The phosphoproteome of a Chlamydomonas reinhardtii eyespot fraction includes key proteins of the light signaling pathway

Plant Physiology

Volumn 146, Issue 2, 2008, Pages 772-788

  Wagner, Volker ^a   Ullmann, Katharina ^b   Mollwo, Anne ^b   Kaminski, Marc ^a   Mittag, Maria ^a   Kreimer, Georg ^b  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

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

EID: 38949093001     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.107.109645     Document Type: Article

References (78)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402
2. 2 adapted cells of Chlamydomonas reinhardtii. DNA Res 7: 305-307
3. Asamizu E, Nakamura Y, Sato S, Fukuzawa H, Tabata S (1999) A large scale structural analysis of cDNAs in a unicellular green alga, Chlamydomonas reinhardtii. I. Generation of 3433 non-redundant expressed sequence tags. DNA Res 6: 369-373
4. Asamizu E, Nakamura Y, Miura K, Fukuzawa H, Fujiwara S, Hirono M, Iwamoto K, Matsuda Y, Minagawa J, Shimogawara K, et al (2004) Establishment of publicly available cDNA material and information resource of Chlamydomonas reinhardtii (Chlorophyta) to facilitate gene function analysis. Phycologia 43: 722-726
5. Bi A, Cui J, Ma YP, Olshevskaya E, Pu M, Dizhoor AM, Pan ZH (2006) Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration. Neuron 50: 23-33
6. Blom N, Gammeltoft S, Brunak S (1999) Sequence- and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294: 1351-1362
7. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268
8. Bruce VG (1970) The biological clock in Chlamydomonas reinhardtii. J Protozool 17: 328-334
9. 2+-modulated heterotrimeric GTPases in the eyespot apparatus of a flagellate green alga. Plant Cell 10: 91-103
10. DeBruyne JP, Weaver DR, Reppert SM (2007) CLOCK and NPAS2 have overlapping roles in the suprachiasmatic circadian clock. Nat Neurosci 10: 543-545
11. Deininger W, Kröger P, Hegemann U, Lottspeich F, Hegemann P (1995) Chlamyrhodopsin represents a new type of sensory photoreceptors. EMBO J 14: 5849-5858
12. Dieckmann CL (2003) Eyespot placement and assembly in the green alga Chlamydomonas. Bioessays 25: 410-416
13. Eng J, McCormack AL, Yates JR (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
14. Erdjument-Bromage H, Lui M, Lacomis L, Grewal A, Annan RS, McNulty DE, Carr SA, Tempst P (1998) Examination of micro-tip reversed-phase liquid chromatographic extraction of peptide pools for mass spectrometric analysis. J Chromatogr A 826: 167-181
15. Fleischmann MM, Ravanel S, Delosme R, Olive J, Zito F, Wollman FA, Rochaix JD (1999) Isolation and characterization of photoautotrophic mutants of Chlamydomonas reinhardtii deficient in state transition. J Biol Chem 274: 30987-30994
16. Fuhrmann M, Stahlberg A, Govorunova E, Rank S, 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
17. Gehring W (2004) Historical perspective on the development and evolution of eyes and photoreceptors. Int J Dev Biol 48: 707-717
18. Govorunova EG, Jung K-H, Sineshchekov OA, Spudich JL (2004) Chlamydomonas sensory rhodopsins A and B: cellular content and role in photophobic responses. Biophys J 86: 2342-2349
19. Gruhler A, Olsen JV, Mohammed S, Mortensen P, Gaergeman NJ, Mann M, Jensen ON (2005) Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol Cell Proteomics 4: 310-327
20. Harz H, Hegemann P (1991) Rhodopsin-regulated calcium currents in Chlamydomonas. Nature 351: 489-491
21. Hofmann K, Stoffel W (1993) TMbase - a database of membrane spanning proteins segments. Biol Chem Hoppe Seyler 374: 166
22. Holland EM, Braun FJ, Nonnengäßer C, Harz H, Hegemann P (1996) The nature of rhodopsin triggered photocurrents in Chlamydomonas. I. Kinetics and influence of divalent cations. Biophys J 70: 924-931
23. Hubbard MJ, Cohen P (1993) On target with a new mechanism fort he regulation of protein phosphorylation. Trends Biochem Sci 18: 172-177
24. Immenschuh S, Iwahara S, Schwennen B (2002) Induction of heme-binding protein23/peroxiredoxin I gene expression by okadaic acid in cultured rat hepatocytes. DNA Cell Biol 21: 347-354
25. Kamps MP, Sefton BM (1989) Acid and base hydrolysis of phosphoproteins bound to immobilon facilitates analysis of phosphoamino acids in gel-fractionated proteins. Anal Biochem 176: 22-27
26. Kateriya S, Nagel G, Bamberg E, Hegemann P (2004) "Vision" in single-celled algae. News Physiol Sci 19: 133-137
27. Keller LC, Romijn EP, Zamora I, Yates JR III, Marshall WF (2005) Proteomic analysis of isolated Chlamydomonas centrioles reveals orthologs of ciliary-disease genes. Curr Biol 15: 1090-1098
28. Kennedy MJ, Lee KA, Niemi GA, Craven KB, Garwin GG, Saari JC, Hurley JB (2001) Multiple phosphorylation of rhodopsin and the in vivo chemistry underlying rod photoreceptor dark adaptation. Neuron 31: 87-101
29. Kreimer G (2001) Light reception and signal modulation during photoorientation of flagellate algae. In M Lebert, D-P Häder, eds, Comprehensive Series in Photosciences. Elsevier/North Holland, Amsterdam, pp 193-227
30. Kreimer G, Brohsonn U, 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
31. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580
32. Krupa A, Preethi G, Srinivasan N (2004) Structural modes of stabilization of permissive phosphorylation sites in protein kinases: distinct strategies in Ser/Thr and Tyr kinases. J Mol Biol 339: 1025-1039
33. Lee KA, Craven KB, Niemi GA, Hurley JB (2002) Mass spectrometric analysis of the kinetics of in vivo rhodopsin phosphorylation. Protein Sci 11: 862-874
34. Linden L, Kreimer G (1995) Calcium modulates rapid protein phosphorylation/dephosphorylation in isolated eyespot apparatuses of the green alga Spermatozopsis similis. Planta 197: 343-351
35. Link AJ, Eng J, Schieltz DM, Carmack E, Mize GJ, Morris DR, Garvik BM, Yates JR III (1999) Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol 17: 676-682
36. Lohr M, Im C-S, Grossman AR (2005) Genome-based examination of chlorophyll and carotenoid biosynthesis in Chlamydomonas reinhardtii. Plant Physiol 138: 490-515
37. Maeda T, Imanishi Y, Palczewski K (2003) Rhodopsin phosphorylation: 30 years later. Prog Retin Eye Res 22: 417-434
38. Mann M, Ong SE, Grønborg M, Steen H, Jensen ON, Pandey A (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol 20: 261-268
39. Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32: 327-331
40. Mecklenburg KL (2007) Drosophila retinophilin contains MORN repeats and is conserved in humans. Mol Genet Genomics 277: 481-489
41. Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, et al (2007) The evolution of key animal and plant functions is revealed by analysis of the Chlamydomonas genome. Science 318: 245-251
42. Mittag M, Kiaulehn S, Johnson CH (2005) The circadian clock in Chlamydomonas reinhardtii. What is it for? What is it similar to? Plant Physiol 137: 399-409
43. Morel-Laurens N (1987) Calcium control of phototactic orientation in Chlamydomonas reinhardtii: sign and strength of response. Photochem Photobiol 45: 119-128
44. Nagel G, Brauner M, Liewald JF, Adeishvili N, Bamberg E, Gottschalk A (2005a) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15: 2279-2284
45. Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM, Bamberg E, Hegemann P (2002) Channelrhodopsin-1: a light-gated proton channel in green algae. Science 296: 2395-2398
46. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci USA 100: 13940-13945
47. Nagel G, Szellas T, Kateriya S, Adeishvili N, Hegemann P, Bamberg E (2005b) Channelrhodopsins: directly light-gated cation channels. Biochem Soc Trans 33: 863-866
48. Nielsen PA, Olsen JV, Podtelejnikov AV, Andersen JR, Mann M, Wisniewski JR (2005) Proteomic mapping of brain plasma membrane proteins. Mol Cell Proteomics 4: 402-408
49. Nühse TS, Stensballe A, Jensen ON, Peck SC (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16: 2394-2405
50. Ohguro H, Yoshida N, Shindou H, Crabb JW, Palczewski K, Tsuda M (1998) Identification of a single phosphorylation site within octopus rhodopsin. Photochem Photobiol 68: 824-828
51. Ouelhadj A, Kaminski M, Mittag M, Humbeck K (2007) Receptor-like protein kinase HvLysMR1 of barley (Hordeum vulgare L.) is induced during leaf senescence and heavy metal stress. J Exp Bot 58: 1381-1396
52. Pazour G, Sineshchekov OA, Witman GB (1995) Mutational analysis of the phototransduction pathway of Chlamydomonas reinhardtii. J Cell Biol 131: 427-440
53. Pazour GJ, Agrin N, Leszyk J, Witman GB (2005) Proteomic analysis of a eukaryotic cilium. J Cell Biol 170: 103-113
54. Reinders J, Sickmann A (2005) State-of-the-art in phosphoproteomics. Proteomics 5: 4052-4061
55. Roberts DGW, Lamb MR, Dieckmann CL (2001) Characterization of the eye2 gene required for eyespot assembly in Chlamydomonas reinhardtii. Genetics 158: 1037-1049
56. Rudrabhatla P, Reddy MM, Rajasekharan R (2006) Genome-wide analysis and experimentation of plant serine/threonine/tyrosine-specific protein kinases. Plant Mol Biol 60: 293-319
57. Sasakura Y, Kanda K, Yoshimura-Suzuki T, Matsui T, Eukuzono S, Shimizu T (2005) Investigation of the relationship between protein-protein interaction and catalytic activity of a heme-regulated phosphodiesterase from Escherichia coli (Ec DOS) by protein microarray. Biochemistry 44: 9598-9605
58. Sato E, Sagami I, Uchida T, Sato A, Kitagawa T, Igarashi J, 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
59. 2+-modulated protein kinases of a plasma membrane-enriched fraction and isolated eyespot apparatuses of Spermatozopsis similis (Chlorophyceae). Eur J Phycol 30: 319-330
60. Schmidt JA, Eckert R (1976) Calcium couples flagellar reversal to photostimulation in Chlamydomonas reinhardtii. Nature 262: 713-715
61. Schmidt M, Geßner G, Luff M, Heiland I, Wagner V, Kaminski M, Geimer S, Eitzinger N, Reißenweber T, Voytsekh O, et al (2006) Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into its components and tactic movements. Plant Cell 18: 1908-1930
62. Schmidt M, Luff M, Mollwo A, Kaminski M, Mittag M, Kreimer G (2007) Evidence for a specialized localization of the chloroplast ATP-synthase subunits alpha, beta, and gamma in the eyespot apparatus of Chlamydomonas reinhardtii (Chlorophyceae). J Phycol 43: 284-294
63. Schweighofer A, Hirt H, Meskiene I (2004) Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci 9: 236-243
64. Shimada H, Koizumi M, Kuroki K, Mochizuki M, Fujimoto H, Ohta H, Masuda T, 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
65. Shu H, Chen S, Bi Q, Mumby M, Brekken DL (2004) Identification of phosphoproteins and their phosphorylation sites in the WEHI-231 B lymphoma cell line. Mol Cell Proteomics 3: 279-286
66. Shukolyukov SA (1999) Key reactions of visual cycle in vertebrates and invertebrates: activation and regeneration of rhodopsin. J Evol Biochem Physiol 35: 579-595
67. Sineshchekov OA, Govorunova EA (2001) Electrical events in photomovement of green flagellated algae. In M Lebert, D-P Häder, eds, Comprehensive Series in Photosciences. Elsevier/North Holland, Amsterdam, pp 245-280
68. Sineshchekov OA, Jung K-H, Spudich JL (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 99: 8689-8694
69. Stauber EJ, Fink A, Markert C, Kruse O, Johanningmeier U, Hippler M (2003) Proteomics of Chlamydomonas reinhardtii light-harvesting proteins. Eukaryot Cell 2: 978-994
70. Suzuki T, Yamasaki K, Fujita S, Oda K, Iseki M, Yoshida K, Watanabe M, Daiyasu H, Toh H, Asamizu E, et al (2003) Archael-type rhodopsins in Chlamydomonas: model structure and intracellular localization. Biochem Biophys Res Commun 301: 711-717
71. Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K (2000) Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 6: 11-22
72. Turkina MV, Blanco-Rivero A, Vainonen JP, Vener AV, Villarejo A (2006a) CO2 limitation induces specific redox-dependent protein phosphorylation in Chlamydomonas reinhardtii. Proteomics 6: 2693-2704
73. Turkina MV, Kargul J, Blanco-Rivero A, Villarejo A, Barber J, Vener AV (2006b) Environmentally modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii. Mol Cell Proteomics 5: 1412-1425
74. Vener AV, Harms A, Sussman MR, Vierstra RD (2001) Mass spectrometric resolution of reversible protein phosphorylation in photosynthetic membranes of Arabidopsis thaliana. J Biol Chem 276: 6959-6966
75. von Heijne G (1992) Membrane protein structure prediction: hydrophobicity analysis and the 'positive inside' rule. J Mol Biol 225: 487-494
76. Wagner V, Geßner G, Heiland I, Kaminski M, Hawat S, Scheffler K, Mittag M (2006) Analysis of the phosphoproteome of Chlamydomonas reinhardtii provides new insights into various cellular pathways. Eukaryot Cell 5: 457-468
77. Witman GB (1993) Chlamydomonas phototaxis. Trends Cell Biol 3: 403-408
78. Zylka MJ, Reppert SM (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