Chapter 4 Regulation and Functions of the Chlorophyll Cycle

Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 31)

Summary

The chlorophyll cycle refers to the interconversion of chlorophyll a and chlorophyll b that occurs within the chloroplasts of higher plants. The forward reaction that converts chlorophyll a to b is catalyzed by chlorophyllide a oxygenase. The backward reaction from chlorophyll b to a is catalyzed by a recently identified enzyme, chlorophyll b reductase, and an unidentified enzyme, which is hypothetically named 7-hydroxymethyl chlorophyll a reductase. The chlorophyll cycle plays two important physiological roles: (a) the chlorophyll cycle adjusts the ratio of the peripheral antenna to the core antenna, and (b) it facilitates the degradation of chlorophyll b, light-harvesting complexes, and thylakoid membranes during leaf senescence. In this article, we summarize the research history, the functions, and the regulation of the chlorophyll cycle. Furthermore, we discuss the evolution of the chlorophyll cycle. Recent progresses in evolutionary aspect are emphasized: those include (a) the discovery of the Prochlorococcus gene for chlorophyllide a oxygenase, (b) the presumable gene separation which occurred in the Prasinophyceae, and (c) the duplication and diversification of the genes encoding chlorophyll b reductase. In addition, our current understanding of the regulatory mechanisms of chlorophyll a to b conversion is described and covers topics such as: (a) transcriptional regulation of chlorophyllide a oxygenase in response to light intensities, (b) the mechanism of chlorophyll b-dependent feedback regulation of chlorophyllide a oxygenase which mechanism involves Clp protease, and (c) the close coordination of the chlorophyll cycle activity and the construction of the photosynthetic machinery. Finally, recent progress in the study of chlorophyll b to a conversion is summarized, the major topic of which is the identification of the genes encoding two isoforms of chlorophyll b reductase.

Keywords

Thylakoid Membrane Core Complex Core Antenna Peripheral Antenna Oxygenic Photosynthetic Organism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

BChl

bacteriochlorophyll;

CAO

chlorophyllide a oxygenase;

Chl

chlorophyll;

CP1

the core complex of the photosystem I;

GFP

green fluorescent protein;

HM

7-hydroxymethyl;

LHC

light-harvesting complexSAM S-adenosyl-L-methionine;

PS

photosystem PCB prochlorophytes chlorophyll b binding proteins

Notes

Acknowledgements

We thank Prof. Isamu Inouye and Ms. Tomoko Chikuni for helpful discussion and for sharing unpublished results with us. We are grateful to Ms. Junko Kishimoto for illustrations. We acknowledge the financial support from the Grant-in-Aid for Creative Scientific Research (17GS0314) to AT and the Grant-in-Aid for Scientific Research (19687003) to RT from the Japanese Ministry of Education, Culture, Sports, Science and Technology.

References

  1. Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P and Jansson S (2003) Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II – effects on photosynthesis, grana stacking and fitness. Plant J 35: 350–361PubMedCrossRefGoogle Scholar
  2. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815CrossRefGoogle Scholar
  3. Barber J (2006) Photosystem II: an enzyme of global significance. Biochem Soc Trans 34: 619–631PubMedCrossRefGoogle Scholar
  4. Barber J, Morris E and Buchel C (2000) Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47. Biochim Biophys Acta 1459: 239–247PubMedCrossRefGoogle Scholar
  5. Bossmann B, Knoetzel J and Jansson S (1997) Screening of chlorina mutants of barley (Hordeum vulgare L.) with antibodies against light-harvesting proteins of PS I and PS II: absence of specific antenna proteins. Photosynth Res 52: 127–136CrossRefGoogle Scholar
  6. Bryant DA and Frigaard NU (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microb 14: 488–496PubMedCrossRefGoogle Scholar
  7. Chen M, Quinnell RG and Larkum AW (2002) The major light-harvesting pigment protein of Acaryochloris marina. FEBS Lett 514: 149–152PubMedCrossRefGoogle Scholar
  8. Courties C, Perasso R, Chretiennot-Dinet MJ, Gouy M, Guillou L and Troussellier M (1998) Phylogenetic analysis and genome size of Ostreococcus tauri (Chlorophyta, Prasinophyceae). J Phycol 34: 844–849CrossRefGoogle Scholar
  9. Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, Partensky F, Degroeve S, Echeynie S, Cooke R, Saeys Y, Wuyts J, Jabbari K, Bowler C, Panaud O, Piegu B, Ball SG, Ral JP, Bouget FY, Piganeau G, De Baets B, Picard A, Delseny M, Demaille J, Van de Peer Y and Moreau H (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103: 11647–11652PubMedCrossRefGoogle Scholar
  10. Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, Barbe V, Duprat S, Galperin MY, Koonin EV, Le Gall F, Makarova KS, Ostrowski M, Oztas S, Robert C, Rogozin IB, Scanlan DJ, Tandeau de Marsac N, Weissenbach J, Wincker P, Wolf YI and Hess WR (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100: 10020–10025PubMedCrossRefGoogle Scholar
  11. Eckhardt U, Grimm B and Hortensteiner S (2004) Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol 56: 1–14PubMedCrossRefGoogle Scholar
  12. Eggink LL, LoBrutto R, Brune DC, Brusslan J, Yamasato A, Tanaka A and Hoober JK (2004) Synthesis of chlorophyll b: localization of chlorophyllide a oxygenase and discovery of a stable radical in the catalytic subunit. BMC Plant Biol 4: 5PubMedCrossRefGoogle Scholar
  13. Espineda C, Linford A, Devine D and Brusslan J (1999) The AtCAO gene, encoding chlorophyll a oxygenase, is required for chlorophyll b synthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 96: 10507–10511PubMedCrossRefGoogle Scholar
  14. Flachmann R (1997) Composition of photosystem II antenna in light-harvesting complex II antisense tobacco plants at varying irradiances. Plant Physiol 113: 787–794PubMedCrossRefGoogle Scholar
  15. Flachmann R and Kuehlbrandt W (1995) Accumulation of plant antenna complexes is regulated by post-transcriptional mechanisms in tobacco. Plant Cell 7: 149–160PubMedGoogle Scholar
  16. Folly P and Engel N (1999) Chlorophyll b to chlorophyll a conversion precedes chlorophyll degradation in Hordeum vulgare L. J Biol Chem 274: 21811–21816PubMedCrossRefGoogle Scholar
  17. Garczarek L, Van Der Staay GWM, Thomas JC and Partensky F (1998) Isolation and characterization of Photosystem I from two strains of the marine oxychlorobacterium Prochlorococcus. Photosynth Res 56: 131–141CrossRefGoogle Scholar
  18. Gough SP, Petersen BO and Duus JO (2000) Anaerobic chlorophyll isocyclic ring formation in Rhodobacter capsulatus requires a cobalamin cofactor. Proc Natl Acad Sci USA 97: 6908–6913PubMedCrossRefGoogle Scholar
  19. Green BR and Durnford DG (1996) The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 47: 685–714PubMedCrossRefGoogle Scholar
  20. Harayama S, Kok M and Neidle EL (1992) Functional and evolutionary relationships among diverse oxygenases. Ann Rev Microb 46: 565–601PubMedCrossRefGoogle Scholar
  21. Harper AL, von Gesjen SE, Linford AS, Peterson MP, Faircloth RS, Thissen MM and Brusslan JA (2004) Chlorophyllide a oxygenase mRNA and protein levels correlate with the chlorophyll a/b ratio in Arabidopsis thaliana. Photosynth Res 79: 149–159PubMedCrossRefGoogle Scholar
  22. Harrison MA, Nemson JA and Melis A (1993) Assembly and composition of the chlorophyll a-b light-harvesting complex of barley (Hordeum vulgare L.): Immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutants. Photosynth Res 38: 141–151CrossRefGoogle Scholar
  23. Hirashima M, Satoh S, Tanaka R and Tanaka A (2006) Pigment shuffling in antenna systems achieved by expressing prokaryotic chlorophyllide a oxygenase in Arabidopsis. J Biol Chem 281: 15385–15393PubMedCrossRefGoogle Scholar
  24. Hirono Y and Redei GP (1963) Multiple allelic control of chlorophyll b level in Arabidopsis thaliana. Nature 197: 1324–1325CrossRefGoogle Scholar
  25. Hoober J and Eggink L (2001) A potential role of chlorophylls b and c in assembly of light-harvesting complexes. FEBS Lett 489: 1–3PubMedCrossRefGoogle Scholar
  26. Hoober JK and Eggink LL (1999) Assembly of light-harvesting complex II and biogenesis of thylakoid membranes in chloroplasts. Photosynth Res 61: 197–215CrossRefGoogle Scholar
  27. Horie Y, Ito H, Kusaba M, Tanaka R and Tanaka A (2009) Participation of chlorophyll b reductase in the initial step of the degradation of light-harvesting chlorophyll a/b-protein complexes in Arabidopsis. J Biol Chem 284: 17449–17456PubMedCrossRefGoogle Scholar
  28. Hortensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57: 55–77PubMedCrossRefGoogle Scholar
  29. Hortensteiner S, Vicentini F and Matile P (1995) Chlorophyll breakdown in senescent cotyledons of rape, brassica-napus L – enzymatic cleavage of phaeophorbide-a in-vitro. New Phytol 129: 237–246CrossRefGoogle Scholar
  30. Ikegami I, Kamiya A and Hase E (1984) Dark formation of chlorophyll in cultured tobacco cells. Plant Cell Physiol 25: 343–348Google Scholar
  31. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436: 793–800CrossRefGoogle Scholar
  32. Ito H, Ohtsuka T and Tanaka A (1996) Conversion of chlorophyll b to chlorophyll a via 7-hydroxymethyl chlorophyll. J Biol Chem 271: 1475–1479PubMedCrossRefGoogle Scholar
  33. Ito H, Takaichi S, Tsuji H and Tanaka A (1994) Properties of synthesis of chlorophyll a from chlorophyll b in cucumber etioplasts. J Biol Chem 269: 22034–22038PubMedGoogle Scholar
  34. Ito H, Tanaka Y, Tsuji H and Tanaka A (1993) Conversion of chlorophyll b to chlorophyll a by isolated cucumber etioplasts. Arch Biochem Biophys 306: 148–151PubMedCrossRefGoogle Scholar
  35. Jen CH, Manfield IW, Michalopoulos I, Pinney JW, Willats WG, Gilmartin PM and Westhead DR (2006) The Arabidopsis co-expression tool (ACT): a WWW-based tool and database for microarray-based gene expression analysis. Plant J 46: 336–348PubMedCrossRefGoogle Scholar
  36. Junker F, Kiewitz R and Cook AM (1997) Characterization of the p-toluenesulfonate operon tsaMBCD and tsaR in Comamonas testosteroni T-2. J Bacteriol 179: 919–927PubMedGoogle Scholar
  37. Kolossov VL and Rebeiz CA (2003) Chloroplast biogenesis 88. Protochlorophyllide b occurs in green but not in etiolated plants. J Biol Chem 278: 49675–49678PubMedGoogle Scholar
  38. Krol M, Spangfort MD, Huner NPA, Oquist G, Gustafsson P and Jansson S (1995) Chlorophyll a/b-binding proteins, pigment conversions, and early light-induced proteins in a chlorophyll b-less barley mutant. Plant Physiol 107: 873–883PubMedCrossRefGoogle Scholar
  39. Kupke DW and Huntington JL (1963) Chlorophyll a appearance in the dark in higher plants: analytical notes. Science 140: 49–51PubMedCrossRefGoogle Scholar
  40. Kusaba M, Ito H, Morita R, Iida S, Sato Y, Fujimoto M, Kawasaki S, Tanaka R, Hirochika H, Nishimura M and Tanaka A (2007) Rice NON-YELLOW COLORING1 is involved in light-harvesting complex II and grana degradation during leaf senescence. Plant Cell 19: 1362–1375PubMedCrossRefGoogle Scholar
  41. Kuttkat A, Edhofer I, Eichacker L and 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: 20451–20455PubMedCrossRefGoogle Scholar
  42. Lee S, Kim JH, Yoo ES, Lee CH, Hirochika H and An G (2005) Differential regulation of chlorophyll a oxygenase genes in rice. Plant Mol Biol 57: 805–818PubMedCrossRefGoogle Scholar
  43. Lindahl M, Yang DH and Andersson B (1995) Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein of photosystem II by a light-induced membrane-associated enzymic system. Eur J Biochem 231: 503–509PubMedCrossRefGoogle Scholar
  44. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X and Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 ANG resolution. Nature (London) 428: 287–292CrossRefGoogle Scholar
  45. Masuda T, Polle JE and Melis A (2002) Biosynthesis and ting recovery of the green alga Dunaliella salina from irradiance stress. Plant Physiol 128: 603–614PubMedCrossRefGoogle Scholar
  46. Masuda T and Takamiya K (2004) Novel insights into the enzymology, regulation and physiological functions of light-dependent protochlorophyllide oxidoreductase in angiosperms. Photosynth Res 81: 1–29PubMedCrossRefGoogle Scholar
  47. Masuda T, Tanaka A and Melis A (2003) Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and Lhcb gene expression. Plant Mol Biol 51: 757–771PubMedCrossRefGoogle Scholar
  48. Matsumoto F, Obayashi T, Sasaki-Sekimoto Y, Ohta H, Takamiya K and Masuda T (2004) Gene expression profiling of the tetrapyrrole metabolic pathway in Arabidopsis with a mini-array system. Plant Physiol 135: 2379–2391PubMedCrossRefGoogle Scholar
  49. Nagata N, Satoh S, Tanaka R and Tanaka A (2004) Domain structures of chlorophyllide a oxygenase of green plants and Prochlorothrix hollandica in relation to catalytic functions. Planta 218: 1019–1025PubMedCrossRefGoogle Scholar
  50. Nakagawara E, Sakuraba Y, Yamasato A, Tanaka R and Tanaka A (2007) Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase. Plant J 49: 800–809PubMedCrossRefGoogle Scholar
  51. Niyogi K (1999) Photoprotection revised: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333–359PubMedCrossRefGoogle Scholar
  52. Nyman ES and Hynninen PH (2004) Research advances in the use of tetrapyrrolic photosensitizers for photodynamic therapy. J Photochem Photobiol B: Biol 73: 1–28PubMedCrossRefGoogle Scholar
  53. Oster U, Tanaka R, Tanaka A and Rudiger W (2000) Cloning and functional expression of the gene encoding the key enzyme for chlorophyll b biosynthesis (CAO) from Arabidopsis thaliana. Plant J 21: 305–310PubMedCrossRefGoogle Scholar
  54. Ouchane S, Steunou AS, Picaud M and Astier C (2004) Aerobic and anaerobic Mg-protoporphyrin monomethyl ester cyclases in purple bacteria: a strategy adopted to bypass the repressive oxygen control system. J Biol Chem 279: 6385–6394PubMedCrossRefGoogle Scholar
  55. Palenik B, Grimwood J, Aerts A, Rouze P, Salamov A, Putnam N, Dupont C, Jorgensen R, Derelle E, Rombauts S, Zhou K, Otillar R, Merchant SS, Podell S, Gaasterland T, Napoli C, Gendler K, Manuell A, Tai V, Vallon O, Piganeau G, Jancek S, Heijde M, Jabbari K, Bowler C, Lohr M, Robbens S, Werner G, Dubchak I, Pazour GJ, Ren Q, Paulsen I, Delwiche C, Schmutz J, Rokhsar D, Van de Peer Y, Moreau H and Grigoriev IV (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci U S A 104: 7705–7710PubMedCrossRefGoogle Scholar
  56. Park SY, Yu JW, Park JS, Li J, Yoo SC, Lee NY, Lee SK, Jeong SW, Seo HS, Koh HJ, Jeon JS, Park YI and Paek NC (2007) The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19: 1649–1664PubMedCrossRefGoogle Scholar
  57. Pattanayak GK, Biswal AK, Reddy VS and Tripathy BC (2005) Light-dependent regulation of chlorophyll b biosynthesis in chlorophyllide a oxygenase overexpressing tobacco plants. Biochem Biophys Res Commun 326: 466–471PubMedCrossRefGoogle Scholar
  58. Pinta V, Picaud M, Reiss-Husson F and Astier C (2002) Rubrivivax gelatinosus acsF (previously orf358) codes for a conserved, putative binuclear-iron-cluster-containing protein involved in aerobic oxidative cyclization of Mg-protoporphyrin IX monomethylester. J Bacteriol 184: 746–753PubMedCrossRefGoogle Scholar
  59. Porra RJ, Schafer W, Cmiel E, Katheder I and Scheer H (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 O-18(2) greening maize leaves. Eur J Biochem 219: 671–679PubMedCrossRefGoogle Scholar
  60. Quail PH (2002) Photosensory perception and signalling in plant cells: new paradigms? Curr Opin Cell Biol 14: 180–188PubMedCrossRefGoogle Scholar
  61. Rebeiz CA, Ioannides IM, Kolossov V and Kopetz KJ (1999) Chloroplast biogenesis 80. Proposal of a unified multibranched chlorophyll a/b biosynthetic pathway. Photosynthetica 36: 117–128Google Scholar
  62. Rebeiz CA, Kolossov VL, Briskin D and Gawienowski M (2003) Chloroplast Biogenesis: Chlorophyll biosynthetic heterogeneity, multiple biosynthetic routes and biological spin-offs. In: Nalwa HS (ed) Handbook of Photochemistry and Photobiology, Vol 4. American Scientific Publishers, Los Angels, CA, pp. 183–248Google Scholar
  63. Reinbothe C, Bartsch S, Eggink LL, Hoober JK, Brusslan J, Andrade-Paz R, Monnet J and Reinbothe S (2006) A role for chlorophyllide a oxygenase in the regulated import and stabilization of light-harvesting chlorophyll a/b proteins. Proc Natl Acad Sci USA 103: 4777–4782PubMedCrossRefGoogle Scholar
  64. Reinbothe S, Pollmann S and Reinbothe C (2003) In situ conversion of protochlorophyllide b to protochlorophyllide a in barley. Evidence for a novel role of 7-formyl reductase in the prolamellar body of etioplasts. J Biol Chem 278: 800–806PubMedCrossRefGoogle Scholar
  65. Ren G, An K, Liao Y, Zhou X, Cao Y, Zhao H, Ge X and Kuai B (2007) Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol 144: 1429–1441PubMedCrossRefGoogle Scholar
  66. Rippka R, Coursin T, Hess W, Lichtle C, Scanlan DJ, Palinska KA, Iteman I, Partensky F, Houmard J and Herdman M (2000) Prochlorococcus marinus Chisholm et al 1992 subsp pastoris subsp nov strain PCC 9511, the first axenic chlorophyll a2/b2-containing cyanobacterium (Oxyphotobacteria). Int J System Evol Microb 50: 1833–1847Google Scholar
  67. Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER and Chisholm SW (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042–1047PubMedCrossRefGoogle Scholar
  68. Ruban A, Wentworth M, Yakushevska A, Andersson J, Lee P, Keegstra W, Dekker J, Boekema E, Jansson S and Horton P (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421: 648–652PubMedCrossRefGoogle Scholar
  69. Rudoi AB, Vezitskii A and Shlyk AA (1982) Enzymatic system transforming chlorophyllide into chlorophyll in etiolated leaves using exogenous substrates. Biokhimiia (Moscow, Russia) 47: 733–739Google Scholar
  70. Rzeznicka K, Walker CJ, Westergren T, Kannangara CG, von Wettstein D, Merchant S, Gough SP and 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 U S A 102: 5886–5891PubMedCrossRefGoogle Scholar
  71. Sakuraba Y, Yamasato A, Tanaka R and Tanaka A (2007) Functional analysis of N-terminal domains of Arabidopsis chlorophyllide a oxygenase. Plant Physiol Biochem 45: 740–749PubMedCrossRefGoogle Scholar
  72. Satoh S, Ikeuchi M, Mimuro M and Tanaka A (2001) Chlorophyll b expressed in cyanobacteria functions as a light-harvesting antenna in photosystem I through flexibility of the proteins. J Biol Chem 276: 4293–4297PubMedCrossRefGoogle Scholar
  73. Satoh S and Tanaka A (2006) Identification of chlorophyllide a oxygenase in the Prochlorococcus genome by a comparative genomic approach. Plant Cell Physiol 47: 1622–1629PubMedCrossRefGoogle Scholar
  74. Scheumann V, Ito H, Tanaka A, Schoch S and Rudiger W (1996) Substrate specificity of chlorophyll(ide) b reductase in etioplasts of barley (Hordeum vulgare L.). Eur J Biochem 242: 163–170PubMedCrossRefGoogle Scholar
  75. Scheumann V, Schoch S and Rudiger W (1998) Chloro­phyll a formation in the chlorophyll b reductase reaction requires reduced ferredoxin. J Biol Chem 273: 35102–35108PubMedCrossRefGoogle Scholar
  76. Scheumann V, Schoch S and Rudiger W (1999) Chlorophyll b reduction during senescence of barley seedlings. Planta 209: 364–370PubMedCrossRefGoogle Scholar
  77. Schnegurt MA and Beale SI (1992) Origin of the chlorophyll b formyl oxygen in Chlorella vulgaris. Biochemistry 31: 11677–11683CrossRefGoogle Scholar
  78. Shedbalkar VP, Ioannides IM and Rebeiz CA (1991) Chloroplast biogenesis. Detection of monovinyl proto­chloro­phyll(ide) b in plants. J Biol Chem 266: 17151–17157PubMedGoogle Scholar
  79. Shlyk A (1971) Biosynthesis of chlorophyll b. Ann Rev. Plant Physiol 22: 169–184CrossRefGoogle Scholar
  80. Standfuss J, Terwisscha van Scheltinga AC, Lamborghini M and Kuhlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24: 919–928PubMedCrossRefGoogle Scholar
  81. Tanaka A, Ito H, Tanaka R, Tanaka NK, Yoshida K and Okada K (1998) Chlorophyll a oxygenase (CAO) is involved in chlorophyll b formation from chlorophyll a. Proc Natl Acad Sci USA 95: 12719–12723PubMedCrossRefGoogle Scholar
  82. Tanaka A and Tsuji H (1981) Changes in Chlorophyll-a and Chlorophyll-B Content in Dark-Incubated Cotyledons Excised from illuminated seedlings – the effect of calcium. Plant Physiol 68: 567–570PubMedCrossRefGoogle Scholar
  83. Tanaka A and Tsuji H (1983) Formation of chlorophyll-protein complexes in greening cucumber cotyledons in light and then in darkness. Plant Cell Physiol 24: 101–108Google Scholar
  84. Tanaka R, Koshino Y, Sawa S, Ishiguro S, Okada K and Tanaka A (2001) Overexpression of chlorophyllide a oxygenase (CAO) enlarges the antenna size of photosystem II in Arabidopsis thaliana. Plant J 26: 365–373PubMedCrossRefGoogle Scholar
  85. Tanaka R and Tanaka A (2005) Effects of chlorophyllide a oxygenase overexpression on light acclimation in Arabidopsis thaliana. Photosynth Res 85: 327–340PubMedCrossRefGoogle Scholar
  86. Tanaka R and Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58: 321–346PubMedCrossRefGoogle Scholar
  87. Tanaka Y, Tanaka A and Tsuji H (1992) Stabilization of apoproteins of light-harvesting chlorophyll-a/b protein complex by feeding 5-aminolevulinic acid under intermittent illumination. Plant Physiol Bioehm 30: 365–370Google Scholar
  88. Tanaka Y, Tanaka A and Tsuji H (1993) Effects of 5-aminolevulinic acid on the accumulation of chlorophyll b and apoproteins of the light-harvesting chlorophyll a/b-protein complex of photosystem II. Plant Cell Physiol 34: 465–472Google Scholar
  89. Thomas H (1997) Tansley review no 92 – chlorophyll: a symptom and a regulator of plastid development. New Phytol 136: 163–181CrossRefGoogle Scholar
  90. Thompson JD, Higgins DG and Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673–4680PubMedCrossRefGoogle Scholar
  91. Ting CS, Rocap G, King J and Chisholm SW (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microb 10: 134–142PubMedCrossRefGoogle Scholar
  92. Tomitani A, Okada K, Miyashita H, Matthijs H, Ohno T and Tanaka A (1999) Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature 400: 159–162PubMedCrossRefGoogle Scholar
  93. Tottey S, Block MA, Allen M, Westergren T, Albrieux C, Scheller HV, Merchant S and Jensen PE (2003) Arabidopsis CHL27, located in both envelope and thylakoid membranes, is required for the synthesis of protochlorophyllide. Proc Natl Acad Sci USA 100: 16119–16124PubMedCrossRefGoogle Scholar
  94. Tzinas G and Argyroudi-Akoyunoglou JH (1988) Chloramphenicol-induced stabilization of light-harvesting complexes in thylakoids during development. FEBS Lett 229: 135–141CrossRefGoogle Scholar
  95. van Der Staay GWM, Yurkova N and Green BR (1998) The 38 kDa chlorophyll a/b protein of the prokaryote Prochlorothrix hollandica is encoded by a divergent pcb gene. Plant Mol Biol 36: 709–716PubMedCrossRefGoogle Scholar
  96. Virgin HI (1960) Pigment transformations in leaves of wheat after irradiation. Physiol Plant 13: 155–164CrossRefGoogle Scholar
  97. Xu H, Vavilin D and Vermaas W (2001) Chlorophyll b can serve as the major pigment in functional photosystem II complexes of cyanobacteria. Proc Natl Acad Sci USA 98: 14168–14173PubMedCrossRefGoogle Scholar
  98. Yamasato A, Nagata N, Tanaka R and Tanaka A (2005) The N-terminal domain of chlorophyllide a oxyge­nase confers protein instability in response to chlorophyll b accumulation in Arabidopsis. Plant Cell 17: 1585–1597PubMedCrossRefGoogle Scholar
  99. Yang DH, Paulsen H and Andersson B (2000) The N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complex (LHCII) is essential for its acclimative proteolysis. FEBS Lett 466: 385–388PubMedCrossRefGoogle Scholar
  100. Zelisko A, Garcia-Lorenzo M, Jackowski G, Jansson S and Funk C (2005) AtFtsH6 is involved in the degradation of the light-harvesting complex II during high-light acclimation and senescence. Proc Natl Acad Sci USA 102: 13699–13704PubMedCrossRefGoogle Scholar
  101. Zhang L, Paakkarinen V, Suorsa M and Aro EM (2001) A SecY homologue is involved in chloroplast-encoded D1 protein biogenesis. J Biol Chem 276: 37809–37814PubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Institute of Low Temperature ScienceHokkaido UniversityKita-kuJapan

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