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Biosynthesis of Chlorophyll and Bilins in Algae

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Photosynthesis in Algae: Biochemical and Physiological Mechanisms

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 45))

Abstract

Chlorophylls and bilins are tetrapyrrole pigments that are synthesized from the universal five carbon precursor aminolevulinic acid (ALA). All algae and cyanobacteria make chlorophylls, and they also appear to have the ability to make bilins. The primary use of chlorophylls and bilins are as light harvesting pigments in these organisms. Chlorophylls are present in the light harvesting complexes and reaction centres while bilins are pigment components of phycobilisomes. Phycobilisomes appear to be restricted to the cyanobacteria, glaucophytes, red algae and the secondary endosymbiotic ancestors of the red algae such as the cryptophytes. This chapter explores the diversity and biosynthesis of both bilins and chlorophylls which are used in light harvesting for photosynthesis in algae and cyanobacteria.

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Bibliography

  • Adams NB, Reid JD (2013) The allosteric role of the AAA+ domain of ChlD protein from the magnesium chelatase of synechocystis species PCC 6803. J Biol Chem 288(40):28727–28732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adams NBP et al (2014) Structural and functional consequences of removing the N-terminal domain from the magnesium chelatase ChlH subunit of Thermosynechococcus elongatus. Biochem J 464(3):315–322

    Article  CAS  PubMed  Google Scholar 

  • Adams NB et al (2016) Nanomechanical and thermophoretic analyses of the nucleotide-dependent interactions between the AAA(+) subunits of magnesium chelatase. J Am Chem Soc 138(20):6591–6597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Addlesee HA et al (1996) Cloning, sequencing and functional assignment of the chlorophyll biosynthesis gene, chlP, of Synechocystis sp. PCC 6803. FEBS Lett 389(2):126–130

    Article  CAS  PubMed  Google Scholar 

  • Adhikari ND et al (2009) Porphyrins promote the association of genomes uncoupled 4 and a Mg-chelatase subunit with chloroplast membranes. J Biol Chem 284(37):24783–24796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adhikari ND et al (2011) GUN4-porphyrin complexes bind the ChlH/GUN5 subunit of Mg-chelatase and promote chlorophyll biosynthesis in arabidopsis. Plant Cell 23(4):1449–1467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akiyama M et al (2001) Detection of chlorophyll d’ and pheophytin a in a chlorophyll d-dominating oxygenic photosynthetic prokaryote Acaryochloris marina. Anal Sci 17(1):205–208

    Article  CAS  PubMed  Google Scholar 

  • Akiyama M et al (2002a) Quest for minor but key chlorophyll molecules in photosynthetic reaction centers – unusual pigment composition in the reaction centers of the chlorophyll d-dominated cyanobacterium Acaryochloris marina. Photosynth Res 74(2):97–107

    Article  CAS  PubMed  Google Scholar 

  • Akiyama M et al (2002b) Detection of chlorophyll d’ and pheophytin a in a chlorophyll d-dominating oxygenic photosynthetic prokaryote Acaryochloris marina. Plant Cell Physiol 43:S170–S170

    Article  Google Scholar 

  • Akutsu S et al (2011) Pigment analysis of a chlorophyll f-containing cyanobacterium strain KC1isolated from Lake Biwa. Photomed Photobiol 33:35–40

    CAS  Google Scholar 

  • Allen MD, Kropat J, Merchant SS (2008) Regulation and localization of isoforms of the aerobic oxidative cyclase in Chlamydomonas reinhardtii. Photochem Photobiol 84(6):1336–1342

    Article  CAS  PubMed  Google Scholar 

  • Arciero DM, Bryant DA, Glazer AN (1988a) In vitro attachment of bilins to apophycocyanin. I. Specific covalent adduct formation at cysteinyl residues involved in phycocyanobilin binding in C-phycocyanin. J Biol Chem 263(34):18343–18349

    Article  CAS  PubMed  Google Scholar 

  • Arciero DM, Dallas JL, Glazer AN (1988b) In vitro attachment of bilins to apophycocyanin. III. Properties of the phycoerythrobilin adduct. J Biol Chem 263(34):18358–18363

    Article  CAS  PubMed  Google Scholar 

  • Arciero DM, Dallas JL, Glazer AN (1988c) In vitro attachment of bilins to apophycocyanin. II. Determination of the structures of tryptic bilin peptides derived from the phycocyanobilin adduct. J Biol Chem 263(34):18350–18357

    Article  CAS  PubMed  Google Scholar 

  • Bernstein LS, Miller KR (1989) Unique location of the phycobiliprotein light-harvesting pigment in the Cryptophyceae. J Phycol 25(3):412–419

    Article  Google Scholar 

  • Biswas A et al (2011) Characterization of the activities of the CpeY, CpeZ, and CpeS bilin lyases in phycoerythrin biosynthesis in Fremyella diplosiphonStrain UTEX 481. J Biol Chem 286(41):35509–35521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bollivar D, Beale S (1995) Formation of the isocyclic ring of chlorophyll by isolated Chlamydomonas reinhardtii chloroplasts. Photosynth Res 43(2):113–124

    Article  CAS  PubMed  Google Scholar 

  • Bollivar D, Beale S (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(1):105–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bollivar D et al (2014) The Ycf54 protein is part of the membrane component of Mg-protoporphyrin IX monomethyl ester cyclase from barley (Hordeum vulgare L.). FEBS J 281(10):2377–2386

    Article  CAS  PubMed  Google Scholar 

  • Bretaudeau A et al (2013) CyanoLyase: a database of phycobilin lyase sequences, motifs and functions. Nucleic Acids Res 41(Database issue):D396–D401

    CAS  PubMed  Google Scholar 

  • Brindley AA et al (2015) Five glutamic acid residues in the C-terminal domain of the ChlD subunit play a major role in conferring Mg(2+) cooperativity upon magnesium chelatase. Biochemistry 54(44):6659–6662

    Article  CAS  PubMed  Google Scholar 

  • Brusslan J, Peterson M (2002) Tetrapyrrole regulation of nuclear gene expression. Photosynth Res 71(3):185–194

    Article  CAS  PubMed  Google Scholar 

  • Brzezowski P et al (2016) Mg chelatase in chlorophyll synthesis and retrograde signaling in Chlamydomonas reinhardtii: CHLI2 cannot substitute for CHLI1. J Exp Bot 67(13):3925–3938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Budzikiewicz H, Taraz K (1971) Chlorophyll c. Tetrahedron 27(7):1447–1460

    Article  CAS  Google Scholar 

  • Cahoon A, Timko M (2000) Yellow-in-the-dark mutants of Chlamydomonas lack the CHLL subunit of light-independent protochlorophyllide reductase. Plant Cell 12(4):559–568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canniffe DP, Chidgey JW, Hunter CN (2014) Elucidation of the preferred routes of C8-vinyl reduction in chlorophyll and bacteriochlorophyll biosynthesis. Biochem J 462(3):433–440

    Article  CAS  PubMed  Google Scholar 

  • Chekounova E et al (2001) Characterization of Chlamydomonas mutants defective in the H subunit of Mg-chelatase. Mol Gen Genomics 266(3):363–373

    Article  CAS  Google Scholar 

  • Chen M et al (2010) A red-shifted chlorophyll. Science 329(5997):1318–1319

    Article  CAS  PubMed  Google Scholar 

  • Chen M et al (2012) A cyanobacterium that contains chlorophyll f--a red-absorbing photopigment. FEBS Lett 586(19):3249–3254

    Article  CAS  PubMed  Google Scholar 

  • Chen X et al (2015a) Crystal structures of GUN4 in complex with porphyrins. Mol Plant 8(7):1125–1127

    Article  CAS  PubMed  Google Scholar 

  • Chen X et al (2015b) Crystal structure of the catalytic subunit of magnesium chelatase. Nat Plant 1:15125

    Article  CAS  Google Scholar 

  • Chen GE et al (2016) Two unrelated 8-vinyl reductases ensure production of mature chlorophylls in Acaryochloris marina. J Bacteriol 198(9):1393–1400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen GE, Canniffe DP, Hunter CN (2017) Three classes of oxygen-dependent cyclase involved in chlorophyll and bacteriochlorophyll biosynthesis. Proc Natl Acad Sci U S A 114(24):6280–6285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davison PA, Hunter CN (2011) Abolition of magnesium chelatase activity by the gun5 mutation and reversal by Gun4. FEBS Lett 585(1):183–186

    Article  CAS  PubMed  Google Scholar 

  • Davison PA et al (2005) Structural and biochemical characterization of Gun4 suggests a mechanism for its role in chlorophyll biosynthesis. Biochemistry 44(21):7603–7612

    Article  CAS  PubMed  Google Scholar 

  • Dorgan KM et al (2006) An enzyme-coupled continuous spectrophotometric assay for S-adenosylmethionine-dependent methyltransferases. Anal Biochem 350(2):249–255

    Article  CAS  PubMed  Google Scholar 

  • Duanmu D, Rockwell NC, Lagarias JC (2017) Algal light sensing and photoacclimation in aquatic environments. Plant Cell Environ 40(11):2558–2570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fairchild CD, Glazer AN (1994a) Nonenzymatic bilin addition to the alpha subunit of an apophycoerythrin. J Biol Chem 269(46):28988–28996

    Article  CAS  PubMed  Google Scholar 

  • Fairchild CD, Glazer AN (1994b) Oligomeric structure, enzyme kinetics, and substrate specificity of the phycocyanin alpha subunit phycocyanobilin lyase. J Biol Chem 269(12):8686–8694

    Article  CAS  PubMed  Google Scholar 

  • Fairchild CD et al (1992) Phycocyanin alpha-subunit phycocyanobilin lyase. Proc Natl Acad Sci U S A 89(15):7017–7021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falciatore A et al (2005) The FLP proteins act as regulators of chlorophyll synthesis in response to light and plastid signals in Chlamydomonas. Genes Dev 19(1):176–187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fodje MN et al (2001) Interplay between an AAA module and an integrin I domain may regulate the function of magnesium chelatase. J Mol Biol 311(1):111–122

    Article  CAS  PubMed  Google Scholar 

  • Fookes C, Jeffrey S (1989) The structure of chlorophyll c3, a novel marine photosynthetic pigment. J Chem Soc Chem Commun 23:1827–1828

    Article  Google Scholar 

  • Formighieri C et al (2012) Retrograde signaling and photoprotection in a gun4 mutant of Chlamydomonas reinhardtii. Mol Plant 5(6):1242–1262

    Article  CAS  PubMed  Google Scholar 

  • Frankenberg N, Lagarias JC (2003) Biosynthesis and biological functions of bilins. In: Kadish KM, Smith KM, Guilard R (eds) The porphyrin handbook. Academic, Amsterdam, pp 211–235

    Chapter  Google Scholar 

  • Fujita Y, Bauer CE (2003) The light-independent protochlorophyllide reductase: a nitrogenase-like enzyme catalysing a key reaction for greening in the dark. In: Kadish KM, Smith KM, Guilard R (eds) The porphyrin handbook. Academic, Amsterdam, pp 109–156

    Chapter  Google Scholar 

  • Fukusumi T et al (2012) Non-enzymatic conversion of chlorophyll-a into chlorophyll-d in vitro: a model oxidation pathway for chlorophyll-d biosynthesis. FEBS Lett 586(16):2338–2341

    Article  CAS  PubMed  Google Scholar 

  • Gabruk M, Mysliwa-Kurdziel B (2015) Light-dependent protochlorophyllide oxidoreductase: phylogeny, regulation, and catalytic properties. Biochemistry 54(34):5255–5262

    Article  CAS  PubMed  Google Scholar 

  • Gan F, Shen G, Bryant DA (2014a) Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria. Life (Basel, Switz) 5(1):4–24

    Google Scholar 

  • Gan F et al (2014b) Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345(6202):1312–1317

    Article  CAS  PubMed  Google Scholar 

  • Garg H et al (2017) The C2(1)-formyl group in chlorophyll f originates from molecular oxygen. J Biol Chem 292(47):19279–19289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garrido JL, Brunet C, Rodríguez F (2016) Pigment variations in Emiliania huxleyi (CCMP370) as a response to changes in light intensity or quality. Environ Microbiol 18(12):4412–4425

    Article  CAS  PubMed  Google Scholar 

  • Gibson LCD et al (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 U S A 92(6):1941–1944

    Article  CAS  PubMed  PubMed Central  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(Pt 2):243–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glazer AN (1989) Light guides. Directional energy transfer in a photosynthetic antenna. J Biol Chem 264(1):1–4

    Article  CAS  PubMed  Google Scholar 

  • Granick S (1949) The pheoporphyrin nature of chlorophyll c. J Biol Chem 179(1):505

    Article  CAS  PubMed  Google Scholar 

  • Granick S (1961) Magnesium protoporphyrin monoester and protoporphyrin monomethyl ester in chlorophyll biosynthesis. J Biol Chem 236:1168–1172

    Article  CAS  PubMed  Google Scholar 

  • Granick S, Kett R (1948) Magnesium protoporphyrin as a precursor of chlorophyll in Chlorella. J Biol Chem 175:333–342

    Article  CAS  PubMed  Google Scholar 

  • Grasses T et al (2001) Loss of alpha-tocopherol in tobacco plants with decreased geranylgeranyl reductase activity does not modify photosynthesis in optimal growth conditions but increases sensitivity to high-light stress. Planta 213(4):620–628

    Article  CAS  PubMed  Google Scholar 

  • Guo R, Luo M, Weinstein JD (1998) Magnesium chelatase from developing pea leaves. Plant Physiol 116:605–615

    Article  CAS  PubMed Central  Google Scholar 

  • Hansson A et al (2002) Three semidominant barley mutants with single amino acid substitutions in the smallest magnesium chelatase subunit form defective AAA+ hexamers. Proc Natl Acad Sci U S A 99(21):13944–13949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hennig M et al (1994) Crystallization and preliminary X-ray analysis of wild-type and K272A mutant glutamate 1-semialdehyde aminotransferase from Synechococcus. J Mol Biol 242(4):591–594

    Article  CAS  PubMed  Google Scholar 

  • Hennig M et al (1997) Crystal structure of glutamate-1-semialdehyde aminomutase: an alpha2-dimeric vitamin B6-dependent enzyme with asymmetry in structure and active site reactivity. Proc Natl Acad Sci U S A 94(10):4866–4871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henningsen K, Boynton J, Wettstein D (1993) Mutants at xantha and albina loci in relation to chloroplast biogenesis in barley (Hordeum vulgare L.). Biologiske Skrifter 42:1–349

    Google Scholar 

  • Herbst J et al (2018) Potential roles of YCF54 and ferredoxin-NADPH reductase for magnesium protoporphyrin monomethylester cyclase. Plant J 94:485–496

    Article  CAS  PubMed  Google Scholar 

  • Hess WR et al (2001) The photosynthetic apparatus of Prochlorococcus: insights through comparative genomics. Photosynth Res 70(1):53–71

    Article  CAS  PubMed  Google Scholar 

  • Ho MY et al (2016) Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353(6302):886

    Article  CAS  Google Scholar 

  • Hollingshead S et al (2012) Conserved chloroplast open-reading frame ycf54 is required for activity of the magnesium protoporphyrin monomethylester oxidative cyclase in Synechocystis PCC 6803. J Biol Chem 287(33):27823–27833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang P et al (2014) Functional analysis of carboxyl-terminal of Oryza sativa Gun4, a regulatory protein of magnesium chelatase. Zhongguo Shengwu Huaxue Yu Fenzi Shengwu Xuebao 30(10):1017–1024

    CAS  Google Scholar 

  • Im C, Matters G, Beale S (1996) Calcium and calmodulin are involved in blue light induction of the Gsa gene for an early chlorophyll biosynthetic step in Chlamydomonas. Plant Cell 8(12):2245–2253

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jahn D (1992) Complex formation between glutamyl-tRNA synthetase and glutamyl-tRNA reductase during the tRNA-dependent synthesis of 5-aminolevulinic acid in Chlamydomonas reinhardtii. FEBS Lett 314(1):77–80

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey SW (1968) Two spectrally distinct components in preparations of chlorophyll c. Nature 220(5171):1032–1033

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey SW (1969) Properties of two spectrally different components in chlorophyll c preparations. Biochim Biophys Acta 177(3):456–467

    Article  CAS  PubMed  Google Scholar 

  • Jensen PE et al (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(28):16662–16667

    Article  CAS  PubMed  Google Scholar 

  • Jensen PE et al (1996b) Structural genes for Mg-chelatase subunits in barley: Xantha-f, -g and -h. Mol Gen Genet 250(4):383–394

    CAS  PubMed  Google Scholar 

  • Jordan P et al (2001) Three-dimensional structure of cyanobacterial photosystem I at 2.5 Ã… resolution. Nature 411(6840):909–917

    Article  CAS  PubMed  Google Scholar 

  • Jung LJ, Chan CF, Glazer AN (1995) Candidate genes for the phycoerythrocyanin alpha subunit lyase. Biochemical analysis of pecE and pecF interposon mutants. J Biol Chem 270(21):12877–12884

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T et al (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. PCC6803. DNA Res 3(3):109–136

    Article  CAS  PubMed  Google Scholar 

  • Kim JI et al (2017) Evolutionary dynamics of cryptophyte plastid genomes. Genome Biol Evol 9(7):1859–1872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi M et al (1988) Chlorophyll a′/P-700 and pheophytin a/P-680 stoichiometries in higher plants and cyanobacteria determined by HPLC analysis. Biochim Biophys Acta Biomembr 936(1):81–89

    Article  CAS  Google Scholar 

  • Kronfel CM et al (2013) Structural and biochemical characterization of the bilin lyase CpcS from Thermosynechococcus elongatus. Biochemistry 52(48):8663–8676

    Article  CAS  PubMed  Google Scholar 

  • Kunugi M, Takabayashi A, Tanaka A (2013) Evolutionary changes in chlorophyllide a oxygenase (CAO) structure contribute to the acquisition of a new light-harvesting complex in micromonas. J Biol Chem 288(27):19330–19341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lake V, Willows R (2003) Rapid extraction of RNA and analysis of transcript levels in Chlamydomonas reinhardtii using real-time RT-PCR: magnesium chelatase chlH, chlD and chlI gene expression. Photosynth Res 77(1):69–76

    Article  CAS  PubMed  Google Scholar 

  • Lake V et al (2004) ATPase activity of magnesium chelatase subunit I is required to maintain subunit D in vivo. Eur J Biochem 271(11):2182–2188

    Article  CAS  PubMed  Google Scholar 

  • Larkin RM et al (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299(5608):902–906

    Article  CAS  PubMed  Google Scholar 

  • Layer G, Krausze J, Moser J (2017) Reduction of chemically stable multibonds: nitrogenase-like biosynthesis of tetrapyrroles. Adv Exp Med Biol 925:147–161

    Article  CAS  PubMed  Google Scholar 

  • Li Y et al (2012) Extinction coefficient for red-shifted chlorophylls: chlorophyll d and chlorophyll f. Biochim Biophys Acta 1817(8):1292–1298

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Bryant DA (2011) Multiple types of 8-vinyl reductases for (bacterio)chlorophyll biosynthesis occur in many green sulfur bacteria. J Bacteriol 193(18):4996–4998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lohr M, Im CS, Grossman AR (2005) Genome-based examination of chlorophyll and carotenoid biosynthesis in Chlamydomonas reinhardtii. Plant Physiol 138(1):490–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loughlin PC, Willows RD, Chen M (2014) In vitro conversion of vinyl to formyl groups in naturally occurring chlorophylls. Sci Rep 4:6069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loughlin PC, Willows RD, Chen M (2015) Hydroxylation of the C132 and C18 carbons of chlorophylls by heme and molecular oxygen. J Porphyrins Phthalocyanines 19(9):1007–1013

    Article  CAS  Google Scholar 

  • Lundqvist J et al (2010) ATP-induced conformational dynamics in the AAA+ motor unit of magnesium chelatase. Structure 18:354–365

    Article  CAS  PubMed  Google Scholar 

  • Lundqvist J et al (2013) Catalytic turnover triggers exchange of subunits of the magnesium chelatase AAA+ motor unit. J Biol Chem 288(33):24012–24019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manning WM, Strain HH (1943) Chlorophyll d, a green pigment of red algae. J Biol Chem 151:1–19

    Article  CAS  Google Scholar 

  • McLean S, Hunter CN (2009) An enzyme-coupled continuous spectrophotometric assay for magnesium protoporphyrin IX methyltransferases. Anal Biochem 394(2):223–228

    Article  CAS  PubMed  Google Scholar 

  • Meinecke L et al (2010) Chlorophyll-deficient mutants of Chlamydomonas reinhardtii that accumulate magnesium protoporphyrin IX. Plant Mol Biol 72:643–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Merchant S et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318(5848):245–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meskauskiene R, 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(1–2):27–30

    Article  CAS  PubMed  Google Scholar 

  • Meskauskiene R et al (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 98(22):12826–12831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Minamizaki K et al (2008) Identification of two homologous genes, chlAI and chlAII, that are differentially involved in isocyclic ring formation of chlorophyll a in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 283(5):2684–2692

    Article  CAS  PubMed  Google Scholar 

  • Miyashita H et al (1997) Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as the major chlorophyll. Plant Cell Physiol 38(3):274–281

    Article  CAS  Google Scholar 

  • Mochizuki N et al (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 U S A 98(4):2053–2058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moseley J et al (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(10):2139–2151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moseley J et al (2002) Reciprocal expression of two candidate di-iron enzymes affecting photosystem I and light-harvesting complex accumulation. Plant Cell 14(3):673–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moser J et al (2001) V-shaped structure of glutamyl-tRNA reductase, the first enzyme of tRNA-dependent tetrapyrrole biosynthesis. EMBO J 20(23):6583–6590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moser J et al (2013) Structure of ADP-aluminium fluoride-stabilized protochlorophyllide oxidoreductase complex. Proc Natl Acad Sci U S A 110(6):2094–2098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller AH et al (2014) Inducing the oxidative stress response in Escherichia coli improves the quality of a recombinant protein: magnesium chelatase ChlH. Protein Expr Purif 101:61–67

    Article  CAS  PubMed  Google Scholar 

  • Nagata N et al (2005) Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species. Plant Cell 17(1):233–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nascimento SMD, Zou Y, Cheng Q (2016) Review of studies on the last enzymes in bacteriochlorophyll (Bchl) and chlorophyll (Chl) biosynthesis. Am J Plant Sci 7(12):1639–1651

    Article  CAS  Google Scholar 

  • Nasrulhaq-Boyce A, Griffiths W, Jones O (1987) The use of continuous assays to characterize the oxidative cyclase that synthesizes the chlorophyll isocyclic ring. Biochem J 243(1):23–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson JR, Wakeham SG (1989) A phytol-substituted chlorophyll c from Emiliania huxleyi (Prymnesiophyceae). J Phycol 25(4):761–766

    Article  CAS  Google Scholar 

  • Nogaj L, Beale S (2005) Physical and kinetic interactions between glutamyl-tRNA reductase and glutamate-1-semialdehyde aminotransferase of Chlamydomonas reinhardtii. J Biol Chem 280(26):24301–24307

    Article  CAS  PubMed  Google Scholar 

  • Nogaj L et al (2005) Cellular levels of glutamyl-tRNA reductase and glutamate-1-semialdehyde aminotransferase do not control chlorophyll synthesis in Chlamydomonas reinhardtii. Plant Physiol 139(1):389–396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oba T et al (2011) A mild conversion from 3-vinyl- to 3-formyl-chlorophyll derivatives. Bioorg Med Chem Lett 21(8):2489–2491

    Article  CAS  PubMed  Google Scholar 

  • 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(15):9671–9676

    Article  CAS  PubMed  Google Scholar 

  • Oster U et al (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J 21(3):305–310

    Article  CAS  PubMed  Google Scholar 

  • Ouchane S et al (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(8):6385–6394

    Article  CAS  PubMed  Google Scholar 

  • Overkamp KE et al (2014) Insights into the biosynthesis and assembly of cryptophycean phycobiliproteins. J Biol Chem 289(39):26691–26707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen BL et al (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(3):699–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porra R, Scheer H (2001) 18O and mass spectrometry in chlorophyll research: derivation and loss of oxygen atoms at the periphery of the chlorophyll macrocycle during biosynthesis, degradation and adaptation. Photosynth Res 66(3):159–175

    Article  Google Scholar 

  • Porra R et al (1993) Derivation of the formyl-group oxygen of chlorophyll b from molecular oxygen in greening leaves of a higher plant (Zea mays). FEBS Lett 323(1–2):31–34

    Article  CAS  PubMed  Google Scholar 

  • Porra RJ et al (1994) The derivation of the formyl-group oxygen of chlorophyll b in higher plants from molecular oxygen. Achievement of high enrichment of the 7-formyl-group oxygen from 18O2 in greening maize leaves. Eur J Biochem 219(1–2):671–679

    Article  CAS  PubMed  Google Scholar 

  • Proctor MS et al (2018) Plant and algal chlorophyll synthases function in Synechocystis and interact with the YidC/Alb3 membrane insertase. FEBS Lett 592(18):3062–3073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reid JD, Hunter CN (2002) Current understanding of the function of magnesium chelatase. Biochem Soc Trans 30(4):643–645

    Article  CAS  PubMed  Google Scholar 

  • Richter AS et al (2016) Phosphorylation of genomes uncoupled 4 alters stimulation of Mg chelatase activity in angiosperms. Plant Physiol 172(3):1578–1595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rissler H et al (2002) Chlorophyll biosynthesis. Expression of a second chl I gene of magnesium chelatase in Arabidopsis supports only limited chlorophyll synthesis. Plant Physiol 128(2):770–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rockwell NC, Lagarias JC (2017) Ferredoxin-dependent bilin reductases in eukaryotic algae: ubiquity and diversity. J Plant Physiol 217:57–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rüdiger W (2003) The last steps in chlorophyll synthesis. In: Kadish KM, Smith KM, Guilard R (eds) The porphyrin handbook. Academic, Amsterdam, pp 71–108

    Chapter  Google Scholar 

  • Saunee NA et al (2008) Biogenesis of phycobiliproteins: II. CpcS-I and CpcU comprise the heterodimeric bilin lyase that attaches phycocyanobilin to CYS-82 OF beta-phycocyanin and CYS-81 of allophycocyanin subunits in Synechococcus sp. PCC 7002. J Biol Chem 283(12):7513–7522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sawicki A, Willows RD (2008) Kinetic analyses of the magnesium chelatase provide insights into the mechanism, structure, and formation of the complex. J Biol Chem 283(46):31294–31302

    Article  CAS  PubMed  Google Scholar 

  • Sawicki A et al (2017) 1-N-histidine phosphorylation of ChlD by the AAA(+) ChlI2 stimulates magnesium chelatase activity in chlorophyll synthesis. Biochem J 474(12):2095–2105

    Article  CAS  PubMed  Google Scholar 

  • Scheer H, Zhao KH (2008) Biliprotein maturation: the chromophore attachment. Mol Microbiol 68(2):263–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schliep M et al (2010) 18O labeling of chlorophyll d in Acaryochloris marina reveals that chlorophyll a and molecular oxygen are precursors. J Biol Chem 285(37):28450–28456

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schluchter WM et al (2010) Phycobiliprotein biosynthesis in cyanobacteria: structure and function of enzymes involved in post-translational modification. In: Protein reviews. Springer Singapore, Springer New York, New York, pp 211–228

    Google Scholar 

  • Shen G et al (2006) Identification and characterization of a new class of bilin lyase: the cpcT gene encodes a bilin lyase responsible for attachment of phycocyanobilin to Cys-153 on the beta-subunit of phycocyanin in Synechococcus sp. PCC 7002. J Biol Chem 281(26):17768–17778

    Article  CAS  PubMed  Google Scholar 

  • Shen G, Schluchter WM, Bryant DA (2008) Biogenesis of phycobiliproteins – I. cpcS-I and cpcU mutants of the cyanobacterium Synechococcus sp PCC 7002 define a heterodimeric phyococyanobilin lyase specific for beta-phycocyanin and allophycocyanin subunits. J Biol Chem 283(12):7503–7512

    Article  CAS  PubMed  Google Scholar 

  • Shepherd M, Hunter CN (2004) Transient kinetics of the reaction catalysed by magnesium protoporphyrin IX methyltransferase. Biochem J 382(Pt 3):1009–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shepherd M, McLean S, Hunter C (2005) Kinetic basis for linking the first two enzymes of chlorophyll biosynthesis. FEBS J 272(17):4532–4539

    Article  CAS  PubMed  Google Scholar 

  • Shin SE et al (2016) CRISPR/Cas9-induced knockout and knock-in mutations in Chlamydomonas reinhardtii. Sci Rep 6:27810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Six C et al (2007) Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study. Genome Biol 8(12):R259

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sobotka R et al (2008) Importance of the cyanobacterial Gun4 protein for chlorophyll metabolism and assembly of photosynthetic complexes. J Biol Chem 283(38):25794–25802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava A et al (2005) The Chlamydomonas reinhardtii gtr gene encoding the tetrapyrrole biosynthetic enzyme glutamyl-tRNA reductase: structure of the gene and properties of the expressed enzyme. Plant Mol Biol 58(5):643–658

    Article  CAS  PubMed  Google Scholar 

  • Stephenson PG, Terry MJ (2008) Light signalling pathways regulating the Mg-chelatase branchpoint of chlorophyll synthesis during de-etiolation in Arabidopsis thaliana. Photochem Photobiol Sci 7(10):1243–1252

    Article  CAS  PubMed  Google Scholar 

  • Stiller JW et al (2014) The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat Commun 5(1):5764

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swanson RV et al (1992) Characterization of phycocyanin produced by cpcE and cpcF mutants and identification of an intergenic suppressor of the defect in bilin attachment. J Biol Chem 267(23):16146–16154

    Article  CAS  PubMed  Google Scholar 

  • Tanaka A, Ito H, Okada K (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formaiton from chlorophyll a. Proc Natl Acad Sci U S A 95(21):12719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka R et al (2001) Overexpression of chlorophyllide a oxygenase (CAO) enlarges the antenna size of photosystem II in Arabidopsis thaliana. Plant J 26(4):365–373

    Article  CAS  PubMed  Google Scholar 

  • Tarahi Tabrizi S et al (2015) Structure of GUN4 from Chlamydomonas reinhardtii. Acta Crystallogr Sect F 71:1094–1099

    Article  CAS  Google Scholar 

  • Tarahi Tabrizi S et al (2016) GUN4-protoporphyrin IX is a singlet oxygen generator with consequences for plastid retrograde signalling. J Biol Chem 291:8978–8984

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tomitani A et al (1999) Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature 400(6740):159–162

    Article  CAS  PubMed  Google Scholar 

  • van Lis R et al (2005) Subcellular localization and light-regulated expression of protoporphyrinogen IX oxidase and ferrochelatase in Chlamydomonas reinhardtii. Plant Physiol 139(4):1946–1958

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vasileuskaya Z, Oster U, Beck C (2005) Mg-protoporphyrin IX and heme control HEMA, the gene encoding the first specific step of tetrapyrrole biosynthesis, in Chlamydomonas reinhardtii. Eukaryot Cell 4(10):1620–1628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verdecia MA et al (2005) Structure of the Mg-chelatase cofactor GUN4 reveals a novel hand-shaped fold for porphyrin binding. PLoS Biol 3(5):12

    Article  Google Scholar 

  • Vijayan P, Whyte B, Castelfranco P (1992) A spectrophotometric analysis of the magnesium protoporphyrin IX monomethyl ester (oxidative) cyclase. Plant Physiol Biochem (Paris) 30(3):271–278

    CAS  Google Scholar 

  • Viney J et al (2007) Direct measurement of metal-ion chelation in the active site of the AAA+ ATPase magnesium chelatase. Biochemistry 46(44):12788–12794

    Article  CAS  PubMed  Google Scholar 

  • Vothknecht U, Kannangara C, von Wettstein D (1998) Barley glutamyl tRNAGlu reductase: mutations affecting haem inhibition and enzyme activity. Phytochemistry 47(4):513–519

    Article  CAS  PubMed  Google Scholar 

  • Walker CJ, Weinstein JD (1991) In vitro assay of the chlorophyll biosynthetic enzyme magnesium chelatase: resolution of the activity into soluble and membrane bound fractions. Proc Natl Acad Sci U S A 88(13):5789–5793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker CJ, Willows RD (1997) Mechanism and regulation of Mg-chelatase. Biochem J 327(Pt 2):321–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker CJ et al (1988) The magnesium-protoporphyrin IX (oxidative) cyclase system. Studies on the mechanism and specificity of the reaction sequence. Biochem J 255(2):685–692

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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(Pt 3):691–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(3):263–269

    CAS  Google Scholar 

  • Wang W-Y et al (1974) Genetic control of chlorophyll biosynthesis in chlamydomonas: analysis of mutants at two loci mediating the conversion of protoporphyrin-IX to magnesium protoporphyrin. J Cell Biol 63:806–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P et al (2013) One divinyl reductase reduces the 8-vinyl groups in various intermediates of chlorophyll biosynthesis in a given higher plant species, but the isozyme differs between species. Plant Physiol 161(1):521–534

    Article  CAS  PubMed  Google Scholar 

  • Whyte B, Castelfranco P (1993) Further observations on the Mg-protoporphyrin IX monomethyl ester (oxidative) cyclase system. Biochem J 290(Pt 2):355–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whyte B, Fijayan P, Castelfranco P (1992) In vitro synthesis of protochlorophyllide: effects of magnesium and other cations on the reconstituted (oxidative) cyclase. Plant Physiol Biochem (Paris) 30(3):279–284

    CAS  Google Scholar 

  • Wilde A et al (2004) The gun4 gene is essential for cyanobacterial porphyrin metabolism. FEBS Lett 571(1–3):119–123

    Article  CAS  PubMed  Google Scholar 

  • Willows R, Beale S (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(51):34206–34213

    Article  CAS  PubMed  Google Scholar 

  • Willows RD et al (1996) Three separate proteins constitute the magnesium chelatase of Rhodobacter sphaeroides. Eur J Biochem 235(1/2):438–443

    Article  CAS  PubMed  Google Scholar 

  • Willows RD et al (1999) Crystallization and preliminary X-ray analysis of the Rhodobacter capsulatus magnesium chelatase BchI subunit. Acta Crystallogr D Biol Crystallogr 55(Pt 3):689–690

    Article  CAS  PubMed  Google Scholar 

  • Wittkopp TM et al (2017) Bilin-dependent photoacclimation in Chlamydomonas reinhardtii. Plant Cell 29(11):2711–2726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamanashi K, Minamizaki K, Fujita Y (2015) Identification of the chlE gene encoding oxygen-independent Mg-protoporphyrin IX monomethyl ester cyclase in cyanobacteria. Biochem Biophys Res Commun 463(4):1328–1333

    Article  CAS  PubMed  Google Scholar 

  • Zapata M, Garrido JL (1997) Occurance of phytylated chlorophyll c in Isochrysis galbana and Isocrysis sp (clone T-ISO) (Prymnesiophyceae). J Phycol 33:209–214

    Article  CAS  Google Scholar 

  • Zhang H et al (2015) A point mutation of magnesium chelatase OsCHLI gene dampens the interaction between CHLI and CHLD subunits in rice. Plant Mol Biol Report 33(6):1975–1987

    Article  CAS  Google Scholar 

  • Zhao KH et al (2000) Novel activity of a phycobiliprotein lyase: both the attachment of phycocyanobilin and the isomerization to phycoviolobilin are catalyzed by the proteins PecE and PecF encoded by the phycoerythrocyanin operon. FEBS Lett 469(1):9–13

    Article  CAS  PubMed  Google Scholar 

  • Zhao KH et al (2007) Lyase activities of CpcS- and CpcT-like proteins from Nostoc PCC7120 and sequential reconstitution of binding sites of phycoerythrocyanin and phycocyanin beta-subunits. J Biol Chem 282(47):34093–34103

    Article  CAS  PubMed  Google Scholar 

  • Zhao C et al (2017) Structures and enzymatic mechanisms of phycobiliprotein lyases CpcE/F and PecE/F. Proc Natl Acad Sci U S A 114(50):13170–13175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J et al (1992) The cpcE and cpcF genes of Synechococcus sp. PCC 7002. Construction and phenotypic characterization of interposon mutants. J Biol Chem 267(23):16138–16145

    Article  CAS  PubMed  Google Scholar 

  • Zhou S et al (2012) C-terminal residues of Oryza sativa GUN4 are required for the activation of the ChlH subunit of magnesium chelatase in chlorophyll synthesis. FEBS Lett 586(3):205–210

    Article  CAS  PubMed  Google Scholar 

  • Zhou W et al (2014) Structure and mechanism of the phycobiliprotein Lyase CpcT. J Biol Chem 289(39):26677–26689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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  1. Department of Molecular Sciences, Macquarie University, Sydney, Australia

    Robert D. Willows

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  1. Global Climate Custer, University of Technology Sydney, Ultimo, NSW, Australia

    Anthony W.D. Larkum

  2. Department of Plant Biology, Carnegie Institution for Science, Stanford University, Stanford, CA, USA

    Arthur R. Grossman

  3. Division of Plant Sciences, University of Dundee at the JHI, Dundee, UK

    John A. Raven

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Willows, R.D. (2020). Biosynthesis of Chlorophyll and Bilins in Algae. In: Larkum, A., Grossman, A., Raven, J. (eds) Photosynthesis in Algae: Biochemical and Physiological Mechanisms. Advances in Photosynthesis and Respiration, vol 45. Springer, Cham. https://doi.org/10.1007/978-3-030-33397-3_5

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