The chloroplast protein import system: From algae to trees

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 2, 2013, Pages 314-331

  Shi, Lan Xin ^a   Theg, Steven M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chloroplast; Evolution; Precursor receptor; Protein conducting channel; Protein import; Toc Tic complex

Indexed keywords

CHLOROPLAST PROTEIN; TRANSLOCON;

ALGA; ARABIDOPSIS; ARTICLE; CHLAMYDOMONAS REINHARDTII; CHLOROPLAST; DIMERIZATION; GREEN ALGA; NONHUMAN; PEA; POPULUS TRICHOCARPA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TARGETING; PROTEIN TRANSPORT; STOICHIOMETRY; TREE;

ALGAE; CHLOROPHYTA; PISUM SATIVUM; VIRIDIPLANTAE;

EID: 84871749722     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2012.10.002     Document Type: Review

References (229)

1. Leister D. Chloroplast research in the genomic age. Trends Genet. 2003, 19:47-56.
2. Yoon H.S., Hackett J.D., Ciniglia C., Pinto G., Bhattacharya D. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 2004, 21:809-818.
3. Reumann S., Keegstra K. The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci. 1999, 4:302-307.
4. Reumann S., Inoue K., Keegstra K. Evolution of the general protein import pathway of plastids (review). Mol. Membr. Biol. 2005, 22:73-86.
5. Gross J., Bhattacharya D. Revaluating the evolution of the Toc and Tic protein translocons. Trends Plant Sci. 2009, 14:13-20.
6. Gross J., Bhattacharya D. Mitochondrial and plastid evolution in eukaryotes: an outsiders' perspective. Nat. Rev. Genet. 2009, 10:495-505.
7. Kalanon M., McFadden G.I. The chloroplast protein translocation complexes of Chlamydomonas reinhardtii: a bioinformatic comparison of Toc and Tic components in plants, green algae and red algae. Genetics 2008, 179:95-112.
8. Bodyl A., Mackiewicz P., Stiller J.W. Early steps in plastid evolution: current ideas and controversies. Bioessays 2009, 31:1219-1232.
9. Gross J., Bhattacharya D. Endosymbiont or host: who drove mitochondrial and plastid evolution?. Biol. Direct 2011, 6:12.
10. Chan C.X., Gross J., Yoon H.S., Bhattacharya D. Plastid origin and evolution: new models provide insights into old problems. Plant Physiol. 2011, 155:1552-1560.
11. Inoue K. Emerging roles of the chloroplast outer envelope membrane. Trends Plant Sci. 2011, 16:550-557.
12. Schnell D.J., Blobel G., Keegstra K., Kessler F., Ko K., Soll J. A consensus nomenclature for the protein-import components of the chloroplast envelope. Trends Cell Biol. 1997, 7:303-304.
13. Bruce B.D. The paradox of plastid transit peptides: conservation of function despite divergence in primary structure. Biochim. Biophys. Acta 2001, 1541:2-21.
14. Bruce B.D. Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol. 2000, 10:440-447.
15. Zhang X.P., Glaser E. Interaction of plant mitochondrial and chloroplast signal peptides with the Hsp70 molecular chaperone. Trends Plant Sci. 2002, 7:14-21.
16. Jarvis P. Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol. 2008, 179:257-285.
17. Theg S.M., Bauerle C., Olsen L.J., Selman B.R., Keegstra K. Internal ATP is the only energy requirement for the translocation of precursor proteins across chloroplastic membranes. J. Biol. Chem. 1989, 264:6730-6736.
18. Shi L.X., Theg S.M. A stromal heat shock protein 70 system functions in protein import into chloroplasts in the moss Physcomitrella patens. Plant Cell 2010, 22:205-220.
19. Su P.H., Li H.M. Stromal Hsp70 is important for protein translocation into pea and Arabidopsis chloroplasts. Plant Cell 2010, 22:1516-1531.
20. Akita M., Nielsen E., Keegstra K. Identification of protein transport complexes in the chloroplastic envelope membranes via chemical cross-linking. J. Cell Biol. 1997, 136:983-994.
21. Nielsen E., Akita M., Davila-Aponte J., Keegstra K. Stable association of chloroplastic precursors with protein translocation complexes that contain proteins from both envelope membranes and a stromal Hsp100 molecular chaperone. EMBO J. 1997, 16:935-946.
22. Cline K., Dabney-Smith C. Plastid protein import and sorting: different paths to the same compartments. Curr. Opin. Plant Biol. 2008, 11:585-592.
23. Schleiff E., Klosgen R.B. Without a little help from 'my' friends: direct insertion of proteins into chloroplast membranes?. Biochim. Biophys. Acta 2001, 1541:22-33.
24. Aldridge C., Cain P., Robinson C. Protein transport in organelles: protein transport into and across the thylakoid membrane. FEBS J. 2009, 276:1177-1186.
25. Celedon J.M., Cline K. Stoichiometry for binding and transport by the twin arginine translocation system. J. Cell Biol. 2012, 197:523-534.
26. Hofmann N.R., Theg S.M. Chloroplast outer membrane protein targeting and insertion. Trends Plant Sci. 2005, 10:450-457.
27. Bolter B., Soll J. Protein import into chloroplasts: dealing with the (membrane) integration problem. Chembiochem 2011, 12:1655-1661.
28. Li H.M., Chiu C.C. Protein transport into chloroplasts. Annu. Rev. Plant Biol. 2010, 61:157-180.
29. Inaba T., Schnell D.J. Protein trafficking to plastids: one theme, many variations. Biochem. J. 2008, 413:15-28.
30. Schemenewitz A., Pollmann S., Reinbothe C., Reinbothe S. A substrate-independent, 14:3:3 protein-mediated plastid import pathway of NADPH:protochlorophyllide oxidoreductase A. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8538-8543.
31. Pollmann S., Springer A., Buhr F., Lahroussi A., Samol I., Bonneville J.M., Tichtinsky G., von Wettstein D., Reinbothe C., Reinbothe S. A plant porphyria related to defects in plastid import of protochlorophyllide oxidoreductase A. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:2019-2023.
32. Kleffmann T., Russenberger D., von Zychlinski A., Christopher W., Sjolander K., Gruissem W., Baginsky S. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Curr. Biol. 2004, 14:354-362.
33. Chen M.H., Huang L.F., Li H.M., Chen Y.R., Yu S.M. Signal peptide-dependent targeting of a rice alpha-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiol. 2004, 135:1367-1377.
34. Nanjo Y., Oka H., Ikarashi N., Kaneko K., Kitajima A., Mitsui T., Munoz F.J., Rodriguez-Lopez M., Baroja-Fernandez E., Pozueta-Romero J. Rice plastidial N-glycosylated nucleotide pyrophosphatase/phosphodiesterase is transported from the ER-golgi to the chloroplast through the secretory pathway. Plant Cell 2006, 18:2582-2592.
35. Villarejo A., Buren S., Larsson S., Dejardin A., Monne M., Rudhe C., Karlsson J., Jansson S., Lerouge P., Rolland N., von Heijne G., Grebe M., Bako L., Samuelsson G. Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast. Nat. Cell Biol. 2005, 7:1124-1131.
36. Radhamony R.N., Theg S.M. Evidence for an ER to Golgi to chloroplast protein transport pathway. Trends Cell Biol. 2006, 16:385-387.
37. Flores-Perez U., Jarvis P. Molecular chaperone involvement in chloroplast protein import. Biochim. Biophys. Acta 2012, 10.1016/j.bbamcr.2012.03.019.
38. Waegemann K., Soll J. Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant J. 1991, 1:149-158.
39. Schnell D.J., Kessler F., Blobel G. Isolation of components of the chloroplast protein import machinery. Science 1994, 266:1007-1012.
40. Kessler F., Blobel G., Patel H.A., Schnell D.J. Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 1994, 266:1035-1039.
41. Hirsch S., Muckel E., Heemeyer F., Von Heijne G., Soll J. A receptor component of the chloroplast protein translocation machinery. Science 1994, 266:1989-1992.
42. Perry S.E., Keegstra K. Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 1994, 6:93-105.
43. Ma Y., Kouranov A., LaSala S.E., Schnell D.J. Two components of the chloroplast protein import apparatus, IAP86 and IAP75, interact with the transit sequence during the recognition and translocation of precursor proteins at the outer envelope. J. Cell Biol. 1996, 134:315-327.
44. Morin X.K., Soll J. Immunogold labelling of cryosectioned pea chloroplasts and initial localization of the proteins associated with the protein import machinery. Planta (Heidelberg) 1997, 201:119-127.
45. Bolter B., May T., Soll J. A protein import receptor in pea chloroplasts, Toc86, is only a proteolytic fragment of a larger polypeptide. FEBS Lett. 1998, 441:59-62.
46. Kouranov A., Schnell D.J. Analysis of the interactions of preproteins with the import machinery over the course of protein import into chloroplasts. J. Cell Biol. 1997, 139:1677-1685.
47. Hiltbrunner A., Bauer J., Vidi P.A., Infanger S., Weibel P., Hohwy M., Kessler F. Targeting of an abundant cytosolic form of the protein import receptor at Toc159 to the outer chloroplast membrane. J. Cell Biol. 2001, 154:309-316.
48. Becker T., Jelic M., Vojta A., Radunz A., Soll J., Schleiff E. Preprotein recognition by the Toc complex. EMBO J. 2004, 23:520-530.
49. Inoue H., Rounds C., Schnell D.J. The molecular basis for distinct pathways for protein import into Arabidopsis chloroplasts. Plant Cell 2010, 22:1947-1960.
50. Agne B., Andres C., Montandon C., Christ B., Ertan A., Jung F., Infanger S., Bischof S., Baginsky S., Kessler F. The acidic A-domain of Arabidopsis TOC159 occurs as a hyperphosphorylated protein. Plant Physiol. 2010, 153:1016-1030.
51. Chen K., Chen X., Schnell D.J. Initial binding of preproteins involving the Toc159 receptor can be bypassed during protein import into chloroplasts. Plant Physiol. 2000, 122:813-822.
52. Lee K.H., Kim S.J., Lee Y.J., Jin J.B., Hwang I. The M domain of atToc159 plays an essential role in the import of proteins into chloroplasts and chloroplast biogenesis. J. Biol. Chem. 2003, 278:36794-36805.
53. Schleiff E., Jelic M., Soll J. A GTP-driven motor moves proteins across the outer envelope of chloroplasts. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:4604-4609.
54. Wallas T.R., Smith M.D., Sanchez-Nieto S., Schnell D.J. The roles of toc34 and toc75 in targeting the toc159 preprotein receptor to chloroplasts. J. Biol. Chem. 2003, 278:44289-44297.
55. Bauer J., Hiltbrunner A., Weibel P., Vidi P.A., Alvarez-Huerta M., Smith M.D., Schnell D.J., Kessler F. Essential role of the G-domain in targeting of the protein import receptor atToc159 to the chloroplast outer membrane. J. Cell Biol. 2002, 159:845-854.
56. Smith M.D., Hiltbrunner A., Kessler F., Schnell D.J. 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. 2002, 159:833-843.
57. Lung S.C., Chuong S.D. A transit peptide-like sorting signal at the C terminus directs the Bienertia sinuspersici preprotein receptor Toc159 to the chloroplast outer membrane. Plant Cell 2012, 24:1560-1578.
58. Kubis S., Patel R., Combe J., Bedard J., Kovacheva S., Lilley K., Biehl A., Leister D., Rios G., Koncz C., Jarvis P. Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 2004, 16:2059-2077.
59. Bauer J., Chen K., Hiltbrunner A., Wehrli E., Eugster M., Schnell D., Kessler F. The major protein import receptor is essential for chloroplast biogenesis. Nature 2000, 403:203-207.
60. Smith M.D., Rounds C.M., Wang F., Chen K., Afitlhile M., Schnell D.J. atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J. Cell Biol. 2004, 165:323-334.
61. Lee D.W., Lee S., Oh Y.J., Hwang I. Multiple sequence motifs in the rubisco small subunit transit peptide independently contribute to Toc159-dependent import of proteins into chloroplasts. Plant Physiol. 2009, 151:129-141.
62. Yu T.-S., Li H.-m. Chloroplast protein translocon components atToc159 and atToc33 are not essential for chloroplast biogenesis in guard cells and root cells. Plant Physiol. 2001, 127:90-96.
63. Asano T., Yoshioka Y., Machida Y. A defect in atToc159 of Arabidopsis thaliana causes severe defects in leaf development. Genes Genet. Syst. 2004, 79:207-212.
64. Bischof S., Baerenfaller K., Wildhaber T., Troesch R., Vidi P.A., Roschitzki B., Hirsch-Hoffmann M., Hennig L., Kessler F., Gruissem W., Baginsky S. Plastid proteome assembly without Toc159: photosynthetic protein import and accumulation of N-acetylated plastid precursor proteins. Plant Cell 2011, 23:3911-3928.
65. Wang F., Agne B., Kessler F., Schnell D.J. The role of GTP binding and hydrolysis at the atToc159 preprotein receptor during protein import into chloroplasts. J. Cell Biol. 2008, 183:87-99.
66. Agne B., Infanger S., Wang F., Hofstetter V., Rahim G., Martin M., Lee D.W., Hwang I., Schnell D., Kessler F. A toc159 import receptor mutant, defective in hydrolysis of GTP, supports preprotein import into chloroplasts. J. Biol. Chem. 2009, 284:8670-8679.
67. Ivanova Y., Smith M.D., Chen K., Schnell D.J. Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol. Biol. Cell 2004, 15:3379-3392.
68. Stanga J.P., Boonsirichai K., Sedbrook J.C., Otegui M.S., Masson P.H. A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiol. 2009, 149:1896-1905.
69. Hiltbrunner A., Grunig K., Alvarez-Huerta M., Infanger S., Bauer J., Kessler F. AtToc90, a new GTP-binding component of the Arabidopsis chloroplast protein import machinery. Plant Mol. Biol. 2004, 54:427-440.
70. Infanger S., Bischof S., Hiltbrunner A., Agne B., Baginsky S., Kessler F. The chloroplast import receptor Toc90 partially restores the accumulation of Toc159 client proteins in the Arabidopsis thaliana pp i2 mutant. Mol. Plant 2011, 4:252-263.
71. Hernandez Torres J., Maldonado M.A., Chomilier J. Tandem duplications of a degenerated GTP-binding domain at the origin of GTPase receptors Toc159 and thylakoidal SRP. Biochem. Biophys. Res. Commun. 2007, 364:325-331.
72. Fulgosi H., Lepedus H., Cesar V., Ljubesic N. Differential accumulation of plastid preprotein translocon components during spruce (Picea abies L. Karst.) needle development. Biol. Chem. 2005, 386:777-783.
73. Goodstein D.M., Shu S., Howson R., Neupane R., Hayes R.D., Fazo J., Mitros T., Dirks W., Hellsten U., Putnam N., Rokhsar D.S. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012, 40:D1178-D1186.
74. Velasco R., Zharkikh A., Affourtit J., Dhingra A., Cestaro A., Kalyanaraman A., Fontana P., Bhatnagar S.K., Troggio M., Pruss D., Salvi S., Pindo M., Baldi P., Castelletti S., Cavaiuolo M., Coppola G., Costa F., Cova V., Dal Ri A., Goremykin V., Komjanc M., Longhi S., Magnago P., Malacarne G., Malnoy M., Micheletti D., Moretto M., Perazzolli M., Si-Ammour A., Vezzulli S., Zini E., Eldredge G., Fitzgerald L.M., Gutin N., Lanchbury J., Macalma T., Mitchell J.T., Reid J., Wardell B., Kodira C., Chen Z., Desany B., Niazi F., Palmer M., Koepke T., Jiwan D., Schaeffer S., Krishnan V., Wu C., Chu V.T., King S.T., Vick J., Tao Q., Mraz A., Stormo A., Stormo K., Bogden R., Ederle D., Stella A., Vecchietti A., Kater M.M., Masiero S., Lasserre P., Lespinasse Y., Allan A.C., Bus V., Chagne D., Crowhurst R.N., Gleave A.P., Lavezzo E., Fawcett J.A., Proost S., Rouze P., Sterck L., Toppo S., Lazzari B., Hellens R.P., Durel C.E., Gutin A., Bumgarner R.E., Gardiner S.E., Skolnick M., Egholm M., Van de Peer Y., Salamini F., Viola R. The genome of the domesticated apple (Malus x domestica Borkh.). Nat. Genet. 2010, 42:833-839.
75. Joshi C., Kangasjarvi J., Karlsson J., Kelleher C., Kirkpatrick R., Kirst M., Kohler A., Kalluri U., Larimer F., Leebens-Mack J., Leple J.C., Locascio P., Lou Y., Lucas S., Martin F., Montanini B., Napoli C., Nelson D.R., Nelson C., Nieminen K., Nilsson O., Pereda V., Peter G., Philippe R., Pilate G., Poliakov A., Razumovskaya J., Richardson P., Rinaldi C., Ritland K., Rouze P., Ryaboy D., Schmutz J., Schrader J., Segerman B., Shin H., Siddiqui A., Sterky F., Terry A., Tsai C.J., Uberbacher E., Unneberg P., Vahala J., Wall K., Wessler S., Yang G., Yin T., Douglas C., Marra M., Sandberg G., Van de Peer Y., Rokhsar D. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006, 313:1596-1604.
76. Seedorf M., Waegemann K., Soll J. A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J. 1995, 7:401-411.
77. Jelic M., Soll J., Schleiff E. Two Toc34 homologues with different properties. Biochemistry 2003, 42:5906-5916.
78. Tsai L.Y., Tu S.L., Li H.M. Insertion of atToc34 into the chloroplastic outer membrane is assisted by at least two proteinaceous components in the import system. J. Biol. Chem. 1999, 274:18735-18740.
79. Chen D., Schnell D.J. Insertion of the 34-kDa chloroplast protein import component, IAP34, into the chloroplast outer membrane is dependent on its intrinsic GTP-binding capacity. J. Biol. Chem. 1997, 272:6614-6620.
80. Qbadou S., Tien R., Soll J., Schleiff E. Membrane insertion of the chloroplast outer envelope protein, Toc34: constrains for insertion and topology. J. Cell Sci. 2003, 116:837-846.
81. May T., Soll J. Positive charges determine the topology and functionality of the transmembrane domain in the chloroplastic outer envelope protein Toc34. J. Cell Biol. 1998, 141:895-904.
82. Jackson-Constan D., Keegstra K. Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol. 2001, 125:1567-1576.
83. Gutensohn M., Pahnke S., Kolukisaoglu U., Schulz B., Schierhorn A., Voigt A., Hust B., Rollwitz I., Stockel J., Geimer S., Albrecht V., Flugge U.I., Klosgen R.B. Characterization of a T-DNA insertion mutant for the protein import receptor atToc33 from chloroplasts. Mol. Genet. Genomics 2004, 272:379-396.
84. Gutensohn M., Schulz B., Nicolay P., Flugge U.I. Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. Plant J. 2000, 23:771-783.
85. Jarvis P., Chen L.J., Li H., Peto C.A., Fankhauser C., Chory J. An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 1998, 282:100-103.
86. Kubis S., Baldwin A., Patel R., Razzaq A., Dupree P., Lilley K., Kurth J., Leister D., Jarvis P. The Arabidopsis pp i1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. Plant Cell 2003, 15:1859-1871.
87. Constan D., Patel R., Keegstra K., Jarvis P. An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J. 2004, 38:93-106.
88. Hust B., Gutensohn M. Deletion of core components of the plastid protein import machinery causes differential arrest of embryo development in Arabidopsis thaliana. Plant Biol. (Stuttg.) 2006, 8:18-30.
89. Sun Y.J., Forouhar F., Li Hm H.M., Tu S.L., Yeh Y.H., Kao S., Shr H.L., Chou C.C., Chen C., Hsiao C.D. Crystal structure of pea Toc34, a novel GTPase of the chloroplast protein translocon. Nat. Struct. Biol. 2002, 9:95-100.
90. Yeh Y.H., Kesavulu M.M., Li H.M., Wu S.Z., Sun Y.J., Konozy E.H., Hsiao C.D. Dimerization is important for the GTPase activity of chloroplast translocon components atToc33 and psToc159. J. Biol. Chem. 2007, 282:13845-13853.
91. Weibel P., Hiltbrunner A., Brand L., Kessler F. Dimerization of Toc-GTPases at the chloroplast protein import machinery. J. Biol. Chem. 2003, 278:37321-37329.
92. Koenig P., Oreb M., Rippe K., Muhle-Goll C., Sinning I., Schleiff E., Tews I. On the significance of Toc-GTPase homodimers. J. Biol. Chem. 2008, 283:23104-23112.
93. Reddick L.E., Vaughn M.D., Wright S.J., Campbell I.M., Bruce B.D. In vitro comparative kinetic analysis of the chloroplast Toc GTPases. J. Biol. Chem. 2007, 282:11410-11426.
94. Koenig P., Oreb M., Hofle A., Kaltofen S., Rippe K., Sinning I., Schleiff E., Tews I. The GTPase cycle of the chloroplast import receptors Toc33/Toc34: implications from monomeric and dimeric structures. Structure 2008, 16:585-596.
95. Rahim G., Bischof S., Kessler F., Agne B. In vivo interaction between atToc33 and atToc159 GTP-binding domains demonstrated in a plant split-ubiquitin system. J. Exp. Bot. 2009, 60:257-267.
96. Aronsson H., Jarvis P. Dimerization of TOC receptor GTPases and its implementation for the control of protein import into chloroplasts. Biochem. J. 2011, 436:e1-e2.
97. Oreb M., Hofle A., Koenig P., Sommer M.S., Sinning I., Wang F., Tews I., Schnell D., Schleiff E. Substrate binding disrupts dimerization and induces nucleotide exchange of the chloroplast GTPase Toc33. Biochem. J. 2011, 436:313-319.
98. Lee J., Wang F., Schnell D.J. Toc receptor dimerization participates in the initiation of membrane translocation during protein import into chloroplasts. J. Biol. Chem. 2009, 284:31130-31141.
99. Aronsson H., Combe J., Patel R., Agne B., Martin M., Kessler F., Jarvis P. Nucleotide binding and dimerization at the chloroplast pre-protein import receptor, atToc33, are not essential in vivo but do increase import efficiency. Plant J. 2010, 63:297-311.
100. Bionda T., Koenig P., Oreb M., Tews I., Schleiff E. pH sensitivity of the GTPase Toc33 as a regulatory circuit for protein translocation into chloroplasts. Plant Cell Physiol. 2008, 49:1917-1921.
101. Sveshnikova N., Soll J., Schleiff E. Toc34 is a preprotein receptor regulated by GTP and phosphorylation. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:4973-4978.
102. Schleiff E., Soll J., Sveshnikova N., Tien R., Wright S., Dabney-Smith C., Subramanian C., Bruce B.D. Structural and guanosine triphosphate/diphosphate requirements for transit peptide recognition by the cytosolic domain of the chloroplast outer envelope receptor, Toc34. Biochemistry 2002, 41:1934-1946.
103. Jelic M., Sveshnikova N., Motzkus M., Horth P., Soll J., Schleiff E. The chloroplast import receptor Toc34 functions as preprotein-regulated GTPase. Biol. Chem. 2002, 383:1875-1883.
104. Aronsson H., Combe J., Jarvis P. Unusual nucleotide-binding properties of the chloroplast protein import receptor, atToc33. FEBS Lett. 2003, 544:79-85.
105. Aronsson H., Combe J., Patel R., Jarvis P. In vivo assessment of the significance of phosphorylation of the Arabidopsis chloroplast protein import receptor, atToc33. FEBS Lett. 2006, 580:649-655.
106. Oreb M., Zoryan M., Vojta A., Maier U.G., Eichacker L.A., Schleiff E. Phospho-mimicry mutant of atToc33 affects early development of Arabidopsis thaliana. FEBS Lett. 2007, 581:5945-5951.
107. Oreb M., Hofle A., Mirus O., Schleiff E. Phosphorylation regulates the assembly of chloroplast import machinery. J. Exp. Bot. 2008, 59:2309-2316.
108. Hirohashi T., Nakai M. Molecular cloning and characterization of maize Toc34, a regulatory component of the protein import machinery of chloroplast. Biochim. Biophys. Acta 2000, 1491:309-314.
109. Voigt A., Jakob M., Klosgen R.B., Gutensohn M. At least two Toc34 protein import receptors with different specificities are also present in spinach chloroplasts. FEBS Lett. 2005, 579:1343-1349.
110. Tranel P.J., Froehlich J., Goyal A., Keegstra K. A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway. EMBO J. 1995, 14:2436-2446.
111. Sveshnikova N., Grimm R., Soll J., Schleiff E. Topology studies of the chloroplast protein import channel Toc75. Biol. Chem. 2000, 381:687-693.
112. Seedorf M., Soll J. Copper chloride, an inhibitor of protein import into chloroplasts. FEBS Lett. 1995, 367:19-22.
113. Schleiff E., Soll J., Kuchler M., Kuhlbrandt W., Harrer R. Characterization of the translocon of the outer envelope of chloroplasts. J. Cell Biol. 2003, 160:541-551.
114. Tranel P.J., Keegstra K. A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope. Plant Cell 1996, 8:2093-2104.
115. Inoue K., Demel R., de Kruijff B., Keegstra K. The N-terminal portion of the preToc75 transit peptide interacts with membrane lipids and inhibits binding and import of precursor proteins into isolated chloroplasts. Eur. J. Biochem. 2001, 268:4036-4043.
116. Inoue K., Keegstra K. A polyglycine stretch is necessary for proper targeting of the protein translocation channel precursor to the outer envelope membrane of chloroplasts. Plant J. 2003, 34:661-669.
117. Baldwin A.J., Inoue K. The most C-terminal tri-glycine segment within the polyglycine stretch of the pea Toc75 transit peptide plays a critical role for targeting the protein to the chloroplast outer envelope membrane. FEBS J. 2006, 273:1547-1555.
118. Shipman R.L., Inoue K. Suborganellar localization of plastidic type I signal peptidase 1 depends on chloroplast development. FEBS Lett. 2009, 583:938-942.
119. Inoue K., Baldwin A.J., Shipman R.L., Matsui K., Theg S.M., Ohme-Takagi M. Complete maturation of the plastid protein translocation channel requires a type I signal peptidase. J. Cell Biol. 2005, 171:425-430.
120. Shipman-Roston R.L., Ruppel N.J., Damoc C., Phinney B.S., Inoue K. The significance of protein maturation by plastidic type I signal peptidase 1 for thylakoid development in Arabidopsis chloroplasts. Plant Physiol. 2010, 152:1297-1308.
121. Voulhoux R., Bos M.P., Geurtsen J., Mols M., Tommassen J. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 2003, 299:262-265.
122. Gentle I., Gabriel K., Beech P., Waller R., Lithgow T. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J. Cell Biol. 2004, 164:19-24.
123. Bolter B., Soll J., Schulz A., Hinnah S., Wagner R. Origin of a chloroplast protein importer. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15831-15836.
124. Reumann S., Davila-Aponte J., Keegstra K. The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:784-789.
125. Hinnah S.C., Wagner R., Sveshnikova N., Harrer R., Soll J. The chloroplast protein import channel Toc75: pore properties and interaction with transit peptides. Biophys. J. 2002, 83:899-911.
126. Arnold T., Zeth K., Linke D. Omp85 from the thermophilic cyanobacterium Thermosynechococcus elongatus differs from proteobacterial Omp85 in structure and domain composition. J. Biol. Chem. 2010, 285:18003-18015.
127. Koenig P., Mirus O., Haarmann R., Sommer M.S., Sinning I., Schleiff E., Tews I. Conserved properties of polypeptide transport-associated (POTRA) domains derived from cyanobacterial Omp85. J. Biol. Chem. 2010, 285:18016-18024.
128. Sanchez-Pulido L., Devos D., Genevrois S., Vicente M., Valencia A. POTRA: a conserved domain in the FtsQ family and a class of beta-barrel outer membrane proteins. Trends Biochem. Sci. 2003, 28:523-526.
129. Ertel F., Mirus O., Bredemeier R., Moslavac S., Becker T., Schleiff E. The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. J. Biol. Chem. 2005, 280:28281-28289.
130. Sommer M.S., Daum B., Gross L.E., Weis B.L., Mirus O., Abram L., Maier U.G., Kuhlbrandt W., Schleiff E. Chloroplast Omp85 proteins change orientation during evolution. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:13841-13846.
131. Tu S.L., Chen L.J., Smith M.D., Su Y.S., Schnell D.J., Li H.M. Import pathways of chloroplast interior proteins and the outer-membrane protein OEP14 converge at Toc75. Plant Cell 2004, 16:2078-2088.
132. Hofmann N.R., Theg S.M. Protein and energy mediated targeting of chloroplast outer envelope membrane proteins. Plant J. 2005, 44:917-927.
133. Baldwin A., Wardle A., Patel R., Dudley P., Park S.K., Twell D., Inoue K., Jarvis P. A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiol. 2005, 138:715-733.
134. Vojta A., Alavi M., Becker T., Hormann F., Kuchler M., Soll J., Thomson R., Schleiff E. The protein translocon of the plastid envelopes. J. Biol. Chem. 2004, 279:21401-21405.
135. Hsu S.C., Nafati M., Inoue K. OEP80, an essential protein paralogous to the chloroplast protein translocation channel Toc75, exists as a 70-kD protein in the Arabidopsis thaliana chloroplast outer envelope. Plant Mol. Biol. 2012, 78:147-158.
136. Eckart K., Eichacker L., Sohrt K., Schleiff E., Heins L., Soll J. A Toc75-like protein import channel is abundant in chloroplasts. EMBO Rep. 2002, 3:557-562.
137. Schleiff E., Eichacker L.A., Eckart K., Becker T., Mirus O., Stahl T., Soll J. Prediction of the plant beta-barrel proteome: a case study of the chloroplast outer envelope. Protein Sci. 2003, 12:748-759.
138. Inoue K., Potter D. 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. 2004, 39:354-365.
139. Patel R., Hsu S.C., Bedard J., Inoue K., Jarvis P. The Omp85-related chloroplast outer envelope protein OEP80 is essential for viability in Arabidopsis. Plant Physiol. 2008, 148:235-245.
140. Hsu S.C., Patel R., Bedard J., Jarvis P., Inoue K. Two distinct Omp85 paralogs in the chloroplast outer envelope membrane are essential for embryogenesis in Arabidopsis thaliana. Plant Signal. Behav. 2008, 3:1134-1135.
141. Huang W., Ling Q., Bedard J., Lilley K., Jarvis P. In vivo analyses of the roles of essential Omp85-related proteins in the chloroplast outer envelope membrane. Plant Physiol. 2011, 157:147-159.
142. Reumann S., Davila-Aponte J., Keegstra K. The evolutionary origin of the protein-translocation channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:784-789.
143. Topel M., Ling Q., Jarvis P. Neofunctionalization within the Omp85 protein superfamily during chloroplast evolution. Plant Signal. Behav. 2012, 7:161-164.
144. Hsu S.C., Inoue K. Two evolutionarily conserved essential beta-barrel proteins in the chloroplast outer envelope membrane. Biosci. Trends 2009, 3:168-178.
145. Summer E.J., Cline K. Red bell pepper chromoplasts exhibit in vitro import competency and membrane targeting of passenger proteins from the thylakoidal sec and DeltapH pathways but not the chloroplast signal recognition particle pathway. Plant Physiol. 1999, 119:575-584.
146. Davila-Aponte J.A., Inoue K., Keegstra K. Two chloroplastic protein translocation components, Tic110 and Toc75, are conserved in different plastid types from multiple plant species. Plant Mol. Biol. 2003, 51:175-181.
147. Sohrt K., Soll J. Toc64, a new component of the protein translocon of chloroplasts. J. Cell Biol. 2000, 148:1213-1221.
148. Becker T., Hritz J., Vogel M., Caliebe A., Bukau B., Soll J., Schleiff E. Toc12, a novel subunit of the intermembrane space preprotein translocon of chloroplasts. Mol. Biol. Cell 2004, 15:5130-5144.
149. Qbadou S., Becker T., Bionda T., Reger K., Ruprecht M., Soll J., Schleiff E. Toc64-a preprotein-receptor at the outer membrane with bipartide function. J. Mol. Biol. 2007, 367:1330-1346.
150. Mirus O., Bionda T., von Haeseler A., Schleiff E. Evolutionarily evolved discriminators in the 3-TPR domain of the Toc64 family involved in protein translocation at the outer membrane of chloroplasts and mitochondria. J. Mol. Model. 2009, 15:971-982.
151. Qbadou S., Becker T., Mirus O., Tews I., Soll J., Schleiff E. The molecular chaperone Hsp90 delivers precursor proteins to the chloroplast import receptor Toc64. EMBO J. 2006, 25:1836-1847.
152. Rosenbaum Hofmann N., Theg S.M. Toc64 is not required for import of proteins into chloroplasts in the moss Physcomitrella patens. Plant J. 2005, 43:675-687.
153. Aronsson H., Boij P., Patel R., Wardle A., Topel M., Jarvis P. Toc64/OEP64 is not essential for the efficient import of proteins into chloroplasts in Arabidopsis thaliana. Plant J. 2007, 52:53-68.
154. Hofmann N.R., Theg S.M. Physcomitrella patens as a model for the study of chloroplast protein transport: conserved machineries between vascular and non-vascular plants. Plant Mol. Biol. 2003, 53:621-632.
155. Lee Y.J., Sohn E.J., Lee K.H., Lee D.W., Hwang I. The transmembrane domain of AtToc64 and its C-terminal lysine-rich flanking region are targeting signals to the chloroplast outer envelope membrane [correction]. Mol. Cells 2004, 17:281-291.
156. Chan N.C., Likic V.A., Waller R.F., Mulhern T.D., Lithgow T. The C-terminal TPR domain of Tom70 defines a family of mitochondrial protein import receptors found only in animals and fungi. J. Mol. Biol. 2006, 358:1010-1022.
157. Schleiff E., Becker T. Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat. Rev. Mol. Cell Biol. 2011, 12:48-59.
158. Chew O., Lister R., Qbadou S., Heazlewood J.L., Soll J., Schleiff E., Millar A.H., Whelan J. A plant outer mitochondrial membrane protein with high amino acid sequence identity to a chloroplast protein import receptor. FEBS Lett. 2004, 557:109-114.
159. Pollmann S., Neu D., Lehmann T., Berkowitz O., Schafer T., Weiler E.W. Subcellular localization and tissue specific expression of amidase 1 from Arabidopsis thaliana. Planta 2006, 224:1241-1253.
160. Schlegel T., Mirus O., von Haeseler A., Schleiff E. The tetratricopeptide repeats of receptors involved in protein translocation across membranes. Mol. Biol. Evol. 2007, 24:2763-2774.
161. McFadden G.I., van Dooren G.G. Evolution: red algal genome affirms a common origin of all plastids. Curr. Biol. 2004, 14:R514-R516.
162. Price D.C., Chan C.X., Yoon H.S., Yang E.C., Qiu H., Weber A.P.M., Schwacke R., Gross J., Blouin N.A., Lane C., Reyes-Prieto A., Durnford D.G., Neilson J.A.D., Lang B.F., Burger G., Steiner J.M., Loffelhardt W., Meuser J.E., Posewitz M.C., Ball S., Arias M.C., Henrissat B., Coutinho P.M., Rensing S.A., Symeonidi A., Doddapaneni H., Green B.R., Rajah V.D., Boore J., Bhattacharya D. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 2012, 335:843-847.
163. Kikuchi S., Oishi M., Hirabayashi Y., Lee D.W., Hwang I., Nakai M. A 1-megadalton translocation complex containing Tic20 and Tic21 mediates chloroplast protein import at the inner envelope membrane. Plant Cell 2009, 21:1781-1797.
164. Ladig R., Sommer M.S., Hahn A., Leisegang M.S., Papasotiriou D.G., Ibrahim M., Elkehal R., Karas M., Zickermann V., Gutensohn M., Brandt U., Klosgen R.B., Schleiff E. A high-definition native polyacrylamide gel electrophoresis system for the analysis of membrane complexes. Plant J. 2011, 67:181-194.
165. Kikuchi S., Hirohashi T., Nakai M. Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE. Plant Cell Physiol. 2006, 47:363-371.
166. Kouranov A., Chen X., Fuks B., Schnell D.J. Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane. J. Cell Biol. 1998, 143:991-1002.
167. Hormann F., Kuchler M., Sveshnikov D., Oppermann U., Li Y., Soll J. Tic32, an essential component in chloroplast biogenesis. J. Biol. Chem. 2004, 279:34756-34762.
168. Kouranov A., Wang H., Schnell D.J. Tic22 is targeted to the intermembrane space of chloroplasts by a novel pathway. J. Biol. Chem. 1999, 274:25181-25186.
169. Vojta L., Soll J., Bolter B. Protein transport in chloroplasts - targeting to the intermembrane space. FEBS J. 2007, 274:5043-5054.
170. Kalanon M., Tonkin C.J., McFadden G.I. Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum. Eukaryot. Cell 2009, 8:1146-1154.
171. van Dooren G.G., Tomova C., Agrawal S., Humbel B.M., Striepen B. Toxoplasma gondii Tic20 is essential for apicoplast protein import. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13574-13579.
172. Kovacs-Bogdan E., Benz J.P., Soll J., Bolter B. Tic20 forms a channel independent of Tic110 in chloroplasts. BMC Plant Biol. 2011, 11:133.
173. Machettira A.B., Gross L.E., Sommer M.S., Weis B.L., Englich G., Tripp J., Schleiff E. The localization of Tic20 proteins in Arabidopsis thaliana is not restricted to the inner envelope membrane of chloroplasts. Plant Mol. Biol. 2011, 77:381-390.
174. Hirabayashi Y., Kikuchi S., Oishi M., Nakai M. In vivo studies on the roles of two closely related Arabidopsis Tic20 proteins, AtTic20-I and AtTic20-IV. Plant Cell Physiol. 2011, 52:469-478.
175. Chen X., Smith M.D., Fitzpatrick L., Schnell D.J. In vivo analysis of the role of atTic20 in protein import into chloroplasts. Plant Cell 2002, 14:641-654.
176. Kasmati A.R., Topel M., Patel R., Murtaza G., Jarvis P. Molecular and genetic analyses of Tic20 homologues in Arabidopsis thaliana chloroplasts. Plant J. 2011, 66:877-889.
177. Topel M., Jarvis P. The Tic20 gene family: phylogenetic analysis and evolutionary considerations. Plant Signal. Behav. 2011, 6:1046-1048.
178. Teng Y.S., Su Y.S., Chen L.J., Lee Y.J., Hwang I., Li H.M. Tic21 is an essential translocon component for protein translocation across the chloroplast inner envelope membrane. Plant Cell 2006, 18:2247-2257.
179. Duy D., Wanner G., Meda A.R., von Wiren N., Soll J., Philippar K. PIC1, an ancient permease in Arabidopsis chloroplasts, mediates iron transport. Plant Cell 2007, 19:986-1006.
180. Duy D., Stube R., Wanner G., Philippar K. The chloroplast permease PIC1 regulates plant growth and development by directing homeostasis and transport of iron. Plant Physiol. 2011, 155:1709-1722.
181. Lv H.X., Guo G.Q., Yang Z.N. Translocons on the inner and outer envelopes of chloroplasts share similar evolutionary origin in Arabidopsis thaliana. J. Evol. Biol. 2009, 22:1418-1428.
182. Lubeck J., Soll J., Akita M., Nielsen E., Keegstra K. Topology of IEP110, a component of the chloroplastic protein import machinery present in the inner envelope membrane. EMBO J. 1996, 15:4230-4238.
183. Lubeck J., Heins L., Soll J. A nuclear-coded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle. J. Cell Biol. 1997, 137:1279-1286.
184. Kessler F., Blobel G. Interaction of the protein import and folding machineries of the chloroplast. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:7684-7689.
185. Jackson D.T., Froehlich J.E., Keegstra K. The hydrophilic domain of Tic110, an inner envelope membrane component of the chloroplastic protein translocation apparatus, faces the stromal compartment. J. Biol. Chem. 1998, 273:16583-16588.
186. Inaba T., Li M., Alvarez-Huerta M., Kessler F., Schnell D.J. atTic110 functions as a scaffold for coordinating the stromal events of protein import into chloroplasts. J. Biol. Chem. 2003, 278:38617-38627.
187. Balsera M., Goetze T.A., Kovacs-Bogdan E., Schurmann P., Wagner R., Buchanan B.B., Soll J., Bolter B. Characterization of Tic110, a channel-forming protein at the inner envelope membrane of chloroplasts, unveils a response to Ca(2+) and a stromal regulatory disulfide bridge. J. Biol. Chem. 2009, 284:2603-2616.
188. Li M., Schnell D.J. Reconstitution of protein targeting to the inner envelope membrane of chloroplasts. J. Cell Biol. 2006, 175:249-259.
189. Vojta L., Soll J., Bolter B. Requirements for a conservative protein translocation pathway in chloroplasts. FEBS Lett. 2007, 581:2621-2624.
190. Chou M.L., Chu C.C., Chen L.J., Akita M., Li H.M. Stimulation of transit-peptide release and ATP hydrolysis by a cochaperone during protein import into chloroplasts. J. Cell Biol. 2006, 175:893-900.
191. Caliebe A., Grimm R., Kaiser G., Lubeck J., Soll J., Heins L. The chloroplastic protein import machinery contains a Rieske-type iron-sulfur cluster and a mononuclear iron-binding protein. EMBO J. 1997, 16:7342-7350.
192. Stahl T., Glockmann C., Soll J., Heins L. Tic40, a new "old" subunit of the chloroplast protein import translocon. J. Biol. Chem. 1999, 274:37467-37472.
193. Kuchler M., Decker S., Hormann F., Soll J., Heins L. Protein import into chloroplasts involves redox-regulated proteins. EMBO J. 2002, 21:6136-6145.
194. Van Den Wijngaard P.W., Vredenberg W.J. The envelope anion channel involved in chloroplast protein import is associated with Tic110. J. Biol. Chem. 1999, 274:25201-25204.
195. Heins L., Mehrle A., Hemmler R., Wagner R., Kuchler M., Hormann F., Sveshnikov D., Soll J. The preprotein conducting channel at the inner envelope membrane of plastids. EMBO J. 2002, 21:2616-2625.
196. Inaba T., Alvarez-Huerta M., Li M., Bauer J., Ewers C., Kessler F., Schnell D.J. Arabidopsis tic110 is essential for the assembly and function of the protein import machinery of plastids. Plant Cell 2005, 17:1482-1496.
197. Kovacheva S., Bedard J., Patel R., Dudley P., Twell D., Rios G., Koncz C., Jarvis P. In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J. 2005, 41:412-428.
198. Ko K., Budd D., Wu C., Seibert F., Kourtz L., Ko Z.W. Isolation and characterization of a cDNA clone encoding a member of the Com44/Cim44 envelope components of the chloroplast protein import apparatus. J. Biol. Chem. 1995, 270:28601-28608.
199. Wu C., Seibert F.S., Ko K. Identification of chloroplast envelope proteins in close physical proximity to a partially translocated chimeric precursor protein. J. Biol. Chem. 1994, 269:32264-32271.
200. Pang P., Meathrel K., Ko K. A component of the chloroplast protein import apparatus functions in bacteria. J. Biol. Chem. 1997, 272:25623-25627.
201. Tripp J., Inoue K., Keegstra K., Froehlich J.E. A novel serine/proline-rich domain in combination with a transmembrane domain is required for the insertion of AtTic40 into the inner envelope membrane of chloroplasts. Plant J. 2007, 52:824-838.
202. Chiu C.C., Li H.M. Tic40 is important for reinsertion of proteins from the chloroplast stroma into the inner membrane. Plant J. 2008, 56:793-801.
203. Chou M.L., Fitzpatrick L.M., Tu S.L., Budziszewski G., Potter-Lewis S., Akita M., Levin J.Z., Keegstra K., Li H.M. Tic40, a membrane-anchored co-chaperone homolog in the chloroplast protein translocon. EMBO J. 2003, 22:2970-2980.
204. Bedard J., Kubis S., Bimanadham S., Jarvis P. Functional similarity between the chloroplast translocon component, Tic40, and the human co-chaperone, Hsp70-interacting protein (Hip). J. Biol. Chem. 2007, 282:21404-21414.
205. Brautigam A., Weber A.P. Proteomic analysis of the proplastid envelope membrane provides novel insights into small molecule and protein transport across proplastid membranes. Mol. Plant 2009, 2:1247-1261.
206. von Zychlinski A., Kleffmann T., Krishnamurthy N., Sjolander K., Baginsky S., Gruissem W. Proteome analysis of the rice etioplast: metabolic and regulatory networks and novel protein functions. Mol. Cell. Proteomics 2005, 4:1072-1084.
207. Singh N.D., Li M., Lee S.B., Schnell D., Daniell H. Arabidopsis Tic40 expression in tobacco chloroplasts results in massive proliferation of the inner envelope membrane and upregulation of associated proteins. Plant Cell 2008, 20:3405-3417.
208. Ko K., Taylor D., Argenton P., Innes J., Pedram B., Seibert F., Granell A., Ko Z. Evidence that the plastid translocon Tic40 components possess modulating capabilities. J. Biol. Chem. 2005, 280:215-224.
209. Dun X., Zhou Z., Xia S., Wen J., Yi B., Shen J., Ma C., Tu J., Fu T. BnaC.Tic40, a plastid inner membrane translocon originating from Brassica oleracea, is essential for tapetal function and microspore development in Brassica napus. Plant J. 2011, 68:532-545.
210. Zhou Z., Dun X., Xia S., Shi D., Qin M., Yi B., Wen J., Shen J., Ma C., Tu J., Fu T. BnMs3 is required for tapetal differentiation and degradation, microspore separation, and pollen-wall biosynthesis in Brassica napus. J. Exp. Bot. 2012, 63:2041-2058.
211. Young N.D., Debelle F., Oldroyd G.E., Geurts R., Cannon S.B., Udvardi M.K., Benedito V.A., Mayer K.F., Gouzy J., Schoof H., Van de Peer Y., Proost S., Cook D.R., Meyers B.C., Spannagl M., Cheung F., De Mita S., Krishnakumar V., Gundlach H., Zhou S., Mudge J., Bharti A.K., Murray J.D., Naoumkina M.A., Rosen B., Silverstein K.A., Tang H., Rombauts S., Zhao P.X., Zhou P., Barbe V., Bardou P., Bechner M., Bellec A., Berger A., Berges H., Bidwell S., Bisseling T., Choisne N., Couloux A., Denny R., Deshpande S., Dai X., Doyle J.J., Dudez A.M., Farmer A.D., Fouteau S., Franken C., Gibelin C., Gish J., Goldstein S., Gonzalez A.J., Green P.J., Hallab A., Hartog M., Hua A., Humphray S.J., Jeong D.H., Jing Y., Jocker A., Kenton S.M., Kim D.J., Klee K., Lai H., Lang C., Lin S., Macmil S.L., Magdelenat G., Matthews L., McCorrison J., Monaghan E.L., Mun J.H., Najar F.Z., Nicholson C., Noirot C., O'Bleness M., Paule C.R., Poulain J., Prion F., Qin B., Qu C., Retzel E.F., Riddle C., Sallet E., Samain S., Samson N., Sanders I., Saurat O., Scarpelli C., Schiex T., Segurens B., Severin A.J., Sherrier D.J., Shi R., Sims S., Singer S.R., Sinharoy S., Sterck L., Viollet A., Wang B.B., Wang K., Wang M., Wang X., Warfsmann J., Weissenbach J., White D.D., White J.D., Wiley G.B., Wincker P., Xing Y., Yang L., Yao Z., Ying F., Zhai J., Zhou L., Zuber A., Denarie J., Dixon R.A., May G.D., Schwartz D.C., Rogers J., Quetier F., Town C.D., Roe B.A. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 2011, 480:520-524.
212. Benz J.P., Soll J., Bolter B. Protein transport in organelles: the composition, function and regulation of the Tic complex in chloroplast protein import. FEBS J. 2009, 276:1166-1176.
213. Bartsch S., Monnet J., Selbach K., Quigley F., Gray J., von Wettstein D., Reinbothe S., Reinbothe C. Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4933-4938.
214. Tanaka R., Hirashima M., Satoh S., Tanaka A. The Arabidopsis-accelerated cell death gene ACD1 is involved in oxygenation of pheophorbide a: inhibition of the pheophorbide a oxygenase activity does not lead to the "stay-green" phenotype in Arabidopsis. Plant Cell Physiol. 2003, 44:1266-1274.
215. Gray J., Wardzala E., Yang M., Reinbothe S., Haller S., Pauli F. A small family of LLS1-related non-heme oxygenases in plants with an origin amongst oxygenic photosynthesizers. Plant Mol. Biol. 2004, 54:39-54.
216. Boij P., Patel R., Garcia C., Jarvis P., Aronsson H. In vivo studies on the roles of Tic55-related proteins in chloroplast protein import in Arabidopsis thaliana. Mol. Plant 2009, 2:1397-1409.
217. Stengel A., Benz J.P., Buchanan B.B., Soll J., Bolter B. Preprotein import into chloroplasts via the Toc and Tic complexes is regulated by redox signals in Pisum sativum. Mol. Plant 2009, 2:1181-1197.
218. Kovacs-Bogdan E., Soll J., Bolter B. Protein import into chloroplasts: the Tic complex and its regulation. Biochim. Biophys. Acta 2010, 1803:740-747.
219. Stengel A., Benz P., Balsera M., Soll J., Bolter B. TIC62 redox-regulated translocon composition and dynamics. J. Biol. Chem. 2008, 283:6656-6667.
220. Benz J.P., Stengel A., Lintala M., Lee Y.H., Weber A., Philippar K., Gugel I.L., Kaieda S., Ikegami T., Mulo P., Soll J., Bolter B. Arabidopsis Tic62 and ferredoxin-NADP(H) oxidoreductase form light-regulated complexes that are integrated into the chloroplast redox poise. Plant Cell 2009, 21:3965-3983.
221. Alte F., Stengel A., Benz J.P., Petersen E., Soll J., Groll M., Bolter B. Ferredoxin:NADPH oxidoreductase is recruited to thylakoids by binding to a polyproline type II helix in a pH-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:19260-19265.
222. Balsera M., Stengel A., Soll J., Bolter B. Tic62: a protein family from metabolism to protein translocation. BMC Evol. Biol. 2007, 7:43.
223. Chigri F., Hormann F., Stamp A., Stammers D.K., Bolter B., Soll J., Vothknecht U.C. Calcium regulation of chloroplast protein translocation is mediated by calmodulin binding to Tic32. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:16051-16056.
224. Chigri F., Soll J., Vothknecht U.C. Calcium regulation of chloroplast protein import. Plant J. 2005, 42:821-831.
225. Nada A., Soll J. Inner envelope protein 32 is imported into chloroplasts by a novel pathway. J. Cell Sci. 2004, 117:3975-3982.
226. Scott S.V., Theg S.M. A new chloroplast protein import intermediate reveals distinct translocation machineries in the two envelope membranes: energetics and mechanistic implications. J. Cell Biol. 1996, 132:63-75.
227. Chiu C.C., Chen L.J., Li H.M. Pea chloroplast DnaJ-J8 and Toc12 are encoded by the same gene and localized in the stroma. Plant Physiol. 2010, 154:1172-1182.
228. Ratnayake R.M., Inoue H., Nonami H., Akita M. Alternative processing of Arabidopsis Hsp70 precursors during protein import into chloroplasts. Biosci. Biotechnol. Biochem. 2008, 72:2926-2935.
229. Huang X.Q., Miller W. A time-efficient, linear-space local similarity algorithm. Adv. Appl. Math. 1991, 12:337-357.