Photosynthesis Research

, Volume 106, Issue 1–2, pp 57–71 | Cite as

Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes

  • Jonathan A. D. Neilson
  • Dion G. DurnfordEmail author


Eukaryotes acquired photosynthetic metabolism over a billion years ago, and during that time the light-harvesting antennae have undergone significant structural and functional divergence. The antenna systems are generally used to harvest and transfer excitation energy into the reaction centers to drive photosynthesis, but also have the dual role of energy dissipation. Phycobilisomes formed the first antenna system in oxygenic photoautotrophs, and this soluble protein complex continues to be the dominant antenna in extant cyanobacteria, glaucophytes, and red algae. However, phycobilisomes were lost multiple times during eukaryotic evolution in favor of a thylakoid membrane-integral light-harvesting complex (LHC) antenna system found in the majority of eukaryotic taxa. While photosynthesis spread across different eukaryotic kingdoms via endosymbiosis, the antenna systems underwent extensive modification as photosynthetic groups optimized their light-harvesting capacity and ability to acclimate to changing environmental conditions. This review discusses the different classes of LHCs within photosynthetic eukaryotes and examines LHC diversification in different groups in a structural and functional context.


Light-harvesting complexes Evolution Antenna Light-harvesting-like 



This research was supported by a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant to DGD and an NSERC Canada Graduate Fellowship to JADN.


  1. Ahn TK, Avenson TJ, Ballottari M, Cheng Y, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797PubMedCrossRefGoogle Scholar
  2. Alboresi A, Caffarri S, Nogue F, Bassi R, Morosinotto T (2008) In silico and biochemical analysis of Physcomitrella patens photosynthetic antenna: identification of subunits which evolved upon land adaptation. PLoS ONE 3:e2033PubMedCrossRefGoogle Scholar
  3. Amunts A, Drory O, Nelson N (2007) The structure of a plant Photosystem I supercomplex at 3.4 Å resolution. Nature 447:58–63PubMedCrossRefGoogle Scholar
  4. Anderson JM, Chow WS, De Las Rivas J (2008) Dynamic flexibility in the structure and function of Photosystem II in higher plant thylakoid membranes: the grana enigma. Photosynth Res 98:575–587PubMedCrossRefGoogle Scholar
  5. Andersson J, Walters RG, Horton P, Jansson S (2001) Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13:1193–1204PubMedCrossRefGoogle Scholar
  6. Archibald JM (2009) The puzzle of plastid evolution. Curr Biol 19:81–88CrossRefGoogle Scholar
  7. Avenson TJ, Ahn TK, Zigmantas D, Niyogi KK, Li Z, Ballottari M, Bassi R, Fleming GR (2008) Zeaxanthin radical cation formation in minor light-harvesting complexes of higher plant antenna. J Biol Chem 283:3550–3558PubMedCrossRefGoogle Scholar
  8. Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801PubMedCrossRefGoogle Scholar
  9. Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behaviour of higher plant Photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958PubMedCrossRefGoogle Scholar
  10. Baurain D, Brinkmann H, Petersen J, Rodríguez-Ezpeleta N, Stechman A, Demoulin V, Roger AJ, Burger G, Lang BF, Philippe H (2010) Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes and stramenopiles. Mol Biol Evol. doi: 10.1093/molbev/msq059
  11. Becker F, Rhiel E (2006) Immuno-electron microscopic quantification of the fucoxanthin chlorophyll a/c binding polypeptides Fcp2, Fcp4, and Fcp6 of Cyclotella cryptica grown under low- and high-light intensities. Int Microbiol 9:29–36PubMedGoogle Scholar
  12. Beer A, Gundermann K, Beckmann J, Büchel C (2006) Subunit composition and pigmentation of fucoxanthin-chlorophyll proteins in diatoms: evidence for a subunit involved in diadinoxanthin and diatoxanthin binding. Biochemistry 45:13046–13053PubMedCrossRefGoogle Scholar
  13. Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant Photosystem I. Nature 426:630–635PubMedCrossRefGoogle Scholar
  14. Bergantino E, Segalla A, Brunetta A, Teardo E, Rigoni F, Giacometti GM, Szabò I (2003) Light- and pH-dependent structural changes in the PsbS subunit of Photosystem II. Proc Natl Acad Sci USA 100:15265–15270PubMedCrossRefGoogle Scholar
  15. Betterle N, Ballottair M, Zorzan S, de Bianchi S, Cazzaniga S, Dall’Osto L, Morosinotto T, Bassi R (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 22:15255–15266CrossRefGoogle Scholar
  16. Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J, Rögner M (1995) Supramolecular structure of the Photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92:175–179PubMedCrossRefGoogle Scholar
  17. Boekema EJ, van Roon H, Dekker JP (1998) Specific association of Photosystem II and light-harvesting complex II in partially solubilized Photosystem II membranes. FEBS Lett 424:95–99PubMedCrossRefGoogle Scholar
  18. Boekema EJ, van Roon H, Calkoen F, Bassi R, Dekker JP (1999a) Multiple types of association of Photosystem II and its light-harvesting antenna in partially solubilized Photosystem II membranes. Biochemistry 38:2233–2239PubMedCrossRefGoogle Scholar
  19. Boekema EJ, van Roon H, van Breemen JFL, Dekker JP (1999b) Supramolecular organization of Photosystem II and its light-harvesting antenna in partially solubilized Photosystem II membranes. Eur J Biochem 266:444–452PubMedCrossRefGoogle Scholar
  20. Bonente G, Howes B, Caffarri S, Smulevich G, Bassi R (2008a) Interactions between the Photosystem II subunit PsbS and xanthophylls studies in vivo and in vitro. J Biol Chem 283:8434–8445PubMedCrossRefGoogle Scholar
  21. Bonente G, Passarini F, Cazzaniga S, Mancone C, Buia MC, Tripodi M, Bassi R, Caffarri S (2008b) The occurrence of the psbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem Photobiol 84:1359–1370PubMedCrossRefGoogle Scholar
  22. Butler PJG, Kühlbrandt W (1988) Determination of the aggregate size in detergent solution of the light-harvesting chlorophyll a/b complex from chloroplast membranes. Proc Natl Acad Sci USA 85:3797–3801PubMedCrossRefGoogle Scholar
  23. Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46:347–366PubMedCrossRefGoogle Scholar
  24. Damkjær JT, Kereïcher S, Johnson MP, Kovacs L, Kiss AZ, Boekema EJ, Ruban AV, Horton P, Jansson S (2009) The Photosystem II light-harvesting protein Lhcb3 affects the macrostructure of Photosystem II and the rate of state transitions in Arabidopsis. Plant Cell 21:3245–3256PubMedCrossRefGoogle Scholar
  25. de Bianchi S, Dall’Osto L, Tognon G, Morosinotto T, Bassi R (2008) Minor antenna proteins CP24 and CP26 affect the interactions between Photosystem II subunits and the electron transport rate in grana membranes of Arabidopsis. Plant Cell 20:1012–1028PubMedCrossRefGoogle Scholar
  26. Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39PubMedCrossRefGoogle Scholar
  27. Dolganov NAM, Bhaya D, Grossman AR (1995) Cyanobacterial protein with similarity to the chlorophyll a/b binding proteins of higher plants: evolution and regulation. Proc Natl Acad Sci USA 92:636–640PubMedCrossRefGoogle Scholar
  28. Douglas SE, Murphy C, Spencer D, Gray MW (1991) Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350:148–151PubMedCrossRefGoogle Scholar
  29. Elrad D, Grossman AR (2004) A genome’s-eye view of the light-harvesting polypeptides of Chlamydomonas reinhardtii. Curr Genet 45:61–75PubMedCrossRefGoogle Scholar
  30. Eppard M, Krumbein W, von Haeseler, Rhiel E (2000) Characterization of fcp4 and fcp12, two additional genes encoding light harvesting proteins of Cyclotella cryptica (Bacillariophyceae) and phylogenetic analysis of this complex gene family. Plant Biol 2:283–289CrossRefGoogle Scholar
  31. 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 38:9397–9404PubMedCrossRefGoogle Scholar
  32. Ganeteg U, Kulheim C, Andersson J, Jansson S (2004a) Is each light-harvesting complex protein important for plant fitness? Plant Physiol 134:502–509Google Scholar
  33. Ganeteg U, Klimmek F, Jansson S (2004b) Lhca5—an LHC-type protein associated with Photosystem I. Plant Mol Biol 54:641–651PubMedCrossRefGoogle Scholar
  34. Germano M, Yakushevska A, Keegstra W, van Gorkom H, Dekker JP, Boekema EJ (2002) Supramolecular organization of photosystem I and light- harvesting complex I in Chlamydomonas reinhardtii. FEBS Lett 525:121–125PubMedCrossRefGoogle Scholar
  35. Green BR (2003) The evolution of light-harvesting antennas. In: Green BR, Parson W (eds) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, The Netherlands, pp 129–168Google Scholar
  36. Green BR, Kühlbrandt W (1995) Sequence conservation of light-harvesting and stress-response proteins in relation to the three-dimensional molecular structure of LHCII. Photosynth Res 44:139–148CrossRefGoogle Scholar
  37. Green BR, Pichersky E (1994) Hypothesis for the evolution of the three-helix Chl a/b and Chl a/c light-harvesting antenna proteins for two-helix and four-helix ancestors. Photosynth Res 39:149–162CrossRefGoogle Scholar
  38. Gundermann K, Büchel C (2008) The fluorescence yield of the trimeric fucoxanthin–chlorophyll–protein FCPa in the diatom Cyclotella meneghiniana is dependent on the amount of bound diatoxanthin. Photosynth Res 95:229–235PubMedCrossRefGoogle Scholar
  39. Havaux M, Guedeney G, He Q, Grossman AR (2003) Elimination of high-light-inducible polypeptides related to eukaryotic chl a/b-binding proteins results in aberrant photoacclimation in Synechocystis PCC6803. Biochim Biophys Acta 1557:21–33PubMedCrossRefGoogle Scholar
  40. He Q, Dolganov N, Björkman O, Grossman AR (2001) The high light-inducible polypeptides in Synechocystis PCC6803. Expression and function in high light. J Biol Chem 276:306–314PubMedCrossRefGoogle Scholar
  41. Heddad M, Adamska I (2000) Light stress-regulated two-helix proteins in Arabidopsis thaliana related to the chlorophyll a/b-binding gene family. Proc Natl Acad Sci USA 97:3741–3746PubMedCrossRefGoogle Scholar
  42. Heddad M, Adamska I (2002) The evolution of light stress proteins in photosynthetic organisms. Comp Funct Genomics 3:504–510PubMedCrossRefGoogle Scholar
  43. Hobe S, Förster R, Klingler J, Paulsen H (1995) N-proximal sequence motif in light-harvesting chlorophyll a/b-binding protein is essential for the trimerization of light-harvesting chlorophyll a/b complex. Biochemistry 34:10224–10228PubMedCrossRefGoogle Scholar
  44. Hoober JK, Eggnik LL, Chen M (2007) Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts. Photosynth Res 94:387–400PubMedCrossRefGoogle Scholar
  45. Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: Does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275:1069–1079PubMedCrossRefGoogle Scholar
  46. Ihalainen JA, Gobets B, Sznee K, Brazzoli M, Croce R, Bassi R, van Grondelle R, Korppi-Tommola JEI, Dekker JP (2000) Evidence for two spectroscopically different dimers of light-harvesting complex I from green plants. Biochemistry 39:8625–8631PubMedCrossRefGoogle Scholar
  47. Im CS, Zhang Z, Shrager J, Chang CW, Grossman AR (2003) Analysis of light and CO2 regulation in Chlamydomonas reinhardtii using genome-wide approaches. Photosynth Res 75:111–125PubMedCrossRefGoogle Scholar
  48. Jansson S (1994) The light-harvesting chlorophyll a/b binding proteins. Biochim Biophys Acta 1184:1–19PubMedCrossRefGoogle Scholar
  49. Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:1360–1365CrossRefGoogle Scholar
  50. Jensen P, Bassi R, Boekema EJ, Dekker JP, Jansson S, Leister D, Robinson C, Scheller H (2007) Structure, function and regulation of plant Photosystem I. Biochim Biophys Acta 1767:335–352PubMedCrossRefGoogle Scholar
  51. Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving Photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100:98–103PubMedCrossRefGoogle Scholar
  52. Kargul J, Nield J, Barber J (2003) Three-dimensional reconstruction of a light-harvesting complex I-Photosystem I (LHCI-PSI) supercomplex from the green alga Chlamydomonas reinhardtii. J Biol Chem 278:16135–16141PubMedCrossRefGoogle Scholar
  53. Kargul J, Turkina MV, Nield J, Benson S, Vener AV, Barber J (2005) Light-harvesting complex II protein CP29 binds to Photosystem I of Chlamydomonas reinhardtii under State 2 conditions. FEBS J 272:4797–4806PubMedCrossRefGoogle Scholar
  54. Keeling PJ (2009) Chromalveolates and the evolution of plastids by secondary endosymbiosis. J Eukaryot Microbiol 56:1–8PubMedCrossRefGoogle Scholar
  55. Kilian O, Steunou AS, Grossman AR, Bhaya D (2007) A novel two domain-fusion protein in cyanobacteria with similarity to the CAB\ELIP\HLIP superfamily: evolutionary implications and regulation. Mol Plant 1:155–166PubMedCrossRefGoogle Scholar
  56. Kim S, Sandusky P, Bowlby N, Aebersold R, Green BR, Vlahakis S, Yocum C, Pichersky E (1992) Characterization of a spinach PsbS cDNA encoding the 22 kDa protein of Photosystem II. FEBS Lett 314:67–71PubMedCrossRefGoogle Scholar
  57. Kirchhoff H, Mukherjee U, Galla H (2002) Molecular architecture of the thylakoid membrane: lipid diffusion space for plastoquinone. Biochemistry 41:4872–4882PubMedCrossRefGoogle Scholar
  58. Kirchhoff H, Haferkamp S, Allen JF, Epstein DBA, Mullineaux CW (2008) Protein diffusion and macromolecular crowding in thylakoid membranes. Plant Physiol 146:1571–1578PubMedCrossRefGoogle Scholar
  59. Kiss AZ, Ruban AV, Horton P (2008) The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J Biol Chem 283:3972–3978PubMedCrossRefGoogle Scholar
  60. Klimmek F, Sjödin A, Noutsos C, Leister D, Jansson S (2006) Abundantly and rarely expressed Lhc protein genes exhibit distinct regulation patterns in plants. Plant Physiol 140:793–804PubMedCrossRefGoogle Scholar
  61. Kovács L, Damkjær J, Kereïche S, Ilioaia C, Ruban AV, Boekema EJ, Jansson S, Horton P (2006) Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18:3106–3120PubMedCrossRefGoogle Scholar
  62. Koziol AG, Borza T, Ishida K, Keeling P, Lee RW, Durnford DG (2007) Tracing the evolution of the light-harvesting antennae in chlorophyll a/b-containing organisms. Plant Physiol 143:1802–1816PubMedCrossRefGoogle Scholar
  63. Kühlbrandt W, Wang DN, Fujiyoshi Y (1994) Atomic model of plant light-harvesting complex by electron crystallography. Nature 367:614–621PubMedCrossRefGoogle Scholar
  64. Larkum AWD, Vesk M (2003) Algal plastids: their fine structure and properties. In: Douglas S, Larkum AWD, Raven J (eds) Photosynthesis in algae. Kluwer Academic Publishers, The Netherlands, pp 11–28Google Scholar
  65. Lavaud J, Rousseau B, van Gorkom HJ, Etienne AL (2002) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 129:1398–1406PubMedCrossRefGoogle Scholar
  66. Lavergne J, Joliot P (1991) Restricted diffusion in photosynthetic membranes. Trends Biochem Sci 16:129–134PubMedCrossRefGoogle Scholar
  67. Ledford HK, Baroli I, Shin JW, Fischer BB, Eggen RIL, Niyogi KK (2004) Comparative profiling of lipid-soluble antioxidants and transcripts reveals two phases of photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas reinhardtii. Mol Genet Genomics 272:470–479PubMedCrossRefGoogle Scholar
  68. Lefebvre SC, Harris G, Webster R, Leonardos N, Geider RJ, Rains C, Read BA, Garrido JL (2010) Characterization and expression analysis of the Lhcf gene family in Emiliania huxleyi (Haptophyta) reveals differential responses to light and CO2. J Phycol 46:123–134CrossRefGoogle Scholar
  69. Lepetit B, Volke D, Szabó M, Hoffmann R, Garab G, Wilhelm C, Goss R (2007) Spectroscopic and molecular characterization of the oligomeric antenna of the diatom Phaeodactylum tricornutum. Biochemistry 46:9813–9822PubMedCrossRefGoogle Scholar
  70. Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395PubMedCrossRefGoogle Scholar
  71. Li XP, Müller-Moulé P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects Photosystem II from photoinhibition. Proc Natl Acad Sci USA 99:15222–15227PubMedCrossRefGoogle Scholar
  72. Li XP, Gilmore AM, Caffari S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874PubMedCrossRefGoogle Scholar
  73. Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260PubMedCrossRefGoogle Scholar
  74. Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gul L, An X, Chang W (2004) Crystal structure of spinach major light- harvesting complex at 2.72 Å resolution. Nature 428:287–292PubMedCrossRefGoogle Scholar
  75. Lucinski R, Schmid VHR, Jansson S, Klimmek F (2006) Lhca5 interaction with plant Photosystem I. FEBS Lett 580:6485–6488PubMedCrossRefGoogle Scholar
  76. Ludwig M, Gibbs SP (1989) Localization of phycoerythrin at the lumenal surface of the thylakoid membrane in Rhodomonas lens. J Cell Biol 108:875–884PubMedCrossRefGoogle Scholar
  77. Macpherson AN, Hiller RG (2003) Light-harvesting systems in chlorophyll c-containing algae. In: Green BR, Parson W (eds) Light-harvesting antennas in photosynthesis. Kluwer Academic Publishers, The Netherlands, pp 129–168Google Scholar
  78. Marquardt J, Rhiel E (1997) The membrane-intrinsic light-harvesting complex of the red alga Galdieria sulphuraria (formerly Cyanidium caldarium): biochemical and immunochemical characterization. Biochim Biophys Acta 1320:153–164CrossRefGoogle Scholar
  79. Mimuro M, Akimoto S (2003) Carotenoids of light harvesting systems: energy transfer processes from fucoxanthin and peridinin to chlorophyll. In: Douglas S, Larkum A, Raven J (eds) Photosynthesis in algae. Kluwer Academic Publishers, The Netherlands, pp 335–349Google Scholar
  80. Miura K, Yamano T, Yoshioka S, Kohinata T, Inoue Y, Taniguchi F, Asamizu E, Nakamura Y, Tabata S, Yamato KT, Ohyama K, Fukuzawa H (2004) Expression profiling-based identification of CO2-responsive genes regulated by CCM1 controlling a carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 135:1595–1607PubMedCrossRefGoogle Scholar
  81. Montanè MH, Kloppstech K (2000) The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function? Gene 258:1–8Google Scholar
  82. Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324:1724–1726PubMedCrossRefGoogle Scholar
  83. Mozzo M, Mantelli M, Passarini F, Caffarri S, Croce R, Bassi R (2010) Functional analysis of Photosystem I light-harvesting complexes (Lhca) gene products of Chlamydomonas reinhardtii. Biochim Biophys Acta 1797:212–221PubMedCrossRefGoogle Scholar
  84. Mullineaux CW (2005) Function and evolution of grana. Trends Plant Sci 10:521–525PubMedCrossRefGoogle Scholar
  85. Naumann B, Stauber E, Busch A, Sommer F, Hippler M (2005) N-terminal processing of Lhca3 is a key step in remodeling of the Photosystem I-light-harvesting complex under iron deficiency in Chlamydomonas reinhardtii. J Biol Chem 280:20431–20441PubMedCrossRefGoogle Scholar
  86. Naumann B, Busch A, Allmer J, Ostendorf E, Zeller M, Kirchhoff H, Hippler M (2007) Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7:3964–3979PubMedCrossRefGoogle Scholar
  87. Neilson JAD, Durnford DG (2010) Evolutionary distribution of light-harvesting complex-like proteins in photosynthetic eukaryotes. Genome 53:68–78PubMedCrossRefGoogle Scholar
  88. Nield J, Kruse O, Ruprecht J, de Fonseca P, Büchel C, Barber J (2000) Three-dimensional structure of Chlamydomonas reinhardtii and Synechococcus elongatus Photosystem II complexes allows for comparison of their oxygen-evolving complex organization. J Biol Chem 275:27940–27946PubMedGoogle Scholar
  89. Nosenko T, Lidie KL, van Dolah FM, Lindquist E, Cheng JF, US Department of Energy–Joint Genome Institute, Bhattacharya D (2007) Chimeric plastid proteome in the Florida “red tide” dinoflagellate Karenia brevis. Mol Biol Evol 23:2026–2038CrossRefGoogle Scholar
  90. Oeltjen A, Krumbein WE, Rhiel E (2002) Investigations on transcript sizes, steady state mRNA concentrations and diurnal expression of genes encoding fucoxanthin chlorophyll a/c light harvesting polypeptides in the centric diatom Cyclotella cryptica. Plant Biol 4:250–257CrossRefGoogle Scholar
  91. Papagiannakis E, van Stokkum IHM, Fey H, Büchel C, van Grondelle R (2005) Spectroscopic characterization of the excitation energy transfer in the fucoxanthin–chlorophyll protein of diatoms. Photosynth Res 86:241–250PubMedCrossRefGoogle Scholar
  92. Park S, Jung G, Hwang Y, Jin E (2010) Dynamic response of the transcriptome of a psychrophilic diatom, Chaetoceros neogracile, to high irradiance. Planta 231:349–360PubMedCrossRefGoogle Scholar
  93. Pascal AA, Liu Z, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Chang W, Ruban AV (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436:134–137PubMedCrossRefGoogle Scholar
  94. Pearson GA, Hoarau G, Lago-Leston A, Coyer JA, Kube M, Reinhardt R, Henckel K, Serrão ETA, Corre E, Olsen JL (2009) An expressed sequence tag analysis of the intertidal brown seaweeds Fucus serratus (L.) and F. vesiculosus (L.) (Heterokontophyta, Phaeophyceae) in response to abiotic stressors. Mar Biotechnol. doi: 10.1007/s10126-009-9208-z
  95. Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–522PubMedCrossRefGoogle Scholar
  96. Peng L, Fukao Y, Fujiwara T, Shikanai T (2009) Efficient Operation of NAD(P)H Dehydrogenase Requires Supercomplex Formation with Photosystem I via Minor LHCI in Arabidopsis. Plant Cell 21:3623–3640PubMedCrossRefGoogle Scholar
  97. Peter GF, Thornber JP (1991) Biochemical evidence that the higher plant Photosystem II core complex is organized as a dimer. Plant Cell Physiol 32:1237–1250Google Scholar
  98. Qiu YL, Li L, Wang B, Chen Z, Knoop V, Groth-Malonek M, Dombrovska O, Lee J, Kent L, Rest J, Estabrook GF, Hendry TA, Taylor DW, Testa CM, Ambros M, Crandall-Stotler B, Duff RJ, Stech M, Frey W, Quandt D, Davis CC (2006) The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA 103:15511–15516PubMedCrossRefGoogle Scholar
  99. Richard C, Ouellet H, Guertin M (2000) Characterization of the LI818 polypeptide from the green unicellular alga Chlamydomonas reinhardtii. Plant Mol Biol 42:303–316PubMedCrossRefGoogle Scholar
  100. Rodríguez-Ezpeleta N, Brinkmann H, Burey SC, Roure B, Burger G, Löffelhardt W, Bohnert HJ, Philippe H, Lang BF (2005) Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 15:1325–1330PubMedCrossRefGoogle Scholar
  101. Rodríguez-Ezpeleta N, Philippe H, Brinkmann H, Becker B, Melkonian M (2007) Phylogenetic analyses of nuclear, mitochondrial, and plastid multigene data sets support the placement of Mesostigma in the Streptophyta. Mol Biol Evol 24:723–731PubMedCrossRefGoogle Scholar
  102. Ruban AV, Wentworth M, Yakushevska AE, Andersson J, Lee PJ, Keegstra W, Dekker JP, Boekema EJ, Jansson S, Horton P (2003) Plants lacking the main light-harvesting complex retain Photosystem II macro-organization. Nature 421:648–652PubMedCrossRefGoogle Scholar
  103. Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JT, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–579PubMedCrossRefGoogle Scholar
  104. Sanchez-Puerta MV, Delwiche CF (2008) A hypothesis for plastid evolution in chromalveolates. J Phycol 44:1097–1107CrossRefGoogle Scholar
  105. Sanchez-Puerta MV, Bachvaroff TR, Delwiche CF (2007) Sorting wheat from chaff in multi-gene analyses of chlorophyll c-containing plastids. Mol Phylogenet Evol 44:885–897PubMedCrossRefGoogle Scholar
  106. Savard F, Richard C, Guertin M (1996) The Chlamydomonas reinhardtii L1818 gene represents a distant relative of the cabl/ll genes that is regulated during the cell cycle and in response to illumination. Plant Mol Biol 32:461–473PubMedCrossRefGoogle Scholar
  107. Schmid VHR, Cammarata KV, Bruns BU, Schmidt GW (1997) In vitro reconstitution of the photosystem I light-harvesting complex LHCI-730: Heterodimerization is required for antenna pigment organization. Proc Natl Acad Sci USA 94:7667–7672PubMedCrossRefGoogle Scholar
  108. Schultes NP, Peterson RB (2007) Phylogeny-directed structural analysis of the Arabidopsis PsbS protein. Biochem Biophys Res Commun 355:464–470PubMedCrossRefGoogle Scholar
  109. Six C, Worden AZ, Rodríguez F, Moreau H, Partensky F (2005) New insights into the nature and phylogeny of prasinophyte antenna proteins: Ostreococcus tauri, a case study. Mol Biol Evol 22:2217–2230PubMedCrossRefGoogle Scholar
  110. Sobotka R, McLean S, Zuberova M, Hunter CN, Tichy M (2008) The C-terminal extension of ferrochelatase is critical for enzyme activity and for functioning of the tetrapyrrole pathway in Synechocystis strain PCC 6803. J Bacteriol 190:2086–2095PubMedCrossRefGoogle Scholar
  111. Stauber E, Busch A, Naumann B, Svatos A, Hippler M (2009) Proteotypic profiling of LHCI from Chlamydomonas reinhardtii provides new insights into structure and function of the complex. Proteomics 9:398–408PubMedCrossRefGoogle Scholar
  112. Stengel A, Soll J, Bölter B (2007) Protein import into chloroplasts: new aspects of a well-known topic. Biol Chem 388:765–772PubMedCrossRefGoogle Scholar
  113. Storf S, Stauber EJ, Hippler M, Schmid VHR (2004) Proteomic analysis of the Photosystem I light-harvesting antenna in tomato (Lycopersicon esculentum). Biochem 43:9214–9224CrossRefGoogle Scholar
  114. Storm P, Hernandez-Prieto MA, Eggink LL, Hoober JK, Funk C (2008) The small CAB-like proteins of Synechocystis sp. PCC 6803 bind chlorophyll. Photosynth Res 98:479–488PubMedCrossRefGoogle Scholar
  115. Takahashi Y, Yasui T, Stauber EJ, Hippler M (2004) Comparison of the subunit compositions of the PSI-LHCI supercomplex and the LHCI in the green alga Chlamydomonas reinhardtii. Biochemistry 43:7813–7823CrossRefGoogle Scholar
  116. Takahashi H, Iwai M, Takahashi Y, Minagawa J (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 103:477–482PubMedCrossRefGoogle Scholar
  117. Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nature 5:123–135Google Scholar
  118. Tokutsu R, Teramoto H, Takahashi Y, Ono T, Minagawa J (2004) The light-harvesting complex of Photosystem I in Chlamydomonas reinhardtii: protein composition, gene structures and phylogenic implications. Plant Cell Physiol 45:138–145PubMedCrossRefGoogle Scholar
  119. Tokutsu R, Iwai M, Minagawa J (2009) CP29 a monomeric light-harvesting complex II protein, is essential for state transitions in Chlamydomonas reinhardtii. J Biol Chem 284:7777–7782PubMedCrossRefGoogle Scholar
  120. Varsano T, Wolf SG, Pick U (2006) A chlorophyll a/b-binding protein homolog that is induced by iron deficiency is associated with enlarged Photosystem I units in the eukaryotic alga Dunaliella salina. J Biol Chem 218:10305–10315CrossRefGoogle Scholar
  121. Vavilin D, Yao D, Vermaas W (2007) Small cab-like proteins retard degradation of Photosystem II-associated chlorophyll in Synechocystis sp. PCC 6803. J Biol Chem 282:37660–37668PubMedCrossRefGoogle Scholar
  122. Veith T, Büchel C (2007) The monomeric Photosystem I-complex of the diatom Phaeodactylum tricornutum binds specific fucoxanthin chlorophyll proteins (FCPs) as light-harvesting complexes. Biochim Biophys Acta 1767:1428–1435PubMedCrossRefGoogle Scholar
  123. Veith T, Brauns J, Weisheit W, Mittag M, Büchel C (2009) Identification of a specific fucoxanthin-chlorophyll protein in the light harvesting complex of Photosystem I in the diatom Cyclotella meneghiniana. Biochim Biophys Acta 1787:905–912PubMedCrossRefGoogle Scholar
  124. Wolfe GR, Cunningham FX, Durnford DG, Green BR, Gantt E (1994) Evidence for a common origin of chloroplasts with light-harvesting complexes of different pigmentation. Nature 367:566–568CrossRefGoogle Scholar
  125. 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 49:149–160PubMedCrossRefGoogle Scholar
  126. Xu H, Vavilin D, Funk C, Vermaas W (2004) Multiple deletions of small cab-like proteins in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 27:27971–27979CrossRefGoogle Scholar
  127. Yakushevska AE, Keegstra W, Boekema EJ, Dekker JP, Andersson J, Jansson S, Ruban AV, Horton P (2003) The structure of Photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes. Biochemistry 42:608–613PubMedCrossRefGoogle Scholar
  128. Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818PubMedCrossRefGoogle Scholar
  129. Zhang Z, Shrager J, Jain M, Chang CW, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348PubMedCrossRefGoogle Scholar
  130. Zhu S, Green BR (2008) Light-harvesting and photoprotection in diatoms: Identification and expression of LI818-like proteins. In: Allen J, Gantt E, Golbeck J, Osmond B (eds) Photosynthesis. Energy from the Sun. 14th International Congress on Photosynthesis. Springer, the Netherlands, pp 261–264Google Scholar
  131. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of Photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of BiologyUniversity of New BrunswickFrederictonCanada

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