The interplay of light and oxygen in the reactive oxygen stress response of chlamydomonas reinhardtii dissected by quantitative mass spectrometry

Molecular and Cellular Proteomics

Volumn 13, Issue 4, 2014, Pages 969-989

  Barth, Johannes ^a   Bergner, Sonja Verena ^a   Jaeger, Daniel ^a   Niehues, Anna ^a   Schulze, Stefan ^a   Scholz, Martin ^a   Fufezan, Christian ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

OXYGEN; REACTIVE OXYGEN METABOLITE;

ARTICLE; BIOINFORMATICS; CHLAMYDOMONAS REINHARDTII; DEFENSE MECHANISM; LIGHT; LIQUID CHROMATOGRAPHY; MARKER GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; STRESS; TANDEM MASS SPECTROMETRY;

ALGAL PROTEINS; CHLAMYDOMONAS REINHARDTII; CHLOROPHYLL; CHROMATOGRAPHY, LIQUID; LIGHT; MITOCHONDRIA; OXIDATIVE STRESS; OXYGEN; PROTEOMICS; REACTIVE OXYGEN SPECIES; TANDEM MASS SPECTROMETRY;

EID: 84898713753     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.032771     Document Type: Article

References (124)

1. Farquhar, J. (2000) Atmospheric Influence of Earth's Earliest Sulfur Cycle. Science 289, 756-758
2. Kirschvink, J. L., Gaidos, E. J., Bertani, L. E., Beukes, N. J., Gutzmer, J., Maepa, L. N., and Steinberger, R. E. (2000) Paleoproterozoic snowball earth: extreme climatic and geochemical global change and its biological consequences. Proc. Natl. Acad. Sci. U.S.A. 97, 1400-1405
3. Kopp, R. E., Kirschvink, J. L., Hilburn, I. A, and Nash, C. Z. (2005) The Paleoproterozoic snowball Earth: a climate disaster triggered by the evolution of oxygenic photosynthesis. Proc. Natl. Acad. Sci. U.S.A. 102, 11131-11136
4. Canfield, D. E., Poulton, S. W., and Narbonne, G. M. (2007) Late-Neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315, 92-95
5. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V. B., Vandepoele, K., Gollery, M., Shulaev, V., and Van Breusegem, F. (2011) ROS signaling: the new wave? Trends Plant Sci. 16, 300-309
6. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M., and Telser, J. (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 39, 44-84
7. Waris, G., and Ahsan, H. (2006) Reactive oxygen species: role in the development of cancer and various chronic conditions. J. Carcinog. 5, 14
8. Andersen, J. K. (2004) Oxidative stress in neurodegeneration: cause or consequence? Nat. Med. 10, S18-S25
9. Diplock, A. T. (1981) Metabolic and Functional Defects in Selenium Deficiency [and Discussion]. Philos. Trans. R. Soc. B Biol. Sci. 294, 105-117
10. Halliwell, B., and Gutteridge, J. (1984) Lipid peroxidation, oxygen radicals, cell damage, and antioxidant therapy. Lancet 4, 1396-1397
11. Gill, S. S., and Tuteja, N. (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909-930
12. Chang, C. C. C., Slesak, I., Jordá, L., Sotnikov, A., Melzer, M., Miszalski, Z., Mullineaux, P. M., Parker, J. E., Karpinska, B., and Karpinski, S. (2009) Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol. 150, 670-683
13. Halliwell, B. (1991). Reactive oxygen species in living systems: source, biochemistry, and role in human disease. Am. J. Med. 91, 14S-22S
14. Rentel, M., Lecourieux, D., Ouaked, F., Usher, S. L., Petersen, L., Okamoto, H., Knight, H., Peck, S. C., Grierson, C. S., Hirt, H., and Knight, M. R. (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427, 858-861
15. op den Camp, R. G. L., Przybyla, D., Ochsenbein, C., Laloi, C., Kim, C., Danon, A., Wagner, D., Hideg, E., Gobel, C., Feussner, I., Nater, M., and Apel, K. (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15, 2320-2332
16. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. (2004) Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498
17. Laloi, C., Stachowiak, M., Pers-Kamczyc, E., Warzych, E., Murgia, I., and Apel, K. (2007) Cross-talk between singlet oxygen-and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 104, 672-677
18. Wagner, D., Przybyla, D., Op den Camp, R., Kim, C., Landgraf, F., Lee, K. P., Wursch, M., Laloi, C., Nater, M., Hideg, E., and Apel, K. (2004) The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana. Science 306, 1183-1185
19. Shao, N., Krieger-Liszkay, A., Schroda, M., and Beck, C. F. (2007) A reporter system for the individual detection of hydrogen peroxide and singlet oxygen: its use for the assay of reactive oxygen species produced in vivo. Plant J. 50, 475-487
20. Meskauskiene, R., Nater, M., Goslings, D., Kessler, F., op den Camp, R., and Apel, K. (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 98, 12826-12831
21. Lee, K. P., Kim, C., Landgraf, F., and Apel, K. (2007) EXECUTER1-and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 104, 10270-10275
22. Falciatore, A., Merendino, L., Barneche, F., Ceol, M., Meskauskiene, R., Apel, K., and Rochaix, J.-D. (2005) The FLP proteins act as regulators of chlorophyll synthesis in response to light and plastid signals in Chlamydomonas. Genes Dev. 19, 176-187
23. Ramel, F., Birtic, S., Ginies, C., Soubigou-Taconnat, L., Triantaphylide s, C., and Havaux, M. (2012) Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. Proc. Natl. Acad. Sci. U.S.A. 109
24. Lundquist, P. K., Poliakov, A., Giacomelli, L., Friso, G., Appel, M., McQuinn, R. P., Krasnoff, S. B., Rowland, E., Ponnala, L., Sun, Q., and van Wijk, K. J. (2013) Loss of plastoglobule kinases ABC1K1 and ABC1K3 causes conditional degreening, modified prenyl-lipids, and recruitment of the jasmonic acid pathway. Plant Cell 25, 1818-1839
25. Schroda, M., Blocker, D., and Beck, C. F. (2000) The HSP70A promoter as a tool for the improved expression of transgenes in Chlamydomonas. Plant J. 21, 121-131
26. Jaeger, D., Barth, J., Niehues, A., and Fufezan, C. (2013) pyGCluster, a novel hierarchical clustering approach. Bioinformatics,
27. Harris, E. (1989) The Chlamydomonas Sourcebook. Harris EH, Stern DB, Witman GB (Eds.) Academic Press
28. Porra, R., Thompson, W., and Kriedemann, P. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophys. Acta 975, 384-394
29. Laemmli, U. K. (1970) Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4. Nature 227, 680-685
30. Naumann, B., Busch, A., Allmer, J., Ostendorf, E., Zeller, M., Kirchhoff, H., and Hippler, M. (2007) Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii. Proteomics 7, 3964-3979
31. Moseley, J. L., Allinger, T., Herzog, S., Hoerth, P., Wehinger, E., Merchant, S., and Hippler, M. (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. EMBO J. 21, 6709-6720
32. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675
33. Horton, P., Ruban, A. V., and Walters, R. G. (1996) Regulation of Light Harvesting in Green Plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 655-684
34. Van Kooten, O., and Snel, J. F. H. (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth. Res. 25, 147-150
35. Wiśniewski, J. R., Zougman, A., Nagaraj, N., and Mann, M. (2009) Universal sample preparation method for proteome analysis. Nat. Methods 6, 359-362
36. Wiśniewski, J. R., Zielinska, D. F., and Mann, M. (2010) Comparison of Ultrafiltration Units for Proteomic and N-Glycoproteomic Analysis by the FASP Method. Anal. Biochem. 410, 307-309
37. Britton, H. T. S., and Robinson, R. A. (1931) CXCVIII.?Universal buffer solutions and the dissociation constant of veronal. J. Chem. Soc., 1456
38. Merchant, S. S., Prochnik, S. E., Vallon, O., Harris, E. H., Karpowicz, S. J., Witman, G. B., Terry, A., Salamov, A., Fritz-Laylin, L. K., Maré chal-Drouard, L., Marshall, W. F., Qu, L.-H., Nelson, D. R., Sanderfoot, A. A., Spalding, M. H., Kapitonov, V. V., Ren, Q., Ferris, P., Lindquist, E., Shapiro, H., Lucas, S. M., Grimwood, J., Schmutz, J., Cardol, P., Cerutti, H., Chanfreau, G., Chen, C.-L., Cognat, V., Croft, M. T., Dent, R., Dutcher, S., Fernández, E., Fukuzawa, H., González-Ballester, D., González-Halphen, D., Hallmann, A., Hanikenne, M., Hippler, M., Inwood, W., Jabbari, K., Kalanon, M., Kuras, R., Lefebvre, P. A., Lemaire, S. D., Lobanov, A. V., Lohr, M., Manuell, A., Meier, I., Mets, L., Mittag, M., Mittelmeier, T., Moroney, J. V., Moseley, J., Napoli, C., Nedelcu, A. M., Niyogi, K., Novoselov, S. V., Paulsen, I. T., Pazour, G., Purton, S., Ral, J.-P., Riano-Pachón, D. M., Riekhof, W., Rymarquis, L., Schroda, M., Stern, D., Umen, J., Willows, R., Wilson, N., Zimmer, S. L., Allmer, J., Balk, J., Bisova, K., Chen, C.-J., Elias, M., Gendler, K., Hauser, C., Lamb, M. R., Ledford, H., Long, J. C., Minagawa, J., Page, M. D., Pan, J., Pootakham, W., Roje, S., Rose, A., Stahlberg, E., Terauchi, A. M., Yang, P., Ball, S., Bowler, C., Dieckmann, C. L., Gladyshev, V. N., Green, P., Jorgensen, R., Mayfield, S., Mueller-Roeber, B., Rajamani, S., Sayre, R. T., Brokstein, P., Dubchak, I., Goodstein, D., Hornick, L., Huang, Y. W., Jhaveri, J., Luo, Y., Martínez, D., Ngau, W. C. A., Otillar, B., Poliakov, A., Porter, A., Szajkowski, L., Werner, G., Zhou, K., Grigoriev, I. V., Rokhsar, D. S., and Grossman, A. R. (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318, 245-250
39. Stanke, M., and Waack, S. (2003) Gene prediction with a hidden Markov model and a new intron submodel. Bioinformatics 19, ii215-ii225
40. Maul, J. E., Lilly, J. W., Cui, L., Claude, W., Miller, W., Harris, E. H., and Stern, D. B. (2002). The Chlamydomonas reinhardtii Plastid Chromosome : Islands of Genes in a Sea of Repeats. 14, 2659-2679
41. Geer, L. Y., Markey, S. P., Kowalak, J. A., Wagner, L., Xu, M., Maynard, D. M., Yang, X., Shi, W., and Bryant, S. H. (2004) Open Mass Spectrometry Search Algorithm. J. Proteome Res. 3, 958-964
42. Craig, R., and Beavis, R. C. (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20, 1466-1467
43. Eng, J. K., 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
44. Specht, M., Kuhlgert, S., Fufezan, C., and Hippler, M. (2011) Proteomics to go: Proteomatic enables the user-friendly creation of versatile MS/MS data evaluation workflows. Bioinformatics 27, 1183-1184
45. Kall, L., Storey, J. D., and Noble, W. S. (2008) Non-parametric estimation of posterior error probabilities associated with peptides identified by tandem mass spectrometry. Bioinformatics 24, i42-8
46. Martens, L., Chambers, M., Sturm, M., Kessner, D., Levander, F., Shofstahl, J., Tang, W. H., Rompp, A., Neumann, S., Pizarro, A. D., Montecchi-Palazzi, L., Tasman, N., Coleman, M., Reisinger, F., Souda, P., Hermjakob, H., Binz, P.-A., and Deutsch, E. W. (2011) mzML-a community standard for mass spectrometry data. Mol. Cell. Proteomics 10, R110.000133
47. Kessner, D., Chambers, M., Burke, R., Agus, D., and Mallick, P. (2008) ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics 24, 2534-2536
48. Bald, T., Barth, J., Niehues, A., Specht, M., Hippler, M., and Fufezan, C. (2012) pymzML-Python module for high-throughput bioinformatics on mass spectrometry data. Bioinformatics 28, 1052-1053
49. Mueller, L. N., Rinner, O., Schmidt, A., Letarte, S., Bodenmiller, B., Brusniak, M.-Y., Vitek, O., Aebersold, R., and Muller, M. (2007) SuperHirn-a novel tool for high resolution LC-MS-based peptide/protein profiling. Proteomics 7, 3470-3480
50. Hoehner, R., Barth, J., Magneschi, L., Jaeger, D., Niehues, A., Bald, T., Grossman, A., Fufezan, C., and Hippler, M. (2013) The metabolic status drives acclimation of iron deficiency responses in Chlamydomonas reinhardtii as revealed by proteomics based hierarchical clustering and reverse genetics. Mol. Cell. Proteomics, 1-59
51. Mullner, D. (2013) fastcluster: Fast Hierarchical, Agglomerative Clustering Routines for R and Python. J. Stat. Softw. 53, 1-18
52. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410
53. Duanmu, D., Casero, D., Dent, R. M., Gallaher, S., Yang, W., Rockwell, N. C., Martin, S. S., Pellegrini, M., Niyogi, K. K., Merchant, S. S., Grossman, A. R., and Lagarias, J. C. (2013) Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival. Proc. Natl. Acad. Sci. U.S.A. 110, 3621-3626
54. Goodstein, D. M., Shu, S., Howson, R., Neupane, R., Hayes, R. D., Fazo, J., Mitros, T., Dirks, W., Hellsten, U., Putnam, N., and Rokhsar, D. S. (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178-D1186
55. Fischer, B. B., Ledford, H. K., Wakao, S., Huang, S. G., Casero, D., Pellegrini, M., Merchant, S. S., Koller, A., Eggen, R. I. L., and Niyogi, K. K. (2012) SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U.S.A., 1-10
56. Ledford, H. K., Chin, B. L., and Niyogi, K. K. (2007) Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii. Eukaryot. Cell 6, 919-930
57. Arabidopsis, T., and Initiative, G. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815
58. Huala, E., Dickerman, A. W., Garcia-Hernandez, M., Weems, D., Reiser, L., LaFond, F., Hanley, D., Kiphart, D., Zhuang, M., Huang, W., Mueller, L. A., Bhattacharyya, D., Bhaya, D., Sobral, B. W., Beavis, W., Meinke, D. W., Town, C. D., Somerville, C., and Rhee, S. Y. (2001) The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant. Nucleic Acids Res. 29, 102-105
59. Barrett, T., Wilhite, S. E., Ledoux, P., Evangelista, C., Kim, I. F., Tomashevsky, M., Marshall, K. A., Phillippy, K. H., Sherman, P. M., Holko, M., Yefanov, A., Lee, H., Zhang, N., Robertson, C. L., Serova, N., Davis, S., and Soboleva, A. (2013) NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res. 41, D991-D995
60. Edgar, R., Domrachev, M., and Lash, A. E. (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210
61. Foyer, C. H., and Shigeoka, S. (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 155, 93-100
62. Peers, G., Truong, T. B., Ostendorf, E., Busch, A., Elrad, D., Grossman, A. R., Hippler, M., and Niyogi, K. K. (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462, 518-521
63. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658
64. Dietz, K.-J. (2011) Peroxiredoxins in plants and cyanobacteria. Antioxid. Redox Signal. 15, 1129-1159
65. Lemaire, S. D., Michelet, L., Zaffagnini, M., Massot, V., and Issakidis-Bourguet, E. (2007) Thioredoxins in chloroplasts. Curr. Genet. 51, 343-365
66. Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G., Clements, J., Heger, A., Holm, L., Sonnhammer, E. L. L., Eddy, S. R., Bateman, A., and Finn, R. D. (2012) The Pfam protein families database. Nucleic Acids Res. 40, D290-301
67. Asada, K. (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391-396
68. Krieger-Liszkay, A., Fufezan, C., and Trebst, A. (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth. Res. 98, 551-564
69. Meurer, J., Plucken, H., Kowallik, K. V., and Westhoff, P. (1998) A nuclearencoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana. EMBO J. 17, 5286-5297
70. Leitner-Dagan, Y., Ovadis, M., Shklarman, E., Elad, Y., Rav David, D., and Vainstein, A. (2006) Expression and functional analyses of the plastid lipid-associated protein CHRC suggest its role in chromoplastogenesis and stress. Plant Physiol. 142, 233-244
71. 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
72. Langenkamper, G., Manac'h, N., Broin, M., Cuiné, S., Becuwe, N., Kuntz, M., and Rey, P. (2001) Accumulation of plastid lipid-associated proteins (fibrillin/CDSP34) upon oxidative stress, ageing and biotic stress in Solanaceae and in response to drought in other species. J. Exp. Bot. 52, 1545-1554
73. Giacomelli, L., Rudella, A., and Van Wijk, K. J. (2006) High Light Response of the Thylakoid Proteome in Arabidopsis Wild Type and the Ascorbate-Deficient Mutant vtc2-2 . A Comparative Proteomics Study 1 [W]. 141, 685-701
74. Lundquist, P. K., Poliakov, A., Bhuiyan, N. H., Zybailov, B., Sun, Q., and van Wijk, K. J. (2012) The functional network of the Arabidopsis plastoglobule proteome based on quantitative proteomics and genomewide coexpression analysis. Plant Physiol. 158, 1172-1192
75. Urzica, E. I., Adler, L. N., Page, M. D., Linster, C. L., Arbing, M. A., Casero, D., Pellegrini, M., Merchant, S. S., and Clarke, S. G. (2012) Impact of oxidative stress on ascorbate biosynthesis in Chlamydomonas via regulation of the VTC2 gene encoding a GDP-L-galactose phosphorylase. J. Biol. Chem. 287, 14234-14245
76. Foyer, C. H., and Noctor, G. (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol. 155, 2-18
77. Ishikawa, T., and Shigeoka, S. (2008) Recent Advances in Ascorbate Biosynthesis and the Physiological Significance of Ascorbate Peroxidase in Photosynthesizing Organisms. Biosci. Biotechnol. Biochem. 72, 1143-1154
78. Buchanan, B. B., Schurmann, P., Wolosiuk, R. A., and Jacquot, J.-P. (2002) The ferredoxin/thioredoxin system: from discovery to molecular structures and beyond. Photosynth. Res. 73, 215-222
79. Kaiser, W. M. (1979) Reversible inhibition of the calvin cycle and activation of oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145, 377-382
80. Mishra, S., Murphy, L. C., Nyomba, B. L. G., and Murphy, L. J. (2005) Prohibitin: a potential target for new therapeutics. Trends Mol. Med. 11, 192-197
81. Nijtmans, L. G., de Jong, L., Artal Sanz, M., Coates, P. J., Berden, J. A., Back, J. W., Muijsers, A. O., van der Spek, H., and Grivell, L. A. (2000) Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO J. 19, 2444-2451
82. Ahn, C. S., Lee, J. H., Reum Hwang, A., Kim, W. T., and Pai, H.-S. (2006) Prohibitin is involved in mitochondrial biogenesis in plants. Plant J. 46, 658-667
83. Alscher, R. G., Erturk, N., and Heath, L. S. (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J. Exp. Bot. 53, 1331-1341
84. Ogren, W. L. (1984) Photorespiration: Pathways, Regulation, and Modification. Annu. Rev. Plant Physiol. 35, 415-442
85. Meskauskiene, R., Wursch, M., Laloi, C., Vidi, P.-A., Coll, N. S., Kessler, F., Baruah, A., Kim, C., and Apel, K. (2009) A mutation in the Arabidopsis mTERF-related plastid protein SOLDAT10 activates retrograde signaling and suppresses (1)O(2)-induced cell death. Plant J. 60, 399-410
86. Wobbe, L., and Nixon, P. J. (2013) The mTERF protein MOC1 terminates mitochondrial DNA transcription in the unicellular green alga Chlamydomonas reinhardtii. Nucleic Acids Res., 1-15
87. Leisinger, U., Rufenacht, K., Fischer, B., Pesaro, M., Spengler, A., Zehnder, A. J., and Eggen, R. I. (2001) The glutathione peroxidase homologous gene from Chlamydomonas reinhardtii is transcriptionally up-regulated by singlet oxygen. Plant Mol. Biol. 46, 395-408
88. Fischer, B. B., Wiesendanger, M., and Eggen, R. I. L. (2006) Growth condition-dependent sensitivity, photodamage and stress response of Chlamydomonas reinhardtii exposed to high light conditions. Plant Cell Physiol. 47, 1135-1145
89. Baruah, A., Simková, K., Apel, K., and Laloi, C. (2009) Arabidopsis mutants reveal multiple singlet oxygen signaling pathways involved in stress response and development. Plant Mol. Biol. 70, 547-563
90. Laloi, C., Przybyla, D., and Apel, K. (2006) A genetic approach towards elucidating the biological activity of different reactive oxygen species in Arabidopsis thaliana. J. Exp. Bot. 57, 1719-1724
91. Fischer, B. B., Krieger-Liszkay, A., and Eggen, R. I. L. (2005) Oxidative stress induced by the photosensitizers neutral red (type I) or rose bengal (type II) in the light causes different molecular responses in Chlamydomonas reinhardtii. Plant Sci. 168, 747-759
92. Bailey, S., Thompson, E., Nixon, P. J., Horton, P., Mullineaux, C. W., Robinson, C., and Mann, N. H. (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J. Biol. Chem. 277, 2006-2011
93. Nixon, P. J., Barker, M., Boehm, M., de Vries, R., and Komenda, J. (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J. Exp. Bot. 56, 357-363
94. Ostersetzer, O., and Adam, Z. (1997) Light-stimulated degradation of an unassembled Rieske FeS protein by a thylakoid-bound protease: the possible role of the FtsH protease. Plant Cell 9, 957-965
95. Sinvany-Villalobo, G., Davydov, O., Ben-Ari, G., Zaltsman, A., Raskind, A., and Adam, Z. (2004) Expression in multigene families. Analysis of chloroplast and mitochondrial proteases. Plant Physiol. 135, 1336-1345
96. Piechota, J., Kolodziejczak, M., Juszczak, I., Sakamoto, W., and Janska, H. (2010) Identification and characterization of high molecular weight complexes formed by matrix AAA proteases and prohibitins in mitochondria of Arabidopsis thaliana. J. Biol. Chem. 285, 12512-12521
97. Barranco-Medina, S., Krell, T., Bernier-Villamor, L., Sevilla, F., Lá zaro, J.-J., and Dietz, K.-J. (2008) Hexameric oligomerization of mitochondrial peroxiredoxin PrxIIF and formation of an ultrahigh affinity complex with its electron donor thioredoxin Trx-o. J. Exp. Bot. 59, 3259-3269
98. Kim, K., and Portis, A. R. (2006) Kinetic analysis of the slow inactivation of Rubisco during catalysis: effects of temperature, O2 and Mg(-). Photosynth. Res. 87, 195-204
99. Kane, H., Wilkin, J., Jr., A. P., and Andrews, T. (1998) Potent Inhibition of Ribulose-Bisphosphate Carboxylase by an Oxidized Impurity in Ribulose-1,5-Bisphosphate. Plant Physiol., 1059-1069
100. Yamano, T., Miura, K., and Fukuzawa, H. (2008) Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol. 147, 340-354
101. Fang, W., Si, Y., Douglass, S., Casero, D., Merchant, S. S., Pellegrini, M., Ladunga, I., Liu, P., and Spalding, M. H. (2012) Transcriptome-wide changes in Chlamydomonas reinhardtii gene expression regulated by carbon dioxide and the CO2-concentrating mechanism regulator CIA5/CCM1. Plant Cell 24, 1876-1893
102. Brueggeman, A. J., Gangadharaiah, D. S., Cserhati, M. F., Casero, D., Weeks, D. P., and Ladunga, I. (2012) Activation of the carbon concentrating mechanism by CO2 deprivation coincides with massive transcriptional restructuring in Chlamydomonas reinhardtii. Plant Cell 24, 1860-1875
103. Magneschi, L., Catalanotti, C., Subramanian, V., Dubini, A., Yang, W., Mus, F., Posewitz, M. C., Seibert, M., Perata, P., and Grossman, A. R. (2012) A mutant in the ADH1 gene of Chlamydomonas reinhardtii elicits metabolic restructuring during anaerobiosis. Plant Physiol. 158, 1293-1305
104. Asada, K. (2000) The water-water cycle as alternative photon and electron sinks. Philos. Trans. R. Soc. Lond. 355, 1419-1431
105. Jordan, D. B., and Ogren, W. L. (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase/oxygenase. Planta 161, 308-313
106. Kubien, D. S., Whitney, S. M., Moore, P. V., and Jesson, L. K. (2008) The biochemistry of Rubisco in Flaveria. J. Exp. Bot. 59, 1767-1777
107. Croft, M. T., Moulin, M., Webb, M. E., and Smith, A. G. (2007) Thiamine biosynthesis in algae is regulated by riboswitches. Proc. Natl. Acad. Sci. U.S.A. 104, 20770-20775
108. Bocobza, S. E., Malitsky, S., Araú jo, W. L., Nunes-Nesi, A., Meir, S., Shapira, M., Fernie, A. R., and Aharoni, A. (2013) Orchestration of thiamin biosynthesis and central metabolism by combined action of the thiamin pyrophosphate riboswitch and the circadian clock in Arabidopsis. Plant Cell 25, 288-307
109. Goyer, A. (2010) Thiamine in plants: aspects of its metabolism and functions. Phytochemistry 71, 1615-1624
110. Formighieri, C., Ceol, M., Bonente, G., Rochaix, J.-D., and Bassi, R. (2012) Retrograde signaling and photoprotection in a gun4 mutant of Chlamydomonas reinhardtii. Mol. Plant 5, 1242-1262
111. Beale, S. I., and Welnsteln, J. (1990) Tetrapyrrole metabolism in photosynthetic organisms. In Biosynthesis of Heme and Chlorophyll Dailey H. A. (Ed.) New York: McGraw-Hill Publishing Co
112. Susek, R. E., Ausubel, F. M., and Chory, J. (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74, 787-799
113. Strand, A., Asami, T., Alonso, J., Ecker, J. R., and Chory, J. (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421, 79-83
114. Duanmu, D., Casero, D., Dent, R. M., Gallaher, S., Yang, W., Rockwell, N. C., Martin, S. S., Pellegrini, M., Niyogi, K. K., Merchant, S. S., Grossman, A. R., and Lagarias, J. C. (2013) Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival. Proc. Natl. Acad. Sci. U.S.A. 110, 3621-3626
115. Saini, G., Meskauskiene, R., Pijacka, W., Roszak, P., Sjogren, L. L. E., Clarke, A. K., Straus, M., and Apel, K. (2011) "Happy on Norflurazon" (Hon) Mutations Implicate Perturbance of Plastid Homeostasis With Activating Stress Acclimatization and Changing Nuclear Gene Expression in Norflurazon-Treated Seedlings. Plant J. 65, 690-702
116. Alboresi, A., Ballottari, M., Hienerwadel, R., Giacometti, G. M., and Morosinotto, T. (2009) Antenna complexes protect Photosystem I from photoinhibition. BMC Plant Biol. 9, 71
117. Morosinotto, T., Caffarri, S., Dall'Osto, L., and Bassi, R. (2003) Mechanistic aspects of the xanthophyll dynamics in higher plant thylakoids. Physiol. Plant. 119, 347-354
118. Gibasiewicz, K., Szrajner, A., Ihalainen, J. A., Germano, M., Dekker, J. P., and van Grondelle, R. (2005) Characterization of low-energy chlorophylls in the PSI-LHCI supercomplex from Chlamydomonas reinhardtii. A site-selective fluorescence study. J. Phys. Chem. B 109, 21180-21186
119. Naumann, B., Stauber, E. J., Busch, A., Sommer, F., and 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, 20431-20441
120. Sonoike, K. (1996) Photoinhibition of Photosystem I: Its Physiological Significance in the Chilling Sensitivity of Plants. Plant Cell Physiol. 37, 239-247
121. Boudreau, E., Takahashi, Y., Lemieux, C., Turmel, M., and Rochaix, J. D. (1997) The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 16, 6095-6104
122. Xu, X. M., and Møller, S. G. (2004) AtNAP7 is a plastidic SufC-like ATPbinding cassette/ATPase essential for Arabidopsis embryogenesis. Proc. Natl. Acad. Sci. U.S.A. 101, 9143-9148
123. Holt, N. E., Zigmantas, D., Valkunas, L., Li, X.-P., Niyogi, K. K., and Fleming, G. R. (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307, 433-436
124. Telfer, A. (2002). What is beta-carotene doing in the photosystem II reaction centre? Philos. Trans. R. Soc. Lond. B. Biol. Sci. 357, 1431-1439; discussion 1439-40:1469-70