Skip to main content

Evolution of light-independent protochlorophyllide oxidoreductase

Abstract

The nonhomologous enzymes, the light-independent protochlorophyllide reductase (DPOR) and the light-dependent protochlorophyllide oxidoreductase (LPOR), catalyze the reduction of protochlorophyllide (Pchlide) to chlorophyllide (Chlide) in the penultimate step of biosynthesis of chlorophyll (Chl) required for photosynthetic light absorption and energy conversion. The two enzymes differ with respect to the requirement of light for catalysis and oxygen sensitivity. DPOR and LPOR initially evolved in the ancestral prokaryotic genome perhaps at different times. DPOR originated in the anoxygenic environment of the Earth from nitrogenase-like enzyme of methanogenic archaea. Due to the transition from anoxygenic to oxygenic photosynthesis in the prokaryote, the DPOR was mostly inactivated in the daytime by photosynthetic O2 leading to the evolution of oxygen-insensitive LPOR that could function in the light. The primary endosymbiotic event transferred the DPOR and LPOR genes to the eukaryotic phototroph; the DPOR remained in the genome of the ancestor that turned into the plastid, whereas LPOR was transferred to the host nuclear genome. From an evolutionary point of view, several compelling theories that explain the disappearance of DPOR from several species cutting across different phyla are as follows: (i) pressure of the oxygenic environment; (ii) change in the light conditions and temperature; and (iii) lineage-specific gene losses, RNA editing, and nonsynonymous substitution. Certain primary amino acid sequence and the physiochemical properties of the ChlL subunit of DPOR have similarity with that of LPOR suggesting a convergence of these two enzymes in certain evolutionary event. The newly obtained sequence data from different phototrophs will further enhance the width of the phylogenetic information on DPOR.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

Bchl:

Bacteriochlorophyll

Bchlide:

Bacteriochlorophyllide

Chl:

Chlorophyll

Chlide:

Chlorophyllide

COR:

Chlorophyllide a reductase

DPOR:

Light-independent protochlorophyllide reductase

LPOR:

Light- dependent protochlorophyllide oxidoreductase

Pchlide:

Protochlorophyllide

References

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

    Article  CAS  Google Scholar 

  • Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:R81–R88

    PubMed  Article  CAS  Google Scholar 

  • Archibald JM (2015) Genomic perspectives on the birth and spread of plastids. Proc Natl Acad Sci U S A 112:10147–10153

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Artz JH, Zadvornyy OA, Mulder DW, King PW, Peters JW (2017) Structural characterization of poised states in the oxygen sensitive hydrogenases and nitrogenases. Methods Enzymol 595:213–259

    PubMed  Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Berman-Frank I, Lundgren P, Chen YB, Küpper H, Kolber Z, Bergman B, Falkowski P (2001) Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294(5546):1534–1537

    PubMed  Article  CAS  Google Scholar 

  • Berman-Frank I, Lundgren P, Falkowski P (2003) Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol 154(3):157–164

    PubMed  Article  CAS  Google Scholar 

  • Biswal AK, Pattanayak GK, Pandey SS, Leelavathi S, Reddy VS, Govindjee, Tripathy BC (2012) Light intensity-dependent modulation of chlorophyll b biosynthesis and photosynthesis by overexpression of chlorophyllide a oxygenase (CAO) in tobacco. Plant Physiol 112

  • Björn LO (2018) Photoenzymes and related topics: an update. Photochem Photobiol 94:459–465

    PubMed  Article  CAS  Google Scholar 

  • Björn LO, Govindjee (2009) The evolution of photosynthesis and chloroplasts. Curr Sci:1466–1474

  • Blankenship RE (2010) Early evolution of photosynthesis. Plant Physiol 154:434–438

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23:94–97

    PubMed  Article  CAS  Google Scholar 

  • Bock R (2010) The give-and-take of DNA: horizontal gene transfer in plants. Trends Plant Sci 15:11–22

    PubMed  Article  CAS  Google Scholar 

  • Boivin R, Richard M, Beauseigle D, Bousquet J, Bellemare G (1996) Phylogenetic inferences from chloroplast chlB gene sequences of Nephrolepis exaltata (Filicopsida), Ephedra altissima (Gnetopsida), and diverse land plants. Mol Phylogenet Evol 6:19–29

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Bordowitz JR, Montgomery BL (2008) Photoregulation of cellular morphology during complementary chromatic adaptation requires sensor-kinase-class protein RcaE in Fremyella diplosiphon. J Bacteriol 190:4069–4074

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Boyd E, Peters JW (2013) New insights into the evolutionary history of biological nitrogen fixation. Front Microbiol 4:201

    PubMed  PubMed Central  Google Scholar 

  • Breznenová K, Demko V, Pavlovič A, Gálová E, Balážová R, Hudák J (2010) Light-independent accumulation of essential chlorophyll biosynthesis- and photosynthesis-related proteins in Pinus mugo and Pinus sylvestris seedlings. Photosynthetica 48:16–22

    Article  CAS  Google Scholar 

  • Brinkhoff T, Buchholz I, Bunk B, Cypionka H, Daniel R, Drepper T, Gerdts G, Hahnke S (2010) The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker’s guide to life in the sea. ISME J 4:61–77

    PubMed  Article  CAS  Google Scholar 

  • Bröcker MJ, Virus S, Ganskow S, Heathcote P, Heinz DW, Schubert WD, Jahn D, Moser J (2008) ATP-driven reduction by dark-operative protochlorophyllide oxidoreductase from Chlorobium tepidum mechanistically resembles nitrogenase catalysis. J Biol Chem 283:10559–10567

  • Bröcker MJ, Schomburg S, Heinz DW, Jahn D, Schubert W-D, Moser J (2010) Crystal structure of the nitrogenase-like dark operative protochlorophyllide oxidoreductase catalytic complex (ChlN/ChlB)2. J Biol Chem 285:27336–27345

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Bryant DA, Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496

    PubMed  Article  CAS  Google Scholar 

  • Brzezowski P, Richter AS, Grimm B (2015) Regulation and function of tetrapyrrole biosynthesis in plants and algae. Biochim Biophys Acta Bioenerg 1847:968–985

    Article  CAS  Google Scholar 

  • Buick R (2008) When did oxygenic photosynthesis evolve? Philos Trans R Soc Lond B Biol Sci 363:2731–2743

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Burke DH, Hearst JE, Sidow A (1993b) Early evolution of photosynthesis: clues from nitrogenase and chlorophyll iron proteins. Proc Natl Acad Sci USA 90(15):7134–7138

    PubMed  Article  CAS  Google Scholar 

  • Burke DH, Raubeson LA, Alberti M, Hearst JE, Jordan ET, Kirch SA, Valinski AEC, Conant DS, Stein DB (1993c) The chlL (frxC) gene: phylogenetic distribution in vascular plants and DNA sequence from Polystichum acrostichoides (Pteridophyta) and Synechococcus sp. 7002 (Cyanobacteria). Plant Syst Evol 187:89–102

    Article  CAS  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Carey EE, Tripathy BC, Rebeiz CA (1985) Chloroplast biogenesis 51: modulation of monovinyl and divinyl protochlorophyllide biosynthesis by light and darkness in vitro. Plant Physiol 79:1059–1063

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Castandet B, Araya A (2011) RNA editing in plant organelles. Why make it easy? Biochem Mosc 76:924–931

    Article  CAS  Google Scholar 

  • Castelfranco PA, Beale SI (1983) Chlorophyll biosynthesis: recent advances and areas of current interest. Annu Rev Plant Physiol 34:241–276

    Article  CAS  Google Scholar 

  • Chen M (2014) Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. Annu Rev Biochem 83:317–340

    PubMed  Article  CAS  Google Scholar 

  • Cheng Q, Day A, Dowson-Day M, Shen GF, Dixon R (2005) The Klebsiella pneumoniae nitrogenase Fe protein gene (nifH) functionally substitutes for the chlL gene in Chlamydomonas reinhardtii. Biochem Biophys Res Commun 329:966–975

    PubMed  Article  CAS  Google Scholar 

  • Chew AGM, Bryant DA (2007) Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. Annu Rev Microbiol 61:113–129

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M, Maruyama S, Arias MC, Ball SG, Gile GH, Hirakawa Y, Hopkins JF (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65

    PubMed  Article  CAS  Google Scholar 

  • del Pozo JC, Ramirez-Parra E (2015) Whole genome duplications in plants: an overview from Arabidopsis. J Exp Bot 66:6991–7003

    PubMed  Article  CAS  Google Scholar 

  • Demko V, Pavlovič A, Valková D, Grimm B, Hudák J (2009) A novel insight into the regulation of light-independent chlorophyll biosynthesis in Larix decidua and Picea abies seedlings. Planta 230:165–176

    PubMed  Article  CAS  Google Scholar 

  • Duggan JX, Rebeiz CA (1982) Chloroplast biogenesis 42: conversion of divinyl chlorophyllide a to monovinyl chlorophyllide a in vivo and in vitro. Plant Sci Lett 27:137–145

    Article  CAS  Google Scholar 

  • Dutta S, Mohanty S, Tripathy BC (2009) Role of temperature stress on chloroplast biogenesis and protein import in pea. Plant Physiol 150:1050–1061

    PubMed  PubMed Central  Article  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 U S A 96:10507–10511

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Esteves-Ferreira AA, Cavalcanti JH, Vaz MG, Alvarenga LV, Nunes-Nesi A, Araújo WL (2017) Cyanobacterial nitrogenases: phylogenetic diversity, regulation and functional predictions. Genet Mol Biol 40(1):261–275

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Fang L, Ge H, Huang X, Liu Y, Lu M, Wang J, Chen W, Xu W, Wang Y (2017) Trophic mode-dependent proteomic analysis reveals functional significance of light-independent chlorophyll synthesis in Synechocystis sp. PCC6803. Mol Plant 10:73–85

    PubMed  Article  CAS  Google Scholar 

  • Fani R, Gallo R, Lio P (2000) Molecular evolution of nitrogen fixation: the evolutionary history of the nifD, nifK, nifE, and nifN genes. J Mol Evol 51(1):1–1

    PubMed  Article  CAS  Google Scholar 

  • Fong A, Archibald JM (2008) Evolutionary dynamics of light-independent protochlorophyllide oxidoreductase genes in the secondary plastids of cryptophyte algae. Eukaryot Cell 7:550–553

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Fujita Y, Yamakawa H (2017) Biochemistry of chlorophyll biosynthesis in photosynthetic prokaryotes. In: Modern topics in the phototrophic prokaryotes. Springer, Cham, pp 67–122

    Chapter  Google Scholar 

  • Fujita Y, Takahashi Y, Kohchi T, Ozeki H, Ohyama K, Matsubara H (1989) Identification of a novel nifH-like (frxC) protein in chloroplasts of the liverwort Marchantia polymorpha. Plant Mol Biol 13:551–556

    PubMed  Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Fujita Y, Takagi H, Hase T (1996) Identification of the chlB gene and the gene product essential for the light-independent chlorophyll biosynthesis in the cyanobacterium Plectonema boryanum. Plant Cell Physiol 37:313–323

    PubMed  Article  CAS  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  Article  CAS  Google Scholar 

  • Fujita Y, Tsujimoto R, Aoki R (2015) Evolutionary aspects and regulation of tetrapyrrole biosynthesis in cyanobacteria under aerobic and anaerobic environments. Life 5:1172–1203

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Gabruk M, Grzyb J, Kruk J, Mysliwa-Kurdziel B (2012) Light-dependent and light-independent protochlorophyllide oxidoreductases share similar sequence motifs in silico studies. Photosynthetica 50:529–540

    Article  CAS  Google Scholar 

  • Grimm B, Porra RJ, Rüdiger W, Scheer H, Melkozernov AN, Blankenship RE (2006) Chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications. In: Grimm B, Porra RJ, Rüdiger W, Scheer H (eds) Advances in photosynthesis and respiration. Springer, Dordrecht, pp 397–412

    Google Scholar 

  • Grossman AR (2003) A molecular understanding of complementary chromatic adaptation. Photosynth Res 76:207–215

    PubMed  Article  CAS  Google Scholar 

  • Gupta RS (2012) Origin and spread of photosynthesis based upon conserved sequence features in key bacteriochlorophyll biosynthesis proteins. Mol Biol Evol 29:3397–3412

    PubMed  Article  CAS  Google Scholar 

  • Gupta RS, Khadka B (2016) Evidence for the presence of key chlorophyll-biosynthesis-related proteins in the genus Rubrobacter (phylum Actinobacteria) and its implications for the evolution and origin of photosynthesis. Photosynth Res 127:201–218

    PubMed  Article  CAS  Google Scholar 

  • Ha JH, Han SH, Lee HJ, Park CM (2017) Environmental adaptation of the heterotrophic-to-autotrophic transition: the developmental plasticity of seedling establishment. Crit Rev Plant Sci 36:128–137

    Article  Google Scholar 

  • Hirose Y, Rockwell NC, Nishiyama K, Narikawa R, Ukaji Y, Inomata K, Lagarias JC, Ikeuchi M (2013) Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle. Proc Natl Acad Sci U S A 110:4974–4979

    PubMed  PubMed Central  Article  Google Scholar 

  • Hirose Y, Katayama M, Ohtsubo Y, Misawa N, Iioka E, Suda W, Oshima K, Hanaoka M, Tanaka K, Eki T, Ikeuchi M (2015) Complete genome sequence of cyanobacterium Geminocystis sp. strain NIES-3708, which performs type II complementary chromatic acclimation. Genome Announc 3:357–315

    Google Scholar 

  • Ho MY, Shen G, Canniffe DP, Zhao C, Bryant DA (2016) Light dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353:9178

    Article  CAS  Google Scholar 

  • Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62:515–548

    PubMed  Article  CAS  Google Scholar 

  • Hunsperger HM, Randhawa T, Cattolico RA (2015) Extensive horizontal gene transfer, duplication, and loss of chlorophyll synthesis genes in the algae. BMC Evol Biol 15:16

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Ito H, Yokono M, Tanaka R, Tanaka A (2008) Identification of a novel vinyl reductase gene essential for the biosynthesis of monovinyl chlorophyll in Synechocystis sp. PCC6803. J Biol Chem 283:9002–9011

    PubMed  Article  CAS  Google Scholar 

  • Janouškovec J, Liu SL, Martone PT, Carré W, Leblanc C, Collén J, Keeling PJ (2013) Evolution of red algal plastid genomes: ancient architectures, introns, horizontal gene transfer, and taxonomic utility of plastid markers. PLoS One 8:59001

    Article  CAS  Google Scholar 

  • Johnson JL, Indermaur LW, Rajagopalan KV (1991) Molybdenum cofactor biosynthesis in Escherichia coli. Requirement of the chlB gene product for the formation of molybdopterin guanine dinucleotide. J Biol Chem 266(19):12140–12145

    PubMed  CAS  Google Scholar 

  • Kaiser JT, Hu Y, Wiig JA, Rees DC, Ribbe MW (2011) Structure of precursor-bound NifEN: a nitrogenase FeMo cofactor maturase/insertase. Science 331(6013):91–94

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Karpinska B, Karpinski S, Hallgren J (1997) The chlB gene encoding a subunit of light-independent protochlorophyllide reductase is edited in chloroplasts of conifers. Curr Genet 31:343–347

    PubMed  Article  CAS  Google Scholar 

  • Kasalický V, Zeng Y, Piwosz K, Šimek K, Kratochvilová H, Koblížek M (2018) Aerobic anoxygenic photosynthesis is commonly present within the genus Limnohabitans. Appl Environ Microbiol 84:2116–2117

    Google Scholar 

  • Kaschner M, Loeschcke A, Krause J, Minh BQ, Heck A, Endres S, Svensson V, Wirtz A, von Haeseler A, Jaeger K-E, Drepper T, Krauss U (2014) Discovery of the first light-dependent protochlorophyllide oxidoreductase in anoxygenic phototrophic bacteria. Mol Microbiol 93:1066–1078

    PubMed  Article  CAS  Google Scholar 

  • Kehoe DM (2010) Chromatic adaptation and the evolution of light color sensing in cyanobacteria. Proc Natl Acad Sci U S A 107:9029–9030

    PubMed  PubMed Central  Article  Google Scholar 

  • Kehoe DM, Grossman AR (1994) Complementary chromatic adaptation: photoperception to gene regulation. Semin Cell Biol 5:303–313

    PubMed  Article  CAS  Google Scholar 

  • Kerfeld CA, Melnicki MR (2016) Assembly, function and evolution of cyanobacterial carboxysomes. Curr Opin Plant Biol 31:66–75

    PubMed  Article  CAS  Google Scholar 

  • Khan H, Archibald JM (2008) Lateral transfer of introns in the cryptophyte plastid genome. Nucleic Acids Res 36:3043–3053

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Khan H, Parks N, Kozera C, Curtis BA, Parsons BJ, Bowman S, Archibald JM (2007) Plastid genome sequence of the cryptophyte alga Rhodomonas salina CCMP1319: lateral transfer of putative DNA replication machinery and a test of chromist plastid phylogeny. Mol Biol Evol 24:1832–1842

    PubMed  Article  CAS  Google Scholar 

  • Kiesel S, Wätzlich D, Lange C, Reijerse E, Bröcker MJ, Rüdiger W, Lubitz W, Scheer H, Moser J, Jahn D (2015) Iron-sulfur cluster-dependent catalysis of chlorophyllide a oxidoreductase from Roseobacter denitrificans. J Biol Chem 290:1141–1154

  • Kim S, Park MG (2016) First marine photosynthetic testate amoeba containing the chromatophore: Paulinella longichromatophora. Protistology 10

  • Kim JI, Yoon HS, Yi G, Kim HS, Yih W, Shin W (2015) The plastid genome of the cryptomonad Teleaulax amphioxeia. PLoS One 10:0129284

    Google Scholar 

  • Kim JI, Moore CE, Archibald JM, Bhattacharya D, Yi G, Yoon HS, Shin W (2017) Evolutionary dynamics of cryptophyte plastid genomes. Genome Biol Evol 9:1859–1872

  • Kinney JN, Salmeen A, Cai F, Kerfeld CA (2012) Elucidating essential role of conserved carboxysomal protein CcmN reveals common feature of bacterial microcompartment assembly. J Biol Chem 287:17729–17736

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    PubMed  Article  CAS  Google Scholar 

  • Kusumi J, Sato A, Tachida H (2006) Relaxation of functional constraint on light-independent protochlorophyllide oxidoreductase in Thuja. Mol Biol Evol 23:941–948

    PubMed  Article  CAS  Google Scholar 

  • Lauritano C, De Luca D, Ferrarini A, Avanzato C, Minio A, Esposito F, Ianora A (2017) De novo transcriptome of the cosmopolitan dinoflagellate Amphidinium carterae to identify enzymes with biotechnological potential. Sci Rep 7:11701

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 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

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Masuda T (2008) Recent overview of the Mg branch of the tetrapyrrole biosynthesis leading to chlorophylls. Photosynth Res 96:121–143

    PubMed  Article  CAS  Google Scholar 

  • Masuda T, Fujita Y (2008) Regulation and evolution of chlorophyll metabolism. Photochem Photobiol Sci 7:1131–1149

    PubMed  Article  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  Article  CAS  Google Scholar 

  • Meinecke L, Alawady A, Schroda M, Willows R, Kobayashi MC, Niyogi KK, Grimm B, Beck CF (2010) Chlorophyll-deficient mutants of Chlamydomonas reinhardtii that accumulate magnesium protoporphyrin IX. Plant Mol Biol 72:643–658

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Mohanty S, Grimm B, Tripathy BC (2006) Light and dark modulation of chlorophyll biosynthetic genes in response to temperature. Planta 224:692–699

    PubMed  Article  CAS  Google Scholar 

  • Moser J, Lange C, Krausze J, Rebelein J, Schubert WD, Ribbe MW, Heinz DW, Jahn D (2013) Structure of ADP-aluminium fluoride-stabilized protochlorophyllide oxidoreductase complex. Proc Natl Acad Sci U S A 110(6):2094–2098

    PubMed  PubMed Central  Article  Google Scholar 

  • Muraki N, Nomata J, Ebata K, Mizoguchi T, Shiba T, Tamiaki H, Kurisu G, Fujita Y (2010) X-ray crystal structure of the light-independent protochlorophyllide reductase. Nature 465(7294):110–114

    PubMed  Article  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(1):233–240

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nazir S, Khan MS (2012) Chloroplast-encoded chlB gene from Pinus thunbergii promotes root and early chlorophyll pigment development in Nicotiana tabaccum. Mol Biol Rep 39(12):10637–10646

    PubMed  Article  CAS  Google Scholar 

  • Nomata J, Swem LR, Bauer CE, Fujita Y (2005) Overexpression and characterization of dark-operative protochlorophyllide reductase from Rhodobacter capsulatus. Biochim Biophys Acta Bioenerg 1708:229–237

    Article  CAS  Google Scholar 

  • Nomata J, Kitashima M, Inoue K, Fujita Y (2006a) 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  Article  CAS  Google Scholar 

  • Nomata J, Mizoguchi T, Tamiaki H, Fujita Y (2006b) A second nitrogenase-like enzyme for bacteriochlorophyll biosynthesis: reconstitution of chlorophyllide a reductase with purified X-protein (BchX) and YZ-protein (BchY-BchZ) from Rhodobacter capsulatus. J Biol Chem 281:15021–15028

    PubMed  Article  CAS  Google Scholar 

  • Nomata J, Ogawa T, Kitashima M, Inoue K, Fujita Y (2008) NB protein (BchN–BchB) of dark operative protochlorophyllide reductase is the catalytic component containing oxygen tolerant Fe–S clusters. FEBS Lett 582:1346–1350

    PubMed  Article  CAS  Google Scholar 

  • Nomata J, Kondo T, Mizoguchi T, Tamiaki H, Itoh S, Fujita Y (2014) Dark-operative protochlorophyllide oxidoreductase generates substrate radicals by an iron-sulphur cluster in bacteriochlorophyll biosynthesis. Sci Rep 4:5455

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Nomata J, Terauchi K, Fujita Y (2016) Stoichiometry of ATP hydrolysis and chlorophyllide formation of dark-operative protochlorophyllide oxidoreductase from Rhodobacter capsulatus. Biochem Biophys Res Commun 470:704–709

    PubMed  Article  CAS  Google Scholar 

  • Nowack EC (2014) Paulinella chromatophora—rethinking the transition from endosymbiont to organelle. Acta Soc Bot Pol 83:387–397

    Article  CAS  Google Scholar 

  • Nowack EC, Grossman AR (2012) Trafficking of protein into the recently established photosynthetic organelles of Paulinella chromatophora. Proc Natl Acad Sci U S A 109:5340–5345

    PubMed  PubMed Central  Article  Google Scholar 

  • Olson JM (2001) ‘Evolution of photosynthesis’ (1970), re-examined thirty years later. Photosynth Res 68:95–112

    PubMed  Article  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  Article  CAS  Google Scholar 

  • Ota S, Vaulot D (2012) Lotharella reticulosa sp. nov.: a highly reticulated network forming Chlorarachniophyte from the Mediterranean Sea. Protist 163:91–104

    PubMed  Article  Google Scholar 

  • Pattanaik B, Whitaker MJ, Montgomery BL (2011) Convergence and divergence of the photoregulation of pigmentation and cellular morphology in Fremyella diplosiphon. Plant Signal Behav 6:2038–2041

    PubMed  PubMed Central  Article  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 14:466–471

    Article  CAS  Google Scholar 

  • Pavlovič A, Slováková Ľ, Demko V, Durchan M, Mikulová K, Hudák J (2009) Chlorophyll biosynthesis and chloroplast development in etiolated seedlings of Ginkgo biloba L. Photosynthetica 47:510–516

    Article  CAS  Google Scholar 

  • Postgate JR (1982) Biological nitrogen fixation: fundamentals. Philos Trans R Soc Lond B 296(1082):375–385

    Article  CAS  Google Scholar 

  • Prechtl J, Kneip C, Lockhart P, Wenderoth K, Maier UG (2004) Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. Mol Biol Evol 21(8):1477–1481

    PubMed  Article  CAS  Google Scholar 

  • Rabinowitch EI, Govindjee (1965) The role of chlorophyll in photosynthesis. Sci Am 213:74–83

    PubMed  Article  CAS  Google Scholar 

  • Rabinowitch EI, Govindjee (1969) Photosynthesis. Wiley, New York, pp 1–273

    Google Scholar 

  • Rebeiz CA, Benning C, Bohnert H, Daniell H, Hoober JK, Lichtenthaler HK, Portis AR, Tripathy BC (eds) (2010) The chloroplast: basics and applications. Advances in photosynthesis and respiration. Springer, Dordrecht

    Google Scholar 

  • Reinbothe S, Reinbothe C (1996) The regulation of enzymes involved in chlorophyll biosynthesis. In: EJB reviews. Springer, Berlin, pp 99–119

    Google Scholar 

  • Reinbothe C, El Bakkouri M, Buhr F, Muraki N, Nomata J, Kurisu G, Fujita Y, Reinbothe S (2010) Chlorophyll biosynthesis: spotlight on protochlorophyllide reduction. Trends Plant Sci 15:614–624

    PubMed  Article  CAS  Google Scholar 

  • Rice DW, Palmer JD (2006) An exceptional horizontal gene transfer in plastids: gene replacement by a distant bacterial paralog and evidence that haptophyte and cryptophyte plastids are sisters. BMC Biol 4:31

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Ruck EC, Linard SR, Nakov T, Theriot EC, Alverson AJ (2017) Hoarding and horizontal transfer led to an expanded gene and intron repertoire in the plastid genome of the diatom, Toxarium undulatum (Bacillariophyta). Curr Genet 63:499–507

    PubMed  Article  CAS  Google Scholar 

  • Santini CL, Iobbi-Nivol C, Romane C, Boxer DH, Giordano G (1992) Molybdoenzyme biosynthesis in Escherichia coli: in vitro activation of purified nitrate reductase from a chlB mutant. J Bacteriol 174(24):7934–7940

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Sarma R, Barney BM, Hamilton TL, Jones A, Seefeldt LC, Peters JW (2008) Crystal structure of the L protein of Rhodobacter sphaeroides light-independent protochlorophyllide reductase with MgADP bound: a homologue of the nitrogenase Fe protein. Biochem 47:13004–13015

    Article  CAS  Google Scholar 

  • Satjarak A, Paasch AE, Graham LE, Kim E (2016) Complete chloroplast genome sequence of phagomixotrophic green alga Cymbomonas tetramitiformis. Genome Announc 4:00551–00516

    Article  Google Scholar 

  • Schirrmeister BE, de Vos JM, Antonelli A, Bagheri HC (2013) Evolution of multicellularity coincided with increased diversification of cyanobacteria and the great oxidation event. Proc Natl Acad Sci U S A 110:1791–1796

    PubMed  PubMed Central  Article  Google Scholar 

  • Schoefs B (2000) The light-dependent and light-independent reduction of protochlorophyllide a to chlorophyllide a. Photosynthetica 36:481–496

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Shi C, Shi X (2006) Expression switching of three genes encoding light-independent protochlorophyllide oxidoreductase in Chlorella protothecoides. Biotechnol Lett 28:261–265

    PubMed  Article  CAS  Google Scholar 

  • Shui J, Saunders E, Needleman R, Nappi M, Cooper J, Hall L, Kehoe D, Stowe-Evans E (2009) Light-dependent and light-independent protochlorophyllide oxidoreductases in the chromatically adapting cyanobacterium Fremyella diplosiphon UTEX 481. Plant Cell Physiol 50:1507–1521

    PubMed  Article  CAS  Google Scholar 

  • Silva PJ (2014) With or without light: comparing the reaction mechanism of dark-operative protochlorophyllide oxidoreductase with the energetic requirements of the light-dependent protochlorophyllide oxidoreductase. PeerJ 2:551

    Article  CAS  Google Scholar 

  • Smith RL, Van Baalen C, Tabita FR (1987) Alteration of the Fe protein of nitrogenase by oxygen in the cyanobacterium Anabaena sp. strain CA. J Bacteriol 169(6):2537–2542

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Soora M, Cypionka H (2013) Light enhances survival of Dinoroseobacter shibae during long-term starvation. PLoS One 8:83960

    Article  CAS  Google Scholar 

  • Sousa FL, Shavit-Grievink L, Allen JF, Martin WF (2012) Chlorophyll biosynthesis gene evolution indicates photosystem gene duplication, not photosystem merger, at the origin of oxygenic photosynthesis. Genome Biol Evol 5:200–216

    PubMed Central  Article  CAS  Google Scholar 

  • Stolárik T, Hedtke B, Šantrůček J, Ilík P, Grimm B, Pavlovič A (2017) Transcriptional and post-translational control of chlorophyll biosynthesis by dark-operative protochlorophyllide oxidoreductase in Norway spruce. Photosynth Res 132:165–179

    PubMed  Article  CAS  Google Scholar 

  • Stolárik T, Nožková V, Nosek L, Pavlovič A (2018) Dark chlorophyll synthesis may provide a potential for shade tolerance as shown by a comparative study with seedlings of European larch (Larix decidua) and Norway spruce (Picea abies). Trees 1–15

  • Stowe WC, Brodie-Kommit J, Stowe-Evans E (2011) Characterization of complementary chromatic adaptation in Gloeotrichia UTEX 583 and identification of a transposon-like insertion in the cpeBA operon. Plant Cell Physiol 52:553–562

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Suzuki JY, Bollivar DW, Bauer CE (1997) Genetic analysis of chlorophyll biosynthesis. Annu Rev Genet 31:61–89

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  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 U S A 95:12719–12723

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Tewari AK, Tripathy BC (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol 117:851–858

    Article  CAS  Google Scholar 

  • Tewari AK, Tripathy BC (1999) Acclimation of chlorophyll biosynthetic reactions to temperature stress in cucumber (Cucumis sativus L). Planta 208:431–437

    Article  CAS  Google Scholar 

  • Thakur S, Bothra AK, Sen A (2013) Functional divergence outlines the evolution of novel protein function in NifH/BchL protein family. J Biosci 38(4):733–740

    PubMed  Article  CAS  Google Scholar 

  • Trapp EM, Adler S, Zau-ner S, Maier UG (2012) Rhopalodia gibba and its endosymbionts as a model for early steps in a cyanobacterial primary endosymbiosis. Endocytobiosis Cell Res, 23

  • Treangen TJ, Rocha EP (2011) Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 7:1001284

    Article  CAS  Google Scholar 

  • Tripathy BC, Pattanayak GK (2010) Singlet oxygen-induced oxidative stress in plants. In: Rebeiz CA et al (eds) The chloroplast: basics and applications, vol 31. Springer, Dordrecht, pp 397–423

    Chapter  Google Scholar 

  • Tripathy BC, Pattanayak GK (2012) Chlorophyll biosynthesis in higher plants. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Advances in photosynthesis and respiration, vol 34. Springer, Dordrecht, pp 63–94

    Chapter  Google Scholar 

  • Tripathy BC, Rebeiz CA (1986) Chloroplast biogenesis. Demonstration of the monovinyl and divinyl monocarboxylic routes of chlorophyll biosynthesis in higher plants. J Biol Chem 261:13556–13564

    PubMed  CAS  Google Scholar 

  • Tripathy BC, Rebeiz CA (1988) Chloroplast biogenesis 60: conversion of divinyl protochlorophyllide to monovinyl protochlorophyllide in green(ing) barley, a dark monovinyl/light divinyl plant species. Plant Physiol 87:89–94

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2006) The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Mol Biol Evol 23:1324–1338

    PubMed  Article  CAS  Google Scholar 

  • Ueda M, Tanaka A, Sugimoto K, Shikanai T, Nishimura Y (2014) Chl B requirement for chlorophyll biosynthesis under short photoperiod in Marchantia polymorpha L. Genome Biol Evol 6:620–628

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Walmsley J, Adamson H, Wright M, Wrench P (1999) Can Psilotum and/or Gnetum synthesise chlorophyll in darkness? In: The chloroplast: from molecular biology to biotechnology. Springer, Dordrecht, pp 201–205

    Chapter  Google Scholar 

  • Whelan S, Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699

    PubMed  Article  CAS  Google Scholar 

  • Wong SS (1991) Chemistry of protein conjugation and cross-linking. CRC, Boca Raton

    Google Scholar 

  • Yamada K, Matsuda M, Fujita Y, Matsubara H, Sugai M (1992) A frxC homologue exists in the chloroplast DNAs from various pteridophytes and gymnosperms. Plant Cell Physiol 33:325–327

    Article  CAS  Google Scholar 

  • Yamamoto H, Nomata J, Fujita Y (2008) Functional expression of nitrogenase-like protochlorophyllide reductase from Rhodobacter capsulatus in Escherichia coli. Photochem Photobiol Sci 7:1238–1242

    PubMed  Article  CAS  Google Scholar 

  • Yamamoto H, Kurumiya S, Ohashi R, Fujita Y (2009) Oxygen sensitivity of a nitrogenase-like protochlorophyllide reductase from the cyanobacterium Leptolyngbya boryana. Plant Cell Physiol 50:1663–1673

    PubMed  Article  CAS  Google Scholar 

  • Yamamoto H, Kurumiya S, Ohashi R, Fujita Y (2011) Functional evaluation of a nitrogenase-like protochlorophyllide reductase encoded by the chloroplast DNA of Physcomitrella patens in the cyanobacterium Leptolyngbya boryana. Plant Cell Physiol 522:1983–1993

    Article  CAS  Google Scholar 

  • Yamamoto H, Kusumi J, Yamakawa H, Fujita Y (2017) The effect of two amino acid residue substitutions via RNA editing on dark-operative protochlorophyllide oxidoreductase in the blackpine chloroplasts. Sci Rep 7:2377

    PubMed  PubMed Central  Article  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  PubMed Central  Article  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  PubMed Central  Article  CAS  Google Scholar 

  • Yang N, Reiher M, Wang M, Harmer J, Duin EC (2007) Formation of a nickel−methyl species in methyl-coenzyme M reductase, an enzyme catalyzing methane formation. J Am Chem Soc 129(36):11028–11029

    PubMed  Article  CAS  Google Scholar 

  • Yoon HS, Hackett JD, Bhattacharya D (2002) A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc Natl Acad Sci U S A 99:11724–11729

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Yoon HS, Nakayama T, Reyes-Prieto A, Andersen RA, Boo SM, Ishida KI, Bhattacharya D (2009) A single origin of the photosynthetic organelle in different Paulinella lineages. BMC Evol Biol 9:98–98

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Zeng Y, Feng F, Medova H, Dean J, Koblizek M (2014) Functional type 2 photosynthetic reaction centers found in the rare bacterial phylum Gemmatimonadetes. Proc Natl Acad Sci U S A 111:7795–7800

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Zheng Q, Zhang R, Fogg PC, Beatty JT, Wang Y, Jiao N (2012) Gain and loss of phototrophic genes revealed by comparison of two Citromicrobium bacterial genomes. PLoS One 7:e35790

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Zsebo KM, Hearst JE (1984) Genetic-physical mapping of a photosynthetic gene cluster from R. capsulata. Cell 37:937–947

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Professor Govindjee, University of Illinois, Urbana, USA, for critical reading of the manuscript.

Funding

Financial assistance from DST (grant no. EMR/2016/004976), UGC resource networking, DST-PURSE and DST-FIST to BCT is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Baishnab C. Tripathy.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Bhumi Nath Tripathi

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vedalankar, P., Tripathy, B.C. Evolution of light-independent protochlorophyllide oxidoreductase. Protoplasma 256, 293–312 (2019). https://doi.org/10.1007/s00709-018-1317-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-018-1317-y

Keywords

  • Chlorophyll biosynthesis
  • Chlorophyllide a reductase
  • Endosymbiosis
  • Light-dependent protochlorophyllide oxidoreductase
  • Light-independent protochlorophyllide reductase
  • Nitrogenase
  • Oxygenic photosynthesis