The green algal eyespot apparatus: a primordial visual system and more?

Most flagellate green algae exhibiting phototaxis posses a singular specialized light sensitive organelle, the eyespot apparatus (EA). Its design principles are similar in all green algae and produce, in conjunction with the movement pattern of the cell, a highly directional optical device. It enables an oriented movement response with respect to the direction and intensity of light. The functional EA involves local specializations of different compartments (plasma membrane, cytosol, and chloroplast) and utilizes specialized microbial-type rhodopsins, which act as directly light-gated ion channels. Due to their elaborate structures and the presence of retinal-based photoreceptors in some lineages, algal EAs are thought to play an important role in the evolution of photoreception and are thus not only of interest to plant biologists. In green algae considerable progress in the molecular dissection of components of this primordial visual system has been made by genetic and proteomic approaches in recent years. This review summarizes general aspects of the green algal EA as well as recent progress in the identification of proteins related to it. Further, novel data supporting a link between eyespot globules and plastoglobules will be presented and potential additional roles of the EA besides those in photoreception will be discussed.

[1]  A. Grossman,et al.  Chlamydomonas reinhardtii in the landscape of pigments. , 2004, Annual review of genetics.

[2]  P. Beyer,et al.  Retinal biosynthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803 , 2004, Molecular microbiology.

[3]  C. Johnson,et al.  The Circadian Clock in Chlamydomonas reinhardtii. What Is It For? What Is It Similar To?1 , 2005, Plant Physiology.

[4]  D. Hopcroft,et al.  A study of chloroplast structure in 3 Megaceros species and 3 Dendroceros species (Anthocerotae) indigenous to New Zealand , 1986 .

[5]  H. Bais,et al.  Genetics, novel weapons and rhizospheric microcosmal signaling in the invasion of Phragmites australis , 2008, Plant signaling & behavior.

[6]  R. Crawford THE PROTOPLASMIC ULTRASTRUCTURE OF THE VEGETATIVE CELL OF MELOSIRA VARIANS C. A. AGARDH 1 , 1973 .

[7]  P. Hegemann,et al.  Desensitization and Dark Recovery of the Photoreceptor Current in Chlamydomonas reinhardtii , 1997, Plant physiology.

[8]  J. Spudich,et al.  Comparative study of phototactic and photophobic receptor chromophore properties in Chlamydomonas reinhardtii. , 1993, Biophysical journal.

[9]  G. Witman Chlamydomonas phototaxis. , 1993, Trends in cell biology.

[10]  R. Brown,et al.  Ultrastructure of the Eyespot and its Possible Significance in Phototaxis of Tetracystis excentrica , 1967 .

[11]  J. Spudich,et al.  Demonstration of a sensory rhodopsin in eubacteria , 2003, Molecular microbiology.

[12]  P. Hegemann,et al.  Volvoxrhodopsin, a Light-Regulated Sensory Photoreceptor of the Spheroidal Green Alga Volvox carteri , 1999, Plant Cell.

[13]  M. Hippler,et al.  Mass spectrometric genomic data mining: Novel insights into bioenergetic pathways in Chlamydomonas reinhardtii , 2006, Proteomics.

[14]  A. Schmid ENDOBACTERIA IN THE DIATOM PINNULARIA (BACILLARIOPHYCEAE). I. “SCATTERED ct‐NUCLEOIDS” EXPLAINED: DAPI–DNA COMPLEXES STEM FROM EXOPLASTIDIAL BACTERIA BORING INTO THE CHLOROPLASTS 1,2 , 2003 .

[15]  N. Okamoto,et al.  A Secondary Symbiosis in Progress? , 2005, Science.

[16]  N. Okamoto,et al.  Hatena arenicola gen. et sp. nov., a katablepharid undergoing probable plastid acquisition. , 2006, Protist.

[17]  U. Rüffer,et al.  High‐speed cinematographic analysis of the movement of Chlamydomonas , 1985 .

[18]  Joseph S. Davis,et al.  HEAVILY LICHENIZED PHYSOLINUM (CHLOROPHYTA) FROM A DIMLY LIT CAVE IN MISSOURI 1 , 1989 .

[19]  H. Fukuzawa,et al.  Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization. , 2003, Biochemical and biophysical research communications.

[20]  M. Hirono,et al.  Phototactic activity in Chlamydomonas 'non-phototactic' mutants deficient in Ca2+-dependent control of flagellar dominance or in inner-arm dynein , 2005, Journal of Cell Science.

[21]  G. Kreimer,et al.  G proteins and Ca2+-modulated protein kinases of a plasma membrane-enriched fraction and isolated eyespot apparatuses of Spermatozopsis similis (chlorophyceae) , 1995 .

[22]  J. Thompson,et al.  Release of Photosynthetic Protein Catabolites by Blebbing from Thylakoids , 1994, Plant physiology.

[23]  B. Zuo,et al.  The response of ultrastructure and function of chloroplasts from cycads to doubled CO2 concentration , 2008, The Botanical Review.

[24]  A. Grossman,et al.  Phototropin involvement in the expression of genes encoding chlorophyll and carotenoid biosynthesis enzymes and LHC apoproteins in Chlamydomonas reinhardtii. , 2006, The Plant journal : for cell and molecular biology.

[25]  Pierre-Alexandre Vidi,et al.  Plastoglobules Are Lipoprotein Subcompartments of the Chloroplast That Are Permanently Coupled to Thylakoid Membranes and Contain Biosynthetic Enzymes , 2006, The Plant Cell Online.

[26]  K. Yoshimura PHOTOACTIVE TERTHIOPHENES: THE INFLUENCE OF SERUM ON ANTI‐HIV (HUMAN IMMUNODEFICIENCY VIRUS) ACTIVITIES , 1994 .

[27]  C. Dieckmann,et al.  Toward a protein map of the green algal eyespot: analysis of eyespot globule-associated proteins , 2006 .

[28]  Kaiyao Huang,et al.  Phototropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[29]  J. W. Hastings,et al.  Action Spectrum for Resetting the Circadian Phototaxis Rhythm in the CW15 Strain of Chlamydomonas: II. Illuminated Cells. , 1991, Plant physiology.

[30]  MOIRA A. Lawson,et al.  Characterization of the Eyespot Regions of “Blind”Chlamydomonas Mutants after Restoration of Photophobic Responses , 1994, The Journal of eukaryotic microbiology.

[31]  K. Kozminski,et al.  High level expression of nonacetylatable α‐tubulin in Chlamydomonas reinhardtii , 1993 .

[32]  S. Dutcher,et al.  Cellular asymmetry in Chlamydomonas reinhardtii. , 1989, Journal of cell science.

[33]  G. Kreimer Light perception and signal modulation during photoorientation of flagellate , 2001 .

[34]  M. Gutensohn,et al.  Characterization of a T-DNA insertion mutant for the protein import receptor atToc33 from chloroplasts , 2004, Molecular Genetics and Genomics.

[35]  High-speed video analysis of the flagellar beat and swimming patterns of algae: possible evolutionary trends in green algae , 1991 .

[36]  T. Kuroiwa,et al.  Genome analysis and its significance in four unicellular algae, Cyanidioschyzon merolae, Ostreococcus tauri, Chlamydomonas reinhardtii, and Thalassiosira pseudonana , 2008, Journal of Plant Research.

[37]  Masaya Satoh,et al.  Isolation of Eyespots of Green Algae and Analyses of Pigments , 1995 .

[38]  G. Kreimer,et al.  Calcium modulates rapid protein phosphorylation/dephosphorylation in isolated eyespot apparatuses of the green alga Spermatozopsis similis , 1995, Planta.

[39]  Douglas S Kim,et al.  Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration , 2008, Nature Neuroscience.

[40]  H. Sakaguchi,et al.  Two photophobic responses in Volvox carteri , 1979 .

[41]  R. Kamiya,et al.  Dominance between the Two Flagella during Phototactic Turning in Chlamydomonas , 2000 .

[42]  P. Walne,et al.  The comparative ultrastructure and possible function of eyespots: Euglena granulata and Chlamydomonas eugametos , 1967, Planta.

[43]  J. Saranak,et al.  Autoregulation of rhodopsin synthesis in Chlamydomonas reinhardtii. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[44]  H. Pakrasi,et al.  The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[45]  S. Dutcher,et al.  Phosphoregulation of an Inner Dynein Arm Complex in Chlamydomonas reinhardtii Is Altered in Phototactic Mutant Strains , 1997, The Journal of cell biology.

[46]  Jureepan Saranak,et al.  A rhodopsin is the functional photoreceptor for phototaxis in the unicellular eukaryote Chlamydomonas , 1984, Nature.

[47]  P. Sitte Hexagonale Anordnung der Globuli in Moos-Chloroplasten , 1963, Protoplasma.

[48]  G. Blobel,et al.  Identification of proteins associated with plastoglobules isolated from pea (Pisum sativum L.) chloroplasts , 1999, Planta.

[49]  K. Foster,et al.  Light Antennas in phototactic algae. , 1980, Microbiological reviews.

[50]  E. Cáceres,et al.  FINE STRUCTURE OF ZOOSPOROGENESIS, ZOOSPORE GERMINATION, AND EARLY GAMETOPHYTE DEVELOPMENT IN CLADOPHORA SURERA (CLADOPHORALES, CHLOROPHYTA) , 1998 .

[51]  Satoru Watanabe,et al.  Screening Effect Diverts the Swimming Directions from Diaphototactic to Positive Phototactic in a Disk-shaped Green Flagellate Mesostigma viride¶ , 2003 .

[52]  G. Kreimer,et al.  Subfractionation of eyespot apparatuses from the green alga Spermatozopsis similis: isolation and characterization of eyespot globules , 2001, Planta.

[53]  W. Vermaas,et al.  The three-dimensional structure of the cyanobacterium Synechocystis sp. PCC 6803 , 2005, Archives of Microbiology.

[54]  E. Govorunova,et al.  Changes in photoreceptor currents and their sensitivity to the chemoeffector tryptone during gamete mating in Chlamydomonas reinhardtii , 2006, Planta.

[55]  E. Bamberg,et al.  Channelrhodopsin-1: A Light-Gated Proton Channel in Green Algae , 2002, Science.

[56]  M. Melkonian,et al.  Phylogenetic analyses of nuclear, mitochondrial, and plastid multigene data sets support the placement of Mesostigma in the Streptophyta. , 2006, Molecular biology and evolution.

[57]  S. Reppert,et al.  Coordination of circadian timing in mammals , 2002, Nature.

[58]  I. Marín,et al.  New Insights into the Evolutionary History of Type 1 Rhodopsins , 2004, Journal of Molecular Evolution.

[59]  P. Hegemann,et al.  In vitro identification of rhodopsin in the green alga Chlamydomonas. , 1991, Biochemistry.

[60]  P. León,et al.  1-Deoxy-d-xylulose-5-phosphate Synthase, a Limiting Enzyme for Plastidic Isoprenoid Biosynthesis in Plants* , 2001, The Journal of Biological Chemistry.

[61]  I. Joint,et al.  Rapid spatiotemporal patterning of cytosolic Ca2+ underlies flagellar excision in Chlamydomonas reinhardtii. , 2007, The Plant journal : for cell and molecular biology.

[62]  T. Hori,et al.  Eyespot behavior during the fertilization of gametes in Ulva arasakii Chihara (Ulvophyceae, Chlorophyta) , 2003 .

[63]  M. Melkonian,et al.  A combined reflection confocal laser scanning, electron and fluorescence microscopy analysis of the eyespot in zoospores of Vischeria spp. (Eustigmatales, Eustigmatophyceae) , 1996 .

[64]  E. H. Harris,et al.  CHLAMYDOMONAS AS A MODEL ORGANISM. , 2003, Annual review of plant physiology and plant molecular biology.

[65]  J. Erickson,et al.  The eyespot of Chlamydomonas reinhardtii: a comparative microspectrophotometric study , 1992, Vision Research.

[66]  B. Diehn,et al.  TERMINOLOGY OF BEHAVIORAL RESPONSES OF MOTILE MICROORGANISMS* , 1977 .

[67]  Satchidananda Panda,et al.  Circadian rhythms from flies to human , 2002, Nature.

[68]  C. Dieckmann,et al.  Eyespot placement and assembly in the green alga Chlamydomonas. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[69]  T. Nakayama,et al.  Ultrastructure of the biflagellate gametes of Collinsiella cava (Ulvophyceae, Chlorophyta) , 2000 .

[70]  J. C. Vuletin,et al.  A Light and Electron Microscopic Study , 1976 .

[71]  E. Cahoon,et al.  Characterization of Tocopherol Cyclases from Higher Plants and Cyanobacteria. Evolutionary Implications for Tocopherol Synthesis and Function1 , 2003, Plant Physiology.

[72]  J. Hastings,et al.  NOVEL DINOFLAGELLATE CLOCK‐RELATED GENES IDENTIFIED THROUGH MICROARRAY ANALYSIS 1 , 2003 .

[73]  J. Yates,et al.  Proteomic Analysis of Isolated Chlamydomonas Centrioles Reveals Orthologs of Ciliary-Disease Genes , 2005, Current Biology.

[74]  Kaiyao Huang,et al.  Localization of the blue-light receptor phototropin to the flagella of the green alga Chlamydomonas reinhardtii. , 2004, Molecular biology of the cell.

[75]  P. Hegemann,et al.  The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. , 2001, Journal of cell science.

[76]  S. Dutcher,et al.  Loss of spatial control of the mitotic spindle apparatus in a Chlamydomonas reinhardtii mutant strain lacking basal bodies. , 1995, Genetics.

[77]  Volker Wagner,et al.  Proteomic Analysis of the Eyespot of Chlamydomonas reinhardtii Provides Novel Insights into Its Components and Tactic Movements[W] , 2006, The Plant Cell Online.

[78]  V. Wagner,et al.  The Phosphoproteome of a Chlamydomonas reinhardtii Eyespot Fraction Includes Key Proteins of the Light Signaling Pathway1[W] , 2007, Plant Physiology.

[79]  P. Hegemann,et al.  All-trans retinal constitutes the functional chromophore in Chlamydomonas rhodopsin. , 1991, Biophysical journal.

[80]  J. Williams,et al.  The osmiophilic globules of chloroplasts: I. Osmiophilic globules as a normal component of chloroplasts and their isolation and composition in Vicia faba L , 1963 .

[81]  K. Nakanishi,et al.  ALL‐trans‐RETINAL IS THE CHROMOPHORE BOUND TO THE PHOTORECEPTOR OF THE ALGA: Chlamydomonas reinhardtii * , 1991, Photochemistry and photobiology.

[82]  Masakatsu Watanabe,et al.  Chlamydomonas reinhardtii Dangeard (Chlamydomonadales, Chlorophyceae) mutant with multiple eyespots , 2001 .

[83]  M. Mittag,et al.  The circadian system of Chlamydomonas reinhardtii , 2006 .

[84]  C. M. Pueschel,et al.  RECONSIDERING PREY SPECIALIZATIONS IN AN ALGAL‐LIMPET GRAZING MUTUALISM: EPITHALLIAL CELL DEVELOPMENT IN CLATHROMORPHUM CIRCUMSCRIPTUM (RHODOPHYTA, CORALLINALES) 1 , 1996 .

[85]  Pierre-Alexandre Vidi,et al.  Plastoglobule lipid bodies: their functions in chloroplasts and their potential for applications. , 2007, Advances in biochemical engineering/biotechnology.

[86]  K. Palczewski,et al.  Activation and inactivation steps in the visual transduction pathway , 1997, Current Opinion in Neurobiology.

[87]  M. Melkonian,et al.  Identification of 11‐cis and all‐trans‐retinal in the photoreceptive organelle of a flagellate green alga , 1991, FEBS letters.

[88]  C. Dieckmann,et al.  Eyespot-assembly mutants in Chlamydomonas reinhardtii. , 1999, Genetics.

[89]  G. Kreimer Reflective properties of different eyespot types in dinoflagellates. , 1999, Protist.

[90]  M. Melkonian,et al.  Eyespot membranes in newly released zoospores of the green algaChlorosarcinopsis gelatinosa (Chlorosarcinales) and their fate during zoospore settlement , 1980, Protoplasma.

[91]  J. Spudich,et al.  Retinal analog restoration of photophobic responses in a blind Chlamydomonas reinhardtii mutant. Evidence for an archaebacterial like chromophore in a eukaryotic rhodopsin. , 1991, Biophysical journal.

[92]  G. Witman,et al.  Submicromolar levels of calcium control the balance of beating between the two flagella in demembranated models of Chlamydomonas , 1984, The Journal of cell biology.

[93]  Carotenoid and ultrastructure variations in plastids of Arum italicum Miller fruit during maturation and ripening. , 2000, Journal of experimental botany.

[94]  M. Melkonian Fate of eyespot lipid globules after zoospore settlement in the green alga Pleurastrum terrestre Fritsch et John , 1981 .

[95]  Oliver P. Ernst,et al.  Channelrhodopsin-1 Initiates Phototaxis and Photophobic Responses in Chlamydomonas by Immediate Light-Induced Depolarization[W] , 2008, The Plant Cell Online.

[96]  Peter Hegemann,et al.  Monitoring Light-induced Structural Changes of Channelrhodopsin-2 by UV-visible and Fourier Transform Infrared Spectroscopy* , 2008, Journal of Biological Chemistry.

[97]  R. Kamiya,et al.  The sensitivity of chlamydomonas photoreceptor is optimized for the frequency of cell body rotation. , 2001, Plant & cell physiology.

[98]  M. Kuntz,et al.  Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. , 2007, Phytochemistry.

[99]  T. Hori,et al.  High-speed video analysis of the flagellar beat and swimming patterns of algae: possible evolutionary trends in green algae , 1991, Protoplasma.

[100]  P. Hegemann,et al.  The Photoreceptor Current of the Green Alga Chlamydomonas , 1992 .

[101]  P. Hegemann,et al.  Sensory Photoreceptors and Light Control of Flagellar Activity , 2009 .

[102]  J. Bewley,et al.  The Effects of Rapid and Very Slow Speeds of Drying on the Ultrastructure and Metabolism of the Desiccation-Sensitive Moss Cratoneuron filicium (Hedw.) Spruce , 1978 .

[103]  T. Brown,et al.  GLAUCOSPHAERA VACUOLATA, ITS ULTRASTRUCTURE AND PHYSIOLOGY 1, 2 , 1970 .

[104]  J. Chappell,et al.  Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathway. , 1999, Critical reviews in biochemistry and molecular biology.

[105]  M. Melkonian,et al.  Functional analysis of the eyespot in Chlamydomonas reinhardtii mutant ey 627, mt− , 1992, Planta.

[106]  M. Schroda RNA silencing in Chlamydomonas: mechanisms and tools , 2006, Current Genetics.

[107]  J. Rochaix,et al.  The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex , 1997, The EMBO journal.

[108]  J. Pozueta-Romero,et al.  A Ubiquitous Plant Housekeeping Gene, PAP, Encodes a Major Protein Component of Bell Pepper Chromoplasts , 1997, Plant physiology.

[109]  Jeff Shrager,et al.  Chlamydomonas reinhardtii at the Crossroads of Genomics , 2003, Eukaryotic Cell.

[110]  C. Dieckmann,et al.  C2 Domain Protein MIN1 Promotes Eyespot Organization in Chlamydomonas reinhardtii , 2008, Eukaryotic Cell.

[111]  W. Gehring,et al.  New perspectives on eye development and the evolution of eyes and photoreceptors. , 2005, The Journal of heredity.

[112]  Sara L. Zimmer,et al.  The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions , 2007, Science.

[113]  E. Bamberg,et al.  Channelrhodopsin-2, a directly light-gated cation-selective membrane channel , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[114]  E. Ermilova,et al.  Phototropin plays a crucial role in controlling changes in chemotaxis during the initial phase of the sexual life cycle in Chlamydomonas , 2004, Planta.

[115]  J. Rochaix,et al.  Biochemical and Structural Studies of the Large Ycf4-Photosystem I Assembly Complex of the Green Alga Chlamydomonas reinhardtii[W] , 2009, The Plant Cell Online.

[116]  R. Uhl,et al.  A microspectrophotometric study of the shielding properties of eyespot and cell body in Chlamydomonas. , 1997, Biophysical journal.

[117]  S. Sattler,et al.  Highly Divergent Methyltransferases Catalyze a Conserved Reaction in Tocopherol and Plastoquinone Synthesis in Cyanobacteria and Photosynthetic Eukaryotes Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.013656. , 2003, The Plant Cell Online.

[118]  L. Barsanti,et al.  A complex photoreceptive structure in the cyanobacterium Leptolyngbya sp. , 2000, Micron.

[119]  M. Gutensohn,et al.  Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. , 2000, The Plant journal : for cell and molecular biology.

[120]  J. Spudich,et al.  Rhodopsin-mediated photoreception in cryptophyte flagellates. , 2005, Biophysical journal.

[121]  Susan K. Dutcher,et al.  Two Flagellar Genes, AGG2 and AGG3, Mediate Orientation to Light in Chlamydomonas , 2006, Current Biology.

[122]  G. Kreimer Cell biology of phototaxis in flagellate algae , 1994 .

[123]  S. Dutcher,et al.  The UNI3 gene is required for assembly of basal bodies of Chlamydomonas and encodes delta-tubulin, a new member of the tubulin superfamily. , 1998, Molecular biology of the cell.

[124]  H. Hoops Motility in the colonial and multicellular Volvocales: structure, function, and evolution , 1997, Protoplasma.

[125]  W. Inwood,et al.  The ultrastructure of a Chlamydomonas reinhardtii mutant strain lacking phytoene synthase resembles that of a colorless alga. , 2008, Molecular plant.

[126]  M. Kuntz,et al.  Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. , 1994, The Plant cell.

[127]  W. Zerges,et al.  Photosystem II Assembly and Repair Are Differentially Localized in Chlamydomonas[W] , 2007, The Plant Cell Online.

[128]  Peter Hegemann,et al.  ALGAL SENSORY PHOTORECEPTORS , 2001 .

[129]  Ernst Bamberg,et al.  Spectral characteristics of the photocycle of channelrhodopsin-2 and its implication for channel function. , 2008, Journal of molecular biology.

[130]  E. Govorunova,et al.  Integration of photo- and chemosensory signaling pathways in Chlamydomonas , 2002, Planta.

[131]  J. Hartshorne THE FUNCTION OF THE EYESPOT IN CHLAM YDOMONAS , 1953 .

[132]  W. Deininger,et al.  Chlamyrhodopsin represents a new type of sensory photoreceptor. , 1995, The EMBO journal.

[133]  J. Dodge The fine structure of algal cells , 1973 .

[134]  G. Pazour,et al.  Mutational analysis of the phototransduction pathway of Chlamydomonas reinhardtii , 1995, The Journal of cell biology.

[135]  Mélanie Schmidt,et al.  EVIDENCE FOR A SPECIALIZED LOCALIZATION OF THE CHLOROPLAST ATP‐SYNTHASE SUBUNITS α, β, AND γ IN THE EYESPOT APPARATUS OF CHLAMYDOMONAS REINHARDTII (CHLOROPHYCEAE) 1 , 2007 .

[136]  M. Melkonian,et al.  Eyespot membranes of Chlamydomonas reinhardii: a freeze-fracture study. , 1980, Journal of ultrastructure research.

[137]  Arana,et al.  Progress in Photosynthesis Research , 1987, Springer Netherlands.

[138]  K. V. van Wijk,et al.  Plastoglobules: versatile lipoprotein particles in plastids. , 2007, Trends in plant science.

[139]  U. Rüffer,et al.  Flagellar photoresponses of Chlamydomonas cells held on micropipettes: II. Change in flagellar beat pattern , 1990 .

[140]  Ø. Moestrup,et al.  ULTRASTRUCTURE OF THE GREEN ALGA DICHOTOMOSIPHON TUBEROSUS WITH SPECIAL REFERENCE TO THE OCCURRENCE OF STRIATED TUBULES IN THE CHLOROPLAST 1 , 1973 .

[141]  M. Melkonian,et al.  Carotenoids in the eyespot apparatus of the flagellate green alga Spermatozopsis similis: Adaptation to the retinal-based photoreceptor , 1994, Planta.

[142]  S. F. Goldstein Flagellar Beat Patterns in Algae , 1992 .

[143]  A. Grossman,et al.  Genome-Based Examination of Chlorophyll and Carotenoid Biosynthesis in Chlamydomonas reinhardtii1[w] , 2005, Plant Physiology.

[144]  K. V. van Wijk,et al.  Protein Profiling of Plastoglobules in Chloroplasts and Chromoplasts. A Surprising Site for Differential Accumulation of Metabolic Enzymes1[W] , 2006, Plant Physiology.

[145]  E. Govorunova,et al.  Chapter 9 Electrical events in photomovement of green flagellated algae , 2001 .

[146]  M. Melkonian,et al.  Reflection confocal laser scanning microscopy of eyespots in flagellated green algae. , 1990, European journal of cell biology.

[147]  C. M. Pueschel,et al.  ULTRASTRUCTURE OF GERMINATING CARPOSPORES OF PORPHYRA VARIEGATA (KJELLM.) HUS (BANGIALES, RHODOPHYTA) 1 , 1985 .

[148]  H. Smith Photosynthetic Pigmentation—Variegations on a Theme , 1999, Plant Cell.

[149]  N. Morel-Laurens CALCIUM CONTROL OF PHOTOTACTIC ORIENTATION IN Chlamydomonas reinhardtii: SIGN AND STRENGTH OF RESPONSE , 1987, Photochemistry and photobiology.

[150]  U. Rüffer,et al.  Flagellar photoresponses ofChlamydomonascells held on micropipettes: II. Change in flagellar beat pattern: Flagellar Beat Pattern Change inchlamydomonas , 1991 .

[151]  W. Gehring Historical perspective on the development and evolution of eyes and photoreceptors. , 2004, The International journal of developmental biology.

[152]  G. T. Boalch,et al.  Observations on the Motile Stage of Halosphaera minor Ostenfeld (Prasinophyceae) with Special Reference to the Cell Structure , 1985 .

[153]  H. Sakaguchi Effect of external ionic environment on phototaxis of Volvox carteri , 1979 .

[154]  Oleg A. Sineshchekov,et al.  Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[155]  Masakatsu Watanabe,et al.  Photosynthesis modulates the sign of phototaxis of wild‐type Chlamydomonas reinhardtii , 1993, FEBS letters.

[156]  F. Taylor,et al.  The Biology of dinoflagellates , 1989 .

[157]  M. Melkonian,et al.  Development of the flagellar apparatus during the cell cycle in unicellular algae , 2005, Protoplasma.

[158]  C. Dieckmann,et al.  Characterization of the EYE2 gene required for eyespot assembly in Chlamydomonas reinhardtii. , 2001, Genetics.

[159]  G. Csucs,et al.  Tocopherol Cyclase (VTE1) Localization and Vitamin E Accumulation in Chloroplast Plastoglobule Lipoprotein Particles* , 2006, Journal of Biological Chemistry.

[160]  V. Wagner,et al.  The power of functional proteomics , 2008, Plant signaling & behavior.

[161]  G. Pazour,et al.  Proteomic analysis of a eukaryotic cilium , 2005, The Journal of cell biology.

[162]  Oliver P. Ernst,et al.  Photoactivation of Channelrhodopsin* , 2008, Journal of Biological Chemistry.

[163]  E. Govorunova,et al.  Chemotaxis in the Green Flagellate Alga Chlamydomonas , 2005, Biochemistry (Moscow).

[164]  J. W. Hastings,et al.  Action Spectrum for Resetting the Circadian Phototaxis Rhythm in the CW15 Strain of Chlamydomonas: I. Cells in Darkness. , 1991, Plant physiology.

[165]  W. Marshall,et al.  The Mother Centriole Plays an Instructive Role in Defining Cell Geometry , 2007, PLoS biology.

[166]  Satoru Watanabe,et al.  Screening Effect Diverts the Swimming Directions from Diaphototactic to Positive Phototactic in a Disk‐shaped Green Flagellate Mesostigma viride ¶ , 2003, Photochemistry and photobiology.

[167]  K. Miyaji Taxonomic study of the genus Spongomorpha (Acrosiphoniales, Chlorophyta) in Japan. I. Spongomorpha spiralis * , 1996 .

[168]  P. Hegemann,et al.  Opsin evolution: out of wild green yonder? , 2000, Trends in genetics : TIG.

[169]  P. Walne The effects of colchicine on cellular organization in Chlamydomonas. I. Light microscopy and cytochemistry. , 1966, American journal of botany.

[170]  P. Lefebvre,et al.  Targeted disruption of the NIT8 gene in Chlamydomonas reinhardtii , 1995, Molecular and cellular biology.

[171]  K. Palczewski,et al.  Rhodopsin phosphorylation: 30 years later , 2003, Progress in Retinal and Eye Research.

[172]  M. Clayton,et al.  THE APICAL MERISTEM OF SPLACHNIDIUM RUGOSUM (PHAEOPHYTA) 1 , 1987 .

[173]  M. A. Farmer,et al.  PLASTID MORPHOLOGY, ULTRASTRUCTURE, AND DEVELOPMENT IN COLACIUM AND THE LORICATE EUGLENOPHYTES (EUGLENOPHYCEAE) 1 , 2003 .

[174]  Ø. Moestrup,et al.  Fine structural studies on an ultraplanktonic species of Pyramimonas, P. virginica (Prasinophyceae), with a discussion of subgenera within the genus Pyramimonas , 1995 .

[175]  G Peltier,et al.  Over-expression of a pepper plastid lipid-associated protein in tobacco leads to changes in plastid ultrastructure and plant development upon stress. , 2000, The Plant journal : for cell and molecular biology.

[176]  M. Feinleib,et al.  PHOTOMOVEMENT IN AN “EYELESS” MUTANT OF Chlamydomonas , 1983 .

[177]  S. Suda LIGHT MICROSCOPY AND ELECTRON MICROSCOPY OF NEPHROSELMIS SPINOSA SP. NOV. (PRASINOPHYCEAE, CHLOROPHYTA) 1 , 2003 .

[178]  Irina Sizova,et al.  Nuclear-Gene Targeting by Using Single-Stranded DNA Avoids Illegitimate DNA Integration in Chlamydomonas reinhardtii , 2005, Eukaryotic Cell.

[179]  G. Witman,et al.  Basal bodies and associated structures are not required for normal flagellar motion or phototaxis in the green alga Chlorogonium elongatum , 1985, The Journal of cell biology.

[180]  M. Melkonian,et al.  REFLECTIVE PROPERTIES OF THE STIGMA IN MALE GAMETES OF ECTOCARPUS SILICULOSUS (PHAEOPHYCEAE) STUDIED BY CONFOCAL LASER SCANNING MICROSCOPY 1 , 1991 .

[181]  Kwang-Hwan Jung,et al.  Chlamydomonas sensory rhodopsins A and B: cellular content and role in photophobic responses. , 2004, Biophysical journal.

[182]  K. Platt,et al.  PLASTID ULTRASTRUCTURE IN THE BARREL CACTUS, ECHINOCACTUS ACANTHODES , 1973 .

[183]  W. Sale,et al.  Casein Kinase I Is Anchored on Axonemal Doublet Microtubules and Regulates Flagellar Dynein Phosphorylation and Activity* , 2000, The Journal of Biological Chemistry.

[184]  D. Mergenhagen Circadian clock: genetic characterization of a short period mutant of Chlamydomonas reinhardii. , 1984, European journal of cell biology.