Emerging roles of the chloroplast outer envelope membrane

Trends in Plant Science

Volumn 16, Issue 10, 2011, Pages 550-557

  Inoue, Kentaro ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; VEGETABLE PROTEIN;

BIOLOGICAL MODEL; CHLOROPLAST; INTRACELLULAR MEMBRANE; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT; REVIEW; ULTRASTRUCTURE;

ACTINS; CHLOROPLASTS; INTRACELLULAR MEMBRANES; LIPID METABOLISM; MODELS, BIOLOGICAL; PLANT PROTEINS; PROTEIN TRANSPORT;

CYANOBACTERIA; EUKARYOTA;

EID: 80053307548     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2011.06.005     Document Type: Review

References (94)

1. Dyall S.D., et al. Ancient invasions: from endosymbionts to organelles. Science 2004, 304:253-257.
2. Thomson W.W., Whatley J.M. Nongreen plastids. Annu. Rev. Plant Physiol. 1980, 31:375-394.
3. Mühlethaler K., Frey-Wyssling A. Entwicklung und Struktur der Proplastiden. J. Biophys. Biochem. Cytol. 1959, 6:507-512.
4. Joyard J., et al. The biochemical machinery of plastid envelope membranes. Plant Physiol. 1998, 118:715-723.
5. Duy D., et al. Solute channels of the outer membrane: from bacteria to chloroplasts. Biol. Chem. 2007, 388:879-889.
6. Inoue K. The chloroplast outer envelope membrane: the edge of light and excitement. J. Integr. Plant Biol. 2007, 49:1100-1111.
7. Kessler F., Schnell D. Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Curr. Opin. Cell Biol. 2009, 21:494-500.
8. Li H.M., Chiu C.C. Protein transport into chloroplasts. Annu. Rev. Plant Biol. 2010, 61:157-180.
9. Strittmatter P., et al. The chloroplast protein import machinery: a review. Methods Mol. Biol. 2010, 619:307-321.
10. Schleiff E., Becker T. Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat. Rev. Mol. Cell Biol. 2011, 12:48-59.
11. Reumann S., et al. Evolution of the general protein import pathway of plastids. Mol. Membr. Biol. 2005, 22:73-86.
12. Inoue K., et al. Complete maturation of the plastid protein translocation channel requires a type I signal peptidase. J. Cell Biol. 2005, 171:425-430.
13. Soll J., Tien R. Protein translocation into and across the chloroplastic envelope membranes. Plant Mol. Biol. 1998, 38:191-207.
14. Jarvis P., et al. An Arabidopsis mutant defective in the plastid general protein import apparatus. Science 1998, 282:100-103.
15. Gutensohn M., et al. Functional analysis of the two Arabidopsis homologues of Toc34, a component of the chloroplast protein import apparatus. Plant J. 2000, 23:771-783.
16. Constan D., et al. An outer envelope membrane component of the plastid protein import apparatus plays an essential role in Arabidopsis. Plant J. 2004, 38:93-106.
17. Bauer J., et al. The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature 2000, 403:203-207.
18. Ivanova Y., et al. Members of the Toc159 import receptor family represent distinct pathways for protein targeting to plastids. Mol. Biol. Cell 2004, 15:3379-3392.
19. Kubis S., et al. Functional specialization amongst the Arabidopsis Toc159 family of chloroplast protein import receptors. Plant Cell 2004, 16:2059-2077.
20. Smith M.D., et al. atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J. Cell Biol. 2004, 165:323-334.
21. Inoue H., et al. The molecular basis for distinct pathways for protein import into Arabidopsis chloroplasts. Plant Cell 2010, 22:1947-1960.
22. Hernández Torres J., et al. 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.
23. Richardson L.G., et al. The acidic domains of the Toc159 chloroplast preprotein receptor family are intrinsically disordered protein domains. BMC Biochem. 2009, 10:35.
24. Gsponer J., Babu M.M. The rules of disorder or why disorder rules. Prog. Biophys. Mol. Biol. 2009, 99:94-103.
25. Agne B., et al. The acidic A-domain of Arabidopsis TOC159 occurs as a hyperphosphorylated protein. Plant Physiol. 2010, 153:1016-1030.
26. 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.
27. 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.
28. Kuroiwa T. Mechanisms of organelle division and inheritance and their implications regarding the origin of eukaryotic cells. Proc. Jpn. Acad. Ser. B. Phys. Biol. Sci. 2010, 86:455-471.
29. Maple J., Møller S.G. The complexity and evolution of the plastid-division machinery. Biochem. Soc. Trans. 2010, 38:783-788.
30. Miyagishima S.-Y. Mechanism of plastid division: from a bacterium to an organelle. Plant Physiol. 2011, 155:1533-1544.
31. Kuroiwa T., et al. Vesicle, mitochondrial, and plastid division machineries with emphasis on dynamin and electrondense rings. Int. Rev. Cell Mol. Biol. 2008, 271:97-152.
32. Yoshida Y., et al. Chloroplasts divide by contraction of a bundle of nanofilaments consisting of polyglucan. Science 2010, 329:949-953.
33. Osteryoung K.W., et al. Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 1998, 10:1991-2004.
34. Gao H., et al. ARC5, a cytosolic dynamin like protein from plants, is part of the chloroplast division machinery. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:4328-4333.
35. Miyagishima S.-Y., et al. A plant-specific dynamin-related protein forms a ring at the chloroplast division site. Plant Cell 2003, 15:655-665.
36. Miyagishima S.-Y., et al. PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 2006, 18:2517-2530.
37. Vitha S., et al. ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 2003, 15:1918-1933.
38. Glynn J.M., et al. Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 2008, 20:2460-2470.
39. Glynn J.M., et al. PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J. 2009, 59:700-711.
40. Yang Y., et al. Plastid division: across time and space. Curr. Opin. Plant Biol. 2008, 11:577-584.
41. Okazaki K., et al. The PLASTID DIVISION1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell 2010, 21:1769-1780.
42. Kasahara M., et al. Chloroplast avoidance movement reduces photodamage in plants. Nature 2002, 420:829-832.
43. Kagawa T., Wada M. Blue light-induced chloroplast relocation. Plant Cell Physiol. 2002, 43:367-371.
44. Kagawa T., et al. Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 2001, 291:2138-2141.
45. Oikawa K., et al. Chloroplast unusual positioning1 is essential for proper chloroplast positioning. Plant Cell 2003, 15:2805-2815.
46. Suetsugu N., et al. Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:8860-8865.
47. Oikawa K., et al. Chloroplast outer envelope protein CHUP1 is essential for chloroplast anchorage to the plasma membrane and chloroplast movement. Plant Physiol. 2008, 148:829-842.
48. Schmidt von Braun S., Schleiff E. The chloroplast outer membrane protein CHUP1 interacts with actin and profilin. Planta 2008, 227:1151-1159.
49. Königer M., et al. Light, genotype, and abscisic acid affect chloroplast positioning in guard cells of Arabidopsis thaliana leaves in distinct ways. Photosynth. Res. 2010, 105:213-227.
50. Kadota A., et al. Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:13106-13111.
51. Whippo C.W., et al. THRUMIN1 is a light-regulated actin-bundling protein involved in chloroplast motility. Curr. Biol. 2011, 21:59-64.
52. Morita M.T. Directional gravity sensing in gravitropism. Annu. Rev. Plant Biol. 2010, 61:705-720.
53. Boonsirichai K., et al. ALTERED RESPONSE TO GRAVITY is a peripheral membrane protein that modulates gravity-induced cytoplasmic alkalinization and lateral auxin transport in plant statocytes. Plant Cell 2003, 15:2612-2625.
54. Stanga J.P., et al. A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiol. 2009, 149:1896-1905.
55. Jouhet J., Gray J.C. Interaction of actin and the chloroplast protein import apparatus. J. Biol. Chem. 2009, 284:19132-19141.
56. Moellering E.R., Benning C. Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci. 2011, 16:98-107.
57. Loll B., et al. Towards complete cofactor arrangement in the 3.0Å resolution structure of photosystem II. Nature 2005, 438:1040-1044.
58. Schaller S., et al. The main thylakoid membrane lipid monogalactosyldiacylglycerol (MGDG) promotes the de-epoxidation of violaxanthin associated with the light-harvesting complex of photosystem II (LHCII). Biochim. Biophys. Acta 2010, 1797:414-424.
59. Xu C., et al. Mutation of the TGD1 chloroplast envelope protein affects phosphatidate metabolism in Arabidopsis. Plant Cell 2005, 17:3094-3110.
60. Awai K., et al. Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:10960-10965.
61. Froehlich J.E., et al. The digalactosyldiacylglycerol (DGDG) synthase DGD1 is inserted into the outer envelope membrane of chloroplasts in a manner independent of the general import pathway and does not depend on direct interaction with monogalactosyldiacylglycerol synthase for DGDG biosynthesis. J. Biol. Chem. 2001, 276:31806-31812.
62. Kelly A.A., et al. Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis. Plant Cell 2003, 15:2694-2706.
63. Heemskerk J.W., et al. Turnover of galactolipids incorporated into chloroplast envelopes an assay for galactolipid:galactopilid galactosyltransferase. Biochim. Biophys. Acta 1983, 754:181-189.
64. Benning C., Ohta H. Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J. Biol. Chem. 2005, 280:2397-2400.
65. Moellering E.R., et al. Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 2010, 330:226-228.
66. Warren G., et al. Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 1996, 111:1011-1019.
67. Thorlby G., et al. The SENSITIVE TO FREEZING2 gene, required for freezing tolerance in Arabidopsis thaliana, encodes a beta-glucosidase. Plant Cell 2004, 16:2192-2203.
68. Fourrier N., et al. A role for SENSITIVE TO FREEZING2 in protecting chloroplasts against freeze-induced damage in Arabidopsis. Plant J. 2008, 55:734-745.
69. Steponkus P.L., et al. Transformation of the cryobehavior of rye protoplasts by modification of the plasma membrane lipid composition. Proc. Natl. Acad. Sci. U.S.A. 1988, 85:9026-9030.
70. Browse J. Plant science. Saving the bilayer. Science 2010, 330:185-186.
71. Block M.A., et al. Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization. J. Biol. Chem. 1983, 258:13281-13286.
72. Bruce B.D. The role of lipids in plastid protein transport. Plant Mol. Biol. 1998, 38:223-246.
73. Chen L.J., Li H.M. A mutant deficient in the plastid lipid DGD is defective in protein import into chloroplasts. Plant J. 1998, 16:33-39.
74. Aronsson H., et al. Monogalactosyldiacylglycerol deficiency in Arabidopsis affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves. Plant Physiol. 2008, 148:580-592.
75. Schnell D.J., Blobel G. Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites. J. Cell Biol. 1993, 120:103-115.
76. Gross J., Bhattacharya D. Endosymbiont or host: who drove mitochondrial and plastid evolution?. Biol. Direct. 2011, 6:12.
77. Alcock F., et al. Evolution. Tinkering inside the organelle. Science 2010, 327:649-650.
78. Hsu S.-C., Inoue K. Two evolutionarily conserved essential beta-barrel proteins in the chloroplast outer envelope membrane. Biosci. Trends 2009, 3:168-178.
79. Eckart K., et al. A Toc75-like protein import channel is abundant in chloroplasts. EMBO Rep. 2002, 3:557-562.
80. 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.
81. Bräutigam 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.
82. Morden C.W., Sherwood A.R. Continued evolutionary surprises among dinoflagellates. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11558-11560.
83. Whatley J.M. Chloroplast evolution--ancient and modern. Ann. N.Y. Acad. Sci. 1981, 361:154-165.
84. Whatley J.M., et al. From extracellular to intracellular: the establishment of mitochondria and chloroplasts. Proc. R. Soc. Lond. B 1979, 204:165-187.
85. Berry S. Endosymbiosis and the design of eukaryotic electron transport. Biochim. Biophys. Acta 2003, 1606:57-72.
86. Cavalier-Smith T. The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann. N.Y. Acad. Sci. 1987, 503:55-71.
87. Schleiff E., Soll J. Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep. 2005, 6:1023-1027.
88. Bos M.P., et al. Biogenesis of the gram-negative bacterial outer membrane. Annu. Rev. Microbiol. 2007, 61:191-214.
89. Kutik S., et al. Evolution of mitochondrial protein biogenesis. Biochim. Biophys. Acta 2009, 1790:409-415.
90. Tommassen J. Assembly of outer-membrane proteins in bacteria and mitochondria. Microbiology 2010, 156:2587-2596.
91. Joyard J., et al. Molecular aspects of plastid envelope biochemistry. Eur. J. Biochem. 1991, 199:489-509.
92. Ratnayake R.M., et al. Alternative processing of Arabidopsis Hsp70 precursors during protein import into chloroplasts. Biosci. Biotechnol. Biochem. 2008, 72:2926-2935.
93. Chiu C.C., et al. Pea chloroplast DnaJ-J8 and Toc12 are encoded by the same gene and localized in the stroma. Plant Physiol. 2010, 154:1172-1182.
94. Maple J., et al. Plastid division is mediated by combinatorial assembly of plastid division proteins. Plant J. 2005, 43:811-823.