Conditional repression of essential chloroplast genes: Evidence for new plastid signaling pathways

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1847, Issue 9, 2015, Pages 986-992

  Rochaix, Jean David ^a   Ramundo, Silvia ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Autophagy; Chaperone; Chloroplast; Plastid gene expression; Protein quality control; Unfolded protein response

Indexed keywords

ENDOPEPTIDASE CLP; PROTEIN; RIBOSOME PROTEIN; RNA POLYMERASE; CHLOROPLAST PROTEIN;

ARTICLE; BIOGENESIS; CELL DEATH; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; CHLOROPLAST GENE; DEFENSE MECHANISM; FEEDBACK SYSTEM; GENE EXPRESSION; NONHUMAN; PLASTID; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN HOMEOSTASIS; SIGNAL TRANSDUCTION; THYLAKOID; UNFOLDED PROTEIN RESPONSE; AUTOPHAGY; GENE EXPRESSION REGULATION; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; QUALITY CONTROL;

CHLAMYDOMONAS REINHARDTII;

AUTOPHAGY; CHLOROPLAST PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENES, CHLOROPLAST; LIPID METABOLISM; PLASTIDS; QUALITY CONTROL; SIGNAL TRANSDUCTION;

EID: 84935031098     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2014.11.011     Document Type: Review

References (89)

1. F. Abdallah, F. Salamini, and D. Leister A prediction of the size and evolutionary origin of the proteome of chloroplasts of Arabidopsis Trends Plant Sci. 5 2000 141 142
2. J.E. Boynton, and N.W. Gillham Chloroplast transformation in Chlamydomonas Methods Enzymol. 217 1993 510 536
3. Z. Svab, P. Hajdukiewicz, and P. Maliga Stable transformation of plastids in higher plants Proc. Natl. Acad. Sci. U. S. A. 87 1990 8526 8530
4. M. Goldschmidt-Clermont Transgenic expression of aminoglycoside adenine transferase in the chloroplast: a selectable marker for site-directed transformation of Chlamydomonas Nucleic Acids Res. 19 1991 4083 4089
5. Z. Svab, and P. Maliga High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene Proc. Natl. Acad. Sci. U. S. A. 90 1993 913 917
6. J.-D. Rochaix Chloroplast reverse genetics: new insights into the function of plastid genes Trends Plant Sci. 2 1997 419 425
7. Y. Takahashi, M. Goldschmidt-Clermont, S.Y. Soen, L.G. Franzen, and J.D. Rochaix Directed chloroplast transformation in Chlamydomonas reinhardtii: insertional inactivation of the psaC gene encoding the iron sulfur protein destabilizes photosystem I Embo J. 10 1991 2033 2040
8. E.H. Harris The Chlamydomonas Source Book: A Comprehensive Guide to Biology and Laboratory Use 1989 Academic Press, Inc. San Diego, CA
9. S. Ramundo, M. Rahire, O. Schaad, and J.D. Rochaix Repression of essential chloroplast genes reveals new signaling pathways and regulatory feedback loops in Chlamydomonas Plant Cell 25 2013 167 186
10. M.R. Kuchka, M. Goldschmidt-Clermont, J. van Dillewijn, and J.D. Rochaix Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II Cell 58 1989 869 876
11. J. Nickelsen, J. van Dillewijn, M. Rahire, and J.-D. Rochaix Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii EMBO J. 13 1994 3182 3191
12. S. Merchant, and L. Bogorad Metal ion regulated gene expression: use of a plastocyanin-less mutant of Chlamydomonas reinhardtii to study the Cu (II)-dependent expression of cytochrome c-552 EMBO J. 6 1987 2531 2535
13. R. Surzycki, L. Cournac, G. Peltier, and J.D. Rochaix Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas Proc. Natl. Acad. Sci. U. S. A. 104 2007 17548 17553
14. M.T. Croft, A.D. Lawrence, E. Raux-Deery, M.J. Warren, and A.G. Smith Algae acquire vitamin B12 through a symbiotic relationship with bacteria Nature 438 2005 90 93
15. K.E. Helliwell, M.A. Scaife, S. Sasso, A.P. Araujo, S. Purton, and A.G. Smith Unraveling vitamin B12-responsive gene regulation in algae Plant Physiol. 165 2014 388 397
16. J.E. Boynton, N.W. Gillham, and J.F. Chabot Chloroplast ribosome deficient mutants in the green alga Chlamydomonas reinhardtii and the question of chloroplast ribosome function J. Cell Sci. 10 1972 267 305
17. E.H. Harris, J.E. Boynton, and N.W. Gillham Chloroplast ribosome biogenesis in Chlamydomonas. Selection and characterization of mutants blocked in ribosome formation J. Cell Biol. 63 1974 160 179
18. J.D. Rochaix Chlamydomonas reinhardtii as the photosynthetic yeast Annu. Rev. Genet. 29 1995 209 230
19. C. Huang, S. Wang, L. Chen, C. Lemieux, C. Otis, M. Turmel, and X.Q. Liu The Chlamydomonas chloroplast clpP gene contains translated large insertion sequences and is essential for cell growth Mol. Gen. Genet. 244 1994 151 159
20. E. Boudreau, M. Turmel, M. Goldschmidt-Clermont, J.D. Rochaix, S. Sivan, A. Michaels, and S. Leu A large open reading frame (orf1995) in the chloroplast DNA of Chlamydomonas reinhardtii encodes an essential protein Mol. Gen. Genet. 253 1997 649 653
21. J. Blamire, V.R. Flechtner, and R. Sager Regulation of nuclear DNA replication by the chloroplast in Chlamydomonas Proc. Natl. Acad. Sci. U. S. A. 71 1974 2867 2871
22. T.T. Fleischmann, L.B. Scharff, S. Alkatib, S. Hasdorf, M.A. Schottler, and R. Bock Nonessential plastid-encoded ribosomal proteins in tobacco: a developmental role for plastid translation and implications for reductive genome evolution Plant Cell 23 2011 3137 3155
23. L.A. Allison, L.D. Simon, and P. Maliga Deletion of rpoB reveals a second distinct transcription system in plastids of higher plants EMBO J. 15 1996 2802 2809
24. W.R. Hess, T. Hübschmann, and T. Börner Ribosome deficient plastids of albostrians barley: extreme representatives of non-photosynthetic plastids Endocytobiosis Cell Res. 10 1994 65 80
25. V. Walbot, and E.H. Coe Nuclear gene iojap conditions a programmed change to ribosome-less plastids in Zea mays Proc. Natl. Acad. Sci. U. S. A. 76 1979 2760 2764
26. N. Bryant, J. Lloyd, C. Sweeney, F. Myouga, and D. Meinke Identification of nuclear genes encoding chloroplast-localized proteins required for embryo development in Arabidopsis Plant Physiol. 155 2011 1678 1689
27. J. Lloyd, and D. Meinke A comprehensive dataset of genes with a loss-of-function mutant phenotype in Arabidopsis Plant Physiol. 158 2012 1115 1129
28. X.Q. Liu, J.P. Hosler, J.E. Boynton, and N.W. Gillham mRNAs for two ribosomal proteins are preferentially translated in the chloroplast of Chlamydomonas reinhardtii under conditions of reduced protein synthesis Plant Mol. Biol. 12 1989 385 394
29. W. Majeran, F.A. Wollman, and O. Vallon Evidence for a role of ClpP in the degradation of the chloroplast cytochrome b(6)f complex Plant Cell 12 2000 137 150
30. M.R. Kuchka, S.P. Mayfield, and J.D. Rochaix Nuclear mutations specifically affect the synthesis and/or degradation of the chloroplast-encoded D2 polypeptide of photosystem II in Chlamydomonas reinhardtii EMBO J. 7 1988 319 324
31. D. Drapier, J. Girard-Bascou, and F.A. Wollman Evidence for nuclear control of the expression of the atpA and atpB Chloroplast genes in Chlamydomonas Plant Cell 4 1992 283 295
32. R. Xu, S.E. Bingham, and A.N. Webber Increased mRNA accumulation in a psaB frame-shift mutant of Chlamydomonas reinhardtii suggests a role for translation in psaB mRNA stability Plant Mol. Biol. 22 1993 465 474
33. F.S. Young, and A.V. Furano Regulation of the synthesis of E. coli elongation factor Tu Cell 24 1981 695 706
34. A. Nott, H.S. Jung, and S. Koussevitzky C. J., Plastid-to-nucleus retrograde signaling Annu. Rev. Plant Biol. 57 2006 739 759
35. R.E. Susek, F.M. Ausubel, and J. Chory Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development Cell 74 1993 787 799
36. J.C. Gray, J.A. Sullivan, J.H. Wang, C.A. Jerome, and D. MacLean Coordination of plastid and nuclear gene expression Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 2003 135 144 (discussion 144-135)
37. J.A. Sullivan, and J.C. Gray Plastid translation is required for the expression of nuclear photosynthesis genes in the dark and in roots of the pea lip1 mutant Plant Cell 11 1999 901 910
38. V. Gohre, F. Ossenbuhl, M. Crevecoeur, L.A. Eichacker, and J.D. Rochaix One of two alb3 proteins is essential for the assembly of the photosystems and for cell survival in Chlamydomonas Plant Cell 18 2006 1454 1466
39. A. Nordhues, M.A. Schottler, A.K. Unger, S. Geimer, S. Schonfelder, S. Schmollinger, M. Rutgers, G. Finazzi, B. Soppa, F. Sommer, T. Muhlhaus, T. Roach, A. Krieger-Liszkay, H. Lokstein, J.L. Crespo, and M. Schroda Evidence for a role of VIPP1 in the structural organization of the photosynthetic apparatus in Chlamydomonas Plant Cell 24 2012 637 659
40. M. Schroda, and O. Vallon Chaperones and proteases D.B. Stern, The Chlamydomonas Sourcebook vol. 2 2009 Elsevier Amsterdam 671 729
41. Y. Choquet, K. Wostrikoff, B. Rimbault, F. Zito, J. Girard-Bascou, D. Drapier, and F.A. Wollman Assembly-controlled regulation of chloroplast gene translation Biochem. Soc. Trans. 29 2001 421 426
42. S. Koussevitzky, A. Nott, T.C. Mockler, F. Hong, G. Sachetto-Martins, M. Surpin, J. Lim, R. Mittler, and J. Chory Signals from chloroplasts converge to regulate nuclear gene expression Science 316 2007 715 719
43. R. Oelmuller, I. Levitan, R. Bergfeld, V.K. Rajasekhar, and H. Mohr Expression of nuclear genes as affected by treatments acting on the plastids Planta 168 1986 482 492
44. N. Mochizuki, J.A. Brusslan, R. Larkin, A. Nagatani, and J. Chory Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction Proc. Natl. Acad. Sci. U. S. A. 98 2001 2053 2058
45. A. Strand, T. Asami, J. Alonso, J.R. Ecker, and J. Chory Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX Nature 421 2003 79 83
46. T. Pfannschmidt, K. Schutze, M. Brost, and R. Oelmuller A novel mechanism of nuclear photosynthesis gene regulation by redox signals from the chloroplast during photosystem stoichiometry adjustment J. Biol. Chem. 276 2001 36125 36130
47. X. Sun, P. Feng, X. Xu, H. Guo, J. Ma, W. Chi, R. Lin, C. Lu, and L. Zhang A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus Nat. Commun. 2 2011 477
48. Z. Adam, and A.K. Clarke Cutting edge of chloroplast proteolysis Trends Plant Sci. 7 2002 451 456
49. J.B. Peltier, D.R. Ripoll, G. Friso, A. Rudella, Y. Cai, J. Ytterberg, L. Giacomelli, J. Pillardy, and K.J. van Wijk Clp protease complexes from photosynthetic and non-photosynthetic plastids and mitochondria of plants, their predicted three-dimensional structures, and functional implications J. Biol. Chem. 279 2004 4768 4781
50. P.D. Olinares, J. Kim, and K.J. van Wijk The Clp protease system; a central component of the chloroplast protease network Biochim. Biophys. Acta 1807 2011 999 1011
51. H. Schuhmann, and I. Adamska Deg proteases and their role in protein quality control and processing in different subcellular compartments of the plant cell Physiol. Plant. 145 2012 224 234
52. Z. Adam Emerging roles for diverse intramembrane proteases in plant biology Biochim. Biophys. Acta 1828 2013 2933 2936
53. B. Zybailov, H. Rutschow, G. Friso, A. Rudella, O. Emanuelsson, Q. Sun, and K.J. van Wijk Sorting signals, N-terminal modifications and abundance of the chloroplast proteome PLoS One 3 2008 e1994
54. B. Derrien, W. Majeran, F.A. Wollman, and O. Vallon Multistep processing of an insertion sequence in an essential subunit of the chloroplast ClpP complex J. Biol. Chem. 284 2009 15408 15415
55. Z. Adam, I. Adamska, K. Nakabayashi, O. Ostersetzer, K. Haussuhl, A. Manuell, B. Zheng, O. Vallon, S.R. Rodermel, K. Shinozaki, and A.K. Clarke Chloroplast and mitochondrial proteases in Arabidopsisn. A proposed nomenclature Plant Physiol. 125 2001 1912 1918
56. L.L. Sjogren, and A.K. Clarke Assembly of the chloroplast ATP-dependent Clp protease in Arabidopsis is regulated by the ClpT accessory proteins Plant Cell 23 2011 322 332
57. T. Shikanai, K. Shimizu, K. Ueda, Y. Nishimura, T. Kuroiwa, and T. Hashimoto The chloroplast clpP gene, encoding a proteolytic subunit of ATP-dependent protease, is indispensable for chloroplast development in tobacco Plant Cell Physiol. 42 2001 264 273
58. H. Kuroda, and P. Maliga The plastid clpP1 protease gene is essential for plant development Nature 425 2003 86 89
59. J. Schelin, F. Lindmark, and A.K. Clarke The clpP multigene family for the ATP-dependent Clp protease in the cyanobacterium Synechococcus Microbiology 148 2002 2255 2265
60. K. Barker-Astrom, J. Schelin, P. Gustafsson, A.K. Clarke, and D.A. Campbell Chlorosis during nitrogen starvation is altered by carbon dioxide and temperature status and is mediated by the ClpP1 protease in Synechococcus elongatus Arch. Microbiol. 183 2005 66 69
61. A.K. Clarke, T.M. MacDonald, and L.L.E. Sjögren The ATP-dependent Clp protease in chloroplasts of higher plants Physiol. Plant. 123 2005 406 412
62. S. Koussevitzky, T.M. Stanne, C.A. Peto, T. Giap, L.L. Sjogren, Y. Zhao, A.K. Clarke, and J. Chory An Arabidopsis thaliana virescent mutant reveals a role for ClpR1 in plastid development Plant Mol. Biol. 63 2007 85 96
63. A. Rudella, G. Friso, J.M. Alonso, J.R. Ecker, and K.J. van Wijk Downregulation of ClpR2 leads to reduced accumulation of the ClpPRS protease complex and defects in chloroplast biogenesis in Arabidopsis Plant Cell 18 2006 1704 1721
64. L.L. Sjogren, T.M. Stanne, B. Zheng, S. Sutinen, and A.K. Clarke Structural and functional insights into the chloroplast ATP-dependent Clp protease in Arabidopsis Plant Cell 18 2006 2635 2649
65. B. Zybailov, G. Friso, J. Kim, A. Rudella, V.R. Rodriguez, Y. Asakura, Q. Sun, and K.J. van Wijk Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism Mol. Cell. Proteome. 8 2009 1789 1810
66. S. Ramundo, D. Casero, T. Muhlhaus, D. Hemme, F. Sommer, M. Crevecoeur, M. Rahire, M. Schroda, J. Rusch, U. Goodenough, M. Pellegrini, M.E. Perez-Perez, J.L. Crespo, O. Schaad, N. Civic, and J.D. Rochaix Conditional depletion of the Chlamydomonas chloroplast ClpP protease activates nuclear genes involved in autophagy and plastid protein quality control Plant Cell 26 2014 2201 2222
67. M.E. Perez-Perez, and J.L. Crespo Autophagy in the Model Alga Chlamydomonas reinhardtii, Autophagy, 6 2010
68. M.E. Perez-Perez, F.J. Florencio, and J.L. Crespo Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii Plant Physiol. 152 2010 1874 1888
69. U. Nair, A. Jotwani, J. Geng, N. Gammoh, D. Richerson, W.L. Yen, J. Griffith, S. Nag, K. Wang, T. Moss, M. Baba, J.A. McNew, X. Jiang, F. Reggiori, T.J. Melia, and D.J. Klionsky SNARE proteins are required for macroautophagy Cell 146 2011 290 302
70. M. Renna, C. Schaffner, A.R. Winslow, F.M. Menzies, A.A. Peden, R.A. Floto, and D.C. Rubinsztein Autophagic substrate clearance requires activity of the syntaxin-5 SNARE complex J. Cell Sci. 124 2011 469 482
71. C. Stroupe Autophagy: cells SNARE selves Curr. Biol. 21 2011 R697 R699
72. A.J. Stein, G. Fuchs, C. Fu, S.L. Wolin, and K.M. Reinisch Structural insights into RNA quality control: the Ro autoantigen binds misfolded RNAs via its central cavity Cell 121 2005 529 539
73. X. Chen, E.J. Wurtmann, J. Van Batavia, B. Zybailov, M.P. Washburn, and S.L. Wolin An ortholog of the Ro autoantigen functions in 23S rRNA maturation in D. radiodurans Genes Dev. 21 2007 1328 1339
74. G. Fuchs, A.J. Stein, C. Fu, K.M. Reinisch, and S.L. Wolin Structural and biochemical basis for misfolded RNA recognition by the Ro autoantigen Nat. Struct. Mol. Biol. 13 2006 1002 1009
75. S.L. Wolin, and E.J. Wurtmann Molecular chaperones and quality control in noncoding RNA biogenesis Cold Spring Harb. Symp. Quant. Biol. 71 2006 505 511
76. S. Saschenbrecker, A. Bracher, K.V. Rao, B.V. Rao, F.U. Hartl, and M. Hayer-Hartl Structure and function of RbcX, an assembly chaperone for hexadecameric Rubisco Cell 129 2007 1189 1200
77. J.M. Heo, N. Livnat-Levanon, E.B. Taylor, K.T. Jones, N. Dephoure, J. Ring, J. Xie, J.L. Brodsky, F. Madeo, S.P. Gygi, K. Ashrafi, M.H. Glickman, and J. Rutter A stress-responsive system for mitochondrial protein degradation Mol. Cell 40 2010 465 480
78. H. Meyer, M. Bug, and S. Bremer Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system Nat. Cell Biol. 14 2012 117 123
79. R.A. White, G.R. Wolfe, Y. Komine, and J.K. Hoober Localization of light-harvesting complex apoproteins in the chloroplast and cytoplasm during greening of Chlamydomonas reinhardtii at 38 degrees C Photosynth. Res. 47 1996 267 280
80. H. Park, L.L. Eggink, R.W. Roberson, and J.K. Hoober Transfer of proteins from the chloroplast to vacuoles in Chlamydomonas reinhardtii (chlorophyta): a pathway for degradation J. Phycol. 35 1999 528 538
81. H.M. Li, Y. Kaneko, and K. Keegstra Molecular cloning of a chloroplastic protein associated with both the envelope and thylakoid membranes Plant Mol. Biol. 25 1994 619 632
82. D. Kroll, K. Meierhoff, N. Bechtold, M. Kinoshita, S. Westphal, U.C. Vothknecht, J. Soll, and P. Westhoff VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation Proc. Natl. Acad. Sci. U. S. A. 98 2001 4238 4242
83. S. Westphal, L. Heins, J. Soll, and U.C. Vothknecht Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis? Proc. Natl. Acad. Sci. U. S. A. 98 2001 4243 4248
84. J.S. Cox, C.E. Shamu, and P. Walter Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase Cell 73 1993 1197 1206
85. Q. Zhao, J. Wang, I.V. Levichkin, S. Stasinopoulos, M.T. Ryan, and N.J. Hoogenraad A mitochondrial specific stress response in mammalian cells EMBO J. 21 2002 4411 4419
86. J.E. Aldridge, T. Horibe, and N.J. Hoogenraad Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements PLoS One 2 2007 e874
87. S. Park, and S.R. Rodermel Mutations in ClpC2/Hsp100 suppress the requirement for FtsH in thylakoid membrane biogenesis Proc. Natl. Acad. Sci. U. S. A. 101 2004 12765 12770
88. F. Yu, X. Liu, M. Alsheikh, S. Park, and S. Rodermel Mutations in suppressor of variegation 1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis Plant Cell 20 2008 1786 1804
89. E. Miura, Y. Kato, R. Matsushima, V. Albrecht, S. Laalami, and W. Sakamoto The balance between protein synthesis and degradation in chloroplasts determines leaf variegation in Arabidopsis yellow variegated mutants Plant Cell 19 2007 1313 1328