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Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls

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Abstract

In plants, chlorophylls (chlorophyll a and chlorophyll b) are the most abundant tetrapyrrole molecules and are essential for photosynthesis. The first committed step of chlorophyll biosynthesis is the insertion of Mg2+ into protoporphyrin IX, and thus subsequent steps of the biosynthesis are called the Mg branch. As the Mg branch in higher plants is complex, it was not until the last decade—after many years of intensive research—that most of the genes encoding the enzymes for the pathway were identified. Biochemical and molecular genetic analyses have certainly modified the classic metabolic map of tetrapyrrole biosynthesis, and only recently have the molecular mechanisms of regulatory pathways governing chlorophyll metabolism been elucidated. As a result, novel functions of tetrapyrroles and biosynthetic enzymes have been proposed. In this review, I summarize the recent findings on enzymes involved in the Mg branch, mainly in higher plants.

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Abbreviations

AAA:

ATPase associated with various cellular activities

ALA:

5-aminolevulinic acid

Bchl:

Bacteriochlorophyll

CAO:

Chlorophyllide a oxygenase

Chl:

Chlorophyll

DVR:

3,8-Divinyl Pchlide a 8-vinyl reductase

DPOR:

Light-independent protochlorophyllide oxidoreductase

GFP:

Green fluorescent protein

gun :

Genome uncoupled

LHC:

Light-harvesting chlorophyll a/b-protein complex

LHCII:

Light-harvesting chlorophyll a/b-protein complex of photosystem II

LHPP:

Light-harvesting protochlorophyllide a/b-binding protein complex

Pchlide:

Protochlorophyllide

PLB:

Prolamellar body

POR:

Light-dependent NADPH:protochlorophyllide oxidoreductase

Ptc:

Protochlorophyllide translocon complex

SAM:

S-adenosyl-l-methionine

ZnPP:

Zinc-protopheophorbide

References

  • Alawady AE, Grimm B (2005) Tobacco Mg protoporphyrin IX methyltransferase is involved in inverse activation of Mg porphyrin and protoheme synthesis. Plant J 41:282–290

    PubMed  CAS  Google Scholar 

  • Alawady A, Reski R, Yaronskaya E, Grimm B (2005) Cloning and expression of the tobacco CHLM sequence encoding Mg protoporphyrin IX methyltransferase and its interaction with Mg-chelatase. Plant Mol Biol 57:679–691

    PubMed  CAS  Google Scholar 

  • Al-Karadaghi S, Franco R, Hansson M, Shelnutt JA, Isaya G, Ferreira GC (2006) Chelatases: distort to select? Trends Biochem Sci 31:135–142

    PubMed  CAS  Google Scholar 

  • Ankele E, Kindgren P, Pesquet E, Strand A (2007) In vivo visualization of Mg-protoporphyrin IX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. Plant Cell 19:1964–1979

    PubMed  CAS  Google Scholar 

  • Apchelimov AA, Soldatova OP, Ezhova TA, Grimm B, Shestakov SV (2007) The analysis of the ChlI 1 and ChlI 2 genes using acifluorfen-resistant mutant of Arabidopsis thaliana. Planta 225:935–943

    PubMed  CAS  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

    CAS  Google Scholar 

  • Armstrong GA, Runge S, Frick G, Sperling U, Apel K (1995) Identification of NADPH:protochlorophyllide oxidoreductases A and B: A branch pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol 108:1505–1517

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Axelsson E, Lundqvist J, Sawicki A, Nilsson S, Schroder I, Al-Karadaghi S, Willows RD, Hansson M (2006) Recessiveness and dominance in barley mutants deficient in Mg-chelatase subunit D, an AAA protein involved in chlorophyll biosynthesis. Plant Cell 18:3606–3616

    PubMed  CAS  Google Scholar 

  • Balmer Y, Koller A, del Val G, Manieri W, Schurmann P, Buchanan BB (2003) Proteomics gives insight into the regulatory function of chloroplast thioredoxins. Proc Natl Acad Sci USA 100:370–375

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Beck CF (2005) Signaling pathways from the chloroplast to the nucleus. Planta 222:743–756

    PubMed  CAS  Google Scholar 

  • Benedetti CE, Arruda P (2002) Altering the expression of the chlorophyllase gene ATHCOR1 in transgenic Arabidopsis caused changes in the chlorophyll-to-chlorophyllide ratio. Plant Physiol 128:1255–1263

    PubMed  CAS  Google Scholar 

  • Block MA, Tewari AK, Albrieux C, Marechal E, 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

    PubMed  CAS  Google Scholar 

  • Bollivar DW (2006) Recent advances in chlorophyll biosynthesis. Photosynth Res 90:173–194

    PubMed  CAS  Google Scholar 

  • Bollivar DW, Bauer CE (1992) Nucleotide sequence of S-adenosyl-l-methionine: magnesium protoporphyrin methyltransferase from Rhodobacter capsulatus. Plant Physiol 98:408–410

    Article  PubMed  CAS  Google Scholar 

  • Bollivar DW, Jiang ZY, Bauer CE, Beale SI (1994a) Heterologous expression of the bchM gene product from Rhodobacter capsulatus and demonstration that it encodes S-adenosyl-l-methionine:Mg-protoporphyrin IX methyltransferase. J Bacteriol 176:5290–5296

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Botler B, May T, 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 

  • Brindley AA, Raux E, Leech HK, Schubert HL, Warren MJ (2003) A story of chelatase evolution: identification and characterization of a small 13–15-kDa “ancestral” cobaltochelatase (CbiXS) in the archaea. J Biol Chem 278:22388–22395

    PubMed  CAS  Google Scholar 

  • Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220

    PubMed  CAS  Google Scholar 

  • Burke DH, Alberti M, Hearst JE (1993) 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

    PubMed  CAS  Google Scholar 

  • Chekounova E, Voronetskaya V, Papenbrock J, Grimm B, Beck CF (2001) Characterization of Chlamydomonas mutants defective in the H subunit of Mg-chelatase. Mol Genet Genomics 266:363–373

    PubMed  CAS  Google Scholar 

  • Chew AG, Bryant DA (2007) Characterization of a plant-like protochlorophyllide a divinyl reductase in green sulfur bacteria. J Biol Chem 282:2967–2975

    PubMed  CAS  Google Scholar 

  • Chisholm SW, Frankel SL, Goericke R, Olson RJ, Palenik B, Waterbury JB, West-Johnsrud L, Zettler ER (1992) Prochlorococcus marinus nov. gen. nov. sp.: A marine prokaryote containing divinylchlorophyll a and b. Arch Microbiol 157:297–300

    CAS  Google Scholar 

  • Coleman ML, Chisholm SW (2007) Code and context: Prochlorococcus as a model for cross-scale biology. Trends Microbiol 15:398–407

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Dahlin C, Sundqvist C, Timko MP (1995) The in vitro assembly of the NADPH-protochlorophyllide oxidoreductase in pea chloroplasts. Plant Mol Biol 29:317–330

    PubMed  CAS  Google Scholar 

  • Davison PA, Schubert HL, Reid JD, Iorg CD, Heroux A, Hill CP, Hunter CN (2005) Structural and biochemical characterization of Gun4 suggests a mechanism for its role in chlorophyll biosynthesis. Biochemistry 44:7603–7612

    PubMed  CAS  Google Scholar 

  • Debussche L, Couder M, Thibaut D, Cameron B, Crouzet J, Blanche F (1992) Assay, purification, and characterization of cobaltochelatase, a unique complex enzyme catalyzing cobalt insertion in hydrogenobyrinic acid a,c-diamide during coenzyme B12 biosynthesis in Pseudomonas denitrificans. J Bacteriol 174:7445–7451

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Domanskii V, Rassadina V, Gus-Mayer S, Wanner G, Schoch S, Rüdiger W (2003) Characterization of two phases of chlorophyll formation during greening of etiolated barley leaves. Planta 216:475–483

    PubMed  CAS  Google Scholar 

  • Douglas SE, Reith M (1993) A bchI homolog, encoding a subunit of Mg-chelatase, is located on the plastid genomes of red and cryptomonad algae. J Mar Biotechnol 1:135–141

    CAS  Google Scholar 

  • Eckhardt U, Grimm B, Hörtensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56:1–14

    PubMed  CAS  Google Scholar 

  • Eggink LL, LoBrutto R, Brune DC, Brusslan J, Yamasato A, Tanaka A, Hoober JK (2004) Synthesis of chlorophyll b: localization of chlorophyllide a oxygenase and discovery of a stable radical in the catalytic subunit. BMC Plant Biol 4:5

    PubMed  Google Scholar 

  • Eriksson M, Moseley JL, Tottey S, Del Campo JA, Quinn J, Kim Y, Merchant S (2004) Genetic dissection of nutritional copper signaling in Chlamydomonas distinguishes regulatory and target genes. Genetics 168:795–807

    PubMed  CAS  Google Scholar 

  • Espineda CE, Linford AS, Devine D, Brusslan JA (1999) The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 96:10507–10511

    PubMed  CAS  Google Scholar 

  • Fisherova H (1975) Linkage relationships of recessive chlorophyll mutants in Arabidopsis thaliana. Biol Plant 17:182–188

    Article  Google Scholar 

  • Fodje MN, Hansson A, Hansson M, Olsen JG, Gough S, Willows RD, Al-Karadaghi S (2001) Interplay between an AAA module and an integrin I domain may regulate the function of magnesium chelatase. J Mol Biol 311:111–122

    PubMed  CAS  Google Scholar 

  • Franck F, Bereza B, 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

    CAS  Google Scholar 

  • Franck F, Sperling U, Frick G, Pochert B, van Cleve B, Apel K, 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

    PubMed  CAS  Google Scholar 

  • Frick G, Su Q, Apel K, 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

    PubMed  CAS  Google Scholar 

  • Fuesler TP, Castelfranco PA, Wong Y-S (1984a) Formation of Mg-containing chlorophyll precursors from protoporphyrin IX, δ-aminolevulinic acid, and glutamate in isolated, photosynthetically competent, developing chloroplasts. Plant Physiol 74:928–933

    CAS  Google Scholar 

  • Fuesler TP, Wong Y-S, Castelfranco PA (1984b) Localization of Mg-chelatase and Mg-protoporphyrin IX monomethyl ester (oxidative) cyclase activities within isolated, developing cucumber chloroplasts. Plant Physiol 75:662–664

    PubMed  CAS  Google Scholar 

  • Fujita Y, Bauer CE (2000) Reconstitution of light-independent protochlorophyllide reductase from purified bchl and BchN-BchB subunits. In vitro confirmation of nitrogenase-like features of a bacteriochlorophyll biosynthesis enzyme. J Biol Chem 275:23583–23588

    PubMed  CAS  Google Scholar 

  • Fujita Y, 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, Guilard R (eds) The porphyrin handbook, vol 13. Elsevier Science, Amsterdam, pp 71–108

    Google Scholar 

  • Fujita Y, Takagi H, Hase T (1998) Cloning of the gene encoding a protochlorophyllide reductase: the physiological significance of the co-existence of light-dependent and -independent protochlorophyllide reduction systems in the cyanobacterium Plectonema boryanum. Plant Cell Physiol 39:177–185

    PubMed  CAS  Google Scholar 

  • Fusada N, Masuda T, Kuroda H, Shiraishi T, Shimada H, Ohta H, Takamiya K (2000) NADPH-protochlorophyllide oxidoreductase in cucumber is encoded by a single gene and its expression is transcriptionally enhanced by illumination. Photosynth Res 64:147–154

    PubMed  CAS  Google Scholar 

  • Gadjieva R, Axelsson E, Olsson U, Hansson M (2005) Analysis of gun phenotype in barley magnesium chelatase and Mg-protoporphyrin IX monomethyl ester cyclase mutants. Plant Physiol Biochem 43:901–908

    PubMed  CAS  Google Scholar 

  • Gibson LC, Willows RD, Kannangara CG, von Wettstein D, Hunter CN (1995) Magnesium-protoporphyrin chelatase of Rhodobacter sphaeroides: reconstitution of activity by combining the products of the bchH, -I, and -D genes expressed in Escherichia coli. Proc Natl Acad Sci USA 92:1941–1944

    PubMed  CAS  Google Scholar 

  • Gibson LCD, Marrison JL, Leech RM, Jensen PE, Bassham DC, Gibson M, Hunter CN (1996) A putative Mg-chelatase subunit from Arabidopsis thaliana cv C24. Plant Physiol 111:61–71

    PubMed  CAS  Google Scholar 

  • Gibson LC, Jensen PE, Hunter CN (1999) Magnesium chelatase from Rhodobacter sphaeroides: initial characterization of the enzyme using purified subunits and evidence for a BchI-BchD complex. Biochem J 337:243–251

    PubMed  CAS  Google Scholar 

  • Gorchein A, Gibson LCD, Hunter CN (1993) Gene expression and control of enzymes for synthesis of magnesium protoporphyrin monomethyl ester in Rhodobacter sphaeroides. Biochem Soc Trans 21:201S

    PubMed  CAS  Google Scholar 

  • Goslings D, Meskauskiene R, Kim C, Lee KP, Nater M, Apel K (2004) Concurrent interactions of heme and FLU with Glu tRNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark- and light-grown Arabidopsis plants. Plant J 40:957–967

    PubMed  CAS  Google Scholar 

  • Gough SP, Petersen BO, Duus JO (2000) Anaerobic chlorophyll isocyclic ring formation in Rhodobacter capsulatus requires a cobalamin cofactor. Proc Natl Acad Sci USA 97:6908–6913

    PubMed  CAS  Google Scholar 

  • Gräfe S, Saluz H-P, Grimm B, Hänel F (1999) Mg-chelatase of tobacco: the role of the subunit CHL D in the chelation step of protoporphyrin IX. Proc Natl Acad Sci USA 96:1941–1946

    PubMed  Google Scholar 

  • Hansson M, Kannangara CG (1997) ATPases and phosphate exchange activities in magnesium chelatase subunits of Rhodobacter sphaeroides. Proc Natl Acad Sci USA 94:13351–13356

    PubMed  CAS  Google Scholar 

  • Hansson A, Kannagara CG, von Wettstein D, Hansson M (1999) Molecular basis for semidominance of missense mutations in the XANTHA-H (42-kDa) subunit of magnesium chelatase. Proc Natl Acad Sci USA 96:1744–1749

    PubMed  CAS  Google Scholar 

  • Hansson A, Willows RD, Roberts TH, Hansson M (2002) Three semidominant barley mutants with single amino acid substitutions in the smallest magnesium chelatase subunit form defective AAA+ hexamers. Proc Natl Acad Sci USA 99:13944–13949

    PubMed  CAS  Google Scholar 

  • Harpaz-Saad S, Azoulay T, Arazi T, Ben-Yaakov E, Mett A, Shiboleth YM, Hörtensteiner S, Gidoni D, Gal-On A, Goldschmidt EE, Eyal Y (2007) Chlorophyllase is a rate-limiting enzyme in chlorophyll catabolism and is posttranslationally regulated. Plant Cell 19:1007–1022

    PubMed  CAS  Google Scholar 

  • Harper AL, von Gesjen SE, Linford AS, Peterson MP, Faircloth RS, Thissen MM, Brusslan JA (2004) Chlorophyllide a oxygenase mRNA and protein levels correlate with the chlorophyll a/b ratio in Arabidopsis thaliana. Photosynth Res 79:149–159

    PubMed  CAS  Google Scholar 

  • Heyes DJ, Hunter CN (2005) Making light work of enzyme catalysis: protochlorophyllide oxidoreductase. Trends Biochem Sci 30:642–649

    PubMed  CAS  Google Scholar 

  • Hinchigeri SB, Hundle B, Richards WR (1997) Demonstration that the BchH protein of Rhodobacter capsulatus activates S-adenosyl-l-methionine:magnesium protoporphyrin IX methyltransferase. FEBS Lett 407:337–342

    PubMed  CAS  Google Scholar 

  • Holtorf H, Reinbothe S, Reinbothe C, Bereza B, Apel K (1995) Two routes of chlorophyllide synthesis that are differentially regulated by light in barley (Hordeum vulgare L.). Proc Natl Acad Sci USA 92:3254–3258

    PubMed  CAS  Google Scholar 

  • Hörtensteiner S (2004) The loss of green color during chlorophyll degradation–a prerequisite to prevent cell death? Planta 219:191–194

    PubMed  Google Scholar 

  • Hudson A, Carpenter R, Doyle S, Coen ES (1993) Olive: a key gene required for chlorophyll biosynthesis in Antirrhinum majus. EMBO J 12:3711–3719

    PubMed  CAS  Google Scholar 

  • Ikegami A, Motohashi K, Yoshimura N, Takahashi S, Romano PGN, Hisabori T, Takamiya K, Masuda T (2007) The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin. J Biol Chem 282:19282–19291

    PubMed  CAS  Google Scholar 

  • Ishijima S, Uchibori A, Takagi H, Maki R, Ohnishi M (2003) Light-induced increase in free Mg2+ concentration in spinach chloroplasts: measurement of free Mg2+ by using a fluorescent probe and necessity of stromal alkalinization. Arch Biochem Biophys 412:126–132

    PubMed  CAS  Google Scholar 

  • Ito H, Tanaka Y, Tsuji H, Tanaka A (1993) Conversion of chlorophyll b to chlorophyll a by isolated cucumber etioplasts. Arch Biochem Biophys 306:148–151

    PubMed  CAS  Google Scholar 

  • Ito H, Takaichi S, Tsuji H, Tanaka A (1994) Properties of synthesis of chlorophyll a from chlorophyll b in cucumber etioplasts. J Biol Chem 269:22034–22038

    PubMed  CAS  Google Scholar 

  • Ito H, Ohtsuka T, Tanaka A (1996) Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll. J Biol Chem 271:1475–1479

    PubMed  CAS  Google Scholar 

  • Jacob-Wilk D, Holland D, Goldschmidt EE, Riov J, Eyal Y (1999) Chlorophyll breakdown by chlorophyllase: isolation and functional expression of the Chlase1 gene from ethylene-treated Citrus fruit and its regulation during development. Plant J 20:653–661

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Jensen PE, Gibson LCD, Henningsen KW, Hunter CN (1996a) Expression of the chlI, chlD, and chlH genes from the cyanobacterium Synechocystis PCC6803 in Escherichia coli and demonstration that the three cognate proteins are required for magnesium-protoporphyrin chelatase activity. J Biol Chem 271:16662–16667

    PubMed  CAS  Google Scholar 

  • Jensen PE, Willows RD, Petersen BL, Vothknecht UC, Stummann BM, Kannangara CG, von Wettstein D, Henningsen KW (1996b) Structural genes for Mg-chelatase subunits in barley: Xantha-f, -g and -h. Mol Gen Genet 250:383–394

    PubMed  CAS  Google Scholar 

  • Jensen PE, Gibson LCD, Hunter CN (1998) Determinants of catalytic activity with the use of purified I, D and H subunits of the magnesium protoporphyrin IX chelatase from Synechocystis PCC6803. Biochem J 334:335–344

    PubMed  CAS  Google Scholar 

  • Jensen PE, Gibson LC, Hunter CN (1999a) ATPase activity associated with the magnesium-protoporphyrin IX chelatase enzyme of Synechocystis PCC6803: evidence for ATP hydrolysis during Mg2+ insertion, and the MgATP-dependent interaction of the ChlI and ChlD subunits. Biochem J 339:127–134

    PubMed  CAS  Google Scholar 

  • Jensen PE, Gibson LCD, Shephard F, Smith V, Hunter CN (1999b) Introduction of a new branchpoint in tetrapyrrole biosynthesis in Escherichia coli by co-expression of genes encoding the chlorophyll-specific enzymes magnesium chelatase and magnesium protoporphyrin methyltransferase. FEBS Lett 455:349–354

    PubMed  CAS  Google Scholar 

  • Jensen PE, Reid JD, Hunter CN (2000) Modification of cysteine residues in the ChlI and ChlH subunits of magnesium chelatase results in enzyme inactivation. Biochem J 352:435–441

    PubMed  CAS  Google Scholar 

  • Kagan RM, Clarke S (1994) Widespread occurrence of three sequence motifs in diverse S-adenosyl methionine-dependent methyltransferases suggests a common structure for these enzymes. Arch Biochem Biophys 310:417–427

    PubMed  CAS  Google Scholar 

  • Karger GA, Reid JD, Hunter CN (2001) Characterization of the binding of deuteroporphyrin IX to the magnesium chelatase H subunit and spectroscopic properties of the complex. Biochemistry 40:9291–9299

    PubMed  CAS  Google Scholar 

  • Kariola T, Brader G, Li J, Palva ET (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell 17:282–294

    PubMed  CAS  Google Scholar 

  • Kim C, Apel K (2004) Substrate-dependent and organ-specific chloroplast protein import in planta. Plant Cell 16:88–98

    PubMed  CAS  Google Scholar 

  • Kim C, Ham H, Apel K (2005) Multiplicity of different cell- and organ-specific import routes for the NADPH-protochlorophyllide oxidoreductases A and B in plastids of Arabidopsis seedlings. Plant J 42:329–340

    PubMed  CAS  Google Scholar 

  • Kollosov VL, Rebeiz CA (2003) Chloroplast biogenesis 88: protochlorophyllide b occurs in green but not in etiolated plants. J Biol Chem 278:49675–49678

    Google Scholar 

  • Koncz C, Mayerhofer R, Koncz-Kalman Z, Nawrath C, Reiss B, Redei GP, Schell J (1990) Isolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana. EMBO J 9:1337–1346

    PubMed  CAS  Google Scholar 

  • Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719

    PubMed  CAS  Google Scholar 

  • Kropat J, Oster U, Rüdiger W, Beck CF (1997) Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes. Proc Natl Acad Sci USA 94:14168–14172

    PubMed  CAS  Google Scholar 

  • Kropat J, Oster U, Rüdiger W, 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

    PubMed  CAS  Google Scholar 

  • Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, Kawasaki S, Tanaka R, Hirochika H, Nishimura M, Tanaka A (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19:1362–1375

    PubMed  CAS  Google Scholar 

  • Kuzuyama T, Seki T, Dairi T, Hidaka T, Seto H (1995) Nucleotide sequence of fortimicin KL1 methyltransferase gene isolated from Micromonospora olivasterospora, and comparison of its deduced amino acid sequence with those of methyltransferases involved in the biosynthesis of bialaphos and fosfomycin. J Antibiot 48:1191–1193

    PubMed  CAS  Google Scholar 

  • Lake V, Olsson U, Willows RD, Hansson M (2004) ATPase activity of magnesium chelatase subunit I is required to maintain subunit D in vivo. Eur J Biochem 271:2182–2188

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Lecerof D, Fodje M, Hansson A, Hansson M, Al-Karadaghi S (2000) Structural and mechanistic basis of porphyrin metallation by ferrochelatase. J Mol Biol 297:221–232

    PubMed  CAS  Google Scholar 

  • Maloney MA, Hoober JK, Marks DB (1989) Kinetics of chlorophyll accumulation and formation of chlorophyll–protein complexes during greening of Chlamydomonas reinhardtii y-1 at 38°C. Plant Physiol 91:1100–1106

    PubMed  CAS  Google Scholar 

  • Masuda T, Takamiya K (2004) Novel insights into the enzymology, regulation and physiological functions of light-dependent protochlorophyllide oxidoreductase in angiosperms. Photosynth Res 81:1–29

    PubMed  CAS  Google Scholar 

  • Masuda T, Inoue K, Masuda M, Nagayama M, Tamaki A, Ohta H, Shimada H, Takamiya K (1999) Magnesium insertion by magnesium chelatase in the biosynthesis of zinc bacteriochlorophyll a in an aerobic acidophilic bacterium Acidiphilium rubrum. J Biol Chem 274:33594–33600

    PubMed  CAS  Google Scholar 

  • Masuda T, Polle JE, Melis A (2002) Biosynthesis and distribution of chlorophyll among the photosystems during recovery of the green alga Dunaliella salina from irradiance stress. Plant Physiol 128:603–614

    PubMed  CAS  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, Takamiya K (2003a) Functional analysis of isoforms of NADPH:protochlorophyllide oxidoreductase (POR), PORB and PORC, in Arabidopsis thaliana. Plant Cell Physiol 44:963–974

    PubMed  CAS  Google Scholar 

  • Masuda T, Tanaka A, Melis A (2003b) Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expression. Plant Mol Biol 51:757–771

    PubMed  CAS  Google Scholar 

  • Matsumoto F, Obayashi T, Sasaki-Sekimoto Y, Ohta H, Takamiya K, Masuda T (2004) Gene expression profiling of the tetrapyrrole metabolic pathway in Arabidopsis with a mini-array system. Plant Physiol 135:2379–2391

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Mochizuki N, Brusslan JA, Larkin R, Nagatani A, 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

    PubMed  CAS  Google Scholar 

  • Moseley J, Quinn J, Eriksson M, Merchant S (2000) The Crd1 gene encodes a putative di-iron enzyme required for photosystem I accumulation in copper deficiency and hypoxia in Chlamydomonas reinhardtii. EMBO J 19:2139–2151

    PubMed  CAS  Google Scholar 

  • Moulin M, Smith AG (2005) Regulation of tetrapyrrole biosynthesis in higher plants. Biochem Soc Trans 33:737–742

    PubMed  CAS  Google Scholar 

  • Moulin M, Smith AG (2008) A robust method for determination of chlorophyll intermediates by tandem mass spectrometry. In: Allen J, Gantt E, Golbeck J, Osmond B (eds) Energy from the sun. Springer (in press)

  • Nagata N, Satoh S, Tanaka R, Tanaka A (2004) Domain structures of chlorophyllide a oxygenase of green plants and Prochlorothrix hollandica in relation to catalytic functions. Planta 218:1019–1025

    PubMed  CAS  Google Scholar 

  • Nagata N, Tanaka R, Satoh S, Tanaka A (2005) Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species. Plant Cell 17:233–240

    PubMed  CAS  Google Scholar 

  • Nakagawara E, Sakuraba Y, Yamasato A, Tanaka R, Tanaka A (2007) Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase. Plant J 49:800–809

    PubMed  CAS  Google Scholar 

  • Nakanishi H, Nozue H, Suzuki K, Kaneko Y, Taguchi G, Hayashida N (2005) Characterization of the Arabidopsis thaliana mutant pcb2 which accumulates divinyl chlorophylls. Plant Cell Physiol 46:467–473

    PubMed  CAS  Google Scholar 

  • Nakayama M, Masuda T, Sato N, Yamagata H, Bowler C, Ohta H, Shioi Y, Takamiya K (1995) Cloning, subcellular localization and expression of CHLI, a subunit of magnesium-chelatase in soybean. Biochem Biophys Res Commun 215:422–428

    PubMed  CAS  Google Scholar 

  • Nakayama M, Masuda T, Bando T, Yamagata H, Ohta H, 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

    PubMed  CAS  Google Scholar 

  • Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27–43

    PubMed  CAS  Google Scholar 

  • Nomata J, Kitashima M, Inoue K, Fujita Y (2006) Nitrogenase Fe protein-like Fe-S cluster is conserved in L-protein (BchL) of dark-operative protochlorophyllide reductase from Rhodobacter capsulatus. FEBS Lett 580:6151–6154

    PubMed  CAS  Google Scholar 

  • Nott A, Jung HS, Koussevitzky S, Chory J (2006) Plastid-to-nucleus retrograde signaling. Annu Rev Plant Biol 57:739–759

    PubMed  CAS  Google Scholar 

  • Obayashi T, Kinoshita K, Nakai K, Shibaoka M, Hayashi S, Saeki M, Shibata D, Saito K, Ohta H (2007) ATTED-II: a database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res 35:D863–D869

    PubMed  CAS  Google Scholar 

  • Oosawa N, Masuda T, Awai K, Fusada N, Shimada H, Ohta H, Takamiya K (2000) Identification and light-induced expression of a novel gene of NADPH-protochlorophyllide oxidoreductase isoform in Arabidopsis thaliana. FEBS Lett 474:133–136

    PubMed  CAS  Google Scholar 

  • Orsat B, Monfort A, Chatellard P, Stutz E (1992) Mapping and sequencing of an actively transcribed Euglena gracilis chloroplast gene (ccsA) homologous to the Arabidopsis thaliana nuclear genome cs (ch-42). FEBS Lett 303:181–184

    PubMed  CAS  Google Scholar 

  • Oster U, Rüdiger W (1997) The G4 gene of Arabidopsis thaliana encodes a chlorophyll synthase of etiolated plants. Bot Acta 110:420–423

    CAS  Google Scholar 

  • Oster U, Bauer CE, Rüdiger W (1997) Characterization of chlorophyll a and bacteriochlorophyll a synthases by heterologous expression in Escherichia coli. J Biol Chem 272:9671–9676

    PubMed  CAS  Google Scholar 

  • Oster U, Tanaka R, Tanaka A, 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

    PubMed  CAS  Google Scholar 

  • Ouchane S, Steunou AS, Picaud M, Astier C (2004) Aerobic and anaerobic Mg-protoporphyrin monomethyl ester cyclases in purple bacteria: a strategy adopted to bypass the repressive oxygen control system. J Biol Chem 279:6385–6394

    PubMed  CAS  Google Scholar 

  • Papenbrock J, Gräfe S, Kruse E, Hänel F, Grimm B (1997) Mg-chelatase of tobacco: identification of a Chl D cDNA sequence encoding a third subunit, analysis of the interaction of the three subunits with the yeast two-hybrid system, and reconstitution of the enzyme activity by co-expression of recombinant CHL D, CHL H and CHL I. Plant J 12:981–990

    PubMed  CAS  Google Scholar 

  • Papenbrock J, Mock H-P, Kruse E, Grimm B (1999) Expression studies in tetrapyrrole biosynthesis: inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods. Planta 208:264–273

    CAS  Google Scholar 

  • Parham R, Rebeiz CA (1995) Chloroplast biogenesis 72: a [4-vinyl]chlorophyllide a reductase assay using divinyl chlorophyllide a as an exogenous substrate. Anal Biochem 231:164–169

    PubMed  CAS  Google Scholar 

  • Pattanayak GK, Tripathy BC (2002) Catalytic function of a novel protein protochlorophyllide oxidoreductase C of Arabidopsis thaliana. Biochem Biophys Res Commun 291:921–924

    PubMed  CAS  Google Scholar 

  • Pattanayak GK, Biswal AK, Reddy VS, Tripathy BC (2005) Light-dependent regulation of chlorophyll b biosynthesis in chlorophyllide a oxygenase overexpressing tobacco plants. Biochem Biophys Res Commun 326:466–471

    PubMed  CAS  Google Scholar 

  • Petersen BL, Jensen PE, Gibson LC, Stummann BM, Hunter CN, Henningsen KW (1998) Reconstitution of an active magnesium chelatase enzyme complex from the bchI, -D, and -H gene products of the green sulfur bacterium Chlorobium vibrioforme expressed in Escherichia coli. J Bacteriol 180:699–704

    PubMed  CAS  Google Scholar 

  • Petersen BL, Kannangara CG, Henningsen KW (1999a) Distribution of ATPase and ATP-to-ADP phosphate exchange activities in magnesium chelatase subunits of Chlorobium vibrioforme and Synechocystis PCC6803. Arch Microbiol 171:146–150

    PubMed  CAS  Google Scholar 

  • Petersen BL, Moller MG, Jensen PE, Henningsen KW (1999b) Identification of the Xan-g gene and expression of the Mg-chelatase encoding genes Xan-f, -g and -h in mutant and wild type barley (Hordeum vulgare L.). Hereditas 131:165–170

    CAS  Google Scholar 

  • Philippar K, Geis T, Ilkavets I, Oster U, Schwenkert S, Meurer J, Soll J (2007) Chloroplast biogenesis: the use of mutants to study the etioplast-chloroplast transition. Proc Natl Acad Sci USA 104:678–683

    PubMed  CAS  Google Scholar 

  • Pinta V, Picaud M, Reiss-Husson F, Astier C (2002) Rubrivivax gelatinosus acsF (previously orf358) codes for a conserved, putative binuclear-iron-cluster-containing protein involved in aerobic oxidative cyclization of Mg-protoporphyrin IX monomethylester. J Bacteriol 184:746–753

    PubMed  CAS  Google Scholar 

  • Pollmann S, Springer A, Buhr F, Lahroussi A, Samol I, Bonneville JM, Tichtinsky G, von Wettstein D, Reinbothe C, Reinbothe S (2007) A plant Porphyria related to defects in plastid import of protochlorophyllide oxidoreductase A. Proc Natl Acad Sci USA 104:2019–2023

    PubMed  CAS  Google Scholar 

  • Pontier D, Albrieux C, Joyard J, Lagrange T, Block MA (2007) Knock-out of the magnesium protoporphyrin IX methyltransferase gene in Arabidopsis. Effects on chloroplast development and on chloroplast-to-nucleus signaling. J Biol Chem 282:2297–2304

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Porra RJ, Urzinger M, Winkler J, Bubenzer C, Scheer H (1998) Biosynthesis of the 3-acetyl and 13(1)-oxo groups of bacteriochlorophyll a in the facultative aerobic bacterium, Rhodovulum sulfidophilum-the presence of both oxygenase and hydratase pathways for isocyclic ring formation. Eur J Biochem 257:185–191

    PubMed  CAS  Google Scholar 

  • Pruzinska A, Tanner G, Aubry S, Anders I, Moser S, Muller T, Ongania KH, Krautler B, Youn JY, Liljegren SJ, Hörtensteiner S (2005) Chlorophyll breakdown in senescent Arabidopsis leaves. Characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol 139:52–63

    PubMed  CAS  Google Scholar 

  • Rebeiz CA, Kolossov VL, Briskin D, Gawienowski M (2003) Chloroplast biogenesis: chlorophyll biosynthetic heterogeneity, multiple biosynthetic routes and biological spin-offs. In: Nalwa HS (ed) handbook of photochemistry and photobiology, vol 4. American Scientific Publishers, Los Angeles, pp 183–248

    Google Scholar 

  • Reid JD, Hunter CN (2002) Current understanding of the function of magnesium chelatase. Biochem Soc Trans 30:643–645

    PubMed  CAS  Google Scholar 

  • Reid JD, Hunter CN (2004) Magnesium-dependent ATPase activity and cooperativity of magnesium chelatase from Synechocystis sp. PCC6803. J Biol Chem 279:26893–26899

    PubMed  CAS  Google Scholar 

  • Reid JD, Siebert CA, Bullough PA, Hunter CN (2003) The ATPase activity of the ChlI subunit of magnesium chelatase and formation of a heptameric AAA+ ring. Biochemistry 42:6912–6920

    PubMed  CAS  Google Scholar 

  • Reinbothe S, Reinbothe C, Runge S, Apel K (1995a) Enzymatic product formation impairs both the chloroplast receptor-binding function as well as translocation competence of the NADPH: protochlorophyllide oxidoreductase, a nuclear-encoded plastid precursor protein. J Cell Biol 129:299–308

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Reinbothe S, Reinbothe C, Neumann D, Apel K (1996) A plastid enzyme arrested in the step of precursor translocation in vivo. Proc Natl Acad Sci USA 93:12026–12030

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Reinbothe C, Lepinat A, Deckers M, Beck E, 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

    PubMed  CAS  Google Scholar 

  • Reinbothe S, Pollmann S, 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

    PubMed  CAS  Google Scholar 

  • Reinbothe S, Quigley F, Gray J, Schemenewitz A, Reinbothe C (2004a) Identification of plastid envelope proteins required for import of protochlorophyllide oxidoreductase A into the chloroplast of barley. Proc Natl Acad Sci USA 101:2197–2202

    PubMed  CAS  Google Scholar 

  • Reinbothe S, Quigley F, Springer A, Schemenewitz A, Reinbothe C (2004b) The outer plastid envelope protein Oep16: role as precursor translocase in import of protochlorophyllide oxidoreductase A. Proc Natl Acad Sci USA 101:2203–2208

    PubMed  CAS  Google Scholar 

  • Reinbothe S, Pollmann S, Springer A, James RJ, Tichtinsky G, Reinbothe C (2005) A role of Toc33 in the protochlorophyllide-dependent plastid import pathway of NADPH:protochlorophyllide oxidoreductase (POR) A. Plant J 42:1–12

    PubMed  CAS  Google Scholar 

  • Reinbothe C, Bartsch S, Eggink LL, Hoober JK, Brusslan J, Andrade-Paz R, Monnet J, Reinbothe S (2006) A role for chlorophyllide a oxygenase in the regulated import and stabilization of light-harvesting chlorophyll a/b proteins. Proc Natl Acad Sci USA 103:4777–4782

    PubMed  CAS  Google Scholar 

  • Rissler HM, Collakova E, DellaPenna D, Whelan J, Pogson BJ (2002) Chlorophyll biosynthesis. Expression of a second chl I gene of magnesium chelatase in Arabidopsis supports only limited chlorophyll synthesis. Plant Physiol 128:770–779

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rodermel S, Park S (2003) Pathways of intracellular communication: tetrapyrroles and plastid-to-nucleus signaling. Bioessays 25:631–636

    PubMed  CAS  Google Scholar 

  • Rüdiger W (2002) Biosynthesis of chlorophyll b and the chlorophyll cycle. Photosynth Res 74:187–193

    PubMed  Google Scholar 

  • Rüdiger W, Benz J, Guthoff C (1980) Detection and partial characterization of activity of chlorophyll synthetase in etioplast membranes. Eur J Biochem 109:193–200

    PubMed  Google Scholar 

  • Rüdiger W, Bohm S, Helfrich M, Schulz S, Schoch S (2005) Enzymes of the last steps of chlorophyll biosynthesis: modification of the substrate structure helps to understand the topology of the active centers. Biochemistry 44:10864–10872

    PubMed  Google Scholar 

  • Ryberg M, 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 

  • Rzeznicka K, Walker CJ, Westergren T, Kannangara CG, von Wettstein D, Merchant S, Gough SP, Hansson M (2005) Xantha-l encodes a membrane subunit of the aerobic Mg-protoporphyrin IX monomethyl ester cyclase involved in chlorophyll biosynthesis. Proc Natl Acad Sci USA 102:5886–5891

    PubMed  CAS  Google Scholar 

  • Satoh S, Tanaka A (2006) Identification of chlorophyllide a oxygenase in the Prochlorococcus genome by a comparative genomic approach. Plant Cell Physiol 47:1622–1629

    PubMed  CAS  Google Scholar 

  • Satoh S, Ikeuchi M, Mimuro M, Tanaka A (2001) Chlorophyll b expressed in Cyanobacteria functions as a light-harvesting antenna in photosystem I through flexibility of the proteins. J Biol Chem 276:4293–4297

    PubMed  CAS  Google Scholar 

  • Sawers RJ, Viney J, Farmer PR, Bussey RR, Olsefski G, Anufrikova K, Hunter CN, Brutnell TP (2006) The maize Oil yellow1 (Oy1) gene encodes the I subunit of magnesium chelatase. Plant Mol Biol 60:95–106

    PubMed  CAS  Google Scholar 

  • Schemenewitz A, Pollmann S, Reinbothe C, Reinbothe S (2007) A substrate-independent, 14:3:3 protein-mediated plastid import pathway of NADPH:protochlorophyllide oxidoreductase A. Proc Natl Acad Sci USA 104:8538–8543

    PubMed  CAS  Google Scholar 

  • Scheumann V, Schoch S, Rüdiger W (1998) Chlorophyll a formation in the chlorophyll b reductase reaction requires reduced ferredoxin. J Biol Chem 273:35102–35108

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Schmid HC, Oster U, Kogel J, Lenz S, Rüdiger W (2001) Cloning and characterisation of chlorophyll synthase from Avena sativa. Biol Chem 382:903–911

    PubMed  CAS  Google Scholar 

  • Schoefs B, Franck F (2003) Protochlorophyllide reduction: mechanisms and evolutions. Photochem Photobiol 78:543–557

    PubMed  CAS  Google Scholar 

  • Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Shepherd M, Hunter CN (2004) Transient kinetics of the reaction catalysed by magnesium protoporphyrin IX methyltransferase. Biochem J 382:1009–1013

    PubMed  CAS  Google Scholar 

  • Shioi Y, Sasa T (1983) Esterification of chlorophyllide b in higher plants. Biochim Biophys Acta 756:127–131

    CAS  Google Scholar 

  • Sirijovski N, Olsson U, Lundqvist J, Al-Karadaghi S, Willows RD, Hansson M (2006) ATPase activity associated with the magnesium chelatase H-subunit of the chlorophyll biosynthetic pathway is an artifact. Biochem J 400:477–484

    PubMed  CAS  Google Scholar 

  • Smith CA, Suzuki JY, Bauer CE (1996) Cloning and characterization of the chlorophyll biosynthesis gene chlM from Synechocystis PCC 6803 by complementation of a bacteriochlorophyll biosynthesis mutant of Rhodobacter capsulatus. Plant Mol Biol 30:1307–1314

    PubMed  CAS  Google Scholar 

  • Smith MD, Rounds CM, Wang F, Chen K, Afitlhile M, Schnell DJ (2004) atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J Cell Biol 165:323–334

    PubMed  CAS  Google Scholar 

  • Soldatova O, Apchelimov A, Radukina N, Ezhova T, Shestakov S, Ziemann V, Hedtke B, Grimm B (2005) An Arabidopsis mutant that is resistant to the protoporphyrinogen oxidase inhibitor acifluorfen shows regulatory changes in tetrapyrrole biosynthesis. Mol Genet Genomics 273:311–318

    PubMed  CAS  Google Scholar 

  • Spano AJ, He Z, Michel H, Hunt DF, 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

    PubMed  CAS  Google Scholar 

  • Sperling U, van Cleve B, Frick G, Apel K, 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

    PubMed  CAS  Google Scholar 

  • Sperling U, Franck F, van Cleve B, Frick G, Apel K, 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

    PubMed  CAS  Google Scholar 

  • Strand A (2004) Plastid-to-nucleus signalling. Curr Opin Plant Biol 7:621–625

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74:787–799

    PubMed  CAS  Google Scholar 

  • Takamiya KI, Tsuchiya T, Ohta H (2000) Degradation pathway(s) of chlorophyll: what has gene cloning revealed? Trends Plant Sci 5:426–431

    PubMed  CAS  Google Scholar 

  • Tanaka R, Tanaka A (2005) Effects of chlorophyllide a oxygenase overexpression on light acclimation in Arabidopsis thaliana. Photosynth Res 85:327–340

    PubMed  CAS  Google Scholar 

  • Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248–255

    PubMed  CAS  Google Scholar 

  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tanaka R, Koshino Y, Sawa S, Ishiguro S, Okada K, Tanaka A (2001) Overexpression of chlorophyllide a oxygenase (CAO) enlarges the antenna size of photosystem II in Arabidopsis thaliana. Plant J 26:365–373

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tomitani A, Okada K, Miyashita H, Matthijs HCP, Ohno T, Tanaka A (1999) Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature 400:159–162

    PubMed  CAS  Google Scholar 

  • Tottey S, Block MA, Allen M, Westergren T, Albrieux C, Scheller HV, Merchant S, Jensen PE (2003) Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide. Proc Natl Acad Sci USA 100:16119–16124

    PubMed  CAS  Google Scholar 

  • Tsuchiya T, Ohta H, Okawa K, Iwamatsu A, Shimada H, Masuda T, Takamiya K (1999) Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: finding of a lipase motif and the induction by methyl jasmonate. Proc Natl Acad Sci USA 96:15362–15367

    PubMed  CAS  Google Scholar 

  • Tsuchiya T, Suzuki T, Yamada T, Shimada H, Masuda T, Ohta H, Takamiya K (2003) Chlorophyllase as a serine hydrolase: identification of a putative catalytic triad. Plant Cell Physiol 44:96–101

    PubMed  CAS  Google Scholar 

  • Vavilin DV, Vermaas WF (2002) Regulation of the tetrapyrrole biosynthetic pathway leading to heme and chlorophyll in plants and cyanobacteria. Physiol Plant 115:9–24

    PubMed  CAS  Google Scholar 

  • Verdecia MA, Larkin RM, Ferrer JL, Riek R, Chory J, Noel JP (2005) Structure of the Mg-chelatase cofactor GUN4 reveals a novel hand-shaped fold for porphyrin binding. PLoS Biol 3:e151

    PubMed  Google Scholar 

  • von Gromoff ED, Schroda M, Oster U, Beck CF (2006) Identification of a plastid response element that acts as an enhancer within the Chlamydomonas HSP70A promoter. Nucleic Acids Res 34:4767–4779

    Google Scholar 

  • Wakao N, Yokoi N, Isoyama N, Hiraishi A, Shimada K, Kobayashi M, Kise H, Iwaki M, Itoh S, Takaichi S, Sakurai Y (1996) Discovery of natural photosynthesis using Zn-containing bacteriochlorophyll in an aerobic bacterium Acidiphilium rubrum. Plant Cell Physiol 37:889–893

    CAS  Google Scholar 

  • Walker CJ, Weinstein JD (1991a) Further characterization of the magnesium chelatase in isolated developing cucumber chloroplasts. Plant Physiol 95:1189–1196

    PubMed  CAS  Google Scholar 

  • Walker CJ, Weinstein JD (1991b) In vitro assay of the chlorophyll biosynthetic enzyme Mg-chelatase: resolution of the activity into soluble and membrane-bound fractions. Proc Natl Acad Sci USA 88:5789–5793

    PubMed  CAS  Google Scholar 

  • Walker CJ, Weinstein JD (1994) The magnesium-insertion step of chlorophyll biosynthesis is a two-stage reaction. Biochem J 299:277–284

    PubMed  CAS  Google Scholar 

  • Walker CJ, Willows RD (1997) Mechanism and regulation of Mg-chelatase. Biochem J 327:321–333

    PubMed  CAS  Google Scholar 

  • Walker CJ, Mansfield KE, Rezzano IN, Hanamoto CM, Smith KM, Castelfranco PA (1988) The magnesium-protoporphyrin IX (oxidative) cyclase system. Studies on the mechanism and specificity of the reaction sequence. Biochem J 255:685–692

    PubMed  CAS  Google Scholar 

  • Walker CJ, Mansfield KE, Smith KM, Castelfranco PA (1989) Incorporation of atmospheric oxygen into the carbonyl functionality of the protochlorophyllide isocyclic ring. Biochem J 257:599–602

    PubMed  CAS  Google Scholar 

  • Wilde A, Mikolajczyk S, Alawady A, Lokstein H, Grimm B (2004) The gun4 gene is essential for cyanobacterial porphyrin metabolism. FEBS Lett 571:119–123

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Willows RD, 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

    PubMed  CAS  Google Scholar 

  • Willows RD, Gibson LCD, Kanangara CG, Hunter CN, von Wettstein D (1996) Three separate proteins constitute the magnesium chelatase of Rhodobacter sphaeroides. Eur J Biochem 235:438–443

    PubMed  CAS  Google Scholar 

  • Willows RD, Hansson A, Birch D, Al-Karadaghi S, Hansson M (2004) EM single particle analysis of the ATP-dependent BchI complex of magnesium chelatase: an AAA+ hexamer. J Struct Biol 146:227–233

    PubMed  CAS  Google Scholar 

  • Wu Q, 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

    PubMed  CAS  Google Scholar 

  • Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289:1724–1730

    PubMed  CAS  Google Scholar 

  • Yamasato A, Nagata N, Tanaka R, Tanaka A (2005) The N-terminal domain of chlorophyllide a oxygenase confers protein instability in response to chlorophyll B accumulation in Arabidopsis. Plant Cell 17:1585–1597

    PubMed  CAS  Google Scholar 

  • Yamazaki S, Nomata J, Fujita Y (2006) Differential operation of dual protochlorophyllide reductases for chlorophyll biosynthesis in response to environmental oxygen levels in the cyanobacterium Leptolyngbya boryana. Plant Physiol 142:911–922

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Zhang H, Li J, Yoo JH, Yoo SC, Cho SH, Koh HJ, Seo HS, Paek NC (2006) Rice Chlorina-1 and Chlorina-9 encode ChlD and ChlI subunits of Mg-chelatase, a key enzyme for chlorophyll synthesis and chloroplast development. Plant Mol Biol 62:325–337

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

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Acknowledgments

I am grateful to Dr. Ryouichi Tanaka for critical reading of the manuscript. I acknowledge the financial support from a Grant-in-Aid for Scientific Research (18570034) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Correspondence to Tatsuru Masuda.

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Masuda, T. Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls. Photosynth Res 96, 121–143 (2008). https://doi.org/10.1007/s11120-008-9291-4

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  • DOI: https://doi.org/10.1007/s11120-008-9291-4

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