Functions of plastid protein import and the ubiquitin-proteasome system in plastid development

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1847, Issue 9, 2015, Pages 939-948

  Ling, Qihua ^a   Jarvis, Paul ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Chloroplast; Plastid; Proteasome; Protein degradation; Protein transport; Ubiquitin

Indexed keywords

CHANNEL PROTEIN; CHLOROPLAST PROTEIN; PROTEASOME; PROTEIN; PROTEIN PRECURSOR; RECEPTOR PROTEIN; TOC159 PROTEIN; TOC34 PROTEIN; UBIQUITIN; UNCLASSIFIED DRUG;

ARTICLE; BIOCHEMICAL ANALYSIS; CELL FATE; CELL MATURATION; CROP; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PLANT DEVELOPMENT; PLASTID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN TRANSPORT; STRESS; UBIQUITINATION; METABOLISM; PHYSIOLOGY;

ALGAE;

CHLOROPLAST PROTEINS; PLASTIDS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN TRANSPORT; UBIQUITIN; UBIQUITINATION;

EID: 84931561206     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2015.02.017     Document Type: Review

References (153)

1. J.M. Whatley A suggested cycle of plastid developmental interrelationships New Phytol. 80 1978 489 502
2. P.J. Keeling The number, speed, and impact of plastid endosymbioses in eukaryotic evolution Annu. Rev. Plant Biol. 64 2013 583 607
3. E. López-Juez, and K.A. Pyke Plastids unleashed: their development and their integration in plant development Int. J. Dev. Biol. 49 2005 557 577
4. N. Nelson, and A. Ben-Shem The complex architecture of oxygenic photosynthesis Nat. Rev. Mol. Cell Biol. 5 2004 971 982
5. H.E. Neuhaus, and M.J. Emes Nonphotosynthetic metabolism in plastids Annu. Rev. Plant Physiol. Plant Mol. Biol. 51 2000 111 140
6. P. Jarvis, and E. López-Juez Biogenesis and homeostasis of chloroplasts and other plastids Nat. Rev. Mol. Cell Biol. 14 2013 787 802
7. M.T. Morita, and M. Nakamura Dynamic behavior of plastids related to environmental response Curr. Opin. Plant Biol. 15 2012 722 728
8. A. Reyes-Prieto, A.P. Weber, and D. Bhattacharya The origin and establishment of the plastid in algae and plants Annu. Rev. Genet. 41 2007 147 168
9. A.W. Larkum, P.J. Lockhart, and C.J. Howe Shopping for plastids Trends Plant Sci. 12 2007 189 195
10. W. Martin, T. Rujan, E. Richly, A. Hansen, S. Cornelsen, T. Lins, D. Leister, B. Stoebe, M. Hasegawa, and D. Penny Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus Proc. Natl. Acad. Sci. U. S. A. 99 2002 12246 12251
11. J.N. Timmis, M.A. Ayliffe, C.Y. Huang, and W. Martin Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes Nat. Rev. Genet. 5 2004 123 135
12. K. Keegstra, and K. Cline Protein import and routing systems of chloroplasts Plant Cell 11 1999 557 570
13. D. Leister Chloroplast research in the genomic age Trends Genet. 19 2003 47 56
14. J. Bédard, and P. Jarvis Recognition and envelope translocation of chloroplast preproteins J. Exp. Bot. 56 2005 2287 2320
15. F. Kessler, and D.J. Schnell The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids Traffic 7 2006 248 257
16. J. Soll, and E. Schleiff Protein import into chloroplasts Nat. Rev. Mol. Cell Biol. 5 2004 198 208
17. T. Inaba, and D.J. Schnell Protein trafficking to plastids: one theme, many variations Biochem. J. 413 2008 15 28
18. P. Jarvis Targeting of nucleus-encoded proteins to chloroplasts in plants (Tansley Review) New Phytol. 179 2008 257 285
19. H.M. Li, and C.C. Chiu Protein transport into chloroplasts Annu. Rev. Plant Biol. 61 2010 157 180
20. L.G. Richardson, Y.D. Paila, S.R. Siman, Y. Chen, M.D. Smith, and D.J. Schnell Targeting and assembly of components of the TOC protein import complex at the chloroplast outer envelope membrane Front. Plant Sci. 5 2014 269
21. E. Demarsy, A.M. Lakshmanan, and F. Kessler Border control: selectivity of chloroplast protein import and regulation at the TOC-complex Front. Plant Sci. 5 2014 483
22. W. Neupert, and J.M. Herrmann Translocation of proteins into mitochondria Annu. Rev. Biochem. 76 2007 723 749
23. O. Schmidt, N. Pfanner, and C. Meisinger Mitochondrial protein import: from proteomics to functional mechanisms Nat. Rev. Mol. Cell Biol. 11 2010 655 667
24. E. Schleiff, and T. Becker Common ground for protein translocation: access control for mitochondria and chloroplasts Nat. Rev. Mol. Cell Biol. 12 2011 48 59
25. M. Gutensohn, E. Fan, S. Frielingsdorf, P. Hanner, B. Hou, B. Hust, R.B. Klösgen, Toc, Tic, and Tat Structure and function of protein transport machineries in chloroplasts J. Plant Physiol. 163 2006 333 347
26. P. Jarvis, and C. Robinson Mechanisms of protein import and routing in chloroplasts Curr. Biol. 14 2004 R1064 R1077
27. D. Schünemann Mechanisms of protein import into thylakoids of chloroplasts Biol. Chem. 388 2007 907 915
28. K. Cline, and C. Dabney-Smith Plastid protein import and sorting: different paths to the same compartments Curr. Opin. Plant Biol. 11 2008 585 592
29. E. Kovacs-Bogdan, J. Soll, and B. Bölter Protein import into chloroplasts: the Tic complex and its regulation Biochim. Biophys. Acta 1803 2010 740 747
30. S.E. Perry, and K. Keegstra Envelope membrane proteins that interact with chloroplastic precursor proteins Plant Cell 6 1994 93 105
31. D.J. Schnell, F. Kessler, and G. Blobel Isolation of components of the chloroplast protein import machinery Science 266 1994 1007 1012
32. F. Kessler, G. Blobel, H.A. Patel, and D.J. Schnell Identification of two GTP-binding proteins in the chloroplast protein import machinery Science 266 1994 1035 1039
33. S. Hirsch, E. Muckel, F. Heemeyer, G. von Heijne, and J. Soll A receptor component of the chloroplast protein translocation machinery Science 266 1994 1989 1992
34. C. Wu, F.S. Seibert, and K. Ko Identification of chloroplast envelope proteins in close physical proximity to a partially translocated chimeric precursor protein J. Biol. Chem. 269 1994 32264 32271
35. M. Seedorf, K. Waegemann, and J. Soll A constituent of the chloroplast import complex represents a new type of GTP-binding protein Plant J. 7 1995 401 411
36. J. Lübeck, J. Soll, M. Akita, E. Nielsen, and K. Keegstra Topology of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane EMBO J. 15 1996 4230 4238
37. D.J. Schnell, G. Blobel, K. Keegstra, F. Kessler, K. Ko, and J. Soll A consensus nomenclature for the protein-import components of the chloroplast envelope Trends Cell Biol. 7 1997 303 304
38. E. Schleiff, M. Jelic, and J. Soll A GTP-driven motor moves proteins across the outer envelope of chloroplasts Proc. Natl. Acad. Sci. U. S. A. 100 2003 4604 4609
39. E. Schleiff, J. Soll, M. Küchler, W. Kuhlbrandt, and R. Harrer Characterization of the translocon of the outer envelope of chloroplasts J. Cell Biol. 160 2003 541 551
40. K.Y. Chen, and H.M. Li Precursor binding to an 880-kDa Toc complex as an early step during active import of protein into chloroplasts Plant J. 49 2007 149 158
41. S. Kikuchi, T. Hirohashi, and M. Nakai Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE Plant Cell Physiol. 47 2006 363 371
42. T. Becker, M. Jelic, A. Vojta, A. Radunz, J. Soll, and E. Schleiff Preprotein recognition by the Toc complex EMBO J. 23 2004 520 530
43. P. Jarvis, L.J. Chen, H. Li, C.A. Peto, C. Fankhauser, and J. Chory An Arabidopsis mutant defective in the plastid general protein import apparatus Science 282 1998 100 103
44. J. Bauer, K. Chen, A. Hiltbrunner, E. Wehrli, M. Eugster, D. Schnell, and F. Kessler The major protein import receptor of plastids is essential for chloroplast biogenesis Nature 403 2000 203 207
45. M. Gutensohn, B. Schulz, P. Nicolay, and U.I. Flügge Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus Plant J. 23 2000 771 783
46. N. Sveshnikova, J. Soll, and E. Schleiff Toc34 is a preprotein receptor regulated by GTP and phosphorylation Proc. Natl. Acad. Sci. U. S. A. 97 2000 4973 4978
47. M.D. Smith, C.M. Rounds, F. Wang, K. Chen, M. Afitlhile, and D.J. Schnell atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins J. Cell Biol. 165 2004 323 334
48. J. Yan, J.H. Campbell, B.R. Glick, M.D. Smith, and Y. Liang Molecular characterization and expression analysis of chloroplast protein import components in tomato (Solanum lycopersicum) PLoS One 9 2014 e95088
49. W. Chang, J. Soll, and B. Bolter A new member of the psToc159 family contributes to distinct protein targeting pathways in pea chloroplasts Front. Plant Sci. 5 2014 239
50. A. Hiltbrunner, J. Bauer, P.A. Vidi, S. Infanger, P. Weibel, M. Hohwy, and F. Kessler Targeting of an abundant cytosolic form of the protein import receptor at Toc159 to the outer chloroplast membrane J. Cell Biol. 154 2001 309 316
51. Y. Ivanova, M.D. Smith, K. Chen, and D.J. Schnell Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids Mol. Biol. Cell 15 2004 3379 3392
52. B. Agne, C. Andres, C. Montandon, B. Christ, A. Ertan, F. Jung, S. Infanger, S. Bischof, S. Baginsky, and F. Kessler The acidic A-domain of Arabidopsis Toc159 occurs as a hyperphosphorylated protein Plant Physiol. 153 2010 1016 1030
53. B. Agne, S. Infanger, F. Wang, V. Hofstetter, G. Rahim, M. Martin, D.W. Lee, I. Hwang, D. Schnell, and F. Kessler A Toc159 import receptor mutant, defective in hydrolysis of GTP, supports preprotein import into chloroplasts J. Biol. Chem. 284 2009 8670 8679
54. B. Bölter, T. May, and J. Soll A protein import receptor in pea chloroplasts, Toc86, is only a proteolytic fragment of a larger polypeptide FEBS Lett. 441 1998 59 62
55. K.H. Lee, S.J. Kim, Y.J. Lee, J.B. Jin, and I. Hwang The M domain of atToc159 plays an essential role in the import of proteins into chloroplasts and chloroplast biogenesis J. Biol. Chem. 278 2003 36794 36805
56. K. Chen, X. Chen, and D.J. Schnell Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts Plant Physiol. 122 2000 813 822
57. S. Kubis, R. Patel, J. Combe, J. Bédard, S. Kovacheva, K. Lilley, A. Biehl, D. Leister, G. Ríos, C. Koncz, and P. Jarvis Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors Plant Cell 16 2004 2059 2077
58. H. Inoue, C. Rounds, and D.J. Schnell The molecular basis for distinct pathways for protein import into Arabidopsis chloroplasts Plant Cell 22 2010 1947 1960
59. A. Hiltbrunner, K. Grunig, M. Alvarez-Huerta, S. Infanger, J. Bauer, and F. Kessler AtToc90, a new GTP-binding component of the Arabidopsis chloroplast protein import machinery Plant Mol. Biol. 54 2004 427 440
60. S. Infanger, S. Bischof, A. Hiltbrunner, B. Agne, S. Baginsky, and F. Kessler The chloroplast import receptor Toc90 partially restores the accumulation of Toc159 client proteins in the Arabidopsis thaliana pp i2 mutant Mol. Plant 4 2010 252 263
61. R. Gasper, S. Meyer, K. Gotthardt, M. Sirajuddin, and A. Wittinghofer It takes two to tango: regulation of G proteins by dimerization Nat. Rev. Mol. Cell Biol. 10 2009 423 429
62. H.R. Bourne, D.A. Sanders, and F. McCormick The GTPase superfamily: conserved structure and molecular mechanism Nature 349 1991 117 127
63. R.J. Keenan, D.M. Freymann, R.M. Stroud, and P. Walter The signal recognition particle Annu. Rev. Biochem. 70 2001 755 775
64. Y.J. Sun, F. Forouhar, H.M. Li Hm, S.L. Tu, Y.H. Yeh, S. Kao, H.L. Shr, C.C. Chou, C. Chen, and C.D. Hsiao Crystal structure of pea Toc34, a novel GTPase of the chloroplast protein translocon Nat. Struct. Biol. 9 2002 95 100
65. P. Weibel, A. Hiltbrunner, L. Brand, and F. Kessler Dimerization of Toc-GTPases at the chloroplast protein import machinery J. Biol. Chem. 278 2003 37321 37329
66. Y.H. Yeh, M.M. Kesavulu, H.M. Li, S.Z. Wu, Y.J. Sun, E.H. Konozy, and C.D. Hsiao Dimerization is important for the GTPase activity of chloroplast translocon components atToc33 and psToc159 J. Biol. Chem. 282 2007 13845 13853
67. P. Koenig, M. Oreb, A. Hofle, S. Kaltofen, K. Rippe, I. Sinning, E. Schleiff, and I. Tews The GTPase cycle of the chloroplast import receptors Toc33/Toc34: implications from monomeric and dimeric structures Structure 16 2008 585 596
68. M. Oreb, A. Hofle, P. Koenig, M.S. Sommer, I. Sinning, F. Wang, I. Tews, D. Schnell, and E. Schleiff Substrate binding disrupts dimerization and induces nucleotide exchange of the chloroplast GTPase Toc33 Biochem. J. 436 2011 313 319
69. H. Aronsson, and P. Jarvis Dimerization of TOC receptor GTPases and its implementation for the control of chloroplast protein import Biochem. J. 436 2011 e1 e2
70. L.E. Reddick, M.D. Vaughn, S.J. Wright, I.M. Campbell, and B.D. Bruce In vitro comparative kinetic analysis of the chloroplast Toc GTPases J. Biol. Chem. 282 2007 11410 11426
71. M. Jelic, J. Soll, and E. Schleiff Two Toc34 homologues with different properties Biochemistry 42 2003 5906 5916
72. M. Jelic, N. Sveshnikova, M. Motzkus, P. Horth, J. Soll, and E. Schleiff The chloroplast import receptor Toc34 functions as preprotein-regulated GTPase Biol. Chem. 383 2002 1875 1883
73. J. Lee, F. Wang, and D.J. Schnell Toc receptor dimerization participates in the initiation of membrane translocation during protein import into chloroplasts J. Biol. Chem. 284 2009 31130 31141
74. H. Aronsson, J. Combe, R. Patel, B. Agne, M. Martin, F. Kessler, and P. Jarvis Nucleotide binding and dimerization at the chloroplast pre-protein import receptor, atToc33, are not essential in vivo but do increase import efficiency Plant J. 63 2010 297 311
75. M.D. Smith, A. Hiltbrunner, F. Kessler, and D.J. Schnell The targeting of the atToc159 preprotein receptor to the chloroplast outer membrane is mediated by its GTPase domain and is regulated by GTP J. Cell Biol. 159 2002 833 843
76. T.R. Wallas, M.D. Smith, S. Sanchez-Nieto, and D.J. Schnell The roles of Toc34 and Toc75 in targeting the Toc159 preprotein receptor to chloroplasts J. Biol. Chem. 278 2003 44289 44297
77. J. Bauer, A. Hiltbrunner, P. Weibel, P.A. Vidi, M. Alvarez-Huerta, M.D. Smith, D.J. Schnell, and F. Kessler Essential role of the G-domain in targeting of the protein import receptor atToc159 to the chloroplast outer membrane J. Cell Biol. 159 2002 845 854
78. G. Rahim, S. Bischof, F. Kessler, and B. Agne In vivo interaction between atToc33 and atToc159 GTP-binding domains demonstrated in a plant split-ubiquitin system J. Exp. Bot. 60 2009 257 267
79. M. Gutensohn, S. Pahnke, U. Kolukisaoglu, B. Schulz, A. Schierhorn, A. Voigt, B. Hust, I. Rollwitz, J. Stockel, S. Geimer, V. Albrecht, U.I. Flügge, and R.B. Klösgen Characterization of a T-DNA insertion mutant for the protein import receptor atToc33 from chloroplasts Mol. Genet. Genomics 272 2004 379 396
80. D. Constan, R. Patel, K. Keegstra, and P. Jarvis An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis Plant J. 38 2004 93 106
81. S. Kubis, A. Baldwin, R. Patel, A. Razzaq, P. Dupree, K. Lilley, J. Kurth, D. Leister, and P. Jarvis The Arabidopsis pp i1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins Plant Cell 15 2003 1859 1871
82. B. Hust, and M. Gutensohn Deletion of core components of the plastid protein import machinery causes differential arrest of embryo development in Arabidopsis thaliana Plant Biol. (Stuttg.) 8 2006 18 30
83. P.J. Tranel, J. Froehlich, A. Goyal, and K. Keegstra A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway EMBO J. 14 1995 2436 2446
84. S.C. Hinnah, K. Hill, R. Wagner, T. Schlicher, and J. Soll Reconstitution of a chloroplast protein import channel EMBO J. 16 1997 7351 7360
85. S.C. Hinnah, R. Wagner, N. Sveshnikova, R. Harrer, and J. Soll The chloroplast protein import channel Toc75: pore properties and interaction with transit peptides Biophys. J. 83 2002 899 911
86. F. Ertel, O. Mirus, R. Bredemeier, S. Moslavac, T. Becker, and E. Schleiff The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains J. Biol. Chem. 280 2005 28281 28289
87. I.E. Gentle, L. Burri, and T. Lithgow Molecular architecture and function of the Omp85 family of proteins Mol. Microbiol. 58 2005 1216 1225
88. S.C. Hsu, and K. Inoue Two evolutionarily conserved essential beta-barrel proteins in the chloroplast outer envelope membrane Biosci. Trends 3 2009 168 178
89. K. Inoue, and D. Potter The chloroplastic protein translocation channel Toc75 and its paralog OEP80 represent two distinct protein families and are targeted to the chloroplastic outer envelope by different mechanisms Plant J. 39 2004 354 365
90. K. Eckart, L. Eichacker, K. Sohrt, E. Schleiff, L. Heins, and J. Soll A Toc75-like protein import channel is abundant in chloroplasts EMBO Rep. 3 2002 557 562
91. L. Sánchez-Pulido, D. Devos, S. Genevrois, M. Vicente, and A. Valencia POTRA: a conserved domain in the FtsQ family and a class of beta-barrel outer membrane proteins Trends Biochem. Sci. 28 2003 523 526
92. P.M. Day, D. Potter, and K. Inoue Evolution and targeting of Omp85 homologs in the chloroplast outer envelope membrane Front. Plant Sci. 5 2014 535
93. I. Gentle, K. Gabriel, P. Beech, R. Waller, and T. Lithgow The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria J. Cell Biol. 164 2004 19 24
94. W. Huang, Q. Ling, J. Bédard, K. Lilley, and P. Jarvis In vivo analyses of the roles of essential Omp85-related proteins in the chloroplast outer envelope membrane Plant Physiol. 157 2011 147 159
95. M. Töpel, Q. Ling, and P. Jarvis Neofunctionalization within the Omp85 protein superfamily during chloroplast evolution Plant Signal. Behav. 7 2012 161 164
96. A. Baldwin, A. Wardle, R. Patel, P. Dudley, S.K. Park, D. Twell, K. Inoue, and P. Jarvis A molecular-genetic study of the Arabidopsis Toc75 gene family Plant Physiol. 138 2005 715 733
97. J.P. Stanga, K. Boonsirichai, J.C. Sedbrook, M.S. Otegui, and P.H. Masson A role for the TOC complex in Arabidopsis root gravitropism Plant Physiol. 149 2009 1896 1905
98. R. Patel, S. Hsu, J. Bédard, K. Inoue, and P. Jarvis The Omp85-related chloroplast outer envelope protein OEP80 is essential for viability in Arabidopsis Plant Physiol. 148 2008 235 245
99. T. Becker, J. Hritz, M. Vogel, A. Caliebe, B. Bukau, J. Soll, and E. Schleiff Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts Mol. Biol. Cell 15 2004 5130 5144
100. C.C. Chiu, L.J. Chen, and H.M. Li Pea chloroplast DnaJ-J8 and Toc12 are encoded by the same gene and localized in the stroma Plant Physiol. 154 2010 1172 1182
101. K. Sohrt, and J. Soll Toc64, a new component of the protein translocon of chloroplasts J. Cell Biol. 148 2000 1213 1221
102. V. Hines, A. Brandt, G. Griffiths, H. Horstmann, H. Brutsch, and G. Schatz Protein import into yeast mitochondria is accelerated by the outer membrane protein MAS70 EMBO J. 9 1990 3191 3200
103. S. Qbadou, T. Becker, T. Bionda, K. Reger, M. Ruprecht, J. Soll, and E. Schleiff Toc64 - a preprotein-receptor at the outer membrane with bipartide function J. Mol. Biol. 367 2007 1330 1346
104. H. Aronsson, P. Boij, R. Patel, A. Wardle, M. Töpel, and P. Jarvis Toc64/OEP64 is not essential for the efficient import of proteins into chloroplasts in Arabidopsis thaliana Plant J. 52 2007 53 68
105. N.R. Hofmann, and S.M. Theg Toc64 is not required for import of proteins into chloroplasts in the moss Physcomitrella patens Plant J. 43 2005 675 687
106. J. Wan, S.D. Blakeley, D.T. Dennis, and K. Ko Transit peptides play a major role in the preferential import of proteins into leucoplasts and chloroplasts J. Biol. Chem. 271 1996 31227 31233
107. X. Yan, S. Khan, T. Hase, M.J. Emes, and C.G. Bowsher Differential uptake of photosynthetic and non-photosynthetic proteins by pea root plastids FEBS Lett. 580 2006 6509 6512
108. T.S. Yu, and H. Li Chloroplast protein translocon components atToc159 and atToc33 are not essential for chloroplast biogenesis in guard cells and root cells Plant Physiol. 127 2001 90 96
109. T. Kakizaki, H. Matsumura, K. Nakayama, F.S. Che, R. Terauchi, and T. Inaba Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling Plant Physiol. 151 2009 1339 1353
110. A. Vojta, M. Alavi, T. Becker, F. Hörmann, M. Küchler, J. Soll, R. Thomson, and E. Schleiff The protein translocon of the plastid envelopes J. Biol. Chem. 279 2004 21401 21405
111. E. López-Juez Plastid biogenesis, between light and shadows J. Exp. Bot. 58 2007 11 26
112. Q. Ling, W. Huang, A. Baldwin, and P. Jarvis Chloroplast biogenesis is regulated by direct action of the ubiquitin-proteasome system Science 338 2012 655 659
113. F. Kessler Plant science. Chloroplast delivery by UPS Science 338 2012 622 623
114. S. Dutta, H.J. Teresinski, and M.D. Smith A split-ubiquitin yeast two-hybrid screen to examine the substrate specificity of atToc159 and atToc132, two Arabidopsis chloroplast preprotein import receptors PLoS One 9 2014 e95026
115. S. Bischof, K. Baerenfaller, T. Wildhaber, R. Troesch, P.A. Vidi, B. Roschitzki, M. Hirsch-Hoffmann, L. Hennig, F. Kessler, W. Gruissem, and S. Baginsky Plastid proteome assembly without Toc159: photosynthetic protein import and accumulation of N-acetylated plastid precursor proteins Plant Cell 23 2011 3911 3928
116. Y.S. Teng, P.T. Chan, and H.M. Li Differential age-dependent import regulation by signal peptides PLoS Biol. 10 2012 e1001416
117. D.W. Lee, S. Lee, Y.J. Oh, and I. Hwang Multiple sequence motifs in the rubisco small subunit transit peptide independently contribute to Toc159-dependent import of proteins into chloroplasts Plant Physiol. 151 2009 129 141
118. L.G. Richardson, M. Jelokhani-Niaraki, and M.D. Smith The acidic domains of the Toc159 chloroplast preprotein receptor family are intrinsically disordered protein domains BMC Biochem. 10 2009 35
119. S. Reiland, J. Grossmann, K. Baerenfaller, P. Gehrig, A. Nunes-Nesi, A.R. Fernie, W. Gruissem, and S. Baginsky Integrated proteome and metabolite analysis of the de-etiolation process in plastids from rice (Oryza sativa L.) Proteomics 11 2011 1751 1763
120. C. Barsan, M. Zouine, E. Maza, W. Bian, I. Egea, M. Rossignol, D. Bouyssie, C. Pichereaux, E. Purgatto, M. Bouzayen, A. Latche, and J.C. Pech Proteomic analysis of chloroplast-to-chromoplast transition in tomato reveals metabolic shifts coupled with disrupted thylakoid biogenesis machinery and elevated energy-production components Plant Physiol. 160 2012 708 725
121. A. Zhang, Q. Lu, Y. Yin, S. Ding, X. Wen, and C. Lu Comparative proteomic analysis provides new insights into the regulation of carbon metabolism during leaf senescence of rice grown under field conditions J. Plant Physiol. 167 2010 1380 1389
122. Z. Adam, and A.K. Clarke Cutting edge of chloroplast proteolysis Trends Plant Sci. 7 2002 451 456
123. F. Li, and R.D. Vierstra Autophagy: a multifaceted intracellular system for bulk and selective recycling Trends Plant Sci. 17 2012 526 537
124. R.D. Vierstra The ubiquitin-26S proteasome system at the nexus of plant biology Nat. Rev. Mol. Cell Biol. 10 2009 385 397
125. D. Finley Recognition and processing of ubiquitin-protein conjugates by the proteasome Annu. Rev. Biochem. 78 2009 477 513
126. S.S. Vembar, and J.L. Brodsky One step at a time: endoplasmic reticulum-associated degradation Nat. Rev. Mol. Cell Biol. 9 2008 944 957
127. Q. Ling, and P. Jarvis Dynamic regulation of endosymbiotic organelles by ubiquitination Trends Cell Biol. 23 2013 399 408
128. G. Shen, Z. Adam, and H. Zhang The E3 ligase AtCHIP ubiquitylates FtsH1, a component of the chloroplast FtsH protease, and affects protein degradation in chloroplasts Plant J. 52 2007 309 321
129. S. Lee, D.W. Lee, Y. Lee, U. Mayer, Y.D. Stierhof, G. Jurgens, and I. Hwang Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis Plant Cell 21 2009 3984 4001
130. K. Sako, Y. Yanagawa, T. Kanai, T. Sato, M. Seki, M. Fujiwara, Y. Fukao, and J. Yamaguchi Proteomic analysis of the 26S proteasome reveals its direct interaction with transit peptides of plastid protein precursors for their degradation J. Proteome Res. 13 2014 3223 3230
131. S.L. Stone, H. Hauksdottir, A. Troy, J. Herschleb, E. Kraft, and J. Callis Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis Plant Physiol. 137 2005 13 30
132. M. Nakamura, M. Toyota, M. Tasaka, and M.T. Morita An Arabidopsis E3 ligase, SHOOT GRAVITROPISM9, modulates the interaction between statoliths and F-actin in gravity sensing Plant Cell 23 2011 1830 1848
133. O. Emanuelsson, H. Nielsen, S. Brunak, and G. von Heijne Predicting subcellular localization of proteins based on their N-terminal amino acid sequence J. Mol. Biol. 300 2000 1005 1016
134. N.R. Hofmann, and S.M. Theg Chloroplast outer membrane protein targeting and insertion Trends Plant Sci. 10 2005 450 457
135. J. Jouhet, and J.C. Gray Interaction of actin and the chloroplast protein import apparatus J. Biol. Chem. 284 2009 19132 19141
136. T. Hruz, O. Laule, G. Szabo, F. Wessendorp, S. Bleuler, L. Oertle, P. Widmayer, W. Gruissem, and P. Zimmermann Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes Adv. Bioinforma. 2008 2008 420747
137. B.M.V.S. Basnayake, D. Li, H. Zhang, G. Li, N. Virk, and F. Song Arabidopsis DAL1 and DAL2, two RING finger proteins homologous to Drosophila DIAP1, are involved in regulation of programmed cell death Plant Cell Rep. 30 2011 37 48
138. D.R. Demartini, C.R. Carlini, and J.J. Thelen Proteome databases and other online resources for chloroplast research in Arabidopsis Methods Mol. Biol. 775 2011 93 115
139. S. Simm, D.G. Papasotiriou, M. Ibrahim, M.S. Leisegang, B. Muller, T. Schorge, M. Karas, O. Mirus, M.S. Sommer, and E. Schleiff Defining the core proteome of the chloroplast envelope membranes Front. Plant Sci. 4 2013 11
140. D.Y. Kim, M. Scalf, L.M. Smith, and R.D. Vierstra Advanced proteomic analyses yield a deep catalog of ubiquitylation targets in Arabidopsis Plant Cell 25 2013 1523 1540
141. J. Svozil, M. Hirsch-Hoffmann, R. Dudler, W. Gruissem, and K. Baerenfaller Protein abundance changes and ubiquitylation targets identified after inhibition of the proteasome with syringolin A Mol. Cell. Proteomics 13 2014 1523 1536
142. L. Sheiner, and B. Striepen Protein sorting in complex plastids Biochim. Biophys. Acta 1833 2013 352 359
143. M.S. Sommer, S.B. Gould, P. Lehmann, A. Gruber, J.M. Przyborski, and U.G. Maier Der1-mediated preprotein import into the periplastid compartment of chromalveolates? Mol. Biol. Evol. 24 2007 918 928
144. S. Agrawal, G.G. van Dooren, W.L. Beatty, and B. Striepen Genetic evidence that an endosymbiont-derived endoplasmic reticulum-associated protein degradation (ERAD) system functions in import of apicoplast proteins J. Biol. Chem. 284 2009 33683 33691
145. F. Hempel, G. Felsner, and U.G. Maier New mechanistic insights into pre-protein transport across the second outermost plastid membrane of diatoms Mol. Microbiol. 76 2010 793 801
146. S. Agrawal, D.W. Chung, N. Ponts, G.G. van Dooren, J. Prudhomme, C.F. Brooks, E.M. Rodrigues, J.C. Tan, M.T. Ferdig, B. Striepen, and K.G. Le Roch An apicoplast localized ubiquitylation system is required for the import of nuclear-encoded plastid proteins PLoS Pathog. 9 2013 e1003426
147. C. Dahlin, and K. Cline Developmental regulation of the plastid protein import apparatus Plant Cell 3 1991 1131 1140
148. S. Dutta, S. Mohanty, and B.C. Tripathy Role of temperature stress on chloroplast biogenesis and protein import in pea Plant Physiol. 150 2009 1050 1061
149. K. Apel, and H. Hirt Reactive oxygen species: metabolism, oxidative stress, and signal transduction Annu. Rev. Plant Biol. 55 2004 373 399
150. N.J. Saibo, T. Lourenco, and M.M. Oliveira Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses Ann. Bot. 103 2009 609 623
151. C.W. Sun, L.J. Chen, L.C. Lin, and H.M. Li Leaf-specific upregulation of chloroplast translocon genes by a CCT motif-containing protein, CIA 2 Plant Cell 13 2001 2053 2061
152. C.W. Sun, Y.C. Huang, and H.Y. Chang CIA2 coordinately up-regulates protein import and synthesis in leaf chloroplasts Plant Physiol. 150 2009 879 888
153. R.D. Vierstra The expanding universe of ubiquitin and ubiquitin-like modifiers Plant Physiol. 160 2012 2 14