Skip to main content
SpringerLink
Log in

Novel Insights into the Enzymology, Regulation and Physiological Functions of Light-dependent Protochlorophyllide Oxidoreductase in Angiosperms

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The reduction of protochlorophyllide (Pchlide) is a key regulatory step in the biosynthesis of chlorophyll in phototrophic organisms. Two distinct enzymes catalyze this reduction; a light-dependent NADPH:protochlorophyllide oxidoreductase (POR) and light-independent Pchlide reductase (DPOR). Both enzymes are widely distributed among phototrophic organisms with the exception that only POR is found in angiosperms and only DPOR in anoxygenic photosynthetic bacteria. Consequently, angiosperms become etiolated in the absence of light, since the reduction of Pchlide in angiosperms is solely dependent on POR. In eukaryotic phototrophs, POR is a nuclear-encoded single polypeptide and post-translationally imported into plastids. POR possesses unique features, its light-dependent catalytic activity, accumulation in plastids of dark-grown angiosperms (etioplasts) via binding to its substrate, Pchlide, and cofactor, NADPH, resulting in the formation of prolamellar bodies (PLBs), and rapid degradation after catalysis under subsequent illumination. During the last decade, considerable progress has been made in the study of the gene organization, catalytic mechanism, membrane association, regulation of the gene expression, and physiological function of POR. In this review, we provide a brief overview of DPOR and then summarize the current state of knowledge on the biochemistry and molecular biology of POR mainly in angiosperms. The physiological and evolutional implications of POR are also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adamson HY, Hiller RG and Walmsley J (1997) Protochlorophyllide reduction and greening in angiosperms: an evolutionary perspective. J Photochem Photobiol B 41: 201–221

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Archibald JM, Rogers MB, Toop M, Ishida K and Keeling PJ (2003) Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans. Proc Natl Acad Sci USA 100: 7678–7683

    Google Scholar 

  • Argyroudi-Akoyunoglou JH and Prombona A (1996) Light-independent endogenous circadian rhythm in the capacity for chlorophyll formation. J Photochem Photobiol B 36: 271–277

    Google Scholar 

  • Armstrong GA (1998) Greening in the dark:light-independent chlorophyll biosynthesis from anoxygenic photosynthetic bacteria to gymnosperms. J Photochem Photobiol B 43: 87–100

    Google Scholar 

  • 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

    Google Scholar 

  • Armstrong GA, Apel K and Rüdiger W (2000) Does a light-harvesting protochlorophyllide a/b-binding protein complex exist? Trends Plant Sci 5: 40–44

    Google Scholar 

  • Aronsson H, Sohrt K and Soll J (2000) NADPH:protochlorophyllide oxidoreductase uses the general import route into chloroplasts. Biol Chem 381: 1263–1267

    Google Scholar 

  • Aronsson H, Sundqvist C, Timko MP and Dahlin C (2001a) 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

    Google Scholar 

  • Aronsson H, Sundqvist C, Timko MP and Dahlin C (2001b) Characterization of the assembly pathway of the pea NADPH:protochlorophyllide (Pchlide) oxidoreductase (POR), with emphasis on the role of its substrate, Pchlide. Physiol Plant 111: 239–244

    Google Scholar 

  • Aronsson H, Sundqvist C and Dahlin C (2003a) POR — import and membrane association of a key element in chloroplast development. Physiol Plant 118: 1–9

    Google Scholar 

  • Aronsson H, Sundqvist C and Dahlin C (2003b) POR hits the road: import and assembly of a plastid protein. Plant Mol Biol 51: 1–7

    Google Scholar 

  • Baker ME (1994) Protochlorophyllide reductase is homologous to human carbonyl reductase and pig 20 beta-hydroxysteroid dehydrogenase. Biochem J 300: 605–607

    Google Scholar 

  • Barnes SA, Nishizawa NK, Quaggio RB, Whitelam GC and Chua N-H (1996) Far-red light blocks greening of Arabidopsis seedlings via a phytochrome A-mediated change in plastid development. Plant Cell 8: 601–615

    Google Scholar 

  • 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

    Google Scholar 

  • Bauer CE, Bolliver DW and Suzuki JY (1993) Genetic analysis of photopigment biosynthesis in eubacteria: a guiding light for algae and plants. J Bacteriol 175: 3919–3925

    Google Scholar 

  • Beale SI (1999) Enzymes of chlorophyll biosynthesis. Photosynth Res 60: 43–73

    Google Scholar 

  • Benli M, Schulz R and Apel K (1991) Effect of light on the NADPH-protochlorophyllide oxidoreductase of Arabidopsis thaliana. Plant Mol Biol 16: 615–625

    Google Scholar 

  • Birve SJ, Selstam E and Johansson LB (1996) Secondary structure of NADPH:protochlorophyllide oxidoreductase examined by circular dichroism and prediction methods. Biochem J 317: 549–555

    Google Scholar 

  • Block MA, Tewari AK, Albrieux C, Marechal E and Joyard J (2002) The plant S-adenosyl-L-methionine:Mg-protoporphyrin IX methyltransferase is located in both envelope and thylakoid chloroplast membranes. Eur J Biochem 269: 240–248

    Google Scholar 

  • Böddi B and Franck F (1997) Room temperature fluorescence spectra of protochlorophyllide and chlorophyllide forms in etiolated bean leaves. J Photochem Photobiol B 41: 73–82

    Google Scholar 

  • Böddi B, Ryberg M and Sundqvist C (1992) Identification of four universal protochlorophyllide forms in dark-grown leaves by analyses of the 77K fluorescence emission spectra. J Photochem Photobiol B Biol 12: 389–401

    Google Scholar 

  • Böddi B, Ryberg M and Sundqvist C (1993) Analysis of the 77K fluorescence emission and excitation spectra of isolated etioplast inner membranes. J Photochem Photobiol B Biol 21: 125–133

    Google Scholar 

  • Böddi B, Keresztes Á, Csapó B, Kovács J, Páldi E and Láng F (1997) Differences in the etioplast ultrastructure and chlorophyll biosynthesis time course of cold tolerant and cold sensitive maize lines under cold treatment. Maydica 42: 305–311

    Google Scholar 

  • Böddi B, Kis-Petik K, Kaposi AD, Fidy J and Sundqvist C (1998) The two spectroscopically different short wavelength protochlorophyllide forms in pea epicotyls are both monomeric. Biochim Biophys Acta 1365: 531–540

    Google Scholar 

  • Böddi B, Popovic R and Franck F (2003) Early reactions of light-induced protochlorophyllide and chlorophyllide transformations analyzed in vivo at room temperature with a diode array spectrofluorometer. J Photochem Photobiol B 69: 31–39

    Google Scholar 

  • Bollivar DW, Suzuki JY, Beatty JT, Dobrowolski JM and Bauer CE (1994) Directed mutational analysis of bacteriochlorophyll a biosynthesis in Rhodobacter capsulatus. J Mol Biol 237: 622–640

    Google Scholar 

  • Botler B, May T and Soll J (1998) A protein import receptor in pea chloroplasts, TOC86, is only a proteolytic fragment of a larger polypeptide. FEBS Lett 441: 59–62

    Google Scholar 

  • Burke DH, Alberti M and Hearst JE (1993a) bchFNBH bacteriochlorophyll synthesis genes of Rhodobacter capsulatus and identification of the third subunit of light-independent protochlorophyllide reductase in bacteria and plants. J Bacteriol 175: 2414–2422

    Google Scholar 

  • 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

    Google Scholar 

  • Choquet Y, Rahire M, Girard-Bascou J, Erickson J and Rochaix J-D (1992) A chloroplast gene is required for the light-independent accumulation of chlorophyll in Chlamydomonas reinhardtii. EMBO J 11: 1697–1704

    Google Scholar 

  • Chory J, Reinecke D, Sim S, Washburn T and Brenner M (1994) A role of cytokinins in de-etiolation in Arabidopsis. Plant Physiol 104: 339–347

    Google Scholar 

  • Coomber SA, Chaudhri M, Connor A, Britton G and Hunter CN (1990) Localized transposon Tn5 mutagenesis of the photosynthetic gene cluster of Rhodobacter sphaeroides. Mol Microbiol 4: 977–989

    Google Scholar 

  • 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

    Google Scholar 

  • Dahlin C, Aronsson H, Wilks HM, Lebedev N, Sundqvist C and Timko MP (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 scanning mutagenesis. Plant Mol Biol 39: 309–323

    Google Scholar 

  • Dahlin C, Aronsson H, Almkvist J and Sundqvist C (2000) Protochlorophyllide-independent import of two NADPH:Pchlide oxidoreductase proteins (PORA and PORB) from barley into isolated plastids. Physiol Plant 109: 298–303

    Google Scholar 

  • Dandekar T, Snel B, Huynen M and Bork P (1998) Conservation of gene order: a fingerprint of proteins that physically interact. Trends Biochem Sci 23: 324–328

    Google Scholar 

  • Darrah PM, Kay SA, Teakle GR and Griffiths WT (1990) Cloning and sequencing of protochlorophyllide reductase. Biochem J 265: 789–798

    Google Scholar 

  • Domanski VP and Rüdiger W (2001) On the nature of the two pathways in chlorophyll formation from protochlorophyllide. Photosynth Res 68: 131–139

    Google Scholar 

  • Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, Barbe V, Duprat S, Galperin MY, Koonin EV, Le Gall F, Makarova KS, Ostrowski M, Oztas S, Robert C, Rogozin IB, Scanlan DJ, Tandeau de Marsac N, Weissenbach J, Wincker P, Wolf YI and Hess WR (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100: 10020–10025

    Google Scholar 

  • Eguchi S, Takano H, Ono K and Takio S (2002) Photosynthetic electron transport regulates the stability of the transcript for the protochlorophyllide oxidoreductase gene in the liverwort, Marchantia paleacea var. diptera. Plant Cell Physiol 43: 573–577

    Google Scholar 

  • Engdahl S, Aronsson H, Sundqvist C, Timko MP and Dahlin C (2001) Association of the NADPH:protochlorophyllide oxidoreductase (POR) with isolated etioplast inner membranes from wheat. Plant J 27: 297–304

    Google Scholar 

  • Eullaffroy P, Salvetat R, Franck F and Ropvic R (1995) Temperature dependence of chlorophyll(ide) spectral shifts and photoactive protochlorophyllide regeneration after flash in etiolated barley leaves. Photochem Photobiol 62: 751–756

    Google Scholar 

  • Fletcher RA and McCullagh D (1971) Benzyladenine as a regulator of chlorophyll synthesis in cucumber cotyledons. Can J Bot 49: 2197–2201

    Google Scholar 

  • Ford C, Mitchell S and Wang W-Y (1981) Protochlorophyllide photoconversion mutants of Chlamydomonas reinhardtii. Mol Gen Genet 184: 460–464

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Franck F, Bereza B and Böddi B (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

    Google Scholar 

  • Franck F, Sperling U, Frick G, Pochert B, van Cleve B, Apel K and Armstrong GA (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

    Google Scholar 

  • Frick G, Su Q, Apel K and Armstrong GA (2003) An Arabidopsis porB porC double mutant lacking light-dependent NADPH:protochlorophyllide oxidoreductases B and C is highly chlorophyll-deficient and developmentally arrested. Plant J 35: 141–153

    Google Scholar 

  • Fujita Y (1996) Protochlorophyllide reduction: a key step in the greening of plants. Plant Cell Physiol 37: 411–421

    Google Scholar 

  • Fujita Y and 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

    Google Scholar 

  • Fujita Y and Bauer CE (2003) The light-independent protochlorophyllide reductase: a nitrogenase-like enzyme catalyzing a key reaction for greening in the dark. In: Kadish KM, Smith KM and Guilard R (eds) The Porphyrin Handbook, Vol 13, pp 71–108. Elsevier Science, Amsterdam

    Google Scholar 

  • Fujita Y, Takahashi Y, Chuganji M and Matsubara H (1992) The nifH-like (frxC) gene is involved in the biosynthesis of chlorophyll in filamentous cyanobacterium Plectonema boryanum. Plant Cell Physiol 33: 81–92

    Google Scholar 

  • Fujita Y, Matsumoto H, Takahashi Y and Matsubara H (1993) Identification of a nifDK-like gene (ORF467) involved in the biosynthesis of chlorophyll in the cyanobacterium Plectonema boryanum. Plant Cell Physiol 34: 305–314

    Google Scholar 

  • Fujita Y, Takagi H and 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

    Google Scholar 

  • Fujita Y, Takagi H and 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

    Google Scholar 

  • Fusada N, Masuda T, Kuroda H, Shiraishi T, Shimada H, Ohta H and 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

    Google Scholar 

  • Gibson LC, Marrison JL, Leech RM, Jensen PE, Bassham DC, Gibson M and Hunter CN (1996) A putative Mg chelatase subunit from Arabidopsis thaliana cv C24. Sequence and transcript analysis of the gene, import of the protein into chloroplasts, and in situ localization of the transcript and protein. Plant Physiol 111: 61–71

    Google Scholar 

  • Griffiths WT (1975) Characterization of the terminal stages of chlorophyll(ide) synthesis in etioplast membrane preparations. Biochem J 152: 623–655

    Google Scholar 

  • Griffiths WT (1978) Reconstitution of chlorophyllide formation by isolated etioplast membranes. Biochem J 174: 681–692

    Google Scholar 

  • Griffiths WT (1991) Protochlorophyllide photoreduction. In: Scheer H (ed) Chlorophylls, pp 433–449. CRC Press, Boca Raton, Florida

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • He Z-H, 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

    Google Scholar 

  • Hearst JE, Alberti M and Doolittle RF (1985) A putative nitrogenase reductase gene found in the nucleotide sequences from the photosynthetic gene cluster of R. capsulata. Cell 40: 219–220

    Google Scholar 

  • Helfrich M, Schoch S, Schäfer W, Ryberg M and Rüdiger W (1996) Absolute configuration of protochlorophyllide a and substrate specificity of NADPH-protochlorophyllide oxidoreductase. J Am Chem Soc 118: 2606–2611

    Google Scholar 

  • Helfrich M, Bommer B, Oster U, Klement H, Mayer K, Larkum AW and Rüdiger W (2003) Chlorophylls of the c family: absolute configuration and inhibition of NADPH:protochlorophyllide oxidoreductase. Biochim Biophys Acta 1605: 97–103

    Google Scholar 

  • Henningsen KW, Thorne SW and Boardman NK (1974) Properties of protochlorophyllide and chlorophyll(ide) holochromes from etiolated and greening leaves. Plant Physiol 53: 419–425

    Google Scholar 

  • Heyes DJ and Hunter CN (2002) Site-directed mutagenesis of Tyr-189 and Lys-193 in NADPH:protochlorophyllide oxidoreductase from Synechocystis. Biochem Soc Trans 30: 601–604

    Google Scholar 

  • Heyes DJ, Martin GE, Reid RJ, Hunter CN and Wilks HM (2000) NADPH:protochlorophyllide oxidoreductase from Synechocystis: overexpression, purification and preliminary characterisation. FEBS Lett 483: 47–51

    Google Scholar 

  • Heyes DJ, Ruban AV, Wilks HM and Hunter CN (2002) Enzymology below 200 K: the kinetics and thermodynamics of the photochemistry catalyzed by protochlorophyllide oxidoreductase. Proc Natl Acad Sci USA 99: 11145–11150

    Google Scholar 

  • Heyes DJ, Hunter CN, Van Stokkum IH, Van Grondelle R and Groot ML (2003a) Ultrafast enzymatic reaction dynamics in protochlorophyllide oxidoreductase. Nat Struct Biol 10: 491–492

    Google Scholar 

  • Heyes DJ, Ruban AV and Hunter CN (2003b) Protochlorophyllide oxidoreductase: 'dark' reactions of a light-driven enzyme. Biochemistry 42: 523–528

    Google Scholar 

  • Holtorf H and Apel K (1996a) Transcripts of the two NADPH-protochlorophyllide oxidoreductase genes PorA and PorB are differentially degraded in etiolated barley seedlings. Plant Mol Biol 31: 387–392

    Google Scholar 

  • Holtorf H and Apel K (1996b) The regulation of NADPH-protochlorophyllide oxidoreductase a and b in green barley plants kept under a diurnal light dark cycle. Planta 199: 289–295

    Google Scholar 

  • 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

    Google Scholar 

  • Ignatov NV and Litvin FF (1981) Energy migration in a pigmented protochlorophyllide complex. Biofizika 26: 664–668

    Google Scholar 

  • Iwamoto K, Fukuda H and Sugiyama M (2001) Elimination of POR expression correlates with red leaf formation in Amaranthus tricolor. Plant J 27: 275–284

    Google Scholar 

  • Jarvis P and Soll J (2001) Toc, Tic, and chloroplast protein import. Biochim Biophys Acta 1541: 64–79

    Google Scholar 

  • Jarvis P, Chen L-J, Li H-M, Peto CA, Fankhauser C and Chory J (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282: 100–103

    Google Scholar 

  • 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

    Google Scholar 

  • Kada S, Koike H, Satoh K, Hase T and 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

    Google Scholar 

  • Kahn A (1968) Developmental physiology of bean leaf plastids. III. Tube transformation and protochlorophyll(ide) photoconversion by flash irradiation. Plant Physiol 43: 1781–1785

    Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M and Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3: 109–136

    Google Scholar 

  • Kaneko T, Nakamura Y, Wolk CP, Kuritz T, Sasamoto S, Watanabe A, Iriguchi M, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kohara M, Matsumoto M, Matsuno A, Muraki A, Nakazaki N, Shimpo S, Sugimoto M, Takazawa M, Yamada M, Yasuda M and Tabata S (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8: 205–213; 227–253

    Google Scholar 

  • Kis-Petik K, Böddi B, Kaposi AD and Fidy J (1999) Protochlorophyllide forms and energy transfer in dark-grown wheat leaves. Studies by conventional and laser excited fluorescence spectroscopy between 10-100 K. Photosynth Res 60: 87–98

    Google Scholar 

  • Klement H, Helfrich M, Oster U, Schoch S and Rüdiger W (1999) Pigment-free NADPH:protochlorophyllide oxidoreductase from Avena sativa L. Purification and substrate specificity. Eur J Biochem 265: 862–874

    Google Scholar 

  • Klement H, Oster U and Rüdiger W (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

    Google Scholar 

  • Kohchi T, Shirai H, Fukuzawa H, Sano T, Komano T, Umesono K, Inokuchi H, Ozeki H and Ohyama K (1988) Structure and organization of Marchantia polymorpha chloroplast genome. IV. Inverted repeat and small single copy regions. J Mol Biol 203: 353–372

    Google Scholar 

  • Kollosov VL and Rebeiz CA (2003) Chloroplast biogenesis 88:protochlorophyllide b occurs in green but not in etiolated plants. J Biol Chem 278: 49675

    Google Scholar 

  • Kovacheva S, Ryberg M and Sundqvist C (2000) ADP/ATP and protein phosphorylation dependence of phototransformable protochlorophyllide in isolated etioplast membranes. Photosynth Res 64: 127–136

    Google Scholar 

  • Kropat J, Oster U, Rüdiger W and Beck CF (2000) Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus. Plant J 24: 523–531

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Kuroda H, Masuda T, Fusada N, Ohta H and Takamiya K (2000) Expression of NADPH-protochlorophyllide oxidoreductase gene in fully green leaves of cucumber. Plant Cell Physiol 41: 226–229

    Google Scholar 

  • Kuroda H, Masuda T, Fusada N, Ohta H and Takamiya K (2001) Cytokinin-induced transcriptional activation of NADPH-protochlorophyllide oxidoreductase gene in cucumber. J Plant Res 114: 1–7

    Google Scholar 

  • Kusnetsov V, Herrmann RG, Kulaeva ON and Oelmüller R (1998) Cytokinin stimulates and abscisic acid inhibits greening of etiolated Lupinus luteus cotyledons by affecting the expression of the light-sensitive protochlorophyllide oxidoreductase. Mol Gen Genet 259: 21–28

    Google Scholar 

  • Larkin RM, Alonso JM, Ecker JR and Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299: 902–906

    Google Scholar 

  • Le Lay P, Böddi B, Kovacevic D, Juneau P, Dewez D and Popovic R (2001) Spectroscopic analysis of desiccation-induced alterations of the chlorophyllide transformation pathway in etiolated barley leaves. Plant Physiol 127: 202–211

    Google Scholar 

  • Lebedev N (1996) Fluorescence analysis of protochlorophyll(ide) to chlorophyll(ide) conversion in the green alga Chlamydomonas reinhardtii mutants. Photosynthetica 32: 569–585

    Google Scholar 

  • Lebedev N and Timko MP (1998) Protochlorophyllide photoreduction. Photosynth Res 58: 5–23

    Google Scholar 

  • Lebedev N and 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

    Google Scholar 

  • Lebedev N and Timko MP (2002) POR structural domains important for the enzyme activity in R. capsulatus complementation system. Photosynth Res 74: 153–163

    Google Scholar 

  • Lebedev N, Siffel P and Krasnovskii AA (1985) Detection of protochlorophyllide forms in irradiated green leaves and chloroplasts by difference fluorescence spectroscopy at 77K. Photosynthetica 19: 183–187

    Google Scholar 

  • Lebedev N, van Cleve 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

    Google Scholar 

  • Lebedev N, Karginova O, McIvor W and Timko MP (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

    Google Scholar 

  • Lee KP, Kim C, Lee DW and Apel K (2003) TIGRINA d, required for regulating the biosynthesis of tetrapyrroles in barley, is an ortholog of the FLU gene of Arabidopsis thaliana. FEBS Lett 553: 119–124

    Google Scholar 

  • 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

    Google Scholar 

  • Li J, Goldschmidt-Clermont M and Timko MP (1993) Chloroplas-tencoded chlB is required for light-independent protochlorophyllide reductase activity in Chlamydomonas reinhardtii. Plant Cell 5: 1817–1829

    Google Scholar 

  • Lindholm J and Gustafsson P (1991) Homologues of the green algal gidA gene and liverwort frxC gene are present in the chloroplast genomes of conifers. Plant Mol Biol 17: 787–798

    Google Scholar 

  • Liu X-Q, Xu H and Huang C (1993) Chloroplast chlB gene is required for light-independent chlorophyll accumulation in Chlamydomonas reinhardtii. Plant Mol Biol 23: 297–308

    Google Scholar 

  • Martin GE, 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

    Google Scholar 

  • Masuda T, Fusada N, Shiraishi T, Kuroda H, Awai K, Shimada H, Ohta H and Takamiya K (2002) Identification of two differentially regulated isoforms of protochlorophyllide oxidoreductase (POR) from tobacco revealed a wide variety of light-and development-dependent regulations of POR gene expression among angiosperms. Photosynth Res 74: 165–172

    Google Scholar 

  • Masuda T, Fusada N, Oosawa N, Takamatsu K, Yamamoto YY, Ohto M, Nakamura K, Goto K, Shibata D, Shirano Y, Hayashi H, Kato T, Tabata S, Shimada H, Ohta H and Takamiya K (2003) Functional analysis of isoforms of NADPH:protochlorophyllide oxidoreductase (POR), PORB and PORC, in Arabidopsis thaliana. Plant Cell Physiol 44: 963–974

    Google Scholar 

  • McCormac AC and Terry MJ (2002) Loss of nuclear gene expression during the phytochrome A-mediated far-red block of greening response. Plant Physiol 130: 402–414

    Google Scholar 

  • McEwen B, Seyedi 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 Plant 96: 51–58

    Google Scholar 

  • Meskauskiene R and Apel K (2002) Interaction of FLU, a negative regulator of tetrapyrrole biosynthesis, with the glutamyl—tRNA reductase requires the tetratricopeptide repeat domain of FLU. FEBS Lett 532: 27–30

    Google Scholar 

  • Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R and Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 12826–12831

    Google Scholar 

  • Mochizuki N, Brusslan JA, Larkin R, Nagatani A and Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98: 2053–2058

    Google Scholar 

  • 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

    Google Scholar 

  • Mysliwa-Kurdziel B, Amirjani MR, Strzalka K and Sundqvist C (2003) Fluorescence lifetimes of protochlorophyllide in plants with different proportions of short-wavelength and long-wavelength protochlorophyllide spectral forms. Photochem Photobiol 78: 205–212

    Google Scholar 

  • Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, Sasamoto S, Watanabe A, Iriguchi M, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M and Tabata S (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res 9: 123–130

    Google Scholar 

  • Nakayama M, Masuda T, Bando T, Yamagata H, Ohta H and Takamiya K (1998) Cloning and expression of the soybean chlH gene encoding a subunit of Mg-chelatase and localization of the Mg2+ concentration-dependent ChlH protein within the chloroplast. Plant Cell Physiol 39: 275–284

    Google Scholar 

  • Nielsen OF (1974) Macromolecular physiology of plastids. XII. Tigrina mutants of barley. Hereditas 76: 269–304

    Google Scholar 

  • Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S, Inokuchi H and Ozeki H (1986) Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha. Nature 322: 572–574

    Google Scholar 

  • Oosawa N, Masuda T, Awai K, Fusada N, Shimada H, Ohta H and 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

    Google Scholar 

  • Oster U, Tanaka R, Tanaka A and Rüdiger W (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J 21: 305–310

    Google Scholar 

  • Papenbrock J, Mock H-P, Kruse E and Grimm B (1999) Expression studies in tetrapyrrole biosynthesis: inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods. Planta 208: 264

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Popperl G, Oster U and Rüdiger W (1998) Light-dependent increase in chlorophyll precursors during the day-night cycle in tobacco and barley seedlings. J Plant Physiol 153: 40–45

    Google Scholar 

  • Porra J (1997) Recent progress in porphyrin and chlorophyll biosynthesis. Photochem Photobiol 65: 492–516

    Google Scholar 

  • Reinbothe S and Reinbothe C (1996) The regulation of enzymes involved in chlorophyll biosynthesis. Eur J Biochem 237: 323–343

    Google Scholar 

  • Reinbothe S, Reinbothe C, Holtorf H and Apel K (1995a) 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

    Google Scholar 

  • Reinbothe S, Reinbothe C, Runge S and Apel K (1995b) 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

    Google Scholar 

  • Reinbothe S, Runge S, Reinbothe C, van Cleve B and Apel K (1995c) Substrate-dependent transport of the NADPH:protochlorophyllide oxidoreductase into isolated plastids. Plant Cell 7: 161–172

    Google Scholar 

  • Reinbothe C, Apel K and Reinbothe S (1995d) A light-induced protease from barley plastids degrades NADPH:protochlorophyllide oxidoreductase complexed with chlorophyllide. Mol Cell Biol 15: 6206–6212

    Google Scholar 

  • Reinbothe S, Reinbothe C, Apel K and Lebedev N (1996a) Evolution of chlorophyll biosynthesis — the challenge to survive photooxidation. Cell 86: 703–705

    Google Scholar 

  • Reinbothe S, Reinbothe C, Lebedev N and Apel K (1996b) PORA and PORB, two light-dependent protochlorophyllide-reducing enzymes of angiosperm chlorophyll biosynthesis. Plant Cell 8: 763–769

    Google Scholar 

  • Reinbothe S, Reinbothe C, Neumann D and Apel K (1996c) A plastid enzyme arrested in the step of precursor translocation in vivo. Proc Natl Acad Sci USA 93: 12026–12034

    Google Scholar 

  • Reinbothe C, Lebedev N, Apel K and Reinbothe S (1997) Regulation of chloroplast protein import through a protochlorophyllide-responsive transit peptide. Proc Natl Acad Sci USA 94: 8890–8894

    Google Scholar 

  • Reinbothe C, Lebedev N and Reinbothe S (1999) A protochlorophyllide light-harvesting complex involved in de-etiolation of higher plants. Nature 397: 80–84

    Google Scholar 

  • Reinbothe S, Mache R and Reinbothe C (2000) A second, substrate-dependent site of protein import into chloroplasts. Proc Natl Acad Sci USA 97: 9795–9800

    Google Scholar 

  • Reinbothe C, Buhr F, Pollmann S and Reinbothe S (2003a) In vitro reconstitution of light-harvesting POR—protochlorophyllide complex with protochlorophyllides a and b. J Biol Chem 278: 807–815

    Google Scholar 

  • Reinbothe C, Lepinat A, Deckers M, Beck E and Reinbothe S (2003b) The extra loop distinguishing POR from the structurally related short-chain alcohol dehydrogenases is dispensable for pigment binding but needed for the assembly of light-harvesting POR—protochlorophyllide complex. J Biol Chem 278: 816–822

    Google Scholar 

  • Reinbothe S, Pollmann S and Reinbothe C (2003c) 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 etioplasts. J Biol Chem 278: 800–806

    Google Scholar 

  • Richard M, Tremblay C and Bellemare G (1994) Chloroplastic genomes of Ginkgo biloba and Chlamydomonas moewusii contain a chlB gene encoding one subunit of a light-independent protochlorophyllide reductase. Curr Genet 26: 159–165

    Google Scholar 

  • Rodermel S (2001) Pathways of plastid-to-nucleus signaling. Trends Plant Sci 6: 471–478

    Google Scholar 

  • Rowe JD and Griffiths WT (1995) Protochlorophyllide reductase in photosynthetic prokaryotes and its role in chlorophyll synthesis. Biochem J 311: 417–424

    Google Scholar 

  • Rüdiger W (1997) Chlorophyll metabolism: from outer space down to the molecular level. Phytochemistry 46: 1151–1167

    Google Scholar 

  • Rüdiger W (2003) The last steps of chlorophyll synthesis. In: Kadish KM, Smith KM and Guilard R (eds) The Porphyrin Handbook, Vol 13, pp 71–108. Elsevier Science, Amsterdam

    Google Scholar 

  • Runge S, van Cleve B, Lebedev N, Armstrong G and Apel K (1995) Isolation and classification of chlorophyll-deficient xantha mutants of Arabidopsis thaliana. Planta 197: 490–500

    Google Scholar 

  • 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

    Google Scholar 

  • Ryberg M and Sundqvist C (1988) The regular ultrastructure of isolated prolamellar bodies depends on the presence of membrane-bound NADPH—protochlorophyllide oxidoreductase. Physiol Plant 73: 216–226

    Google Scholar 

  • 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, Florida

    Google Scholar 

  • Scheumann V, Klement H, Helfrich M, Oster U, Schoch S and Rüdiger W (1999) Protochlorophyllide b does not occur in barley etioplasts. FEBS Lett 445: 445–448

    Google Scholar 

  • Schoch S, Helfrich M, Wiktorsson B, Sundqvist C, Rüdiger 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

    Google Scholar 

  • Schoefs B, Bertrand M and Franck F (2000a) Spectroscopic properties of protochlorophyllide analyzed in situ in the course of etiolation and in illuminated leaves. Photochem Photobiol 72: 85–93

    Google Scholar 

  • Schoefs B, Bertrand M and Funk C (2000b) Photoactive protochlorophyllide regeneration in cotyledons and leaves from higher plants. Photochem Photobiol 72: 660–668

    Google Scholar 

  • Schulz R and Senger H (1993) Protochlorophyllide reductase: a key enzyme in the greening process. In: Sundqvist C and Ryberg M (eds) Pigment-Protein Complexes in Plastids; Synthesis and Assembly, pp 179–218. Academic Press, New York

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Seyedi M, Selstam E, Timko MP and Sundqvist C (2001a) The cytokinin 2-isopentenyladenine causes partial reversion to skotomorphogenesis and induces formation of prolamellar bodies and protochlorophyllide657 in the lip1 mutant of pea. Physiol Plant 112: 261–272

    Google Scholar 

  • Seyedi M, Timko MP and Sundqvist C (2001b) The distribution of protochlorophyllide and chlorophyll within seedlings of the lip1 mutant of pea. Plant Cell Physiol 42: 931–941

    Google Scholar 

  • Shedbalkar VP, Ioannides IM and Rebeiz CA (1991) Chloroplast biogenesis. Detection of monovinyl protochlorophyll(ide) b in plants. J Biol Chem 266: 17151–17157

    Google Scholar 

  • Shibata K (1957) Spectroscopic studies on chlorophyll formation in intact leaves. J Biochem 44: 147–173

    Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayasida N, Matsubayashi T, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng B-Y, Sugita M, Deno H, Kamogashira T, Yamada K, Fusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H and Sugiura M (1986) The complete nucleotide sequence of the tobacco chloroplast genome: its organization and expression. EMBO J 5: 2043–2049

    Google Scholar 

  • Skinner JS and Timko MP (1998) Loblolly pine (Pinus taeda L.) contains multiple expressed genes encoding light-dependent NADPH:protochlorophyllide oxidoreductase (POR). Plant Cell Physiol 39: 795–806

    Google Scholar 

  • Skinner JS and Timko MP (1999) Differential expression of genes encoding the light-dependent and light-independent enzymes for protochlorophyllide reduction during development in loblolly pine. Plant Mol Biol 39: 577–592

    Google Scholar 

  • Skribanek A, Apatini D, Inaoka M and Böddi B (2000) Protochlorophyllide and chlorophyll forms in dark-grown stems and stem-related organs. J Photochem Photobiol B 55: 172–177

    Google Scholar 

  • Smeller L, Solymosi K, Fidy J and Böddi B (2003) Activation parameters of the blue shift (Shibata shift) subsequent to protochlorophyllide phototransformation. Biochim Biophys Acta 1651: 130–138

    Google Scholar 

  • Spano AJ, He Z, Michel H, Hunt DF and Timko MP (1992) Molecular cloning, nuclear gene structure, and developmental expression of NADPH:protochlorophyllide oxidoreductase in pea (Pisum sativum L.). Plant Mol Biol 18: 967–972

    Google Scholar 

  • Sperling U, van Cleve B, Frick G, Apel K and Armstrong GA (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

    Google Scholar 

  • Sperling U, Franck F, van Cleve B, Frick G, Apel K and Armstrong GA (1998) Etioplast differentiation in Arabidopsis: both PORA and PORB restore the prolamellar body and photoactive protochlorophyllide-F655 to the cop1 photomorphogenic mutant. Plant Cell 10: 283–296

    Google Scholar 

  • Strand A, Asami T, Alonso J, Ecker JR and Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrin IX. Nature 421: 79–83

    Google Scholar 

  • Su Q, Frick G, Armstrong G and Apel K (2001) POR C of Arabidopsis thaliana: a third light-and NADPH-dependent protochlorophyllide oxidoreductase that is differentially regulated by light. Plant Mol Biol 47: 805–813

    Google Scholar 

  • Sundqvist C and Dahlin C (1997) With chlorophyll from prolamellar bodies to light-harvesting complexes. Physiol Plant 100: 748–759

    Google Scholar 

  • Surpin M, Larkin RM and Chory J (2002) Signal transduction between the chloroplast and the nucleus. Plant Cell 14: S327–S338

    Google Scholar 

  • Susek J and Chory J (1992) A tale of two genomes: role of a chloroplast signal in coordinating nuclear and plastid genome expression. Aust J Plant Physiol 19: 387–399

    Google Scholar 

  • Susek RE, Ausubel FM and Chory J (1993) Signal transduction mutants of arabidopsis uncoupled nuclear cab and rbcS gene expression from chloroplast development. Cell 74: 787–799

    Google Scholar 

  • Suzuki JY and Bauer CE (1992) Light-independent chlorophyll biosynthesis: involvement of the chloroplast gene chlL (frxC). Plant Cell 4: 929–940

    Google Scholar 

  • Suzuki JY and Bauer CE (1995) A prokaryotic origin for light-dependent chlorophyll biosynthesis of plants. Proc Natl Acad Sci USA 92: 3749–3753

    Google Scholar 

  • Suzuki T, Takio S, Yamamoto I and Satoh T (2001) Characterization of cDNA of the liverwort phytochrome gene, and phytochrome involvement in the light-dependent and light-independent protochlorophyllide oxidoreductase gene expression in Marchantia paleacea var. diptera. Plant Cell Physiol 42: 576–582

    Google Scholar 

  • Suzuki T, Masuda T, Singh DP, Tan FC, Tsuchiya T, Shimada H, Ohta H, Smith AG and Takamiya K (2002) Two types of ferrochelatase in photosynthetic and nonphotosynthetic tissues of cucumber: their difference in phylogeny, gene expression, and localization. J Biol Chem 277: 4731–4737

    Google Scholar 

  • Takio S, Nakao N, Suzuki T, Tanaka K, Yamamoto I and Satoh T (1998) Light-dependent expression of protochlorophyllide oxidoreductase gene in the liverwort, Marchantia paleacea var. diptera. Plant Cell Physiol 39: 665–669

    Google Scholar 

  • Tanaka A, Ito H, Tanaka R, Tanaka NK, Yoshida K and Okada K (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci USA 95: 12719–12723

    Google Scholar 

  • Teakle GR and Griffiths WT (1993) Cloning, characterization and import studies on protochlorophyllide reductase from wheat (Triticum aestivum). Biochem J 296: 225–230

    Google Scholar 

  • Thomas H (1997) Chlorophyll: a symptom and a regulator of plastid development. N Physiologist 136: 163–181

    Google Scholar 

  • Timko MP (1998) Pigment biosynthesis: chlorophylls, heme, and carotenoids. In: Rochaix J-D, Goldschmidt-Clermont M and Merchant S (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas, pp 377–414. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • 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

    Google Scholar 

  • Townley HE, Sessions RB, Clarke AR, Dafforn TR and Griffiths WT (2001) Protochlorophyllide oxidoreductase: a homology model examined by site-directed mutagenesis. Proteins 44: 329–335

    Google Scholar 

  • Urbig T, Knaust RKC, Schiller H and Senger H (1995) Kinetic studies of protochlorophyllide reduction in vitro in the greening mutant C-2A′ of the unicellular green alga Scenedesmus obliquus. Z. Naturforsch C Biosci 50: 775–780

    Google Scholar 

  • von Wettstein D, Gough S and Kannangara CG (1995) Chlorophyll biosynthesis. Plant Cell 7: 1039–1057

    Google Scholar 

  • Wiktorsson B, Engdahl S, Zhong LB, Böddi B, Ryberg M and Sundqvist C (1993) The effect of cross-linking of the subunits of NADPH—protochlorophyllide oxidoreductase on the aggregational state of protochlorophyllide. Photosynthetica 29: 205–218

    Google Scholar 

  • Wiktorsson B, Ryberg M and Sundqvist C (1996) Aggregation of NADPH—protochlorophyllide oxidoreductase—pigment complexes is favoured by protein phospholylation. Plant Physiol Biochem 34: 23–34

    Google Scholar 

  • 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 enzyme activity. Proc Natl Acad Sci USA 92: 724–728

    Google Scholar 

  • 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

    Google Scholar 

  • Willows RD (2003) Biosynthesis of chlorophylls from protoporphyrin IX. Nat Prod Rep 20: 327–341

    Google Scholar 

  • Willows RD and Beale SI (1998) Heterologous expression of the Rhodobacter capsulatus BchI,-D, and-H genes that encode magnesium chelatase subunits and characterization of the reconstituted enzyme. J Biol Chem 273: 34206–34213

    Google Scholar 

  • 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

    Google Scholar 

  • Xu H, Vavilin D and Vermaas W (2001) Chlorophyll b can serve as the major pigment in functional Photosystem II complexes of cyanobacteria. Proc Natl Acad Sci USA 98: 14168–14173

    Google Scholar 

  • Xu H, Vavilin D and Vermaas W (2002) The presence of chlorophyll b in Synechocystis sp. PCC 6803 disturbs tetrapyrrole biosynthesis and enhances chlorophyll degradation. J Biol Chem 277: 42726–42732

    Google Scholar 

  • Yang ZM and Bauer CE (1990) Rhodobacter capsulatus genes involved in early steps of the bacteriochlorophyll biosynthetic pathway. J Bacteriol 172: 5001–5010

    Google Scholar 

  • Yoshida K, Chen RM, Tanaka A, Teramoto H, Tanaka R, Timko MP and Tsuji H (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

    Google Scholar 

  • 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 Plant 95: 336–346

    Google Scholar 

  • Zsebo KM and Hearst JE (1984) Genetic-physical mapping of a photosynthetic gene cluster from R. capsulata. Cell 38: 937–947

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, Yokohama, 226-8501, Japan

    Tatsuru Masuda & Ken-ichiro Takamiya

Authors
  1. Tatsuru Masuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ken-ichiro Takamiya
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Masuda, T., Takamiya, Ki. Novel Insights into the Enzymology, Regulation and Physiological Functions of Light-dependent Protochlorophyllide Oxidoreductase in Angiosperms. Photosynthesis Research 81, 1–29 (2004). https://doi.org/10.1023/B:PRES.0000028392.80354.7c

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PRES.0000028392.80354.7c

Search

Navigation