) PORC of Arabidopsis thaliana: a third light- and NADPH-dependent protochlorophyllide oxidoreductase that is differentially regulated by light. Plant Mol. Biol. 47, 805-813.
Apel, K (1981) The protochlorophyllide holochrome of barley (Hordeum vulgare). Phytochrome-induced decrease of translatable mRNA coding for the NADPH: protochlorophyllide oxidoreductase. Eur. J. Biochem. 120, 89-93.
Darrah, P. M., S. A. Kay, G. R. Teakle and W. T. Griffiths (1990) Cloning and sequencing of protochlorophyllide reductase. Biochem. J. 265, 789-798.
Teakle, G. R. and W. T. Griffiths (1993) Cloning, characterization and import studies on protochlorophyllide reductase from wheat (Triticum aestivum). Biochem. J. 296, 225-230.
Benli, M., R. Schulz and K. Apel (1991) Effect of light on the NADPH-protochlorophyllide oxidoreductase in Arabidopsis thaliana. Plant Mol. Biol. 16, 615-625.
Spano, A. J., Z. He and M. P. Timko (1992b) NADPH:protochlorophyllide oxidoreductases in white pine (Pinus strobus) and loblolly pine (P. taeda). Evidence for light and development regulation and protein structure between angiosperms and gymnosperms. Mol. Gen. Genet. 236, 86-95.
Fujita, Y., Y. Takahashi, T. Koschi, H. Ozeki, K. Ohyama and H. Matsubara (1989) Identification of a novel nifH-like (frxC) protein in chloroplasts of liverwort Marchantia polymorpha. Plant Mol. Biol. 13, 551-561.
Fujita, Y., Y. Takahashi, T. Koschi, H. Ozeki, K. Ohyama and H. Matsubara (1991) Cloning, nucleotide sequences and differential expression of the nifH and nifH-like (frxC) genes from the filamentous nitrogen-fixing cyanobacterium Plectonema boryanum. Plant Cell Physiol. 32, 1093a.
Von Heijne, G., J. Steppuhn and R. G. Herrmann (1989) Domain structure of mitochondrial and chloroplast targeting peptides. Eur. J. Biol. 180, 535-545.
Bruce, D. B. (2000) Chloroplast transit peptides: structure, function and evolution. Trends Cell. Biol. 10, 440-447.
Oliver, R. P. and W. T. Griffiths (1982) Pigment-protein complexes of illuminate d etiolated leaves. Plant Physiol. 70, 1019-1025.
Dahlin, C., H. Aronsson, H. M. Wilks, N. Lebedev, C. Sundqvist and M. P. Timko (1999) The role of protein surface charge in catalytic activity and chloroplast membrane association of the pea NADPH:-protochlorophyllide oxidoreductase (POR) as revealed by alanine mutagenesis. Plant Mol. Biol. 39, 309-323.
Wilks, H. M. and M. P. Timko (1995) A light-dependent complexation 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.
Lebedev, N., O. Karginova, W. McIvor and M. P. Timko (2001) Tyr275 and Lys279 stabilize NADPH within the catalytic site of NADPH:protochlorophyllide oxidoreductase and are involved in the formation of the enzyme photoactive state. Biochemistry 40, 12562-12574.
Heyes, D. J. and C. N. Hunter (2002) Site-directed mutagenesis of Tyr-189 and Lys-193 in NADPH:protochlorophyllide oxidoreductase from Synechocycstis. Biochem. Soc. Trans. 30, 601-604.
Guinery, G., A. Luzzati and J. Duranton (1974) On the specific binding of protochlorophyllide and chlorophyll to different peptide chains. Planta 115, 227-243.
Baker, M. E. (1994) Protochlorophyllide reduction is homologous to human carbonyl reductase and pig 20-beta-hydroxysteroid déhydrogénase. Biochem. J. 300, 605-607.
Labesse, G., A. Vidal-Cros, J. Chomilier, M. Gaudry and J. P. Morno (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.
Persson, B., M. Krook and H. Jörnvall (1991) Characteristics of short-chain alcohol dehydrogenase and related enzymes. Eur. J. Biochem. 201, 537-543.
Jörnval, H., B. Persson, M. Krrok, S. Atrian, R. Gonzalez-Duarte, J. Jeefery and D. Ghosh (1995) Short-chain dehydrogenase/reductase (SDR). Biochemistry 34, 6003-6015.
Chen, Z., L. Lu, M. Shirley, W. R. Lee and S. H. Chang (1990) Site directed mutagenesis of glycine-14 and two "critical" cystein residues in Drosophila alcohol déhydrogénase. Biochemistry 29, 1112-1118.
Wierenga, R. K., M. C. De Maeyer and W. G. J. Hol (1985) Interaction of pyrophosphate moieties with alpha-helixes in dinucleotide-binding proteins biochemistry. Biochemistry 24, 1346-1357.
Chen, Z., Z. G. Lin, W. R. Lee and S. H. Chang (1991) Role of aspartic acid 38 in the cofactor specificity of Drosophila alcohol dehydrogenase. Eur. J. Biochem. 202, 263-267.
Grimshaw, C. E., D. A. Matthews, K. I. Varughese, M. Skinner, N. H. Xuong, T. Bray, J. Hoch and J. M. Whiteley (1992) Characterization and nucleotide binding properties of a mutant dihydropterine reductase containing an aspartate 37-isoleucine replacement. J. Biol. Chem. 267, 15334-15339.
Townley, H. E., R. B. Sessions, A. R. Clarke, T. R. Dafforn and W. T. Griffiths (2001) Protochlorophyllide oxidoreductase: a homology model examined by site-directed mutagenesis. Proteins 44, 329-335.
Rebeiz, C. A., R. Parham, D. A. Fasoula and I. M. Ioannides (1994) Chlorophyll a biosynthetic pathway. In The Biosynthesis of Tetrapyrrole Pigments, Ciba Foundation Symposium, Vol. 180, pp. 177-193. Wiley, New York, USA.
Scheer, H. (1996) Tetrapyrroles in photosynthesis. In Biology, Biochemistry and Molecular Biology of Photosynthesis (Edited by B. Schoefs, F. Franck and J. Aghion). Bull. Soc. R. Sci. Liège 65, 310-320.
Schoch, S., M. Helfrich, B. Wiktorsson, C. Sundqvist, W. Rüdiger and M. Ryberg (1995) Photoreduction of zinc protopheophorbide b with NADPH-protochlorophyllide oxidoreductase from etiolated wheat (Triticum aestivum L.). Eur. J. Biochem. 229, 291-298.
Scheumann, V., H. Klement, M. Helfrich, U. Oster, S. Schoch and W. Rüdiger (1999) Protochlorophyllide b does not occur in barley leaves. FEBS Lett. 445, 445-448.
Reinbothe, C., F. Buhr, S. Pollmann and S. Reinbothe (2003) In vitro reconstitution of light-harvesting POR-protochlorophyllide complex with protochlorophyllides a and b. J. Biol. Chem. 278, 807-815.
Shedbalkar, V. P., I. M. Ioannides and C. A. Rebeiz (1991) Chloroplast biogenesis. Detection of monovinyl protochlorophyll(ide) b in plants. J. Biol. Chem. 266, 17152-17157.
Belanger, F. C. and C. A. Rebeiz (1985) Chloroplast biogenesis: detection of divinyl and monovinyl protochlorophyllides in higher plants. J. Biol. Chem. 255, 1266-1272.
Whyte, B. J. and W. T. Griffiths (1993) 8-vinyl reduction and chlorophyll a biosynthesis in higher plants. Biochem. J. 291, 939-944.
Adra, A. N. and C. A. Rebeiz (1998) Chloroplast biogenesis 81. Transient formation of divinyl chlorophyll a following a 2.5 ms light flash treatment of etiolated cucumber cotyledons. Photochem. Photobiol. 68, 852-856.
Ioannides, I. M., D. A. Fasoula, K. R. Robertson and C. A. Rebeiz (1994) An evolutionary study of chlorophyll biosynthetic heterogeneity on green plants. Biochem. Syst. Ecol. 22, 211-220.
Griffiths, W. T. (1980) Substrate-specificity studies on protochlorophyllide reductase in barley (Hordeum vulgare) etioplast membranes. Biochem. J. 186, 267-278.
Bombart, P. and E. Dujardin (1984) The photoreduction of Zn-protochlorophyllide by isolated etioplast lamellae. In Protochlorophyllide Reduction and Greening (Edited by C. Sironval and M. Brouers), pp. 175-179. Martinus Nijhoff/Dr W. Junk Publishers, The Hague, The Netherlands.
Krasnosvky, A. A., M. I. Bystrova and I. A. Safronova (1984) Photochemical reduction of protochlorophyllide in detergent micelles with the final chlorophyllide formation. In Protochlorophyllide Reduction and Greening (Edited by C. Sironval and M. Brouers), pp. 331-339. Martinus Nijhoff/Dr W. Junk Publishers, The Hague, The Netherlands.
Helfrich, M., S. Schoch, W. Schafer, M. Ryberg and W. Rüdiger (1996) Absolute configuration of protochlorophyllide a and substrate specificity of NADPH-protochlorophyllide oxidoreductase. J. Am. Chem. Soc. 118, 2606-2611.
Nakamura, A. and T. Watanabe (1998) HPLC determination of photosynthetic pigments during freening of etiolated barley leaves. Evidence for the biosynthesis of chlorophyll a'. FEBS Lett. 426, 201-204.
Griffiths, W. T. (1974a) Protochlorophyll and protochlorophyllide as precursors for chlorophyll synthesis in vitro. FEBS Lett. 49, 196-200.
Horton, P. and R. M. Leech (1975) The effect of ATP on the photoconversion of protochlorophyllide in isolated etioplasts of Zea mays. Plant Physiol. 56, 113-120.
Griffiths, W. T. (1991) Protochlorophyllide reduction. In Chlorophylls (Edited by H. Scheer), pp. 433-450. CRC Press, Boca Raton, FL.
Kotzabasis, K., M. P. Schüring and H. Senger (1989) Occurrence of protochlorophyll and its transformation to chlorophyll in mutant C-2A' of Scenedesmus obliquus. Physiol. Plant. 75, 221-226.
Vezitskii, A. Y. and R. A. Sherbakov (1987) Metal analogues of chlorophyll pigments as the substrates of enzymes catalyzing chlorophyllide esterification and chlorophyll hydrolysis in plants. Biokhimiya 52, 788-793.
Helfrich, M. and W. Rüdiger (1992) Various metallopheophorbides as substrates for chlorophyll synthase. Z. Naturforsch. 47c, 231-238.
Begley, T. P. and H. Young (1989) Protochlorophyllide reductase. I. Determination of the regiochemistry and the stereochemistry of the reduction of protochlorophyllide to chlorophyllide. J. Am. Chem. Soc. 111, 3095-3096.
Griffiths, W. T. (1974b) Source of reducing equivalent for the in vivo synthesis of chlorophyll from protochlorophyll. FEBS Lett. 46, 301-304.
Valera, V., M. Fung, A. N. Wessler and W. R. Richards (1987) Synthesis of 4R- and 4S-tritium labelled NADPH for the determination of the coenzyme stereospecificity of NADPH:protochlorophyllide oxi doreductase. Biochem. Biophys. Res. Commun. 148, 515-520.
Raskin, V. I. (1976) Mechanism of protochlorophyllide photoreduction in intact etiolated leaves. Vesti Akad Bauk BSSR 1976, 43-46.
Dujardin, E. and C. Sironval (1977) Transitory pigment-protein complexes similar to photosynthesis active centers during protochlorophyll(ide) photoreduction. Plant Sci. Lett. 10, 347-355.
Franck, F. and P. Mathis (1980) A short-lived intermediates in the photoenzymatic reduction of protochlorophyll(ide) to chlorophyll(ide) at a physiological temperature. Photochem. Photobiol. 32, 794-803.
Dobek, A., E. Dujardin, F. Franck, C. Sironval, J. Breton and E. Roux (1981) The first events of protochlorophyll(ide) photoreduction investigated in etiolated leaves by means of the fluorescence excited by short, 610 nm laser flashes at room temperature. Photobiochem. Photobiophys. 2, 35-44.
Iwai, J., M. Ikeuchi, Y. Inoue and T. Kobayashi (1984) Early processes of protochlorophyllide photoreduction as measured by nanosecond and picosecond spectrophotometry. In Protochlorophyllide Photoreduction and Greening (Edited by C. Sironval and M. Brouers), pp. 99-112. Martinus Nijhoff/Dr W. Junk Publishers, The Hague, The Netherlands.
Mysliwa-Kurdziel, B., F. Franck and K. Strzalka (1999) Analysis of fluorescence lifetime of protochlorophyllide and chlorophyllide in isolated etioplast membranes measured from multifrequency cross-correlation phase fluorometry. Photochem. Photobiol. 70, 616-623.
Griffiths, W. T., T. McHugh and R. E. Blankenship (1996) The light intensity dependence of protochlorophyllide photoconversion and its significance to the catalytic mechanism of protochlorophyllide reductase. FEBS Lett. 398, 235-238.
Litvin, F. F., N. V. Ignatov and E. I. Efimstev (1976) Energy migration in photoactive complexes of chlorophyll precursors in etiolated leaves and spectroscopic characteristics of pigment forms. Biofizika 21, 307-312.
Mathis, P. and K. Sauer (1973) Chlorophyll formation in greening bean leaves during the early stages. Plant Physiol. 51, 115-119.
Belyaeva, O. B., K. N. Timofee and F. F. Litvin (1988) The primary reaction in the protochlorophyll(ide) photoreduction as investigated by optical and ESR spectroscopy. Photosynth. Res. 15, 247-256.
Raskin, V. I. and A. Schwartz (2002) The charge-transfer complex between protochlorophyllide and NADPH: an intermediate in protochlorophyllide photoreduction. Photosynth. Res. 74, 181-186.
Heyes, D. J., A. V. Ruban, H. M. Wilks and C. N. Hunter (2002) Enzymology below 200 K: the kinetics and thermodynamics of the photochemistry catalyzed by protochlorophyllide oxidoreductase. Proc. Natl. Acad. Sci. USA 99, 11145-11150.
Ghosh, D., C. M. Weeks, P. Groschulski, W. L. Duax, M. Erman, R. L. Rimsay and J. C. Orr (1991) Three-dimensional structure of holo-3-α-β -hydroxysteroid dehydrogenase: a member of a short-chain dehydrogenase family. Proc. Natl. Acad. Sci. USA 88, 10064-10068.
Chen, Z., J. C. Jiang, Z. G. Lin, W. R. Lee, M. E. Baker and S. H. Chang (1993) Site-specific mutagenesis of Drosophila alcohol dehydrogenase. Evidence for involvement of tyrosine 152 and lysine 156 in catalysis. Biochemistry 32, 3342-3346.
Varughese, K. I., N. H. Xuong, P. M. Kiefer, D. A. Mathhews and J. M. Whiteley (1994) Structural and mechanistic characteristics of dihydropteridine reductase: a member of the Tyr-(Xaa)3-Lys-containing family of reductases and dehydrogenases. Proc. Natl. Acad. Sci. USA 91, 5582-5586.
Smith, J. H. C. and C. S. French (1958) Quantum Yield for the Protochlorophyll Conversion, Vol. 57. Year Book Camegie Institution, Washington, DC.
Van Bochove, A. C., W. T. Griffiths and R. Van Grondelle (1984) The primary reaction in the photoreduction of protochlorophyllide. A nanosecond fluorescence study. In Protochlorophyllide Reduction and Greening (Edited by C. Sironval and M. Brouers), pp. 113-125. Martinus Nijhoff/Dr W. Junk Publishers, The Hague, The Netherlands.
Böddi, B. and F. Franck (1997) Room temperature spectra of protochlorophyllide and chlorophyllide forms in etiolated bean leaves. J. Photochem. Photobiol. B: Biol. 41, 73-83. [Corrected in 42 165]
Böddi, B., A. Lindsten, M. Ryberg and C. Sundqvist (1989) On the aggregational states of protochlorophyllide and its protein complexes in wheat etioplasts. Physiol. Plant. 76, 135-146.
Martin, G. E. M., M. P. Timko and H. M. Wilks (1997) Purification and kinetic analysis of pea (Pisum sativum L.) NADPH:protochlorophyllide oxidoreductase expressed as fusion with maltose-binding protein in Escherichia coli. Biochem. J. 325, 139-145.
Schoefs, B., M. Bertrand and F. Franck (2000a) Spectroscopic properties of protochlorophyllide analyzed in situ in the course of etiolation and in illuminated leaves. Photochem. Photobiol. 72, 90-93.
Schoefs, B., M. Bertrand and C. Funk (2000b) Photoactive protochlorophyllide regeneration in cotyledons and leaves from higher plants. Photochem. Photobiol. 72, 660-668.
Kahn, A., N. K. Boardman and S. W. Thome (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.
Brouers, M., Y. Kuyper and C. Sironval (1972) The reduction of protochlorophyllide into chlorophyllide. V. Demonstration of energy transfer inside the P688-676 molecular units. Photosynthetica 6, 169-176.
Sironval, C. and M. Brouers (1980) The reduction of protochlorophyllide into chlorophyllide. VIII. The theory of the transfer units. Photosynthetica 14, 213-221.
Sironval, C. (1972) The reduction of protochlorophyllide into chlorophyllide. VI. Calculation of the size of the transfer unit and the initial quantum yield of the reduction in vivo. Photosynthetica 6, 375-380.
Schoefs, B., H. P. Garnir and M. Bertrand (1994) Comparison of the photoreduction of protochlorophyllide to chlorophyllide in leaves and cotyledons from dark grown bean as a function of age. Photosynth. Res. 41, 405-417.
Wiktorsson, B., S. Engeldhal, L. B. Zhong, B. Böddi, M. Ryberg and C. Sundqvist (1993) The effect of cross-linking of the subunit of NADPH-protochlorophyllide oxidoreductase on the aggregational state of protochlorophyllide. Photosynthetica 29, 205-218.
Cohen, C. E. and C. A. Rebeiz (1981) Chloroplast biogenesis 34. Spectrofluorimetric characterization in situ of the protochlorophyll species in etiolated tissues of higher plants. Plant Physiol. 67, 98-103.
Böddi, B., M. Ryberg and C. Sundqvist (1991) The formation of short wavelength chlorophyllide forms at partial phototransformation of protochlorophyllide in etioplast inner membranes. Photochem. Photobiol. 53, 667-673.
Schoefs, B. and F. Franck (1995) Role of NADPH: protochlorophyllide oxidoreductase in photoprotection of newly formed chlorophyllide. In Photosynthesis from Light to Biosphere, Vol. 3 (Edited by P. Mathis), pp. 1013-1017. Kluwer Academic Publishers, The Hague, The Netherlands.
Böddi, B., M. Ryberg and C. Sundqvist (1992) Identification of four universal protochlorophyllide forms in dark-grown leaves by analyses of the 77 K fluorescence spectra. J. Photochem. Photobiol. B: Biol. 12, 389-403.
Ignatov, N. V. and F. F. Litvin (2002) A new pathway of chlorophyll biosynthesis from long-wavelength protochlorophyllide Pchlide688/ 676 in juvenile etiolated plants. Photosynth. Res. 71, 195-207.
Klein, S. and J. A. Schiff (1972) The correlated appearance of prolamellar bodies, protochlorophyll(ide) species, and the Shibata shift during the development of bean etioplasts in the dark. Plant Physiol. 49, 619-626.
Schoefs, B. and F. Franck (1993) Photoreduction of protochlorophyllide to chlorophyllide in 2-d-old dark-grown bean (Phaseolus vulgaris cv Commodore) leaves. Comparison with 10-d-old dark-grown (etiolated leaves). J. Exp. Bot. 44, 1053-1057.
Seliskar, C. J. and B. Ke (1968) Protochlorophyllide aggregation in solution and associated spectral changes. Biochim. Biophys. Acta 153, 685-691.
Brouers, M. (1972) Optical properties of in vitro aggregates of protochlorophyllide in non-polar solvents. I. Visible and fluorescence spectra. Photosynthetica 6, 415-423.
Brouers, M. and C. Sironval (1975) Restoration of a P657-647 form from P645-638 in extracts of etiolated primary bean leaves. Plant Sci. Lett. 4, 175-181.
El Hamouri, B. and C. Sironval (1980) NADP+/NADPH control of the protochlorophyllide-chlorophyllide proteins in cucumber etioplasts. Photobiochem. Photobiophys. 1, 219-223.
Franck, F., B. Bereza and B. Böddi (1999) Protochlorophyllide-NADP+ and protochlorophyllide-NADPH complexes and their regeneration after flash illumination in leaves and etioplast membranes of dark-grown wheat. Photosynth. Res. 59, 53-61.
Henningsen, K. W., J. E. Boynton and D. Von Wettstein (1993) Mutants at xantha and albina loci in relation to chloroplast biogenesis in barley (Hordeum vulgare L). Biol. Skr. Dan. Vid. Selsk 42, 1-348.
Franck, F., X. Barthélemy and K. Strazlka (1993) Spectroscopic characterization of protochlorophyllide reduction in the greening leaf. Photosynthetica 29, 185-194.
Schoefs, B. and F. Franck (1998) Chlorophyll synthesis in dark-grown pine primary needles. Plant Physiol. 118, 1159-1168.
Klement, H., U. Oster and W. Rüdiger (2000) The influence of glycerol and chloroplast lipids on the spectral shifts of pigments associated with NADPH:protochlorophyllide oxidoreductase from Avena sativa L. FEBS Lett. 480, 306-310.
Belyaeva, O. B., W. T. Griffiths, J. V. Kovalek, K. N. Timofeev and F. F. Litvin (2001) Participation of free radicals in photoreduction of protochlorophyllide to chlorophyllide in an artificial pigment-protein complex. Biochemistry (Mosc) 66, 173-177.
Reinbothe, S., S. Pollmann and C. Reinbothe (2003) In situ conversion of protochlorophyllide b to protochlorophyllide a in barley. Evidence for a novel role of 7-formyl-reductase in the prolamellar body of etioplast. J. Biol. Chem. 278, 800-806.
Adamson, H. Y., R. G. Hiller and J. Walmsley (1997) Protochlorophyllide reduction and greening in angiosperms: an evolutionary perspective. J. Photochem. Photobiol. B: Biol. 41, 201-221.
Shinozaki, K., M. Ohme, M. Tanaka, T. Wakasugi, N. Hayashida, T. Matsubayashi, J. Chunwongse, J. Obokata, K. Yamaguchi-Shinozaki, C. Ohto, K. Torazawa, B. Y. Meng, M., Sugita, H. Deno, T. Kamogashira, K. Yamada, J. Kusuda, F. Takaiwa, A. Kato, N. Tohdoh, H. Shimada and M. Sugiura (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 5, 2043-2049.
Hiratsuka, J., H. Shimada, R. Whittier, T. Ishibashi, M. Sakamoto, M. Mori, C. Kondo, Y. Honji, C. R. Sun, B. Y. Meng, Y. Q. Li, A. Kanno, Y. Nishizawa, K. Shinozaki and M. Sugiura (1989) The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol. Gen. Genet. 217, 185-194.
Lidholm, J. and P. Gustafsson (1991) Homologues of the green algal gidA and the liverwort frxC gene are present on the chloroplast genomes of conifers. Plant Mol. Biol. 17, 787-798.
Choquet, Y., M. Rahire, J. Girard-Bascou, J. Erickson and J. D. Rochaix (1992) A chloroplast gene is required for the light-independent accumulation of chlorophyll in Chlamydomonas reinhardtii. EMBO J. 11, 1697-1704.
Suzuki, J. Y., D. W. Bollivar and C. E. Bauer. Genetic analysis of chlorophyll synthesis. Annu. Rev. Genet. 31, 61-89.
Armstrong, G. A. (1998) Greening in the dark: light-independent chlorophyll synthesis from anoxygenic photosynthetic bacteria to gymnosperms. J. Photochem. Photobiol. B: Biol. 43, 87-100.
Zsebo, K. M. and J. E. Hearst (1984) Genetic physical mapping of a photosynthetic gene cluster from R. capsulata. Cell 37, 937-947.
Bauer, C. E., D. A. Young and B. L. Marrs (1988) Analysis of the Rhodobacter capsulatus puf operon. Location of the oxygen-regulated promoter region and the identification of an additional puf-encoded gene. J. Biol. Chem. 263, 4820-4827.
Yang, Z. Y. and C. E. Bauer (1990) Rhodobacter capsulatus genes involved in early steps of bacteriochlorophyll biosynthesis pathway. J. Bacteriol. 172, 5001-5010.
Naylor, G. W., H. A. Addlesee, L. C. D. Gibson and C. N. Hunter (1999) The photosynthesis gene cluster of Rhodobacter sphaeroides. Photosynth. Res. 62, 121-129.
Kohchi, T., H. Shirai, H. Fukuzawa, T. Sano and T. Komano (1988) Structure and organization of Marchantia polymorpha chloroplast genome. IV. Inverted repeat and small single copy regions. J. Mol. Biol. 203, 353-372.
Fujita, Y., Y. Takahashi, M. Chuganji and H. Matsubara (1992) The nifH-like (frxC) gene is involved in the biosynthesis of chlorophyll in the filamentous cyanobacterium Plectonema boryanum. Plant Cell Physiol. 33, 81-92.
Burke, D., J. Hearst and A. Sidow (1993) Early evolution of photosynthesis: clues for nitrogenase and chlorophyll iron proteins. Proc. Natl. Acad. Sci. USA 90, 7134-7138.
Komarek, J. (1970) Genetic identity of the Anacystis nidulans strain Kratz-Allen/Bloom 625 with Synechococcus Nag 1849. Arch. Protistenk. 112, 343-364.
Fujita, Y. and C. E. Bauer (2000) Reconstitution of light-independent protochlorophyllide reductase from purified BchL and BchN-BchB subunits. In vitro confirmation of nitrogen-like features of a bacteriochlorophyll biosynthesis enzyme. J. Biol. Chem. 275, 23583-23588.
Adamson, H., C. Walker, A. Beer and W. T. Griffiths (1987) Protochlorophyllide reduction in Anabeana. In Progress in Photosynthesis Research (Edited by J. Biggins), pp. 483-486. Martinus Nijhoff Publishers, Dr. W. Junk, The Hague, The Netherlands.
Peschek, G. A., B. Hinterstoisser, M. Wastyn, O. Kuntner, B. Pineau, A. Missbichler and J. Lang (1989) 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.
Michel-Wolwertz, M.-R. (1977) Chlorophyll formation in cotyledons of Pinus jeffreyi during germination in the dark. Occasional accumulation of protochlorophyll(ide) forms. Plant Sci. Lett. 8, 125-134.
Virgin, H. I. (1956) Light induced stomatal transpiration of etiolated leaves as related to chlorophyll a content. Physiol. Plant. 9, 482-493.
Tripathy, B. and N. Chakraborty (1991) 5-aminolevulinic acid induced photodynamic damage of the photosynthetic electron transport chain of cucumber (Cucumis sativus L) cotyledons. Plant Physiol. 96, 761-767.
Spikes, J. D. and J. C. Bommer (1991) Chlorophyll and related pigments as photosensitizers in biological medicine. In Chlorophylls (Edited by H. Scheer), pp. 1024-1181. CRC Press, Boca Raton, FL.
Rebeiz, C. A., U. B. Nandihalli and K. Reddy (1995) Photodynamic herbicides and chlorophyll biosynthesis inhibitors. In Herbicides (Edited by N. R. Baker and M. Percival), pp. 173-208. Elsevier, Amsterdam.
Ricchelli, F. (1995) Photophysical properties of porphyrins in biological membranes. J. Photochem. Photobiol. B: Biol. 29, 109-118.
Ebermann, R., G. Alth, M. Kreitner and A. Kubin (1996) Natural products derived from plants and potential drugs for the photodynamic destruction of tumor cells. J. Photochem. Photobiol. B: Biol. 36, 95-97.
Siefermann-Harms, D. (1987) The light-harvesting and protective functions of carotenoids in photosynthetic membranes. Biochim. Biophys. Acta 811, 325-355.
Kitmitts, A., A. O. Mustafa, A. Holzenburg and R. C. Ford (1998) Three-dimensional structure of higher plant photosystem I determined by electron crystallography. J. Biol. Chem. 273, 29592-29599.
Ermel, U., G. Fritzsch, S. K. Buchanan and H. Michel (1994) Structure of the photosynthetic reaction center from Rhodobacter sphaeroides at 2.65 Å resolution: cofactors and protein-cofactor interactions. Structure 2, 925-936.
Deisenhofer, J., O. Epp, I. Sinning and H. Michel (1995) Crystallographic refinement at 2.3 Å resolution and refined model to the photosynthetic reaction centers from Rhodopseudomonas viridis. J. Mol. Biol. 246, 429-457.
Kühlbrandt, W., D. N. Wang and Y. Fujiyoshi (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367, 614-621.
Mcdermott, G., S. M. Prince, A. A. Freer, A. M. Hauthornthwaitelawless, M. Z. Papiz, R. J. Cogdell and N. W. Isaacs (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 674, 517-521.
Shioi, Y. and M. Doi (1988) Control of bacteriochlorophyll accumulation by light in an aerobic photosynthetic bacterium, Erythrobacter sp. Och 114. Arch. Biochem. Biophys. 266, 470-477.
Fradkin, L. I., A. A. Shlyk, L. M. Kalinina and A. Faludi-Daniel (1969) Fluorescence studies on the reaction centres of chlorophyll biosynthesis at the early stages of greening. Photosynthetica 3, 326-337.
Blankenship, R. E. (2001) Molecular evidences for the evolution of photosynthesis. Trends Plant Sci. 6, 4-6.
Shiba, T. (1989) Overview of the aerobic photosynthetic bacteria. In Aerobic Photosynthetic Bacteria (Edited by K. Harashima, T. Shiba and N. Murata), pp. 1-8. Springer-Verlag, Berlin.
Shiba, T. and K. Shimada (1997) Photosynthetic aspects of aerobic photosynthetic bacteria. In Handbook of Photosynthesis (Edited by M. Pessarakli), pp. 505-512. Marcel Dekker, New York.
Van Niel, C. B. (1944) The culture, general physiology, morphology and classification of the non-sulfur purple and brown bacteria. Bacteriol. Rev. 8, 1-118.
Lascelles, J. (1975) The regulation of heme and chlorophyll synthesis in bacteria. Ann. N. Y. Acad. Sci. 244, 334-347.
Cohen-Bazire, G., W. R. Sistrom and R. Y. Stanier (1957) Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J. Cell. Comp. Physiol. 49, 5-47.
Lascelles, J. (1978) Regulation of pyrrole synthesis. In The Photosynthetic Bacteria (Edited by R. K. Clayton and W. R. Sistrom), pp. 795-808. Plenum Press, New York.
Ferretti, J. J. and E. D. Gray (1967) Control of enzyme synthesis during adaptation in synchronously dividing populations of Rhodopseudomonas spheroides. Biochem. Biophys. Res. Commun. 29, 501-507.
Fay, P. (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol. Rev. 56, 340-349.
Fujita, Y., H. Takagi and T. Hase (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.
Saitou, N. and M. Nei (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
Franck, F. and K. Strzalka (1992) Detection of the photoactive protochlorophyllide-protein complex in the light during the greening of barley. FEBS Lett. 309, 73-77.
Sperling, U., B. Van Cleve, G. Frick, K. Apel and G. A. Armstrong (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.
Schoefs, B. and M. Bertrand (2000) The formation of chlorophyll from chlorophyllide in leaves containing propalstids is a four-step process. FEBS Lett. 486, 243-246.
Schoch, S. (1978) The esterification of chlorophyllide a in greening bean leaves. Z. Naturforsch. 33, 712-714.
Domanskii, V. P. and W. Rüdiger (2001) On the nature of the two pathways in chlorophyll formation from protochlorophyllide. Photosynth. Res. 68, 131-139.
Bauer, S. and H. W. Siegleman (1972) Photoconversion of chlorophyllide 684 to chlorophyllide 678. FEBS Lett. 20, 352-354.
Franck, F. and Y. Inoue (1984) Light-driven reversible transformation of chlorophyllide P696,684 into chlorophyllide P688,678 in illuminated etiolated bean leaves. Photobiochem. Photobiophys. 8, 85-96.
Franck, F. and G. H. Schmid (1985) The role of NADPH in the reversible phototransformation of chlorophyllide P682 into chlorophyllide P678 in etioplasts of oat. Z. Naturforsch. 40c, 832-838.
Franck, F., B. Schoefs, X. Barthélemy, B. Mysliwa-Kurziel, K. Strazlka and R. Popovic (1995) Protection of native chlorophyll(ide) forms and of photosystem II against photodamage during the early stages of chloroplast differentiation. Acta Physiol. Plant. 17, 123-132.
Aronsson, H., C. Sundqvist, M. P. Timko and C. Dahlin (2001) The importance of the C-terminal region and Cys residues for the membrane association of the NADPH:protochlorophyllide oxidoreductase in pea. FEBS Lett. 502, 11-15.