A nucleus-encoded chloroplast phosphoprotein governs expression of the photosystem i subunit PsaC in chlamydomonas reinhardtii

Plant Cell

Volumn 28, Issue 5, 2016, Pages 1182-1199

  Douchi, Damien ^a   Qu, Yujiao ^b   Longoni, Paolo ^a   Legendre Lefebvre, Linnka ^a   Johnson, Xenie ^c,d,e,f   Schmitz Linneweber, Christian ^b   Goldschmidt Clermont, Michel ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b HUMBOLDT UNIVERSITY   (Germany)

^c National de la Recherche Scientifique Université Pierre et Marie Curie   (France)

^d IRFM   (France)

^e CNRS   (France)

^f AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHOTOSYSTEM I; PROTEIN BINDING;

CELL NUCLEUS; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM I;

CELL NUCLEUS; CHLAMYDOMONAS REINHARDTII; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PROTEIN BINDING;

EID: 84973598768     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.15.00725     Document Type: Article

References (101)

1. Baginsky, S., and Gruissem, W. (2004). Chloroplast proteomics: potentials and challenges. J. Exp. Bot. 55: 1213-1220.
2. Bai, Y., Auperin, T. C., Chou, C. Y., Chang, G. G., Manley, J. L., and Tong, L. (2007). Crystal structure of murine CstF-77: dimeric association and implications for polyadenylation of mRNA precursors. Mol. Cell 25: 863-875.
3. Barkan, A. (2011). Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol. 155: 1520-1532.
4. Barkan, A., Rojas, M., Fujii, S., Yap, A., Chong, Y. S., Bond, C. S., and Small, I. (2012). A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet. 8: e1002910.
5. Barkan, A., and Small, I. (2014). Pentatricopeptide repeat proteins in plants. Annu. Rev. Plant Biol. 65: 415-442.
6. Bayer, R. G., Stael, S., Rocha, A. G., Mair, A., Vothknecht, U. C., and Teige, M. (2012). Chloroplast-localized protein kinases: a step forward towards a complete inventory. J. Exp. Bot. 63: 1713-1723.
7. Berthold, P., Schmitt, R., and Mages, W. (2002). An engineered Streptomyces hygroscopicus aph 7" gene mediates dominant resistance against hygromycin B in Chlamydomonas reinhardtii. Protist 153: 401-412.
8. Bonardi, V., Pesaresi, P., Becker, T., Schleiff, E., Wagner, R., Pfannschmidt, T., Jahns, P., and Leister, D. (2005). Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437: 1179-1182.
9. 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.
10. Boulouis, A., Raynaud, C., Bujaldon, S., Aznar, A., Wollman, F. A., and Choquet, Y. (2011). The nucleus-encoded trans-acting factor MCA1 plays a critical role in the regulation of cytochrome f synthesis in Chlamydomonas chloroplasts. Plant Cell 23: 333-349.
11. Busch, A., Rimbauld, B., Naumann, B., Rensch, S., and Hippler, M. (2008). Ferritin is required for rapid remodeling of the photosynthetic apparatus and minimizes photo-oxidative stress in response to iron availability in Chlamydomonas reinhardtii. Plant J. 55: 201-211.
12. Choquet, Y., Goldschmidt-Clermont, M., Girard-Bascou, J., Kück, U., Bennoun, P., and Rochaix, J. D. (1988). Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell 52: 903-913.
13. Choquet, Y., and Vallon, O. (2000). Synthesis, assembly and degradation of thylakoid membrane proteins. Biochimie 82: 615-634.
14. Dauvillée, D., Stampacchia, O., Girard-Bascou, J., and Rochaix, J. D. (2003). Tab2 is a novel conserved RNA binding protein required for translation of the chloroplast psaB mRNA. EMBO J. 22: 6378-6388.
15. Depège, N., Bellafiore, S., and Rochaix, J. D. (2003). Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299: 1572-1575.
16. Felder, S., Meierhoff, K., Sane, A. P., Meurer, J., Driemel, C., Plücken, H., Klaff, P., Stein, B., Bechtold, N., and Westhoff, P. (2001). The nucleus-encoded HCF107 gene of Arabidopsis provides a link between intercistronic RNA processing and the accumulation of translation-competent psbH transcripts in chloroplasts. Plant Cell 13: 2127-2141.
17. Fisk, D. G., Walker, M. B., and Barkan, A. (1999). Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression. EMBO J. 18: 2621-2630.
18. Fristedt, R., Willig, A., Granath, P., Crèvecoeur, M., Rochaix, J. D., and Vener, A. V. (2009). Phosphorylation of photosystem II controls functional macroscopic folding of photosynthetic membranes in Arabidopsis. Plant Cell 21: 3950-3964.
19. Gibson, D. G., Young, L., Chuang, R. Y., Venter, J. C., Hutchison III, C. A., and Smith, H. O. (2009). Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6: 343-345.
20. Glaesener, A. G., Merchant, S. S., and Blaby-Haas, C. E. (2013). Iron economy in Chlamydomonas reinhardtii. Front. Plant Sci. 4: 337.
21. Goldschmidt-Clermont, M., Choquet, Y., Girard-Bascou, J., Michel, F., Schirmer-Rahire, M., and Rochaix, J. D. (1991). A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell 65: 135-143.
22. Goldschmidt-Clermont, M., Girard-Bascou, J., Choquet, Y., and Rochaix, J. D. (1990). Trans-splicing mutants of Chlamydomonas reinhardtii. Mol. Gen. Genet. 223: 417-425.
23. Gray, M. W., Lukes, J., Archibald, J. M., Keeling, P. J., and Doolittle, W. F. (2010). Cell biology. Irremediable complexity? Science 330: 920-921.
24. Guertin, M., and Bellemare, G. (1979). Synthesis of chloroplast ribonucleic acid in Chlamydomonas reinhardtii toluene-treated cells. Eur. J. Biochem. 96: 125-129.
25. Hammani, K., Bonnard, G., Bouchoucha, A., Gobert, A., Pinker, F., Salinas, T., and Giegé, P. (2014). Helical repeats modular proteins are major players for organelle gene expression. Biochimie 100: 141-150.
26. Hammani, K., Cook, W. B., and Barkan, A. (2012). RNA binding and RNA remodeling activities of the half-a-tetratricopeptide (HAT) protein HCF107 underlie its effects on gene expression. Proc. Natl. Acad. Sci. USA 109: 5651-5656.
27. Höhner, 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 12: 2774-2790.
28. Hosler, J. P., Wurtz, E. A., Harris, E. H., Gillham, N. W., and Boynton, J. E. (1989). Relationship between gene dosage and gene expression in the chloroplast of Chlamydomonas reinhardtii. Plant Physiol. 91: 648-655.
29. Houille-Vernes, L., Rappaport, F., Wollman, F. A., Alric, J., and Johnson, X. (2011). Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc. Natl. Acad. Sci. USA 108: 20820-20825.
30. Ibrahim, F., Rymarquis, L. A., Kim, E. J., Becker, J., Balassa, E., Green, P. J., and Cerutti, H. (2010). Uridylation of mature miRNAs and siRNAs by the MUT68 nucleotidyltransferase promotes their degradation in Chlamydomonas. Proc. Natl. Acad. Sci. USA 107: 3906-3911.
31. Johnson, X., Wostrikoff, K., Finazzi, G., Kuras, R., Schwarz, C., Bujaldon, S., Nickelsen, J., Stern, D. B., Wollman, F. A., and Vallon, O. (2010). MRL1, a conserved pentatricopeptide repeat protein, is required for stabilization of rbcL mRNA in Chlamydomonas and Arabidopsis. Plant Cell 22: 234-248.
32. Kanekatsu, M., Ezumi, A., Nakamura, T., and Ohtsuki, K. (1995). Chloroplast ribonucleoproteins (RNPs) as phosphate acceptors for casein kinase II: purification by ssDNA-cellulose column chromatography. Plant Cell Physiol. 36: 1649-1656.
33. Kanekatsu, M., Saito, H., Motohashi, K., and Hisabori, T. (1998). The beta subunit of chloroplast ATP synthase (CF0CF1-ATPase) is phosphorylated by casein kinase II. Biochem. Mol. Biol. Int. 46: 99-105.
34. Ke, J., Chen, R. Z., Ban, T., Zhou, X. E., Gu, X., Tan, M. H., Chen, C., Kang, Y., Brunzelle, J. S., Zhu, J. K., Melcher, K., and Xu, H. E. (2013). Structural basis for RNA recognition by a dimeric PPRprotein complex. Nat. Struct. Mol. Biol. 20: 1377-1382.
35. Kinoshita, E., and Kinoshita-Kikuta, E. (2011). Improved Phos-tag SDS-PAGE under neutral pH conditions for advanced protein phosphorylation profiling. Proteomics 11: 319-323.
36. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K., and Koike, T. (2006). Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 5: 749-757.
37. Klinkert, B., Schwarz, C., Pohlmann, S., Pierre, Y., Girard-Bascou, J., and Nickelsen, J. (2005). Relationship between mRNA levels and protein accumulation in a chloroplast promoter-mutant of Chlamydomonas reinhardtii. Mol. Genet. Genomics 274: 637-643.
38. Kropat, J., Hong-Hermesdorf, A., Casero, D., Ent, P., Castruita, M., Pellegrini, M., Merchant, S. S., and Malasarn, D. (2011). A revised mineral nutrient supplement increases biomass and growth rate in Chlamydomonas reinhardtii. Plant J. 66: 770-780.
39. Kuchka, M. R., Goldschmidt-Clermont, M., van Dillewijn, J., and Rochaix, J. D. (1989). Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell 58: 869-876.
40. Kück, U., Choquet, Y., Schneider, M., Dron, M., and Bennoun, P. (1987). Structural and transcription analysis of two homologous genes for the P700 chlorophyll a-apoproteins in Chlamydomonas reinhardii: evidence for in vivo trans-splicing. EMBO J. 6: 2185-2195.
41. Kupsch, C., Ruwe, H., Gusewski, S., Tillich, M., Small, I., and Schmitz-Linneweber, C. (2012). Arabidopsis chloroplast RNA binding proteins CP31A and CP29A associate with large transcript pools and confer cold stress tolerance by influencing multiple chloroplast RNA processing steps. Plant Cell 24: 4266-4280.
42. Lefebvre-Legendre, L., Choquet, Y., Kuras, R., Loubery, S., Douchi, D., and Goldschmidt-Clermont, M. (2015). A nucleusencoded chloroplast protein regulated by iron availability governs expression of the photosystem I subunit PsaA in Chlamydomonas reinhardtii. Plant Physiol. 167: 1527-1540.
43. Lefebvre-Legendre, L., Merendino, L., Rivier, C., and Goldschmidt-Clermont, M. (2014). On the complexity of chloroplast RNA metabolism: psaA trans-splicing can be bypassed in Chlamydomonas. Mol. Biol. Evol. 31: 2697-2707.
44. Lefebvre, P. A., and Silflow, C. D. (1999). Chlamydomonas: the cell and its genomes. Genetics 151: 9-14.
45. Lemeille, S., and Rochaix, J. D. (2010). State transitions at the crossroad of thylakoid signalling pathways. Photosynth. Res. 106: 33-46.
46. Liere, K., and Link, G. (1997). Chloroplast endoribonuclease p54 involved in RNA 39-end processing is regulated by phosphorylation and redox state. Nucleic Acids Res. 25: 2403-2408.
47. Lisitsky, I., and Schuster, G. (1995). Phosphorylation of a chloroplast RNA-binding protein changes its affinity to RNA. Nucleic Acids Res. 23: 2506-2511.
48. Lohrig, K., Müller, B., Davydova, J., Leister, D., and Wolters, D. A. (2009). Phosphorylation site mapping of soluble proteins: bioinformatical filtering reveals potential plastidic phosphoproteins in Arabidopsis thaliana. Planta 229: 1123-1134.
49. Loiselay, C., Gumpel, N. J., Girard-Bascou, J., Watson, A. T., Purton, S., Wollman, F. A., and Choquet, Y. (2008). Molecular identification and function of cis-and trans-acting determinants for petA transcript stability in Chlamydomonas reinhardtii chloroplasts. Mol. Cell. Biol. 28: 5529-5542.
50. Loizeau, K., Qu, Y., Depp, S., Fiechter, V., Ruwe, H., Lefebvre-Legendre, L., Schmitz-Linneweber, C., and Goldschmidt-Clermont, M. (2014). Small RNAs reveal two target sites of the RNA-maturation factor Mbb1 in the chloroplast of Chlamydomonas. Nucleic Acids Res. 42: 3286-3297.
51. Longoni, P., Douchi, D., Cariti, F., Fucile, G., and Goldschmidt-Clermont, M. (2015). Phosphorylation of the light-harvesting complex II isoform Lhcb2 is central to state transitions. Plant Physiol. 169: 2874-2883.
52. Lukeš, J., Archibald, J. M., Keeling, P. J., Doolittle, W. F., and Gray, M. W. (2011). How a neutral evolutionary ratchet can build cellular complexity. IUBMB Life 63: 528-537.
53. Maier, U. G., Bozarth, A., Funk, H. T., Zauner, S., Rensing, S. A., Schmitz-Linneweber, C., Börner, T., and Tillich, M. (2008). Complex chloroplast RNA metabolism: just debugging the genetic programme? BMC Biol. 6: 36.
54. Matsuo, T., Onai, K., Okamoto, K., Minagawa, J., and Ishiura, M. (2006). Real-time monitoring of chloroplast gene expression by a luciferase reporter: evidence for nuclear regulation of chloroplast circadian period. Mol. Cell. Biol. 26: 863-870.
55. Michelet, L., Lefebvre-Legendre, L., Burr, S. E., Rochaix, J. D., and Goldschmidt-Clermont, M. (2011). Enhanced chloroplast transgene expression in a nuclear mutant of Chlamydomonas. Plant Biotechnol. J. 9: 565-574.
56. Monod, C., Goldschmidt-Clermont, M., and Rochaix, J. D. (1992). Accumulation of chloroplast psbB RNA requires a nuclear factor in Chlamydomonas reinhardtii. Mol. Gen. Genet. 231: 449-459.
57. 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.
58. 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.
59. Naver, H., Boudreau, E., and Rochaix, J. D. (2001). Functional studies of Ycf3: its role in assembly of photosystem I and interactions with some of its subunits. Plant Cell 13: 2731-2745.
60. Nickelsen, J., Fleischmann, M., Boudreau, E., Rahire, M., and Rochaix, J. D. (1999). Identification of cis-acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas. Plant Cell 11: 957-970.
61. Ozawa, S., Nield, J., Terao, A., Stauber, E. J., Hippler, M., Koike, H., Rochaix, J. D., and Takahashi, Y. (2009). Biochemical and structural studies of the large Ycf4-photosystem I assembly complex of the green alga Chlamydomonas reinhardtii. Plant Cell 21: 2424-2442.
62. Pfalz, J., Bayraktar, O. A., Prikryl, J., and Barkan, A. (2009). Sitespecific binding of a PPR protein defines and stabilizes 59 and 39 mRNA termini in chloroplasts. EMBO J. 28: 2042-2052.
63. Preker, P. J., and Keller, W. (1998). The HAT helix, a repetitive motif implicated in RNA processing. Trends Biochem. Sci. 23: 15-16.
64. Prikryl, J., Rojas, M., Schuster, G., and Barkan, A. (2011). Mechanism of RNA stabilization and translational activation by a pentatricopeptide repeat protein. Proc. Natl. Acad. Sci. USA 108: 415-420.
65. Puthiyaveetil, S., Kavanagh, T. A., Cain, P., Sullivan, J. A., Newell, C. A., Gray, J. C., Robinson, C., van der Giezen, M., Rogers, M. B., and Allen, J. F. (2008). The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc. Natl. Acad. Sci. USA 105: 10061-10066.
66. Rahire, M., Laroche, F., Cerutti, L., and Rochaix, J. D. (2012). Identification of an OPR protein involved in the translation initiation of the PsaB subunit of photosystem I. Plant J. 72: 652-661.
67. Ramundo, S., Rahire, M., Schaad, O., and Rochaix, J. D. (2013). Repression of essential chloroplast genes reveals new signaling pathways and regulatory feedback loops in Chlamydomonas. Plant Cell 25: 167-186.
68. Raynaud, C., Loiselay, C., Wostrikoff, K., Kuras, R., Girard-Bascou, J., Wollman, F. A., and Choquet, Y. (2007). Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast. Proc. Natl. Acad. Sci. USA 104: 9093-9098.
69. Redding, K. (2009). Photosystem I. In The Chlamydomonas Sourcebook, D. Stern, ed (Oxford, UK: Academic Press), pp. 541-572.
70. Redding, K., MacMillan, F., Leibl, W., Brettel, K., Hanley, J., Rutherford, A. W., Breton, J., and Rochaix, J. D. (1998). A systematic survey of conserved histidines in the core subunits of Photosystem I by site-directed mutagenesis reveals the likely axial ligands of P700. EMBO J. 17: 50-60.
71. Reiland, S., Finazzi, G., Endler, A., Willig, A., Baerenfaller, K., Grossmann, J., Gerrits, B., Rutishauser, D., Gruissem, W., Rochaix, J. D., and Baginsky, S. (2011). Comparative phosphoproteome profiling reveals a function of the STN8 kinase in finetuning of cyclic electron flow (CEF). Proc. Natl. Acad. Sci. USA 108: 12955-12960.
72. Reiland, S., Messerli, G., Baerenfaller, K., Gerrits, B., Endler, A., Grossmann, J., Gruissem, W., and Baginsky, S. (2009). Largescale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol. 150: 889-903.
73. Rio, D. C., Hannon, G. J., and Nilsen, T. W. (2011). RNA: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
74. Rivier, C., Goldschmidt-Clermont, M., and Rochaix, J. D. (2001). Identification of an RNA-protein complex involved in chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J. 20: 1765-1773.
75. Ruwe, H., and Schmitz-Linneweber, C. (2012). Short non-coding RNA fragments accumulating in chloroplasts: footprints of RNA binding proteins? Nucleic Acids Res. 40: 3106-3116.
76. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). Molecular Cloning. A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
77. Sane, A. P., Stein, B., and Westhoff, P. (2005). The nuclear gene HCF107 encodes a membrane-associated R-TPR (RNA tetratricopeptide repeat)-containing protein involved in expression of the plastidial psbH gene in Arabidopsis. Plant J. 42: 720-730.
78. Schmitz-Linneweber, C., Kushnir, S., Babiychuk, E., Poltnigg, P., Herrmann, R. G., and Maier, R. M. (2005a). Pigment deficiency in nightshade/tobacco cybrids is caused by the failure to edit the plastid ATPase alpha-subunit mRNA. Plant Cell 17: 1815-1828.
79. Schmitz-Linneweber, C., Williams-Carrier, R., and Barkan, A. (2005b). RNA immunoprecipitation and microarray analysis show a chloroplast Pentatricopeptide repeat protein to be associated with the 59 region of mRNAs whose translation it activates. Plant Cell 17: 2791-2804.
80. Schweer, J., Türkeri, H., Kolpack, A., and Link, G. (2010). Role and regulation of plastid sigma factors and their functional interactors during chloroplast transcription-recent lessons from Arabidopsis thaliana. Eur. J. Cell Biol. 89: 940-946.
81. Shimogawara, K., Fujiwara, S., Grossman, A., and Usuda, H. (1998). High-efficiency transformation of Chlamydomonas reinhardtii by electroporation. Genetics 148: 1821-1828.
82. Stampacchia, O., Girard-Bascou, J., Zanasco, J. L., Zerges, W., Bennoun, P., and Rochaix, J. D. (1997). A nuclear-encoded function essential for translation of the chloroplast psaB mRNA in Chlamydomonas. Plant Cell 9: 773-782.
83. Stern, D. B., Goldschmidt-Clermont, M., and Hanson, M. R. (2010). Chloroplast RNA metabolism. Annu. Rev. Plant Biol. 61: 125-155.
84. Takahashi, Y., Goldschmidt-Clermont, M., Soen, S. Y., Franzén, L. G., and Rochaix, J. D. (1991). Directed chloroplast transformation in Chlamydomonas reinhardtii: insertional inactivation of the psaC gene encoding the iron sulfur protein destabilizes photosystem I. EMBO J. 10: 2033-2040.
85. Takahashi, Y., Matsumoto, H., Goldschmidt-Clermont, M., and Rochaix, J. D. (1994). Directed disruption of the Chlamydomonas chloroplast psbK gene destabilizes the photosystem II reaction center complex. Plant Mol. Biol. 24: 779-788.
86. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6. 0. Mol. Biol. Evol. 30: 2725-2729.
87. Terauchi, A. M., Peers, G., Kobayashi, M. C., Niyogi, K. K., and Merchant, S. S. (2010). Trophic status of Chlamydomonas reinhardtii influences the impact of iron deficiency on photosynthesis. Photosynth. Res. 105: 39-49.
88. Tikkanen, M., Nurmi, M., Kangasjärvi, S., and Aro, E. M. (2008). Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim. Biophys. Acta 1777: 1432-1437.
89. Urzica, E. I., Casero, D., Yamasaki, H., Hsieh, S. I., Adler, L. N., Karpowicz, S. J., Blaby-Haas, C. E., Clarke, S. G., Loo, J. A., Pellegrini, M., and Merchant, S. S. (2012). Systems and transsystem level analysis identifies conserved iron deficiency responses in the plant lineage. Plant Cell 24: 3921-3948.
90. Urzica, E. I., Vieler, A., Hong-Hermesdorf, A., Page, M. D., Casero, D., Gallaher, S. D., Kropat, J., Pellegrini, M., Benning, C., and Merchant, S. S. (2013). Remodeling of membrane lipids in ironstarved Chlamydomonas. J. Biol. Chem. 288: 30246-30258.
91. Vaistij, F. E., Boudreau, E., Lemaire, S. D., Goldschmidt-Clermont, M., and Rochaix, J. D. (2000a). Characterization of Mbb1, a nucleusencoded tetratricopeptide-like repeat protein required for expression of the chloroplast psbB/psbT/psbH gene cluster in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 97: 14813-14818.
92. Vaistij, F. E., Goldschmidt-Clermont, M., Wostrikoff, K., and Rochaix, J. D. (2000b). Stability determinants in the chloroplast psbB/T/H mRNAs of Chlamydomonas reinhardtii. Plant J. 21: 469-482.
93. Wang, F., Johnson, X., Cavaiuolo, M., Bohne, A. V., Nickelsen, J., and Vallon, O. (2015). Two Chlamydomonas OPR proteins stabilize chloroplast mRNAs encoding small subunits of photosystem II and cytochrome b6 f. Plant J. 82: 861-873.
94. Wang, H., Gau, B., Slade, W. O., Juergens, M., Li, P., and Hicks, L. M. (2014). The global phosphoproteome of Chlamydomonas reinhardtii reveals complex organellar phosphorylation in the flagella and thylakoid membrane. Mol. Cell. Proteomics 13: 2337-2353.
95. Wei, L., Derrien, B., Gautier, A., Houille-Vernes, L., Boulouis, A., Saint-Marcoux, D., Malnoë, A., Rappaport, F., de Vitry, C., Vallon, O., Choquet, Y., and Wollman, F. A. (2014). Nitric oxidetriggered remodeling of chloroplast bioenergetics and thylakoid proteins upon nitrogen starvation in Chlamydomonas reinhardtii. Plant Cell 26: 353-372.
96. Wessel, D., and Flügge, U. I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138: 141-143.
97. Williams-Carrier, R., Kroeger, T., and Barkan, A. (2008). Sequencespecific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA 14: 1930-1941.
98. Wollman, F. A., and Delepelaire, P. (1984). Correlation between changes in light energy distribution and changes in thylakoid membrane polypeptide phosphorylation in Chlamydomonas reinhardtii. J. Cell Biol. 98: 1-7.
99. Wostrikoff, K., Girard-Bascou, J., Wollman, F. A., and Choquet, Y. (2004). Biogenesis of PSI involves a cascade of translational autoregulation in the chloroplast of Chlamydomonas. EMBO J. 23: 2696-2705.
100. Yin, P., et al. (2013). Structural basis for the modular recognition of single-stranded RNA by PPR proteins. Nature 504: 168-171.
101. Zhelyazkova, P., Hammani, K., Rojas, M., Voelker, R., Vargas-Suárez, M., Börner, T., and Barkan, A. (2012). Protein-mediated protection as the predominant mechanism for defining processed mRNA termini in land plant chloroplasts. Nucleic Acids Res. 40: 3092-3105.