In vivo analyses of the roles of essential Omp85-related proteins in the chloroplast outer envelope membrane

Plant Physiology

Volumn 157, Issue 1, 2011, Pages 147-159

  Huang, Weihua ^a,c   Ling, Qihua ^a   Bédard, Jocelyn ^a   Lilley, Kathryn ^b,d   Jarvis, Paul ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; PISUM SATIVUM;

EID: 80052411081     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.181891     Document Type: Article

References (56)

1. Agne B, Andrès C, Montandon C, Christ B, Ertan A, Jung F, Infanger S, Bischof S, Baginsky S, Kessler F (2010) The acidic A-domain of Arabidopsis TOC159 occurs as a hyperphosphorylated protein. Plant Physiol 153: 1016-1030
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410
3. Aronsson H, Boij P, Patel R, Wardle A, Töpel M, Jarvis P (2007) Toc64/OEP64 is not essential for the efficient import of proteins into chloroplasts in Arabidopsis thaliana. Plant J 52: 53-68
4. Aronsson H, Combe J, Jarvis P (2003) Unusual nucleotide-binding properties of the chloroplast protein import receptor, atToc33. FEBS Lett 544: 79-85
5. Aronsson H, Jarvis P (2002) A simple method for isolating import-competent Arabidopsis chloroplasts. FEBS Lett 529: 215-220
6. Baldwin A, Wardle A, Patel R, Dudley P, Park SK, Twell D, Inoue K, Aarvis P (2005) A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiol 138: 715-733
7. Bauer J, Chen K, Hiltbunner A, Wehrli E, Eugster M, Schnell D, Kessler F (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 403: 203-207
8. Bédard J, Kubis S, Bimanadham S, Jarvis P (2007) Functional similarity between the chloroplast translocon component, Tic40, and the human co-chaperone, Hsp70-interacting protein (Hip). J Biol Chem 282: 21404-21414
9. Bolender N, Sickmann A, Wagner R, Meisinger C, Pfanner N (2008) Multiple pathways for sorting mitochondrial precursor proteins. EMBO Rep 9: 42-49
10. Bos MP, Robert V, Tommassen J (2007) Functioning of outer membrane protein assembly factor Omp85 requires a single POTRA domain. EMBO Rep 8: 1149-1154
11. Bredemeier R, Schlegel T, Ertel F, Vojta A, Borissenko L, Bohnsack MT, Groll M, von Haeseler A, Schleiff E (2007) Functional and phylogenetic properties of the pore-forming beta-barrel transporters of the Omp85 family. J Biol Chem 282: 1882-1890
12. Chiu CC, Li HM (2008) Tic40 is important for reinsertion of proteins from the chloroplast stroma into the inner membrane. Plant J 56: 793-801
13. Chou ML, Fitzpatrick LM, Tu SL, Budziszewski G, Potter-Lewis S, Akita M, Levin JZ, Keegstra K, Li HM (2003) Tic40, a membrane-anchored cochaperone homolog in the chloroplast protein translocon. EMBO J 22: 2970-2980
14. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium- mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
15. Constan D, Patel R, Keegstra K, Jarvis P (2004) An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J 38: 93-106
16. Dávila-Aponte JA, Inoue K, Keegstra K (2003) Two chloroplastic protein translocation components, Tic110 and Toc75, are conserved in different plastid types from multiple plant species. Plant Mol Biol 51: 175-181
17. Eckart K, Eichacker L, Sohrt K, Schleiff E, Heins L, Soll J (2002) A Toc75- like protein import channel is abundant in chloroplasts. EMBO Rep 3:557-562
18. Ertel F, Mirus O, Bredemeier R, Moslavac S, Becker T, Schleiff E (2005) The evolutionarily related beta-barrel polypeptide transporters from Pisum sativum and Nostoc PCC7120 contain two distinct functional domains. J Biol Chem 280: 28281-28289
19. Fourrier N, Bédard J, Lopez-Juez E, Barbrook A, Bowyer J, Jarvis P, Warren G, Thorlby G (2008) A role for SENSITIVE TO FREEZING2 in protecting chloroplasts against freeze-induced damage in Arabidopsis. Plant J 55: 734-745
20. Gentle IE, Burri L, Lithgow T (2005) Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58: 1216-1225
21. Goldberg RB, de Paiva G, Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266: 605-614
22. Habib SJ, Waizenegger T, Niewienda A, Paschen SA, Neupert W, Rapaport D (2007) The N-terminal domain of Tob55 has a receptorlike function in the biogenesis of mitochondrial beta-barrel proteins. J Cell Biol 176: 77-88
23. Hill K, Model K, Ryan MT, Dietmeier K, Martin F, Wagner R, Pfanner N (1998) Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins [see comment]. Nature 395: 516-521
24. Hinnah SC, Wagner R, Sveshnikova N, Harrer R, Soll J (2002) The chloroplast protein import channel Toc75: pore properties and interaction with transit peptides. Biophys J 83: 899-911
25. Hofmann NR, Theg SM (2005) Chloroplast outer membrane protein targeting and insertion. Trends Plant Sci 10: 450-457
26. Hsu SC, Patel R, Bédard J, Jarvis P, Inoue K (2008) Two distinct Omp85 paralogs in the chloroplast outer envelope membrane are essential for embryogenesis in Arabidopsis thaliana. Plant Signal Behav 3: 1134-1135
27. Hust B, Gutensohn M (2006) Deletion of core components of the plastid protein import machinery causes differential arrest of embryo development in Arabidopsis thaliana. Plant Biol (Stuttg) 8: 18-30
28. Inaba T, Schnell DJ (2008) Protein trafficking to plastids: one theme, many variations. Biochem J 413: 15-28
29. Inoue K, Potter D (2004) 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: 354-365
30. Ivanova Y, Smith MD, Chen K, Schnell DJ (2004) Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol Biol Cell 15: 3379-3392
31. Jackson-Constan D, Keegstra K (2001) Arabidopsis genes encoding components of the chloroplastic protein import apparatus. Plant Physiol 125: 1567-1576
32. Jarvis P (2008) Targeting of nucleus-encoded proteins to chloroplasts in plants. New Phytol 179: 257-285
33. Jarvis P, Chen LJ, Li H, Peto CA, Fankhauser C, Chory J (1998) An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 282: 100-103
34. Kessler F, Schnell DJ (2006) The function and diversity of plastid protein import pathways: a multilane GTPase highway into plastids. Traffic 7: 248-257
35. Kikuchi S, Hirohashi T, Nakai M(2006) Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE. Plant Cell Physiol 47: 363-371
36. Kouranov A, Chen X, Fuks B, Schnell DJ (1998) Tic20 and Tic22 are new components of the protein import apparatus at the chloroplast inner envelope membrane. J Cell Biol 143: 991-1002
37. Kovacheva S, Bédard J, Patel R, Dudley P, Twell D, Rios G, Koncz C, Jarvis P (2005) In vivo studies on the roles of Tic110, Tic40 and Hsp93 during chloroplast protein import. Plant J 41: 412-428
38. Kubis S, Baldwin A, Patel R, Razzaq A, Dupree P, Lilley K, Kurth J, Leister D, Jarvis P (2003) The Arabidopsis ppi1 mutant is specifically defective in the expression, chloroplast import, and accumulation of photosynthetic proteins. Plant Cell 15: 1859-1871
39. Kubis S, Patel R, Combe J, Bédard J, Kovacheva S, Lilley K, Biehl A, Leister D, Ríos G, Koncz C, et al (2004) Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 16: 2059-2077
40. Kubis SE, Lilley KS, Jarvis P (2008) Isolation and preparation of chloroplasts from Arabidopsis thaliana plants. Methods Mol Biol 425: 171-186
41. Meyer U, Kollner B, Willenbrink J, Krause GHM (1997) Physiological changes on agricultural crops induced by different ambient ozone exposure regimes. I. Effects on photosynthesis and assimilate allocation in spring wheat. New Phytol 136: 645-652
42. Patel R, Hsu SC, Bédard J, Inoue K, Jarvis P (2008) The Omp85-related chloroplast outer envelope protein OEP80 is essential for viability in Arabidopsis. Plant Physiol 148: 235-245
43. Sánchez-Pulido L, Devos D, Genevrois S, Vicente M, Valencia A (2003) POTRA: a conserved domain in the FtsQ family and a class of betabarrel outer membrane proteins. Trends Biochem Sci 28: 523-526
44. Schleiff E, Soll J (2005) Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep 6: 1023-1027
45. Schleiff E, Soll J, Küchler M, Kühlbrandt W, Harrer R (2003) Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol 160: 541-551
46. Schnell DJ, Blobel G, Keegstra K, Kessler F, Ko K, Soll J (1997) A consensus nomenclature for the protein-import components of the chloroplast envelope. Trends Cell Biol 7: 303-304
47. Schnell DJ, Kessler F, Blobel G (1994) Isolation of components of the chloroplast protein import machinery. Science 266: 1007-1012
48. Smith MD (2006) Protein import into chloroplasts: an ever-evolving story. Can J Bot 84: 531-542
49. Soll J, Schleiff E (2004) Protein import into chloroplasts. Nat Rev Mol Cell Biol 5: 198-208
50. Stanga JP, Boonsirichai K, Sedbrook JC, Otegui MS, Masson PH (2009) A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiol 149: 1896-1905
51. Summer EJ, Cline K (1999) 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 119: 575-584
52. Sveshnikova N, Grimm R, Soll J, Schleiff E (2000) Topology studies of the chloroplast protein import channel Toc75. Biol Chem 381: 687-693
53. Tranel PJ, Froehlich J, Goyal A, Keegstra K (1995) A component of the chloroplastic protein import apparatus is targeted to the outer envelope membrane via a novel pathway. EMBO J 14: 2436-2446
54. Tu SL, Chen LJ, Smith MD, Su YS, Schnell DJ, Li HM (2004) Import pathways of chloroplast interior proteins and the outer-membrane protein OEP14 converge at Toc75. Plant Cell 16: 2078-2088
55. Wallas TR, Smith MD, Sanchez-Nieto S, Schnell DJ (2003) The roles of toc34 and toc75 in targeting the toc159 preprotein receptor to chloroplasts. J Biol Chem 278: 44289-44297
56. Wielopolska A, Townley H, Moore I, Waterhouse P, Helliwell C (2005) A high-throughput inducible RNAi vector for plants. Plant Biotechnol J 3: 583-590