Photosynthesis Research

, Volume 126, Issue 2–3, pp 189–202 | Cite as

Organization of chlorophyll biosynthesis and insertion of chlorophyll into the chlorophyll-binding proteins in chloroplasts

  • Peng Wang
  • Bernhard GrimmEmail author


Oxygenic photosynthesis requires chlorophyll (Chl) for the absorption of light energy, and charge separation in the reaction center of photosystem I and II, to feed electrons into the photosynthetic electron transfer chain. Chl is bound to different Chl-binding proteins assembled in the core complexes of the two photosystems and their peripheral light-harvesting antenna complexes. The structure of the photosynthetic protein complexes has been elucidated, but mechanisms of their biogenesis are in most instances unknown. These processes involve not only the assembly of interacting proteins, but also the functional integration of pigments and other cofactors. As a precondition for the association of Chl with the Chl-binding proteins in both photosystems, the synthesis of the apoproteins is synchronized with Chl biosynthesis. This review aims to summarize the present knowledge on the posttranslational organization of Chl biosynthesis and current attempts to envision the proceedings of the successive synthesis and integration of Chl into Chl-binding proteins in the thylakoid membrane. Potential auxiliary factors, contributing to the control and organization of Chl biosynthesis and the association of Chl with the Chl-binding proteins during their integration into photosynthetic complexes, are discussed in this review.


Tetrapyrrole biosynthesis Chloroplast biogenesis Chlorophyll Photosynthesis Light-harvesting antenna complex Chloroplast signal recognition particle 



This work was supported by a grant of the Deutsche Forschungsgemeinschaft given to BG in the framework of the Priority Program 1710 (Dynamics of Thiol-based Redox Switches in Cellular Physiology). We thank Pawel Brzezowski, Andreas Richter and Boris Hedtke for critically reading the manuscript. No conflict of interest declared.


  1. Adams NB, Marklew CJ, Qian P, Brindley AA, Davison PA, Bullough PA, Hunter CN (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. doi: 10.1042/BJ20140463 PubMedCentralPubMedCrossRefGoogle Scholar
  2. Adamska I, Roobol-Boza M, Lindahl M, Andersson B (1999) Isolation of pigment-binding early light-inducible proteins from pea. European J Biochem 260(2):453–460CrossRefGoogle Scholar
  3. Adhikari ND, Orler R, Chory J, Froehlich JE, Larkin RM (2009) Porphyrins promote the association of GENOMES UNCOUPLED 4 and a Mg-chelatase subunit with chloroplast membranes. J Biol Chem 284(37):24783–24796. doi: 10.1074/jbc.M109.025205 PubMedCentralPubMedCrossRefGoogle Scholar
  4. Adhikari ND, Froehlich JE, Strand DD, Buck SM, Kramer DM, Larkin RM (2011) GUN4-porphyrin complexes bind the ChlH/GUN5 subunit of Mg-Chelatase and promote chlorophyll biosynthesis in Arabidopsis. Plant Cell 23(4):1449–1467. doi: 10.1105/tpc.110.082503 PubMedCentralPubMedCrossRefGoogle Scholar
  5. Albus CA, Salinas A, Czarnecki O, Kahlau S, Rothbart M, Thiele W, Lein W, Bock R, Grimm B, Schottler MA (2012) LCAA, a novel factor required for magnesium protoporphyrin monomethylester cyclase accumulation and feedback control of aminolevulinic acid biosynthesis in tobacco. Plant Physiol 160(4):1923–1939. doi: 10.1104/pp.112.206045 PubMedCentralPubMedCrossRefGoogle Scholar
  6. Aldridge C, Cain P, Robinson C (2009) Protein transport in organelles: protein transport into and across the thylakoid membrane. FEBS J 276(5):1177–1186. doi: 10.1111/j.1742-4658.2009.06875.x PubMedCrossRefGoogle Scholar
  7. Allan RK, Ratajczak T (2011) Versatile TPR domains accommodate different modes of target protein recognition and function. Cell Stress Chaperones 16(4):353–367. doi: 10.1007/s12192-010-0248-0 PubMedCentralPubMedCrossRefGoogle Scholar
  8. Amato S, Liu X, Zheng B, Cantley L, Rakic P, Man HY (2011) AMP-activated protein kinase regulates neuronal polarization by interfering with PI 3-kinase localization. Science 332(6026):247–251. doi: 10.1126/science.1201678 PubMedCentralPubMedCrossRefGoogle Scholar
  9. Amin P, Sy DA, Pilgrim ML, Parry DH, Nussaume L, Hoffman NE (1999) Arabidopsis mutants lacking the 43- and 54-kilodalton subunits of the chloroplast signal recognition particle have distinct phenotypes. Plant Physiol 121(1):61–70PubMedCentralPubMedCrossRefGoogle Scholar
  10. Amunts A, Drory O, Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4 A resolution. Nature 447(7140):58–63. doi: 10.1038/nature05687 PubMedCrossRefGoogle Scholar
  11. Andersson U, Heddad M, Adamska I (2003) Light stress-induced one-helix protein of the chlorophyll a/b-binding family associated with photosystem I. Plant Physiol 132(2):811–820. doi: 10.1104/pp.102.019281 PubMedCentralPubMedCrossRefGoogle Scholar
  12. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi: 10.1146/annurev.arplant.55.031903.141701 PubMedCrossRefGoogle Scholar
  13. Baginsky S, Hennig L, Zimmermann P, Gruissem W (2010) Gene expression analysis, proteomics, and network discovery. Plant Physiol 152(2):402–410. doi: 10.1104/pp.109.150433 PubMedCentralPubMedCrossRefGoogle Scholar
  14. Bals T, Dunschede B, Funke S, Schunemann D (2010) Interplay between the cpSRP pathway components, the substrate LHCP and the translocase Alb3: an in vivo and in vitro study. FEBS Lett 584(19):4138–4144. doi: 10.1016/j.febslet.2010.08.053 PubMedCrossRefGoogle Scholar
  15. Berthold DA, Stenmark P (2003) Membrane-bound diiron carboxylate proteins. Annu Rev Plant Biol 54(1):497–517. doi: 10.1146/annurev.arplant.54.031902.134915 PubMedCrossRefGoogle Scholar
  16. Blatch GL, Lassle M (1999) The tetratricopeptide repeat: a structural motif mediating protein–protein interactions. BioEssays 21(11):932–939. doi: 10.1002/(SICI)1521-1878(199911)21:11<932:AID-BIES5>3.0.CO;2-N PubMedCrossRefGoogle Scholar
  17. Chi W, Sun X, Zhang L (2013) Intracellular signaling from plastid to nucleus. Annu Rev Plant Biol 64(1):559–582. doi: 10.1146/annurev-arplant-050312-120147 PubMedCrossRefGoogle Scholar
  18. Chidgey JW, Linhartova M, Komenda J, Jackson PJ, Dickman MJ, Canniffe DP, Konik P, Pilny J, Hunter CN, Sobotka R (2014) A cyanobacterial chlorophyll synthase-HliD complex associates with the Ycf39 protein and the YidC/Alb3 insertase. Plant Cell 26(3):1267–1279. doi: 10.1105/tpc.114.124495 PubMedCentralPubMedCrossRefGoogle Scholar
  19. Chow KS, Singh DP, Roper JM, Smith AG (1997) A single precursor protein for ferrochelatase-I from Arabidopsis is imported in vitro into both chloroplasts and mitochondria. J Biol Chem 272(44):27565–27571PubMedCrossRefGoogle Scholar
  20. Chow KS, Singh DP, Walker AR, Smith AG (1998) Two different genes encode ferrochelatase in Arabidopsis: mapping, expression and subcellular targeting of the precursor proteins. Plant J 15(4):531–541PubMedCrossRefGoogle Scholar
  21. Czarnecki O, Grimm B (2012) Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. J Exp Bot 63(4):1675–1687. doi: 10.1093/jxb/err437 PubMedCrossRefGoogle Scholar
  22. Czarnecki O, Hedtke B, Melzer M, Rothbart M, Richter A, Schroter Y, Pfannschmidt T, Grimm B (2011) An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. Plant Cell 23(12):4476–4491. doi: 10.1105/tpc.111.086421 PubMedCentralPubMedCrossRefGoogle Scholar
  23. D’Andrea LD, Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28(12):655–662. doi: 10.1016/j.tibs.2003.10.007 PubMedCrossRefGoogle Scholar
  24. 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(21):7603–7612. doi: 10.1021/bi050240x PubMedCrossRefGoogle Scholar
  25. Du SY, Zhang XF, Lu Z, Xin Q, Wu Z, Jiang T, Lu Y, Wang XF, Zhang DP (2012) Roles of the different components of magnesium chelatase in abscisic acid signal transduction. Plant Mol Biol 80(4–5):519–537. doi: 10.1007/s11103-012-9965-3 PubMedCentralPubMedCrossRefGoogle Scholar
  26. Eichacker LA, Helfrich M, Rudiger W, Muller B (1996) Stabilization of chlorophyll a-binding apoproteins P700, CP47, CP43, D2, and D1 by chlorophyll a or Zn-pheophytin a. J Biol Chem 271(50):32174–32179PubMedCrossRefGoogle Scholar
  27. Engelken J, Brinkmann H, Adamska I (2010) Taxonomic distribution and origins of the extended LHC (light-harvesting complex) antenna protein superfamily. BMC Evol Biol 10:233. doi: 10.1186/1471-2148-10-233 PubMedCentralPubMedGoogle Scholar
  28. Falk S, Ravaud S, Koch J, Sinning I (2010) The C terminus of the Alb3 membrane insertase recruits cpSRP43 to the thylakoid membrane. J Biol Chem 285(8):5954–5962. doi: 10.1074/jbc.M109.084996 PubMedCentralPubMedCrossRefGoogle Scholar
  29. Ferro M, Brugiere S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S, Kieffer-Jaquinod S, Bruley C, Garin J, Joyard J, Masselon C, Rolland N (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9(6):1063–1084. doi: 10.1074/mcp.M900325-MCP200 PubMedCentralPubMedCrossRefGoogle Scholar
  30. Funk C, Vermaas W (1999) A cyanobacterial gene family coding for single-helix proteins resembling part of the light-harvesting proteins from higher plants. Biochemistry 38(29):9397–9404. doi: 10.1021/bi990545+ PubMedCrossRefGoogle Scholar
  31. Gabruk M, Stecka A, Strzalka W, Kruk J, Strzalka K, Mysliwa-Kurdziel B (2015) Photoactive protochlorophyllide-enzyme complexes reconstituted with PORA, PORB and PORC proteins of A. thaliana: fluorescence and catalytic properties. PLoS ONE 10(2):e0116990. doi: 10.1371/journal.pone.0116990 PubMedCentralPubMedCrossRefGoogle Scholar
  32. Garczarek L, Poupon A, Partensky F (2003) Origin and evolution of transmembrane Chl-binding proteins: hydrophobic cluster analysis suggests a common one-helix ancestor for prokaryotic (Pcb) and eukaryotic (LHC) antenna protein superfamilies. FEMS Microbiol Lett 222(1):59–68PubMedCrossRefGoogle Scholar
  33. Green BR, Pichersky E, Kloppstech K (1991) Chlorophyll a/b-binding proteins: an extended family. Trends Biochem Sci 16(5):181–186PubMedCrossRefGoogle Scholar
  34. Grimm B, Kloppstech K (1987) The early light-inducible proteins of barley. Characterization of two families of 2-h-specific nuclear-coded chloroplast proteins. Eur J Biochem 167(3):493–499PubMedCrossRefGoogle Scholar
  35. Grimm B, Smith AJ, Kannangara CG, Smith M (1991) Gabaculine-resistant glutamate 1-semialdehyde aminotransferase of Synechococcus. Deletion of a tripeptide close to the NH2 terminus and internal amino acid substitution. J Biol Chem 266(19):12495–12501PubMedGoogle Scholar
  36. Haggie PM, Verkman AS (2002) Diffusion of tricarboxylic acid cycle enzymes in the mitochondrial matrix in vivo. Evidence for restricted mobility of a multienzyme complex. J Biol Chem 277(43):40782–40788. doi: 10.1074/jbc.M207456200 PubMedCrossRefGoogle Scholar
  37. Heddad M, Adamska I (2002) The evolution of light stress proteins in photosynthetic organisms. Comp Funct Genomics 3(6):504–510. doi: 10.1002/cfg.221 PubMedCentralPubMedCrossRefGoogle Scholar
  38. Hernandez-Prieto MA, Tibiletti T, Abasova L, Kirilovsky D, Vass I, Funk C (2011) The small CAB-like proteins of the cyanobacterium Synechocystis sp. PCC 6803: their involvement in chlorophyll biogenesis for Photosystem II. Biochim Biophys Acta 1807:1143–1151. doi: 10.1016/j.bbabio.2011.05.002 PubMedCrossRefGoogle Scholar
  39. 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(3):337–342PubMedCrossRefGoogle Scholar
  40. Hoffman NE, Franklin AE (1994) Evidence for a stromal GTP requirement for the integration of a chlorophyll a/b-binding polypeptide into thylakoid membranes. Plant Physiol 105(1):295–304PubMedCentralPubMedCrossRefGoogle Scholar
  41. Hollingshead S, Kopecna J, Jackson PJ, Canniffe DP, Davison PA, Dickman MJ, Sobotka R, Hunter CN (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. doi: 10.1074/jbc.M112.352526 PubMedCentralPubMedCrossRefGoogle Scholar
  42. Hoober JK, Eggink LL (1999) Assembly of light-harvesting complex II and biogenesis of thylakoid membranes in chloroplasts. Photosynth Res 61:197–215CrossRefGoogle Scholar
  43. Hutin C, Havaux M, Carde JP, Kloppstech K, Meiherhoff K, Hoffman N, Nussaume L (2002) Double mutation cpSRP43−/cpSRP54− is necessary to abolish the cpSRP pathway required for thylakoid targeting of the light-harvesting chlorophyll proteins. Plant J 29(5):531–543PubMedCrossRefGoogle Scholar
  44. Ikegami A, Yoshimura N, Motohashi K, Takahashi S, Romano PG, Hisabori T, Takamiya K, Masuda T (2007) The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin. J Biol Chem 282(27):19282–19291. doi: 10.1074/jbc.M703324200 PubMedCrossRefGoogle Scholar
  45. Jahn D, Chen MW, Soll D (1991) Purification and functional characterization of glutamate-1-semialdehyde aminotransferase from Chlamydomonas reinhardtii. J Biol Chem 266(1):161–167PubMedGoogle Scholar
  46. Jansson S (1994) The light-harvesting chlorophyll a/b-binding proteins. Biochim Biophys Acta 1184(1):1–19PubMedCrossRefGoogle Scholar
  47. Jansson S, Andersson J, Kim SJ, Jackowski G (2000) An Arabidopsis thaliana protein homologous to cyanobacterial high-light-inducible proteins. Plant Mol Biol 42(2):345–351PubMedCrossRefGoogle Scholar
  48. Jarvis P, Lopez-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nat Rev Mol Cell Biol 14(12):787–802. doi: 10.1038/nrm3702 PubMedCrossRefGoogle Scholar
  49. Jensen PE, Gibson LC, Hunter CN (1999) ATPase activity associated with the magnesium-protoporphyrin IX chelatase enzyme of Synechocystis PCC6803: evidence for ATP hydrolysis during Mg2+ insertion, and the MgATP-dependent interaction of the ChlI and ChlD subunits. Biochem J 339(Pt 1):127–134PubMedCentralPubMedCrossRefGoogle Scholar
  50. Jorgensen K, Rasmussen AV, Morant M, Nielsen AH, Bjarnholt N, Zagrobelny M, Bak S, Moller BL (2005) Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr Opin Plant Biol 8(3):280–291. doi: 10.1016/j.pbi.2005.03.014 PubMedCrossRefGoogle Scholar
  51. Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N (2009) Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol Plant 2(6):1154–1180. doi: 10.1093/mp/ssp088 PubMedCrossRefGoogle Scholar
  52. Kauss D, Bischof S, Steiner S, Apel K, Meskauskiene R (2012) FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg(++)-branch of this pathway. FEBS Lett 586(3):211–216. doi: 10.1016/j.febslet.2011.12.029 PubMedCrossRefGoogle Scholar
  53. Kim J, Klein PG, Mullet JE (1991) Ribosomes pause at specific sites during synthesis of membrane-bound chloroplast reaction center protein D1. J Biol Chem 266(23):14931–14938PubMedGoogle Scholar
  54. Klimmek F, Sjodin A, Noutsos C, Leister D, Jansson S (2006) Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol 140(3):793–804. doi: 10.1104/pp.105.073304 PubMedCentralPubMedCrossRefGoogle Scholar
  55. Klimyuk VI, Persello-Cartieaux F, Havaux M, Contard-David P, Schuenemann D, Meiherhoff K, Gouet P, Jones JD, Hoffman NE, Nussaume L (1999) A chromodomain protein encoded by the arabidopsis CAO gene is a plant-specific component of the chloroplast signal recognition particle pathway that is involved in LHCP targeting. Plant Cell 11(1):87–99PubMedCentralPubMedCrossRefGoogle Scholar
  56. Kloppstech K (1985) Diurnal and circadian rhythmicity in the expression of light-induced plant nuclear messenger RNAs. Planta 165(4):502–506. doi: 10.1007/BF00398095 PubMedCrossRefGoogle Scholar
  57. Knoppova J, Sobotka R, Tichy M, Yu J, Konik P, Halada P, Nixon PJ, Komenda J (2014) Discovery of a chlorophyll binding protein complex involved in the early steps of photosystem II assembly in Synechocystis. Plant Cell 26(3):1200–1212. doi: 10.1105/tpc.114.123919 PubMedCentralPubMedCrossRefGoogle Scholar
  58. Koch M, Breithaupt C, Kiefersauer R, Freigang J, Huber R, Messerschmidt A (2004) Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. The EMBO journal 23(8):1720–1728. doi: 10.1038/sj.emboj.7600189 PubMedCentralPubMedCrossRefGoogle Scholar
  59. Komenda J, Sobotka R, Nixon PJ (2012) Assembling and maintaining the photosystem II complex in chloroplasts and cyanobacteria. Curr Opin Plant Biol 15(3):245–251. doi: 10.1016/j.pbi.2012.01.017 PubMedCrossRefGoogle Scholar
  60. Kuttkat A, Edhofer I, Eichacker LA, Paulsen H (1997) Light-harvesting chlorophyll a/b-binding protein stably inserts into etioplast membranes supplemented with Zn-pheophytin a/b. J Biol Chem 272(33):20451–20455PubMedCrossRefGoogle Scholar
  61. Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299(5608):902–906. doi: 10.1126/science.1079978 PubMedCrossRefGoogle Scholar
  62. Lermontova I, Kruse E, Mock HP, Grimm B (1997) Cloning and characterization of a plastidal and a mitochondrial isoform of tobacco protoporphyrinogen IX oxidase. Proc Natl Acad Sci USA 94(16):8895–8900PubMedCentralPubMedCrossRefGoogle Scholar
  63. Li X, Henry R, Yuan J, Cline K, Hoffman NE (1995) A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes. Proc Natl Acad Sci USA 92(9):3789–3793PubMedCentralPubMedCrossRefGoogle Scholar
  64. Li XP, Bjorkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403(6768):391–395. doi: 10.1038/35000131 PubMedCrossRefGoogle Scholar
  65. Lister R, Chew O, Rudhe C, Lee MN, Whelan J (2001) Arabidopsis thaliana ferrochelatase-I and -II are not imported into Arabidopsis mitochondria. FEBS Lett 506(3):291–295PubMedCrossRefGoogle Scholar
  66. Little HN, Jones OT (1976) The subcellular loclization and properties of the ferrochelatase of etiolated barley. Biochem J 156(2):309–314PubMedCentralPubMedCrossRefGoogle Scholar
  67. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 A resolution. Nature 428(6980):287–292. doi: 10.1038/nature02373 PubMedCrossRefGoogle Scholar
  68. Luer C, Schauer S, Mobius K, Schulze J, Schubert WD, Heinz DW, Jahn D, Moser J (2005) Complex formation between glutamyl-tRNA reductase and glutamate-1-semialdehyde 2,1-aminomutase in Escherichia coli during the initial reactions of porphyrin biosynthesis. J Biol Chem 280(19):18568–18572. doi: 10.1074/jbc.M500440200 PubMedCrossRefGoogle Scholar
  69. Lunn JE (2007) Compartmentation in plant metabolism. J Exp Bot 58(1):35–47. doi: 10.1093/jxb/erl134 PubMedCrossRefGoogle Scholar
  70. Luo T, Fan T, Liu Y, Rothbart M, Yu J, Zhou S, Grimm B, Luo M (2012) Thioredoxin redox regulates ATPase activity of magnesium chelatase CHLI subunit and modulates redox-mediated signaling in tetrapyrrole biosynthesis and homeostasis of reactive oxygen species in pea plants. Plant Physiol 159(1):118–130. doi: 10.1104/pp.112.195446 PubMedCentralPubMedCrossRefGoogle Scholar
  71. Lutz C, Roper U, Beer NS, Griffiths T (1981) Sub-etioplast localization of the enzyme NADPH: protochlorophyllide oxidoreductase. Eur J Biochem 118(2):347–353PubMedCrossRefGoogle Scholar
  72. Masuda T, Fusada N, Oosawa N, Takamatsu K, Yamamoto YY, Ohto M, Nakamura K, Goto K, Shibata D, Shirano Y, Hayashi H, Kato T, Tabata S, Shimada H, Ohta H, Takamiya K (2003a) Functional analysis of isoforms of NADPH: protochlorophyllide oxidoreductase (POR), PORB and PORC, Arabidopsis thaliana. Plant Cell Physiol 44(10):963–974PubMedCrossRefGoogle Scholar
  73. Masuda T, Suzuki T, Shimada H, Ohta H, Takamiya K (2003b) Subcellular localization of two types of ferrochelatase in cucumber. Planta 217(4):602–609. doi: 10.1007/s00425-003-1019-2 PubMedCrossRefGoogle Scholar
  74. Matringe M, Camadro JM, Block MA, Joyard J, Scalla R, Labbe P, Douce R (1992) Localization within chloroplasts of protoporphyrinogen oxidase, the target enzyme for diphenylether-like herbicides. J Biol Chem 267(7):4646–4651PubMedGoogle Scholar
  75. 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(22):12826–12831. doi: 10.1073/pnas.221252798 PubMedCentralPubMedCrossRefGoogle Scholar
  76. Minamizaki K, Mizoguchi T, Goto T, Tamiaki H, Fujita Y (2008) Identification of two homologous genes, chlAI and chlA(II), 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. doi: 10.1074/jbc.M708954200 PubMedCrossRefGoogle Scholar
  77. Mochizuki N, Tanaka R, Grimm B, Masuda T, Moulin M, Smith AG, Tanaka A, Terry MJ (2010) The cell biology of tetrapyrroles: a life and death struggle. Trends Plant Sci 15(9):488–498. doi: 10.1016/j.tplants.2010.05.012 PubMedCrossRefGoogle Scholar
  78. Moore M, Harrison MS, Peterson EC, Henry R (2000) Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem 275(3):1529–1532PubMedCrossRefGoogle Scholar
  79. Moore M, Goforth RL, Mori H, Henry R (2003) Functional interaction of chloroplast SRP/FtsY with the ALB3 translocase in thylakoids: substrate not required. J Cell Biol 162(7):1245–1254. doi: 10.1083/jcb.200307067 PubMedCentralPubMedCrossRefGoogle Scholar
  80. 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(10):2139–2151. doi: 10.1093/emboj/19.10.2139 PubMedCentralPubMedCrossRefGoogle Scholar
  81. Moser J, Schubert WD, Beier V, Bringemeier I, Jahn D, Heinz DW (2001) V-shaped structure of glutamyl-tRNA reductase, the first enzyme of tRNA-dependent tetrapyrrole biosynthesis. The EMBO journal 20(23):6583–6590. doi: 10.1093/emboj/20.23.6583 PubMedCentralPubMedCrossRefGoogle Scholar
  82. Müller B, Eichacker LA (1999) Assembly of the D1 precursor in monomeric photosystem II reaction center precomplexes precedes chlorophyll a-triggered accumulation of reaction center II in barley etioplasts. Plant Cell 11(12):2365–2377PubMedCentralPubMedCrossRefGoogle Scholar
  83. Muller AH, Hansson M (2009) The barley magnesium chelatase 150-kd subunit is not an abscisic acid receptor. Plant Physiol 150(1):157–166. doi: 10.1104/pp.109.135277 PubMedCentralPubMedCrossRefGoogle Scholar
  84. Naver H, Boudreau E, Rochaix JD (2001) Functional studies of Ycf3: its role in assembly of photosystem I and interactions with some of its subunits. Plant Cell 13(12):2731–2745PubMedCentralPubMedCrossRefGoogle Scholar
  85. Nickelsen J, Rengstl B (2013) Photosystem II assembly: from cyanobacteria to plants. Annu Rev Plant Biol 64:609–635. doi: 10.1146/annurev-arplant-050312-120124 PubMedCrossRefGoogle Scholar
  86. Nickelsen J, Zerges W (2013) Thylakoid biogenesis has joined the new era of bacterial cell biology. Front Plant Sci 4:458. doi: 10.3389/fpls.2013.00458 PubMedCentralPubMedCrossRefGoogle Scholar
  87. Nilsson R, van Wijk KJ (2002) Transient interaction of cpSRP54 with elongating nascent chains of the chloroplast-encoded D1 protein; ‘cpSRP54 caught in the act’. FEBS Lett 524(1–3):127–133PubMedCrossRefGoogle Scholar
  88. Nussaume L (2008) Chloroplast SRP takes another road. Nat Chem Biol 4(9):529–531. doi: 10.1038/nchembio0908-529 PubMedCrossRefGoogle Scholar
  89. Papenbrock J, Mishra S, Mock HP, Kruse E, Schmidt EK, Petersmann A, Braun HP, Grimm B (2001) Impaired expression of the plastidic ferrochelatase by antisense RNA synthesis leads to a necrotic phenotype of transformed tobacco plants. Plant J 28(1):41–50PubMedCrossRefGoogle Scholar
  90. Peter E, Grimm B (2009) GUN4 is required for posttranslational control of plant tetrapyrrole biosynthesis. Mol Plant 2(6):1198–1210. doi: 10.1093/mp/ssp072 PubMedCrossRefGoogle Scholar
  91. Peter E, Salinas A, Wallner T, Jeske D, Dienst D, Wilde A, Grimm B (2009) Differential requirement of two homologous proteins encoded by sll1214 and sll1874 for the reaction of Mg protoporphyrin monomethylester oxidative cyclase under aerobic and micro-oxic growth conditions. Biochim Biophys Acta 1787(12):1458–1467. doi: 10.1016/j.bbabio.2009.06.006 PubMedCrossRefGoogle Scholar
  92. Pilgrim ML, van Wijk KJ, Parry DH, Sy DA, Hoffman NE (1998) Expression of a dominant negative form of cpSRP54 inhibits chloroplast biogenesis in Arabidopsis. Plant J 13(2):177–186PubMedCrossRefGoogle Scholar
  93. 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(3):746–753PubMedCentralPubMedCrossRefGoogle Scholar
  94. Plumley GF, Schmidt GW (1995) Light-harvesting chlorophyll a/b complexes: interdependent pigment synthesis and protein assembly. Plant Cell 7(6):689–704. doi: 10.1105/tpc.7.6.689 PubMedCentralPubMedCrossRefGoogle Scholar
  95. Pool MR (2005) Signal recognition particles in chloroplasts, bacteria, yeast and mammals (review). Mol Membr Biol 22(1–2):3–15PubMedCrossRefGoogle Scholar
  96. Porra RJ, Lascelles J (1968) Studies on ferrochelatase. The enzymic formation of haem in proplastids, chloroplasts and plant mitochondria. Biochem J 108(2):343–348PubMedCentralPubMedCrossRefGoogle Scholar
  97. Promnares K, Komenda J, Bumba L, Nebesarova J, Vacha F, Tichy M (2006) Cyanobacterial small chlorophyll-binding protein ScpD (HliB) is located on the periphery of photosystem II in the vicinity of PsbH and CP47 subunits. J Biol Chem 281(43):32705–32713. doi: 10.1074/jbc.M606360200 PubMedCrossRefGoogle Scholar
  98. Reisinger V, Ploscher M, Eichacker LA (2008) Lil3 assembles as chlorophyll–binding protein complex during deetiolation. FEBS Lett 582(10):1547–1551. doi: 10.1016/j.febslet.2008.03.042 PubMedCrossRefGoogle Scholar
  99. Rengstl B, Oster U, Stengel A, Nickelsen J (2011) An intermediate membrane subfraction in cyanobacteria is involved in an assembly network for photosystem II biogenesis. J Biol Chem 286(24):21944–21951. doi: 10.1074/jbc.M111.237867 PubMedCentralPubMedCrossRefGoogle Scholar
  100. Richter AS, Grimm B (2013) Thiol-based redox control of enzymes involved in the tetrapyrrole biosynthesis pathway in plants. Front Plant Sci 4:371. doi: 10.3389/fpls.2013.00371 PubMedCentralPubMedCrossRefGoogle Scholar
  101. Richter CV, Trager C, Schunemann D (2008) Evolutionary substitution of two amino acids in chloroplast SRP54 of higher plants cause its inability to bind SRP RNA. FEBS Lett 582(21–22):3223–3229. doi: 10.1016/j.febslet.2008.08.014 PubMedCrossRefGoogle Scholar
  102. Richter A, Peter E, Pors Y, Lorenzen S, Grimm B, Czarnecki O (2010a) Rapid dark repression of 5-aminolevulinic acid synthesis in green barley leaves. Plant Cell Physiol 51(5):670–681. doi: 10.1093/pcp/pcq047 PubMedCrossRefGoogle Scholar
  103. Richter CV, Bals T, Schunemann D (2010b) Component interactions, regulation and mechanisms of chloroplast signal recognition particle-dependent protein transport. Eur J Cell Biol 89(12):965–973. doi: 10.1016/j.ejcb.2010.06.020 PubMedCrossRefGoogle Scholar
  104. Rosenblad MA, Samuelsson T (2004) Identification of chloroplast signal recognition particle RNA genes. Plant Cell Physiol 45(11):1633–1639. doi: 10.1093/pcp/pch185 PubMedCrossRefGoogle Scholar
  105. 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(16):5886–5891. doi: 10.1073/pnas.0501784102 PubMedCentralPubMedCrossRefGoogle Scholar
  106. Schlicke H, Hartwig AS, Firtzlaff V, Richter AS, Glässer C, Maier K, Finkemeier I, Grimm B (2014) Induced deactivation of genes encoding chlorophyll biosynthesis enzymes disentangles tetrapyrrole-mediated retrograde signaling. Mol Plant 7:1211–1217PubMedCrossRefGoogle Scholar
  107. Schottkowski M, Ratke J, Oster U, Nowaczyk M, Nickelsen J (2009) Pitt, a novel tetratricopeptide repeat protein involved in light-dependent chlorophyll biosynthesis and thylakoid membrane biogenesis in Synechocystis sp. PCC 6803. Mol Plant 2(6):1289–1297. doi: 10.1093/mp/ssp075 PubMedCrossRefGoogle Scholar
  108. Schottkowski M, Peters M, Zhan Y, Rifai O, Zhang Y, Zerges W (2012) Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 109(47):19286–19291. doi: 10.1073/pnas.1209860109 PubMedCentralPubMedCrossRefGoogle Scholar
  109. Schüenemann D, Gupta S, Persello-Cartieaux F, Klimyuk VI, Jones JD, Nussaume L, Hoffman NE (1998) A novel signal recognition particle targets light-harvesting proteins to the thylakoid membranes. Proc Natl Acad Sci USA 95(17):10312–10316PubMedCentralPubMedCrossRefGoogle Scholar
  110. Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Wang XL, Peng CC, Yu XC, Zhu SY, Fan RC, Xu YH, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443(7113):823–826. doi: 10.1038/nature05176 PubMedCrossRefGoogle Scholar
  111. Shlyk AA (1971) Biosynthesis of chlorophyll b. Annu Rev Plant Physiol 22:169–184CrossRefGoogle Scholar
  112. Sinha RK, Komenda J, Knoppova J, Sedlarova M, Pospisil P (2012) Small CAB-like proteins prevent formation of singlet oxygen in the damaged photosystem II complex of the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Environ 35(4):806–818. doi: 10.1111/j.1365-3040.2011.02454.x PubMedCrossRefGoogle Scholar
  113. Sobotka R (2014) Making proteins green; biosynthesis of chlorophyll-binding proteins in cyanobacteria. Photosynth Res 119(1–2):223–232. doi: 10.1007/s11120-013-9797-2 PubMedCrossRefGoogle Scholar
  114. Sobotka R, Tichy M, Wilde A, Hunter CN (2011) Functional assignments for the carboxyl-terminal domains of the ferrochelatase from Synechocystis PCC 6803: the CAB domain plays a regulatory role, and region II is essential for catalysis. Plant Physiol 155(4):1735–1747. doi: 10.1104/pp.110.167528 PubMedCentralPubMedCrossRefGoogle Scholar
  115. Sperling U, Franck F, van Cleve B, Frick G, Apel K, Armstrong GA (1998) Etioplast differentiation in arabidopsis: both PORA and PORB restore the prolamellar body and photoactive protochlorophyllide-F655 to the cop1 photomorphogenic mutant. Plant Cell 10(2):283–296PubMedCentralPubMedGoogle Scholar
  116. Storm P, Hernandez-Prieto MA, Eggink LL, Hoober JK, Funk C (2008) The small CAB-like proteins of Synechocystis sp. PCC 6803 bind chlorophyll. In vitro pigment reconstitution studies on one-helix light-harvesting-like proteins. Photosynth Res 98(1–3):479–488. doi: 10.1007/s11120-008-9368-0 PubMedCrossRefGoogle Scholar
  117. Sundberg E, Slagter JG, Fridborg I, Cleary SP, Robinson C, Coupland G (1997) ALBINO3, an Arabidopsis nuclear gene essential for chloroplast differentiation, encodes a chloroplast protein that shows homology to proteins present in bacterial membranes and yeast mitochondria. Plant Cell 9(5):717–730PubMedCentralPubMedGoogle Scholar
  118. Suzuki T, Masuda T, Singh DP, Tan FC, Tsuchiya T, Shimada H, Ohta H, Smith AG, Takamiya K (2002) Two types of ferrochelatase in photosynthetic and nonphotosynthetic tissues of cucumber: their difference in phylogeny, gene expression, and localization. J Biol Chem 277(7):4731–4737. doi: 10.1074/jbc.M105613200 PubMedCrossRefGoogle Scholar
  119. Sweetlove LJ, Fernie AR (2013) The spatial organization of metabolism within the plant cell. Annu Rev Plant Biol 64:723–746. doi: 10.1146/annurev-arplant-050312-120233 PubMedCrossRefGoogle Scholar
  120. Takahashi K, Takabayashi A, Tanaka A, Tanaka R (2014) Functional analysis of light-harvesting-like protein 3 (LIL3) and its light-harvesting chlorophyll-binding motif in Arabidopsis. J Biol Chem 289(2):987–999. doi: 10.1074/jbc.M113.525428 PubMedCentralPubMedCrossRefGoogle Scholar
  121. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346. doi: 10.1146/annurev.arplant.57.032905.105448 PubMedCrossRefGoogle Scholar
  122. Tanaka R, Rothbart M, Oka S, Takabayashi A, Takahashi K, Shibata M, Myouga F, Motohashi R, Shinozaki K, Grimm B, Tanaka A (2010) LIL3, a light-harvesting-like protein, plays an essential role in chlorophyll and tocopherol biosynthesis. Proc Natl Acad Sci USA 107(38):16721–16725. doi: 10.1073/pnas.1004699107 PubMedCentralPubMedCrossRefGoogle Scholar
  123. Tanaka R, Kobayashi K, Masuda T (2011) Tetrapyrrole metabolism in Arabidopsis thaliana. Arabidopsis Book 9:e0145. doi: 10.1199/tab.0145 PubMedCentralPubMedCrossRefGoogle Scholar
  124. Tomiyama M, Inoue S, Tsuzuki T, Soda M, Morimoto S, Okigaki Y, Ohishi T, Mochizuki N, Takahashi K, Kinoshita T (2014) Mg-chelatase I subunit 1 and Mg-protoporphyrin IX methyltransferase affect the stomatal aperture in Arabidopsis thaliana. J Plant Res 127(4):553–563. doi: 10.1007/s10265-014-0636-0 PubMedCrossRefPubMedCentralGoogle Scholar
  125. 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(26):16119–16124. doi: 10.1073/pnas.2136793100 PubMedCentralPubMedCrossRefGoogle Scholar
  126. Trager C, Rosenblad MA, Ziehe D, Garcia-Petit C, Schrader L, Kock K, Richter CV, Klinkert B, Narberhaus F, Herrmann C, Hofmann E, Aronsson H, Schunemann D (2012) Evolution from the prokaryotic to the higher plant chloroplast signal recognition particle: the signal recognition particle RNA is conserved in plastids of a wide range of photosynthetic organisms. Plant Cell 24(12):4819–4836. doi: 10.1105/tpc.112.102996 PubMedCentralPubMedCrossRefGoogle Scholar
  127. Tu CJ, Schüenemann D, Hoffman NE (1999) Chloroplast FtsY, chloroplast signal recognition particle, and GTP are required to reconstitute the soluble phase of light-harvesting chlorophyll protein transport into thylakoid membranes. J Biol Chem 274(38):27219–27224PubMedCrossRefGoogle Scholar
  128. Tzvetkova-Chevolleau T, Franck F, Alawady AE, Dall’Osto L, Carriere F, Bassi R, Grimm B, Nussaume L, Havaux M (2007) The light stress-induced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. Plant J 50(5):795–809. doi: 10.1111/j.1365-313X.2007.03090.x PubMedCrossRefGoogle Scholar
  129. Umena Y, Kawakami K, Shen JR, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 A. Nature 473(7345):55–60. doi: 10.1038/nature09913 PubMedCrossRefGoogle Scholar
  130. Uniacke J, Zerges W (2007) Photosystem II assembly and repair are differentially localized in Chlamydomonas. Plant Cell 19(11):3640–3654. doi: 10.1105/tpc.107.054882 PubMedCentralPubMedCrossRefGoogle Scholar
  131. Uniacke J, Zerges W (2009) Chloroplast protein targeting involves localized translation in Chlamydomonas. Proc Natl Acad Sci U S A 106(5):1439–1444. doi: 10.1073/pnas.0811268106 PubMedCentralPubMedCrossRefGoogle Scholar
  132. van Lis R, Atteia A, Nogaj LA, Beale SI (2005) Subcellular localization and light-regulated expression of protoporphyrinogen IX oxidase and ferrochelatase in Chlamydomonas reinhardtii. Plant Physiol 139(4):1946–1958. doi: 10.1104/pp.105.069732 PubMedCentralPubMedCrossRefGoogle Scholar
  133. Vavilin D, Yao D, Vermaas W (2007) Small Cab-like proteins retard degradation of photosystem II-associated chlorophyll in Synechocystis sp. PCC 6803: kinetic analysis of pigment labeling with 15N and 13C. J Biol Chem 282(52):37660–37668. doi: 10.1074/jbc.M707133200 PubMedCrossRefGoogle Scholar
  134. 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(5):e151. doi: 10.1371/journal.pbio.0030151 PubMedCentralPubMedCrossRefGoogle Scholar
  135. Wang Q, Jantaro S, Lu B, Majeed W, Bailey M, He Q (2008) The high light-inducible polypeptides stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803. Plant Physiol 147(3):1239–1250. doi: 10.1104/pp.108.121087 PubMedCentralPubMedCrossRefGoogle Scholar
  136. Wang P, Liu J, Liu B, Feng D, Da Q, Shu S, Su J, Zhang Y, Wang J, Wang HB (2013) Evidence for a role of chloroplastic m-type thioredoxins in the biogenesis of photosystem II in Arabidopsis. Plant Physiol 163(4):1710–1728. doi: 10.1104/pp.113.228353 PubMedCentralPubMedCrossRefGoogle Scholar
  137. Watanabe N, Che FS, Iwano M, Takayama S, Yoshida S, Isogai A (2001) Dual targeting of spinach protoporphyrinogen oxidase II to mitochondria and chloroplasts by alternative use of two in-frame initiation codons. J Biol Chem 276(23):20474–20481. doi: 10.1074/jbc.M101140200 PubMedCrossRefGoogle Scholar
  138. Winkel BS (2004) Metabolic channeling in plants. Annu Rev Plant Biol 55:85–107. doi: 10.1146/annurev.arplant.55.031903.141714 PubMedCrossRefGoogle Scholar
  139. Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9(5):383–395. doi: 10.1038/nrg2348 PubMedCrossRefGoogle Scholar
  140. Woodson JD, Perez-Ruiz JM, Schmitz RJ, Ecker JR, Chory J (2013) Sigma factor-mediated plastid retrograde signals control nuclear gene expression. Plant Journal 73(1):1–13. doi: 10.1111/tpj.12011 PubMedCentralPubMedCrossRefGoogle Scholar
  141. Xu H, Vavilin D, Funk C, Vermaas W (2002) Small Cab-like proteins regulating tetrapyrrole biosynthesis in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol Biol 49(2):149–160PubMedCrossRefGoogle Scholar
  142. Yang L, Lin C, Liu W, Zhang J, Ohgi KA, Grinstein JD, Dorrestein PC, Rosenfeld MG (2011) ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell 147(4):773–788. doi: 10.1016/j.cell.2011.08.054 PubMedCentralPubMedCrossRefGoogle Scholar
  143. Yao D, Kieselbach T, Komenda J, Promnares K, Prieto MA, Tichy M, Vermaas W, Funk C (2007) Localization of the small CAB-like proteins in photosystem II. J Biol Chem 282(1):267–276. doi: 10.1074/jbc.M605463200 PubMedCrossRefGoogle Scholar
  144. Yao DC, Brune DC, Vavilin D, Vermaas WF (2012) Photosystem II component lifetimes in the cyanobacterium Synechocystis sp. strain PCC 6803: small Cab-like proteins stabilize biosynthesis intermediates and affect early steps in chlorophyll synthesis. J Biol Chem 287(1):682–692. doi: 10.1074/jbc.M111.320994 PubMedCentralPubMedCrossRefGoogle Scholar
  145. Yu B, Gruber MY, Khachatourians GG, Zhou R, Epp DJ, Hegedus DD, Parkin IA, Welsch R, Hannoufa A (2012) Arabidopsis cpSRP54 regulates carotenoid accumulation in Arabidopsis and Brassica napus. J Exp Bot 63(14):5189–5202. doi: 10.1093/jxb/ers179 PubMedCentralPubMedCrossRefGoogle Scholar
  146. Yuan M, Zhang DW, Zhang ZW, Chen YE, Yuan S, Guo YR, Lin HH (2012) Assembly of NADPH: protochlorophyllide oxidoreductase complex is needed for effective greening of barley seedlings. J Plant Physiol 169(13):1311–1316. doi: 10.1016/j.jplph.2012.05.010 PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Institute of Biology/Plant PhysiologyHumboldt-University BerlinBerlinGermany

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