Abstract
The importance of chlorophyll (Chl) to the process of photosynthesis is obvious, and there is clear evidence that the regulation of Chl biosynthesis has a significant role in the regulation of assembly of the photosynthetic apparatus. The understanding of Chl biosynthesis has rapidly advanced in recent years. The identification of genetic loci associated with each of the biochemical steps has been accompanied by a greater appreciation of the role of Chl biosynthesis intermediates in intracellular signaling. The purpose of this review is to provide a source of information for all the steps in Chl and bacteriochlorophyll a biosynthesis, with an emphasis on steps that are believed to be key regulation points.
Similar content being viewed by others
Abbreviations
- Chl:
-
Chlorophyll
- Bchl:
-
Bacteriochlorophyll
- MP:
-
Mg-protoporphyrin IX
- MPE:
-
Mg-protoporphyrin IX monomethyl ester
- Pchlide:
-
Protochlorophyllide
- ALA:
-
δ-aminolevulinic acid
- PIX:
-
protoporphyrin IX
- POR:
-
protochlorophyllide oxidoreductase
- Chlide:
-
Chlorophyllide
References
Addlesee HA, Gibson LC, Jensen PE, Hunter CN (1996) Cloning, sequencing and functional assignment of the chlorophyll biosynthesis gene, chlP, of Synechocystis sp. PCC 6803. FEBS Lett 389:126–130
Aklujkar M, Prince RC, Beatty JT (2005) The puhE gene of Rhodobacter capsulatus is needed for optimal transition from aerobic to photosynthetic growth and encodes a putative negative modulator of bacteriochlorophyll production. Arch Biochem Biophys 437:186–198
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
Armstrong GA, Runge S, Frick G, Sperling U, Apel K (1995) Identification of NADPH:protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol 108:1505–1517
Avissar YJ, Moberg P (1995) The common origins of the pigments of life-early steps of chlorophyll biosynthesis. Photosynth Res 44: 221–242
Bauer CE, Bird TH (1996) Regulatory circuits controlling photosynthesis gene expression. Cell 85:5–8
Bauer CE, Marrs BL (1988) Rhodobacter capsulatus puf operon encodes a regulatory protein (PufQ) for bacteriochlorophyll biosynthesis. Proc Natl Acad Sci USA 85:7074–7078
Bauer CE, Bollivar DW, Suzuki JY (1993) Genetic analyses of photopigment biosynthesis in eubacteria: a guiding light for algae and plants. J Bacteriol 175:3919–3925
Beale SI (2005) Green genes gleaned. Trends Plant Sci 10:309–312
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
Bollivar DW (2003) Intermediate steps in chlorophyll biosynthesis: methylation and cyclization. In: Kadish KM et al (eds) The Porphyrin handbook, 13. Elsevier, New York, pp 49–69
Bollivar DW, Beale SI (1996) The chlorophyll biosynthetic enzyme Mg-protoporphyrin IX monomethyl ester (oxidative) cyclase: characterization and partial purification from Chlamydomonas reinhardtii and Synechocystis sp. PCC 6803). Plant Physiol 112:105–114
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
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
Bollivar DW, Wang S, Allen JP, Bauer CE (1994c) Molecular genetic analysis of terminal steps in bacteriochlorophyll a biosynthesis: characterization of a Rhodobacter capsulatus strain that synthesizes geranylgeraniol-esterified bacteriochlorophyll a. Biochemistry 33:12763–12768
Braatsch S, Moskvin OV, Klug G, Gomelsky M (2004) Responses of the Rhodobacter sphaeroides transcriptome to blue light under semiaerobic conditions. J Bacteriol 186:7726–7735
Brusslan J, Peterson MP (2002) Tetrapyrrole regulation of nuclear gene expression. Photosynth Res 71:185–194
Cahoon AB, Timko MP (2000) Yellow-in-the-dark mutants of Chlamydomonas lack the CHLL subunit of light-independent protochlorophyllide reductase. Plant Cell 12:559–568
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
DeLano WL, Lam JW (2005). PyMOL, 0.98 ed. DeLano Scientific LLC, South San Francisco, CA
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
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 U S A 96:10507–10511
Fidai S, Hinchigeri SB, Borgford TJ, Richards WR (1994a) Identification of the PufQ protein in membranes of Rhodobacter capsulatus. J Bacteriol 176:7244–7251
Fidai S, Hinchigeri SB, Richards WR (1994b) Association of protochlorophyllide with the PufQ protein of Rhodobacter capsulatus. Biochem Biophys Res Commun 200:1679– 1684
Fidai S, Dahl JA, Richards WR (1995) Effect of the PufQ protein on early steps in the pathway of bacteriochlorophyll biosynthesis in Rhodobacter capsulatus. FEBS Lett 372:264–268
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
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
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
Fujita Y, Bauer CE (2003) The light-dependent protochlorophyllide reductase: a nitrogenase-like enzyme catalyzing a key reaction for greening in the dark. In: Kadish KM et al (eds) The porphyrin handbook, 13. Elsevier, New York, pp 109–156
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
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
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
Gibson LC, Hunter CN (1994) The bacteriochlorophyll biosynthesis gene, bchM, of Rhodobacter sphaeroides encodes S-adenosyl-L-methionine: Mg protoporphyrin IX methyltransferase. FEBS Lett 352:127–130
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
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
Gomelsky M, Kaplan S (1995a) appA, a novel gene encoding a trans-acting factor involved in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J␣Bacteriol 177:4609–4618
Gomelsky M, Kaplan S (1995b) Genetic evidence that PpsR from Rhodobacter sphaeroides 2.4.1 functions as a repressor of puc and bchF expression. J Bacteriol 177:1634–1637
Gomelsky M, Kaplan S (1997) Molecular genetic analysis suggesting interactions between AppA and PpsR in regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol 179:128–134
Gomelsky M, Kaplan S (1998) AppA, a redox regulator of photosystem formation in Rhodobacter sphaeroides 2.4.1, is a flavoprotein. Identification of a novel FAD binding domain. J Biol Chem 273:35319–35325
Gomelsky M, Horne IM, Lee HJ, Pemberton JM, McEwan AG, Kaplan S (2000) Domain structure, oligomeric state, and mutational analysis of PpsR, the Rhodobacter sphaeroides repressor of photosystem gene expression. J Bacteriol 182:2253–2261
Gorchein A (1972) Magnesium protoporphyrin chelatase activity in Rhodopseudomonas spheroides. Studies with whole cells. Biochem J 127:97–106
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
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
Grafe S, Saluz HP, Grimm B, Hanel 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
Granick S (1949) The structural and functional relationships between heme and chlorophyll. Harvey Lect 44:220–245
Gray JC (2003) Chloroplast-to-nucleus signalling: a role for Mg-protoporphyrin. Trends Genet 19:526–529
Grimm B (2003) Regulatory mechanisms in eukaryotic tetrapyrrole biosynthesis. In: Kadish KM et al (eds) The Porphyrin Handbook, 12. Elsevier, New York, pp 1–32
Grinstead JS, Hsu ST, Laan W, Bonvin AM, Hellingwerf KJ, Boelens R, Kaptein R (2006) The solution structure of the AppA BLUF domain: insight into the mechanism of light-induced signaling. Chembiochem 7:187–193
Guo R, Luo M, Weinstein JD (1998) Mg-chelatase from developing pea leaves: characterization of a soluble extract from chloroplasts and resolution into three required protein fractions. Plant Physiol 116:605–615
Hansson A, Kannangara 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
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
He Q, Brune D, Nieman R, Vermaas W (1998) Chlorophyll a synthesis upon interruption and deletion of por coding for the light-dependent NADPH: protochlorophyllide oxidoreductase in a photosystem-I-less/chlL- strain of Synechocystis sp. PCC 6803. Eur J Biochem 253:161–172
Heyes DJ, Hunter CN (2002) Site-directed mutagenesis of Tyr-189 and Lys-193 in NADPH: protochlorophyllide oxidoreductase from Synechocystis. Biochem Soc Trans 30:601–604
Heyes DJ, Hunter CN (2004) Identification and characterization of the product release steps within the catalytic cycle of protochlorophyllide oxidoreductase. Biochemistry 43:8265–8271
Heyes DJ, Hunter CN (2005) Making light work of enzyme catalysis: protochlorophyllide oxidoreductase. Trends Biochem Sci 30:642–649
Heyes DJ, Martin GE, Reid RJ, Hunter CN, Wilks HM (2000) NADPH:protochlorophyllide oxidoreductase from Synechocystis: overexpression, purification and preliminary characterisation. FEBS Lett 483:47–51
Heyes DJ, Ruban AV, Wilks HM, 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
Heyes DJ, Hunter CN, van Stokkum IH, van Grondelle R, Groot ML (2003) Ultrafast enzymatic reaction dynamics in protochlorophyllide oxidoreductase. Nat Struct Biol 10:491–492
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
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
Huq E, Al-Sady B, Hudson M, Kim C, Apel K, Quail PH (2004) Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305:1937–1941
Jaffe EK (2003) An unusual phylogenetic variation in the metal ion binding sites of porphobilinogen synthase. Chem Biol 10:25–34
Jaffe EK (2004) The porphobilinogen synthase catalyzed reaction mechanism. Bioorg Chem 32:316–325
Jensen PE, Gibson LC, Henningsen KW, Hunter CN (1996) 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
Jensen PE, Gibson LC, Shephard F, Smith V, Hunter CN (1999) 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
Kannangara CG, Vothknecht UC, Hansson M, von Wettstein D (1997) Magnesium chelatase: association with ribosomes and mutant complementation studies identify barley subunit Xantha-G as a functional counterpart of Rhodobacter subunit BchD. Mol Gen Genet 254:85–92
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
Kim C, Apel K (2004) Substrate-dependent and organ-specific chloroplast protein import in planta. Plant Cell 16:88–98
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
Klement H, Helfrich M, Oster U, Schoch S, Rudiger W (1999) Pigment-free NADPH:protochlorophyllide oxidoreductase from Avena sativa L. Purification and substrate specificity. Eur J Biochem 265:862–874
Kovacs AT, Rakhely G, Kovacs KL (2005) The PpsR regulator family. Res Microbiol 156:619–625
Kropat J, Oster U, Rudiger 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
Kropat J, Oster U, Rudiger 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
Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299:902–906
Lebedev N, Karginova O, McIvor W, 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
Lee KP, Kim C, Lee DW, 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
Li J, 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
Lopez JC, Ryan S, Blankenship RE (1996) Sequence of the bchG gene from Chloroflexus aurantiacus: relationship between chlorophyll synthase and other polyprenyltransferases. J Bacteriol 178:3369–3373
Masuda S, Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613–623
Masuda S, Dong C, Swem D, Setterdahl AT, Knaff DB, Bauer CE (2002) Repression of photosynthesis gene expression by formation of a disulfide bond in CrtJ. Proc Natl Acad Sci USA 99:7078–7083
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 (2003) Functional analysis of isoforms of NADPH: protochlorophyllide oxidoreductase (POR), PORB and PORC, in Arabidopsis thaliana. Plant Cell Physiol 44:963–974
McFarlane MJ, Hunter CN, Heyes DJ (2005) Kinetic characterisation of the light-driven protochlorophyllide oxidoreductase (POR) from Thermosynechococcus elongatus. Photochem Photobiol Sci 4:1055–1059
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
Mochizuki N, Susek R, Chory J (1996) An intracellular signal transduction pathway between the chloroplast and nucleus␣is involved in de-etiolation. Plant Physiol 112:1465–1469
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
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
Moseley JL, Page MD, Alder NP, Eriksson M, Quinn J, Soto F, Theg SM, Hippler M, Merchant S (2002) Reciprocal expression of two candidate di-iron enzymes affecting photosystem I and light-harvesting complex accumulation. Plant Cell 14:673–688
Moskvin OV, Gomelsky L, Gomelsky M (2005) Transcriptome analysis of the Rhodobacter sphaeroides PpsR regulon: PpsR as a master regulator of photosystem development. J␣Bacteriol 187:2148–2156
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
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
Nomata J, Swem LR, Bauer CE, Fujita Y (2005) Overexpression and characterization of dark-operative protochlorophyllide reductase from Rhodobacter capsulatus. Biochim Biophys Acta 1708:229–237
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
Oster U, Bauer CE, Rudiger W (1997) Characterization of chlorophyll a and bacteriochlorophyll a synthases by heterologous expression in Escherichia coli. J Biol Chem 272:9671–9676
Oster U, Tanaka R, Tanaka A, Rudiger 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
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
Ougham HJ, Thomas AM, Thomas BJ, Frick GA, Armstrong GA (2001) Both light-dependent protochlorophyllide oxidoreductase A and protochlorophyllide oxidoreductase B are down-regulated in the slender mutant of barley. J Exp Bot 52:1447–1454
Papenbrock J, Grimm B (2001) Regulatory network of tetrapyrrole biosynthesis–studies of intracellular signalling involved in metabolic and developmental control of plastids. Planta 213:667–681
Papenbrock J, Mock HP, Tanaka R, Kruse E, Grimm B (2000) Role of magnesium chelatase activity in the early steps of the tetrapyrrole biosynthetic pathway. Plant Physiol 122:1161–1169
Pemberton JM, Horne IM, McEwan AG (1998) Regulation of photosynthetic gene expression in purple bacteria. Microbiology 144:267–278
Penfold RJ, Pemberton JM (1994) Sequencing, chromosomal inactivation, and functional expression in Escherichia coli of ppsR, a gene which represses carotenoid and bacteriochlorophyll synthesis in Rhodobacter sphaeroides. J Bacteriol 176:2869–2876
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
Ponnampalam SN, Bauer CE (1997) DNA binding characteristics of CrtJ. A redox-responding repressor of bacteriochlorophyll, carotenoid, and light harvesting-II gene expression in Rhodobacter capsulatus. J Biol Chem 272:18391–18396
Ponnampalam SN, Buggy JJ, Bauer CE (1995) Characterization of an aerobic repressor that coordinately regulates bacteriochlorophyll, carotenoid, and light harvesting-II expression in Rhodobacter capsulatus. J Bacteriol 177:2990–2997
Ponnampalam SN, Elsen S, Bauer CE (1998) Aerobic repression of the Rhodobacter capsulatus bchC promoter involves cooperative interactions between CrtJ bound to neighboring palindromes. J Biol Chem 273:30757–30761
Porra RJ, Schafer W, Katheder I, Scheer H (1995) The derivation of the oxygen atoms of the 13(1)-oxo and 3-acetyl groups of bacteriochlorophyll a from water in Rhodobacter sphaeroides cells adapting from respiratory to photosynthetic conditions: evidence for an anaerobic pathway for the formation of isocyclic ring E. FEBS Lett 371:21–24
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
Rebeiz CA, Parham R, Fasoula DA, Ioannides IM (1994) Chlorophyll a biosynthetic heterogeneity. Ciba Found Symp 180:177–189; discussion 190–173
Reid JD, Hunter CN (2004) Magnesium-dependent ATPase activity and cooperativity of magnesium chelatase from Synechocystis sp. PCC6803. J Biol Chem 279:26893– 26899
Reinbothe C, Lebedev N, Reinbothe S (1999) A protochlorophyllide light-harvesting complex involved in de-etiolation of higher plants. Nature 397:80–84
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
Reinbothe S, Pollmann S, Reinbothe C (2003b) 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
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
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
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
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
Rudiger W (2003) The last steps of chlorophyll biosynthesis. In: Kadish KM et al (eds) The Porphyrin Handbook, 13. Elsevier, New York, pp 71–108
Rudiger W, Benz J, Guthoff C (1980) Detection and partial characterization of activity of chlorophyll synthetase in etioplast membranes. Eur J Biochem 109:193–200
Runge S, Sperling U, Frick G, Apel K, 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
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
Sager R (1955) Inheritance in the green alga Chlamydomonas reinhardtii. Genetics 40:476–489
Santel HJ, Apel K (1981) The protochlorophyllide holochrome of barley (Hordeum vulgare L.). The effect of light on the NADPH:protochlorophyllide oxidoreductase. Eur J Biochem 120:95–103
Scheumann V, Klement H, Helfrich M, Oster U, Schoch S, Rudiger W (1999) Protochlorophyllide b does not occur in barley etioplasts. FEBS Lett 445:445–448
Schmid HC, Oster U, Kogel J, Lenz S, Rudiger W (2001) Cloning and characterisation of chlorophyll synthase from Avena sativa. Biol Chem 382:903–911
Schoefs B (2001) The protochlorophyllide-chlorophyllide cycle. Photosynth Res 70:257–271
Schoefs B, Franck F (2003) Protochlorophyllide reduction: mechanisms and evolutions. Photochem Photobiol 78:543–557
Shedbalkar VP, Ioannides IM, Rebeiz CA (1991) Chloroplast biogenesis. Detection of monovinyl protochlorophyll(ide) b in plants. J Biol Chem 266:17151–17157
Shepherd M, Hunter CN (2004) Transient kinetics of the reaction catalysed by magnesium protoporphyrin IX methyltransferase. Biochem J 382:1009–1013
Shepherd M, Reid JD, Hunter CN (2003) Purification and kinetic characterization of the magnesium protoporphyrin IX methyltransferase from Synechocystis PCC6803. Biochem J 371:351–360
Shepherd M, McLean S, Hunter CN (2005) Kinetic basis for linking the first two enzymes of chlorophyll biosynthesis. FEBS J 272:4532–4539
Shioi Y, Sasa T (1984) Terminal steps of bacteriochlorophyll a phytol formation in purple photosynthetic bacteria. J Bacteriol 158:340–343
Shoolingin-Jordan PM (2003) The biosynthesis of Coproporphyrinogen III. In:Kadish KM et al (eds) The Porphyrin Handbook, 12. Elsevier Science, Amsterdam, pp 33– 74
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
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
Steunou AS, Astier C, Ouchane S (2004) Regulation of photosynthesis genes in Rubrivivax gelatinosus: transcription factor PpsR is involved in both negative and positive control. J␣Bacteriol 186:3133–3142
Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421:79–83
Su Q, Frick G, Armstrong G, 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
Surpin M, Chory J (1997) The co-ordination of nuclear and organellar genome expression in eukaryotic cells. Essays Biochem 32:113–125
Susek R, Ausubel F, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74:787–799
Suzuki JY, Bollivar DW, Bauer CE (1997) Genetic analysis of chlorophyll biosynthesis. Annu Rev Genet 31:61–89
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
Tanaka R, Oster U, Kruse E, Rudiger W, Grimm B (1999) Reduced activity of geranylgeranyl reductase leads to loss of chlorophyll and tocopherol and to partially geranylgeranylated chlorophyll in transgenic tobacco plants expressing antisense RNA for geranylgeranyl reductase. Plant Physiol 120:695–704
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
Townley HE, Sessions RB, Clarke AR, Dafforn TR, Griffiths WT (2001) Protochlorophyllide oxidoreductase: a homology model examined by site-directed mutagenesis. Proteins 44:329–335
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
Vinti G, Hills A, Campbell S, Bowyer JR, Mochizuki N, Chory J, Lopez-Juez E (2000) Interactions between hy1 and gun mutants of Arabidopsis, and their implications for plastid/nuclear signaling. Plant J 24:883–894
Walker CJ, Weinstein JD (1991) 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
Walker CJ, Weinstein JD (1994) The magnesium-insertion step of chlorophyll biosynthesis is a two-stage reaction. Biochem J 299:277–284
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
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
Walker CJ, Castelfranco PA, Whyte BJ (1991) Synthesis of divinyl protochlorophyllide. Enzymological properties of the Mg-protoporphyrin IX monomethyl ester oxidative cyclase system. Biochem J 276:691–697
Walker CJ, Hupp LR, Weinstein JD (1992) Activation and stabilization of Mg-chelatase activity by ATP as revealed by a novel in vitro continuous assay. Plant Physiol Biochem 30:263–269
Whyte BJ, Castelfranco PA (1993) Further observations on the Mg-protoporphyrin IX monomethyl ester (oxidative) cyclase system. Biochem J 290:355–359
Willows RD (2003) Biosynthesis of chlorophylls from protoporphyrin IX. Nat Prod Rep 20:327–341
Willows RD, Hansson M (2003) Mechanism, structure, and regulation of magnesium chelatase. In: Kadish KM et al (eds) The Porphyrin Handbook, 13. Elsevier Science, Amsterdam, pp 1–48
Willows RD, Hansson M, Beale SI, Laurberg M, Al-Karadaghi S (1999) Crystallization and preliminary X-ray analysis of the Rhodobacter capsulatus magnesium chelatase BchI␣subunit. Acta Crystallogr D Biol Crystallogr 55:689–690
Willows RD, Lake V, Roberts TH, Beale SI (2003a) Inactivation of Mg chelatase during transition from anaerobic to aerobic growth in Rhodobacter capsulatus. J Bacteriol 185:3249– 3258
Willows RD, Sirijovski N, Olsson U, Lake V, Hansson M (2003b) Comparison of dynamic binding with equilibrium␣binding methods in estimation of Kd values for porphyrin binding to the BchH subunit of magnesium chelatase. Eds Combio combined conference abstracts, 155, ASBMB
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
Wong Y-S, Castelfranco PA (1984) Resolution and reconstitution of Mg-protoporphyrin IX monomethyl ester (oxidative) cyclase, the enzyme system responsible for the formation of the chlorophyll isocyclic ring. Plant Physiol 75:658–661
Wong Y-S, Castelfranco PA, Goff DA, Smith KM (1985) Intermediates in the formation of the chlorophyll isocyclic ring. Plant Physiol 79:725–729
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
Yang ZM, Bauer CE (1990) Rhodobacter capsulatus genes involved in early steps of the bacteriochlorophyll biosynthetic pathway. J Bacteriol 172:5001–5010
Acknowledgements
The author is indebted to several colleagues, including Dr. Mats Hansson for graciously providing Fig. 3 and Dr. Sarah H. Lawrence for extensive help in generating Fig. 4. He is also indebted to Dr. Eileen Jaffe who served as a host for his sabbatical, and members of her laboratory for stimulating scientific discussion. The author also recognizes the support received from a National Science Foundation Grant MCB-0109909.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bollivar, D.W. Recent advances in chlorophyll biosynthesis. Photosynth Res 89, 1–22 (2006). https://doi.org/10.1007/s11120-006-9076-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-006-9076-6