Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into its components and tactic movements

Plant Cell

Volumn 18, Issue 8, 2006, Pages 1908-1930

  Schmidt, Melanie ^a   Geßner, Gunther ^b   Luff, Matthias ^a   Heiland, Ines ^b   Wagner, Volker ^b   Kaminski, Marc ^b   Geimer, Stefan ^c   Eitzinger, Nicole ^a   Reißenweber, Tobias ^a   Voytsekh, Olga ^b   Fiedler, Monika ^b   Mittag, Maria ^b   Kreimer, Georg ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c UNIVERSITY OF BAYREUTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; DATA PROCESSING; MOLECULAR ORIENTATION; PROTEINS; RNA; SIGNAL PROCESSING;

ALGAL VISUAL SYSTEM; EYESPOT APPARATUS; FLAGELLATE GREEN ALGAE; PROTEOMIC ANALYSIS;

ALGAE;

ALGAE; CELLS; DATA PROCESSING; MOLECULAR STRUCTURE; NUCLEIC ACIDS; PROTEINS; SIGNALS;

ALGAE; CHLAMYDOMONAS REINHARDTII; CHLOROPHYTA; MASTIGOPHORA (FLAGELLATES);

EID: 33747470676     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.106.041749     Document Type: Article

References (111)

1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
2. Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G., and Deisseroth, K. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268.
3. Braun, F.-J., and Hegemann, P. (1999). Two independent photoreceptor currents in the spheroid alga Volvox carteri. Biophys. J. 76, 1668-1678.
4. Bruce, V.G. (1970). The biological clock in Chlamydomonas reinhardtii. J. Protozool. 17, 328-334.
5. Byrne, T.E., Wells, M.R., and Johnson, C.H. (1992). Circadian rhythms of chemotaxis to ammonium and methylammonium uptake in Chlamydomonas. Plant Physiol. 98, 879-886.
6. 2+-modulated heterotrimeric GTPases in the eyespot apparatus of a flagellate green alga. Plant Cell 10, 91-103.
7. Carter, C., Pan, S., Zouhar, J., Avila, E.L, Girke, T., and Raikhel, N.V. (2004). The vegetative vacuole proteome of Arabidopsis thaliana reveals predicted und unexpected proteins. Plant Cell 16, 3285-3303.
8. Chua, N.-H., and Bennoun, P. (1975). Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: Wild-type and mutant strains deficient in photosystem II reaction center. Proc. Natl. Acad. Sci. USA 72, 2175-2179.
9. 2-tubulin promoter in Chlamydomonas reinhardtii. Nucleic Acids Res. 20, 2959-2965.
10. Deininger, W., Kroger, P., Hegemann, U., Lottspeich, F., and Hegemann, P. (1995). Chlamyrhodopsin represents a new type of sensory photoreceptors. EMBO J. 14, 5849-5858.
11. Deruère, J., Römer, S., D'Harlingue, A., Backhaus, R.A., Kuntz, M., and Camara, B. (1994). Fibril assembly and carotenoid overaccumulation in chromoplasts: A model for supramolecular lipoprotein structures. Plant Cell 6, 119-133.
12. Dieckmann, C.L. (2003). Eyespot placement and assembly in the green alga Chlamydomonas. Bioessays 25, 410-416.
13. Dunlap, J.C. (1999). Molecular bases for circadian clocks. Cell 96, 271-290.
14. Dunlap, J.C., and Loros, J.J. (2004). The Neurospora circadian system. J. Biol. Rhythms 19, 414-424.
15. Eng, J., McCormack, A.L., and Yates, J.R. (1994). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989.
16. Ermilova, E.V., Zalutskaya, Z.M., Huang, K., and Beck, C.B. (2004). Phototropin plays a crucial role in controlling changes in chemotaxis during the initial phase of the sexual life cycle in Chlamydomonas. Planta 219, 420-427.
17. Eymery, F., and Rey, P. (1999). Immunocytolocalization of two chloroplastic drought-induced stress proteins in well-watered or wilted Solanum tuberosum L. plants. Plant Physiol. Biochem. 37, 305-312.
18. Foster, K.W., and Smyth, R.D. (1980). Light antennas in phototactic alga. Microbiol. Rev. 44, 572-630.
19. Friso, G., Giacomelli, L., Ytterberg, A.J., Peltier, J.-B., Rudella, A., Sun, Q., and van Wijk, K.J. (2004). In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: New proteins, new functions, and a plastid proteome database. Plant Cell 16, 478-499.
20. Fuhrmann, M., Deininger, W., Kateriya, S., and Hegemann, P. (2003). Rhodopsin-related proteins, cop1, cop2, and chop1, in Chlamydomonas reinhardtii. In Photoreceptors and Light Signaling, A. Batschauer, ed (Cambridge, UK: Royal Society of Chemistry), pp. 124-135.
21. Fuhrmann, M., Oertel, W., and Hegemann, P. (1999). A synthetic gene coding for the green fluorescent protein (GFP) is a versatile reporter in Chlamydomonas reinhardtii. Plant J. 19, 353-361.
22. Fuhrmann, M., Stahlberg, A., Govorunova, E., Rank, S., and Hegemann, P. (2001). The abundant retinal protein of the Chlamydomonas eye is not the photoreceptor for phototaxis and photophobic responses. J. Cell Sci. 114, 3857-3863.
23. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.R., Appel, R.D., and Bairoch, A. (2005). Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook, J.M. Walker, ed (Totowa, NJ: Humana Press), pp. 571-607.
24. Gehring, W. (2004). Historical perspective on the development and evolution of eyes and photoreceptors. Int. J. Dev. Biol. 48, 707-717.
25. Gillet, B., Beyly, A., Peltier, G., and Rey, P. (1998). Molecular characterization of CDSP 34 a chloroplastic protein induced by water deficit in Solanum tuberosum L. plants and regulation of CDSP 34 expression by ABA and high illumination. Plant J. 16, 257-262.
26. Govorunova, E.G., Jung, K.-H., Sineshchekov, O.A., and Spudich, J.L. (2004). Chlamydomonas sensory rhodopsins A and B: Cellular content and role in photophobic responses. Biophys. J. 86, 2342-2349.
27. Govorunova, E.G., and Sineshchekov, O.A. (2003). Integration of photo- and chemosensory signalling pathways in Chlamydomonas. Planta 216, 535-540.
28. Govorunova, E.G., and Sineshchekov, O.A. (2005). Chemotaxis in the green flagellate alga Chlamydomonas. Biochemistry (Mosc.) 70, 717-725.
29. Grossman, A., Lohr, M., and Im, C.S. (2004). Chlamydomonas reinhardtii in the landscape of pigments. Annu. Rev. Genet. 38, 119-173.
30. Harmer, S.L, Satchidananda, P., and Kay, S.A. (2001). Molecular bases of circadian rhythms. Annu. Rev. Cell Dev. Biol. 17, 215-253.
31. Harris, E.H. (1989). The Chlamydomonas Sourcebook. (San Diego, CA: Academic Press).
32. Hartshorne, J.N. (1953). The function of the eyespot in Chlamydomonas. New Phytol. 52, 292-297.
33. Harz, H., and Hegemann, P. (1991). Rhodopsin-regulated calcium currents in Chlamydomonas. Nature 351, 489-491.
34. Harz, H., Nonnengässer, C., and Hegemann, P. (1992). The photoreceptor current of the green alga Chlamydomonas. Phil. Trans. R. Soc. London B Biol. Sci. 338, 39-52.
35. Hegemann, P., and Harz, H. (1998). How microalgae see the light. In Microbial Responses to Light and Time. S. Caddick, D. Baumberg, A. Hodgson, and M.K. Phillips-Jones, eds (Cambridge, UK: Cambridge University Press), pp. 95-105.
36. Hofmann, K., and Stoffel, W. (1993). TMbase - A database of membrane spanning proteins segments. Biol. Chem. Hoppe Seyler 374, 166.
37. Holland, E.M., Braun, F.J., Nonnengäßer, C., Harz, H., and Hegemann, P. (1996). The nature of rhodopsin triggered photocurrents in Chlamydomonas. I. Kinetics and influence of divalent cations. Biophys. J. 70, 924-931.
38. Huang, K., and Beck, C.F. (2003). Phototropin is the blue-light receptor that controls multiple steps in the sexual life cycle of the green alga Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 100, 6269-6274.
39. Huang, K., Kunkel, T., and Beck, C.F. (2004). Localization of the blue-light receptor phototropin to the flagella of the green alga Chlamydomonas reinhardtii. Mol. Biol. Cell 15, 3605-3614.
40. Huang, K., Merkle, T., and Beck, C.F. (2002). Isolation and characterization of a Chlamydomonas gene that encodes a putative blue-light photoreceptor of the phototropin family. Physiol. Plant 115, 613-622.
41. Johnson, C.H., Kondo, T., and Hastings, J.W. (1991). Action spectrum for resetting the circadian phototaxis rhythm in the CW15 strains of Chlamydomonas. II. Illuminated cells. Plant Physiol. 97, 1122-1129.
42. Kateriya, S., Nagel, G., Bamberg, E., and Hegemann, P. (2004). "Vision" in single-celled algae. News Physiol. Sci. 19, 133-137.
43. Keller, L.C., Romijn, E.P., Zamora, I., Yates, I.I.I., Jr., and Marshall, W.F. (2005). Proteomic analysis of isolated Chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr. Biol. 15, 1090-1098.
44. Kessler, F., Schnell, D., and Blobel, G. (1999). Identification of proteins associated with plastoglobules isolated from pea (Pisum sativum L.) chloroplasts. Planta 208, 107-113.
45. Kindle, K.L. (1990). High-frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 87, 1228-1232.
46. King, S.M. (1995). Large scale isolation of Chlamydomonas flagella. Methods Cell Biol. 47, 9-12.
47. Kondo, T., Johnson, C.H., and Hastings, J.W. (1991). Action spectrum for resetting the circadian phototaxis rhythm in the cw 15 strains of Chlamydomonas. I. Cells in darkness. Plant Physiol. 95, 197-205.
48. Kreimer, G., Brohsonn, U., and Melkonian, M. (1991). Isolation and partial characterization of the photoreceptive organelle for phototaxis of a flagellate green alga. Eur. J. Cell Biol. 55, 318-327.
49. Kreimer, G., and Melkonian, M. (1990). Reflection confocal laser scanning microscopy of eyespots in flagellate green alga. Eur. J. Cell Biol. 53, 101-111.
50. Kreimer, G., Overländer, C., Sineshchekov, O.A., Stolzis, H., Nultsch, W., and Melkonian, M. (1992). Functional analysis of the eyespot in Chlamydomonas reinhardtii mutant ey 627, mt. Planta 188, 513-521.
51. Kreimer, G. (1994). Cell biology of phototaxis in flagellated algae. Int. Rev. Cytol. 148, 229-310.
52. Kreimer, G. (2001). Light reception and signal modulation during photoorientation of flagellate algae. In Comprehensive Series in Photosciences, M. Lebert and D.-P. Hader, eds (Amsterdam, The Netherlands: Elsevier/North Holland), pp. 193-227.
53. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L.L. (2001). Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305, 567-580.
54. Lamb, M.R., Dutcher, S.K., Worley, C.K., and Dieckmann, C.L. (1999). Eyespot assembly mutants in Chlamydomonas reinhardtii. Genetics 153, 721-729.
55. Lichtenthaler, H.K. (1987). Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods Enzymol. 148, 350-382.
56. Linden, L., and Kreimer, G. (1995). Calcium modulates rapid protein phosphorylation/dephosporylation in isolated eyespot apparatuses of the green alga Spermatozopsis similis. Planta 197, 343-351.
57. Link, A.J., Eng, J., Schieltz, D.M., Carmack, E., Mize, G.J., Morris, D.R., Garvik, B.M., and Yates III, J.R. (1999). Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17, 676-682.
58. Majeran, W., Cai, Y., Sun, Q., and van Wijk, K.J. (2005). Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell 17, 3111-3140.
59. Marmagne, A., Rouet, M.-A., Ferro, M., Rolland, N., Alcon, C., Joyard, J., Garin, J., Barbier-Brygoo, H., and Ephritikhine, G. (2004). Identification of new intrinsic proteins in Arabidopsis plasma membrane proteome. Mol. Cell. Proteomics 3, 675-691.
60. Melkonian, M., and Robenek, H. (1984). The eyespot apparatus of green algae: A critical review. Prog. Phycol. Res. 3, 193-268.
61. Mergenhagen, D. (1984). Circadian clock: Genetic characterization of a short period mutant of Chlamydomonas reinhardtii. Eur. J. Cell Biol. 33, 13-18.
62. Mittag, M. (1996). Conserved circadian elements in phylogenetically diverse algae. Proc. Natl. Acad. Sci. USA 93, 14401-14404.
63. Mittag, M., Kiaulehn, S., and Johnson, C.H. (2005). The circadian clock in Chlamydomonas reinhardtii. What is it for? What is it similar to? Plant Physiol. 137, 399-409.
64. Morel-Laurens, N., and Feinleib, M.E. (1983). Photomovement in an "eyeless" mutant of Chlamydomonas. Photochem. Photobiol. 37, 189-194.
65. Nagel, G., Brauner, M., Liewald, J.F., Adeishvili, N., Bamberg, E., and Gottschalk, A. (2005). Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr. Biol. 15, 2279-2284.
66. Nagel, G., Ollig, D., Fuhrmann, M., Kateriya, S., Musti, A.M., Bamberg, E., and Hegemann, P. (2002). Channelrhodopsin-1: A light-gated proton channel in green algae. Science 296, 2395-2398.
67. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., Ollig, D., Hegemann, P., and Bamberg, E. (2003). Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc. Natl. Acad Sci. USA 100, 13940-13945.
68. Nakamura, S., Ogihara, H., Jinbo, K., Tateishi, M., Takahashi, T., Yoshimura, K., Kubota, M., Watanabe, M., and Nakamura, S. (2001). Chlamydomonas reinhardtii Dangeard (Chlamydomonadales, Chlorophyceae) mutant with multiple eyespots. Phycol. Res. 49, 115-121.
69. Neuhoff, V., Phillip, K., Zimmer, H.G., and Mesecke, S. (1979). A simple versatile sensitive and volume-independent method for quantitative protein determination which is independent of other external influences. Hoppe Seylers Z. Physiol. Chem. 360, 1657-1670.
70. Nultsch, W. (1975). Phototaxis and photokinesis. In Primitive Sensory and Communication Systems, M.J. Carlyle, ed (London, New York, San Francisco: Academic Press), pp. 29-90.
71. Palczewski, K., and Saari, J.C. (1997). Activation and inactivation steps in the visual transduction pathway. Curr. Opin. Neurobiol. 7, 500-504.
72. Panda, S., Hogenesch, J.B., and Kay, S.A. (2002). Circadian rhythms from flies to human. Nature 417, 329-335.
73. Pazour, G., Sineshchekov, O.A., and Witman, G.B. (1995). Mutational analysis of the phototransduction pathway of Chlamydomonas reinhardtii. J. Cell Biol. 131, 427-440.
74. Pazour, G.J., Agrin, N., Leszyk, J., and Witman, G.B. (2005). Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 170, 103-113.
75. Peltier, J.B., Emnnuelsson, O., Kalume, D.E., Ytterberg, J., Friso, G., Rudella, A., Liberles, D.A., Soderberg, L., Roepstorff, P., von Heijne, G., and van Wijk, K.J. (2002). Central functions of the luminal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14, 211-236.
76. Porter, M.E., and Sale, W.S. (2000). The 9+2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J. Cell Biol. 151, F37-F42.
77. Pozueta-Romero, J., Rafia, F., Houlné, G., Cheniclet, C., Carde, J.P., Schantz, M.-L., and Schantz, R. (1997). A ubiquitous plant housekeeping gene, PAP, encodes a major protein component of bell pepper chromoplasts. Plant Physiol. 115, 1185-1194.
78. Preuss, F., Fan, J.Y., Kalive, M., Bao, S., Schuenemann, E., Bjes, E.S., and Price, J.L. (2004). Drosophila doubletime mutations which either shorten or lengthen the period of circadian rhythms decrease the protein kinase activity of casein kinase I. Mol. Cell. Biol. 24, 886-898.
79. Rabilloud, T., Carpentier, G., and Tarroux, P. (1988). Improvement and simplificat on of low-background silver staining by using sodium dithionite. Electrophoresis 9, 288-291.
80. Reinders, J., Lewandrowski, U., Moebius, J., Wagner, Y., and Sickmann, A. (2004). Challenges in mass spectrometry-based proteomics. Proteomics 4, 3686-3703.
81. Renninger, S., Backendorf, E., and Kreimer, G. (2001). Subfractionation of eyespot apparatuses from the green alga Spermatozopsis similis: Isolation and characterization of eyespot globules. Planta 213, 51-63.
82. Renninger, S., Dieckmann, C.L., and Kreimer, G. (2006). Towards a protein map of the green algal eyespot: Analysis of eyespot globule-associated proteins. Phycologia 45, 199-212.
83. Reppert, S.M., and Weaver, D.R. (2002). Coordination of circadian timing in mammals. Nature 418, 935-941.
84. Rey, P., Gillet, B., Römer, S., Eymery, F., Massimino, J., Peltier, G., and Kuntz, M. (2000). Over-expression of a pepper plastid-lipid-associated protein in tobacco leads to changes in plastid-ultrastructure and plant development upon stress. Plant J. 21, 483-494.
85. Roberts, D.G.W., Lamb, M.R., and Dieckmann, C.L (2001). Characterization of the eye2 gene required for eyespot assembly in Chlamydomonas reinhardtii. Genetics 158, 1037-1049.
86. Ruch, S., Beyer, P., Ernst, H.G., and Al-Babili, S. (2005). Retinal biosynthesis in Eubacteria: In vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803. Mol. Microbiol. 55, 1015-1024.
87. Sambrook, J., and Russell, D.W. (2001). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
88. Sato, E., Sagami, I., Uchida, T., Sato, A., Kitagawa, T., Igarashi, J., and Shimizu, T. (2004). SOUL in mouse eyes is a new hexameric heme-binding protein with characteristic optical absorption, resonance raman spectral, and heme-binding properties. Biochemistry 43, 14189-14198.
89. Schaller, K., and Uhl, R. (1997). A microspectrophotometric study of the shielding properties of eyespot and cell body in Chlamydomonas. Biophys. J. 73, 1573-1578.
90. Schweighofer, A., Hirt, H., and Meskiene, I. (2004). Plant PP2C phosphatases: Emerging functions in stress signaling. Trends Plant Sci. 9, 236-243.
91. Shimada, H., Koizumi, M., Kuroki, K., Mochizuki, M., Fujimoto, H., Ohta, H., Masuda, T., and Takamiya, K.-I. (2004). ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of a eukaryotic phosphatidylinositol- 4-phosphate 5-kinase. Plant Cell Physiol. 45, 960-967.
92. Sineshchekov, O.A., and Govorunova, E.G. (1999). Rhodopsin-mediated photosensing in green flagellated algae. Trends Plant Sci. 4, 58-63.
93. Sineshchekov, O.A., and Govorunova, E.A. (2001). Electrical events in photomovement of green flagellated algae. In Comprehensive Series in Photosciences, M. Lebert and D.-P. Hader, eds (Amsterdam, The Netherlands: Elsevier/North Holland), pp. 245-280.
94. Sineshchekov, O.A., Jung, K.-H., and Spudich, J.L. (2002). Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 99, 8689-8694.
95. Sizova, I., Fuhrmann, M., and Hegemann, P. (2001). A Streptomyces rimosus aphVIII gene coding for a new type phosphotransferase provides stable antibiotic resistance to Chlamydomonas reinhardtii. Gene 227, 221-229.
96. Suzuki, T., et al. (2003). Archael-type rhodopsins in Chlamydomonas: Model structure and intracellular localization. Biochem. Biophys. Res. Commun. 301, 711-717.
97. Szurmant, H., and Ordal, G.W. (2004). Diversity in Chemotaxis mechanisms among bacteria and archea. Microbiol. Mol. Biol. Rev. 68, 301-319.
98. Takeshima, H., Komazaki, S., Nishi, M., Iino, M., and Kangawa, K. (2000). Junctophilins: A novel family of junctional membrane complex proteins. Mol. Cell 6, 11-22.
99. von Heijne, G. (1992). Membrane protein structure prediction: Hydrophobicity analysis and the 'positive inside' rule. J. Mol. Biol. 225, 487-494.
100. Wagner, V., Fiedler, M., Markert, C., Hippler, M., and Mittag, M. (2004). Functional proteomics of circadian expressed proteins from Chlamydomonas reinhardtii. FEBS Lett. 559, 129-135.
101. Wagner, V., Geßner, G., Heiland, I., Kaminski, M., Hawat, S., Scheffler, K., and Mittag, M. (2006). Analysis of the phosphoproteome of Chlamydomonas reinhardtii provides new insights into various cellular pathways. Eukaryot. Cell 5, 457-468.
102. Walne, P.L., and Arnott, H.J. (1967). The comparative ultrastructure and possible function of eyespots: Euglena granulata and Chlamydomonas eugametos. Planta 77, 325-353.
103. Waltenberger, H., Schneid, C., Grosch, J.O., Bareiß, A., and Mittag, M. (2001). Identification of target mRNAs from C. reinhardtii for the clock-controlled RNA-binding protein Chlamy 1. Mol. Genet. Genomics 265, 180-188.
104. Washburn, M.P., Wolters, D., and Yates III, J.R. (2001). Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 19, 242-247.
105. Webre, D.J., Wolanin, P.M., and Stock, J.B. (2003). Bacterial chemotaxis. Curr. Biol. 13, R47-R49.
106. Wei, Z.M., Laby, R.J., Zumoff, C.H., Bauer, D.W., He, S.Y., Collmer, A., and Beer, S.V. (1992). Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257, 85-88.
107. Witman, G.B. (1993). Chlamydomonas phototaxis. Trends Cell Biol. 3, 403-408.
108. Yamaguchi, K., Prieto, S., Beligni, M.V., Haynes, P.A., McDonald, W.H., Yates III, J.R., and Mayfield, S.P. (2002). Proteomic characterization of the small subunit of Chlamydomonas reinhardtii chloroplast ribosome: Identification of a novel S1 domain-containing protein and unusually large orthologs of bacterial S2, S3, and S5. Plant Cell 14, 2957-2974.
109. Yang, P., and Sale, W.S. (2000). Casein kinase I is anchored on axonemal doublet microtubules and regulates flagellar dynein phosphorylation and activity. J. Biol. Chem. 275, 18905-18912.
110. Zhao, B., Schneid, C., Illiev, D., Schmidt, E.-M., Wagner, V., Wollnik, F., and Mittag, M. (2004). The circadian RNA-binding protein CHLAMY 1 represents a novel type heteromer of RNA recognition motif and lysine homology-containing subunits. Eukaryot. Cell 3, 815-825.
111. Zylka, M.J., and Reppert, S.M. (1999). Discovery of a putative heme-binding protein family (SOUL/HBP) by two-tissue suppression subtractive hybridization and database searches. Brain Res. Mol. Brain Res. 74, 175-181.