Import and routing of nucleus-encoded chloroplast proteins

Annual Review of Cell and Developmental Biology

Volumn 12, Issue , 1996, Pages 1-26

  Cline, Kenneth ^a   Henry, Ralph ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

protein transport; SecA; signal peptide; signal recognition particle (SRP); thylakoid membrane

Indexed keywords

ADENOSINE TRIPHOSPHATE; COMPLEMENTARY DNA; ENVELOPE PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE PROTEIN; NUCLEAR PROTEIN; PROTEIN PRECURSOR; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE;

ALGA; BACTERIAL MEMBRANE; CELL NUCLEUS MEMBRANE; CHLOROPLAST; ENDOPLASMIC RETICULUM; HIGHER PLANT; NONHUMAN; PLASTID; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN SYNTHESIS; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; THYLAKOID; THYLAKOID MEMBRANE;

AMINO ACID SEQUENCE; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CHLOROPLASTS; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PLANTS;

ALGAE; BACTERIA (MICROORGANISMS); EMBRYOPHYTA; PROKARYOTA;

EID: 0029731659     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.12.1.1     Document Type: Review

References (104)

1. Bassham DC, Bartling D, Mould RM, Dunbar B, Weisbeek P, et al. 1991. Transport of proteins into chloroplasts: delineation of envelope "transit" and thylakoid "transfer" signals within the presequences of three imported thylakoid lumen proteins. J. Biol. Chem. 266(35):23606-10
2. Bauerle C, Dorl J, Keegstra K. 1991. Kinetic analysts of the transport of thylakoid lumenal proteins in experiments using intact chloroplasts. J. Biol. Chem. 266(9):5884-90
3. Berghöfer J, Karnauchov I, Herrmann RG, Klösgen RB. 1995. Isolation and characterization of a cDNA encoding the secA protein from spinach chloroplasts. J. Biol. Chem. 270(31):18341-46
4. Bourne HR, Sanders DA, McCormick F. 1991. The GTPase superfamily: conserved structure and molecular mechanism. Nature 349:117-27
5. Brink S, Fischer K, Klösgen RB, Flügge U-I. 1995. Sorting of nuclear-encoded chloroplast membrane proteins to the envelope and the thylakoid membrane. J. Biol. Chem. 270(35):20808-15
6. Bulychev A, Pilon M, Dassen H, van't Hof R, Vredenberg W, de Kruijff B. 1994. Precursor-mediated opening of translocation pores in chloroplast envelopes. FEBS Lett. 356:204-6
7. Chaddock AM, Mant A, Karnauchov I, Brink S, Herrmann RG, et al. 1995. A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the ΔpH-dependent thylakoidal protein translocase. EMBO J. 14(12):2715-22
8. Clausmeyer S, Klösgen RB, Herrmann RG. 1993. Protein import into chloroplasts: the hydrophilic lumenal proteins exhibit unexpected import and sorting specificities in spite of structurally conserved transit peptides. J. Biol. Chem. 268(19):13869-76
9. Cline K. 1986. Membrane integration of a thylakoid precursor protein reconstituted in chloroplast lysates. J. Biol. Chem. 261(31):14804-10
10. Cline K, Ettinger WF, Theg SM. 1992a. Protein-specific energy requirements for protein transport across or into thylakoid membranes. J. Biol. Chem. 267(4):2688-96
11. Cline K, Fulsom DR, Viitanen PV. 1989. An imported thylakoid protein accumulates in the stroma when insertion into thylakoids is inhibited. J. Biol. Chem. 264(24):14225-32
12. Cline K, Henry R, Li CJ, Yuan J. 1992b. Pathways and intermediates for the biogenesis of nuclear-encoded thylakoid proteins. In Research in Photosynthesis, ed. N Murata, 3:149-56. The Netherlands: Kluwer
13. Cline K, Henry R, Li C, Yuan J. 1993. Multiple pathways for protein transport into or across the thylakoid membrane. EMBO J. 12(11):4105-14
14. Cline K, Keegstra K, Staehelin LA. 1985. Freeze-fracture electron microscopic analysis of ultrarapidly frozen envelope membranes on intact chloroplasts and after purification. Protoplasma 125:111-23
15. Creighton AM, Hulford A, Mant A, Robinson D, Robinson C. 1995. A monomeric, tightly folded stromal intermediate on the ΔpH-dependent thylakoidal protein transport pathway. J. Biol. Chem. 270(4):1663-69
16. Creissen G, Reynolds H, Xue Y, Mullineaux P. 1995. Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria in transgenic tobacco. Plant J. 8(2):167-75
17. de Boer AD, Weisbeek PJ. 1991. Chloroplast protein topogenesis: import, sorting and assembly. Biochim. Biophys. Acta 1071:221-53
18. Dobberstein B. 1994. On the beaten pathway. Nature 367:599-600
19. Endo T, Kawamura K, Naka M. 1992. The chloroplast-targeting domain of plastocyanin transit peptide can form a helical structure but does not have a high affinity for lipid bilayers. Eur. J. Biochem. 207:671-75
20. Fischer K, Weber A, Arbinger B, Brink S, Eckerskorn C, Flügge U-I. 1994. The 24 kDa outer envelope membrane protein from spinach chloroplasts: molecular cloning, in vivo expression and import pathways of a protein with unusual properties. Plant Mol. Biol. 25:167-77
21. Franklin AE, Hoffman NE. 1993. Characterization of a chloroplast homologue of the 54-kDa subunit of the signal recognition particle. J. Biol. Chem. 268(29):22175-80
22. Friedman AL, Keegstra K. 1989. Chloroplast protein import: quantitative analysis of precursor binding. Plant Physiol. 89:993-99
23. Glick BS. 1995. Can Hsp70 proteins act as force-generating motors? Cell 80:11-14
24. Glick BS, Brandt A, Cunningham K, Müller S, Hallberg RL, et al. 1992. Cytochromes c1 and b2 are sorted to the intermembrane space of yeast mitochondria by a stop-transfer mechanism. Cell 69:809-22
25. Gray JC, Row PE. 1995. Protein translocation across chloroplast envelope membranes. Trends Cell Biol. 5:243-47
26. Hageman J, Baecke C, Ebskamp M, Pilon R, Smeekens S, Weisbeek P. 1990. Protein import into and sorting inside the chloroplast are independent processes. Plant Cell 2:479-94
27. Halpin C, Elderfield PD, James HE, Zimmerman R, Dunbar B, Robinson C. 1989. The reaction specificities of the thylakoidal processing peptidase and Escherichia coli leader peptidase are identical. EMBO J. 8(12):3917-21
28. Hartl FU, Neupert W. 1990. Protein sorting to mitochondria: evolutionary conservations of folding and assembly. Science 247:930-38
29. Henry R, Kapazoglou A, McCaffery M, Cline K. 1994. Differences between lumen targeting domains of chloroplast transit peptides determine pathway specificity for thylakoid transport. J. Biol. Chem. 269(14):10189-92
30. Hirsch S, Muckel E, Heemeyer F, von Heijne G, Soll J. 1994. A receptor component of the chloroplast protein translocation machinery. Science 266:1989-92
31. Hoffman NE, Franklin AE. 1994. Evidence for a stromal GTP requirement for the integration of a chlorophyll a/b binding polypeptide into thylakoid membranes. Plant Physiol. 105:295-304
32. Hoober JK, Boyd CO, Paavola LG. 1991. Origin of thylakoid membranes in Chlamydomonas reinhardtii y-1 at 38°C. Plant Physiol. 96:1321-28
33. Howe G, Merchant S. 1993. Maturation of thylakoid lumen proteins proceeds posttranslationally through an intermediate in vivo. Proc. Natl. Acad. Sci. USA 90:1862-66
34. Hugueney P, Bouvier F, Badillo A, d'Harlingue A, Kuntz M, Camara B. 1995. Identification of a plastid protein involved in vesicle fusion and/or membrane protein translocation. Proc. Natl. Acad. Sci. USA 92:5630-34
35. Hulford A, Hazell L, Mould RM, Robinson C. 1994. Two distinct mechanisms for the translocation of proteins across the thylakoid membrane, one requiring the presence of a stromal protein factor and nucleotide triphosphates. J. Biol. Chem. 269(5):3251-56
36. Hwang ST, Wachter C, Schatz G. 1991. Protein import into the yeast mitochondrial matrix: a new translocation intermediate between the two mitochondrial membranes. J. Biol. Chem. 266(31):21083-89
37. Karnauchov I, Cai D, Schmidt I, Herrmann RG, Klösgen RB. 1994. The thylakoid translocation of subunit 3 of photosystem I, the psaF gene product, depends on a bipartite transit peptide and proceeds along an azide-sensitive pathway. J. Biol. Chem. 269(52):32871-78
38. Keegstra K, Bruce B, Hurley M, Li HM, Perry S. 1995. Targeting of proteins into chloroplasts. Physiol. Plant. 93:157-62
39. Kessler F, Blobel G, Patel HA, Schnell DJ. 1994. Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 266:1035-39
40. Kirwin PM, Meadows JW, Shackleton JB, Musgrove JE, Elderfield PD, et al. 1989. ATP-dependent import of a lumenal protein by isolated thylakoid vesicles. EMBO J. 8(8):2251-55
41. Knight JS, Gray JC. 1995. The N-terminal hydrophobic region of the mature phosphate translocator is sufficient for targeting to the chloroplast inner envelope membrane. Plant Cell 7:1421-32
42. Knight JS, Madueño F, Gray JC. 1993. Import and sorting of proteins by chloroplasts. Biochem. Soc. Trans. 21:31-36
43. Knott TG, Robinson C. 1994. The secA inhibitor, azide, reversibly blocks the translocation of a subset of proteins across the chloroplast thylakoid membrane. J. Biol. Chem. 269(11):7843-46
44. Ko K, Cashmore AR. 1989. Targeting of proteins to the thylakoid lumen by the bipartite transit peptide of the 33 kd oxygen-evolving protein. EMBO J. 8(11):3187-94
45. Konishi T, Watanabe A. 1993. Transport of proteins into the thylakoid lumen: stromal processing and energy requirements for the import of the precursor to the 23-kDa protein of PS II. Plant Cell Physiol. 34(2):315-19
46. Kuhn A, Kiefer D, Köhne C, Zhu HY, Tschantz WR, Dalbey RE. 1994. Evidence for a loop-like insertion mechanism of pro-Omp A into the inner membrane of Escherichia coli. Eur. J. Biochem. 226:891-97
47. Laidler V, Chaddock AM, Knott TG, Walker D, Robinson C. 1995. A secY homolog in Arabidopsis thaliana. J. Biol. Chem. 270(30):17664-67
48. Li HM, Moore T, Keegstra K. 1991. Targeting of proteins to the outer envelope membrane uses a different pathway than transport into chloroplasts. Plant Cell 3:709-17
49. Li HM, Sullivan TD, Keegstra K. 1992. Information for targeting to the chloroplastic inner envelope membrane is contained in the mature region of the maize Bt1-encoded protein. J. Biol. Chem. 267(26):18999-9004
50. Li X, Henry R, Yuan J, Cline K, Hoffman NE. 1995. A chloroplast homologue of the signal recognition particle subunit SRP54 is involved in the posttranslational integration of a protein into thylakoid membranes. Proc. Natl. Acad. Sci. USA 92:3789-93
51. Madueno F, Bradshaw SA, Gray JC. 1994. The thylakoid-targeting domain of the chloroplast Rieske iron-sulfur protein is located in the N-terminal hydrophobic region of the mature protein. J. Biol. Chem. 269(26):17458-63
52. Madueño F, Napier JA, Gray JC. 1993. Newly imported Rieske iron-sulfur protein associates with both cpn60 and hsp70 in the chloroplast stroma. Plant Cell 5:1865-76
53. Mant A, Nielsen VS, Knott TG, Möller BL, Robinson C. 1994. Multiple mechanisms for the targeting of photosystem I subunits F, H, K, L, and N into and across the thylakoid membrane. J. Biol. Chem. 269(44):27303-9
54. Michl D, Robinson C, Shackleton JB, Herrmann RG, Klösgen RB. 1994. Targeting of proteins to the thylakoids by bipartite presequences: CFoII is imported by a novel, third pathway. EMBO J. 13(6):1310-17
55. Mould RM, Robinson C. 1991. A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane. J. Biol. Chem. 266(19):12189-93
56. Nakai M, Goto A, Nohara T, Sugita D, Endo T. 1994. Identification of the secA protein homolog in pea chloroplasts and its possible involvement in thylakoidal protein transport. J. Biol. Chem. 269(50):31338-41
57. Nielsen VS, Mant A, Knoetzel J, Möller BL, Robinson C. 1994. Import of barley photosystem I subunit N into the thylakoid lumen is mediated by a bipartite presequence lacking an intermediate processing site. J. Biol. Chem. 269(5):3762-66
58. Nohara T, Nakai M, Goto A, Endo T. 1995. Isolation and characterization of the cDNA for pea chloroplast secA evolutionary conservation of the bacterial-type secA-dependent protein transport within chloroplasts. FEBS Lett. 364:305-08
59. Oliver DB, Cabelli RJ, Dolan KM, Jarosik GP. 1990. Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery. Proc. Natl. Acad. Sci. USA 87:8227-31
60. Olsen LJ, Keegstra K. 1992. The binding of precursor proteins to chloroplasts requires nucleoside triphosphates in the intermembrane space. J. Biol. Chem. 267(1):433-39
61. Payan LA, Cline K. 1991. A stromal protein factor maintains the solubility and insertion competence of an imported thylakoid membrane protein. J. Cell Biol. 112(4):603-13
62. Perry SE, Keegstra K. 1994. Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 6:93-105
63. Pfisterer J, Lachmann P, Kloppstech K. 1982. Transport of proteins into chloroplasts: binding of nuclear-coded chloroplast proteins to the chloroplast envelope. Eur. J. Biochem. 126:143-48
64. Pilon M, Rietveld AG, Weisbeek PJ, de Kruijff B. 1992a. Secondary structure and folding of a functional chloroplast precursor protein. J. Biol. Chem. 267(28):19907-13
65. Pilon M, Weisbeek PJ, de Kruijff B. 1992b. Kinetic analysis of translocation into isolated chloroplasts of the purified ferredoxin precursor. FEBS Lett. 302:65-68
66. Pugsley AP. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57(1):50-108
67. Reed JE, Cline K, Stephens LC, Bacot KO, Viitanen PV. 1990. Early events in the import/assembly pathway of an integral thylakoid protein. Eur. J. Biochem. 194:33-42
68. Reinbothe S, Runge S, Reinbothe C, van Cleve B, Apel K. 1995. Substrate-dependent transport of the NADPH:protochlorophyllide oxidoreductase into isolated plastids. Plant Cell 7:161-72
69. Robinson C, Cai D, Hulford A, Brock IW, Michl D, et al. 1994. The presequence of a chimeric construct dictates which of two mechanisms are utilized for translocation across the thylakoid membrane: evidence for the existence of two distinct translocation systems. EMBO J. 13(2):279-85
70. Robinson C, Klösgen RB. 1994. Targeting of proteins into and across the thylakoid membrane: a multitude of mechanisms. Plant Mol. Biol. 26:15-24
71. Ryan KR, Jensen RE. 1995. Protein translocation across mitochondrial membranes: what a long, strange trip it is. Cell 83:517-19
72. Salomon M, Fischer K, Flügge U-I, Soll J. 1990. Sequence analysis and protein import studies of an outer chloroplast envelope polypeptide. Proc. Natl. Acad. Sci. USA 87:5778-82
73. Schnell DJ. 1995. Shedding light on the chloroplast protein import machinery. Cell 83:521-24
74. Schnell DJ, Blobel G. 1993. Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites. J. Cell Biol. 120(1):103-15
75. Schnell DJ, Kessler F, Blobel G. 1994. Isolation of components of the chloroplast protein import machinery. Science 266:1007-12
76. Schwaiger M, Herzog V, Neupert W. 1987. Characterization of translocation contact sites involved in the import of mitochondrial proteins. J. Cell Biol. 105:235-46
77. Scott SV, Theg SM. 1996. A new intermediate on the chloroplast protein import pathway reveals distinct translocation machineries in the two envelope membranes: energetics and mechanistic implications. J. Cell Biol. 132:63-75
78. Seedorf M, Soll J. 1995. Copper chloride, an inhibitor of protein import into chloroplasts. FEBS Lett. 367:19-22
79. Seedorf M, Waegemann K, Soll J. 1995. A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J. 7(3):401-11
80. Segui-Real B, Kispal G, Lill R, Neupert W. 1993. Functional independence of the protein translocation machineries in mitochondrial outer and inner membranes: passage of preproteins through the intermembrane space. EMBO J. 12(5):2211-18
81. Siegel V. 1995. A second signal recognition event required for translocation into the endoplasmic reticulum. Cell 82:167-70
82. Simon SM, Blobel G. 1991. A protein-conducting channel in the endoplasmic reticulum. Cell 65:371-80
83. Smeekens S, Bauerle C, Hageman J, Keegstra K, Weisbeek P. 1986. The role of the transit peptide in the routing of precursors toward different chloroplast compartments. Cell 46:365-75
84. Smith TA, Kohorn BD. 1994. Mutations in a signal sequence for the thylakoid membrane identify multiple protein transport pathways and nuclear suppressors. J. Cell Biol. 126(2):365-74
85. Soll J. 1995. New insights into the protein import machinery of the chloroplast's outer envelope. Bot. Acta 108:277-82
86. Stader J, Gansheroff LJ, Silhavy TJ. 1989. New suppressors of signal-sequence mutations, prlG, are linked tightly to the secE gene of Escherichia coli. Genes Dev. 3:1045-52
87. Sweet DJ, Gerace L. 1995. Taking from the cytoplasm and giving to the pore: soluble transport factors in nuclear protein import. Trends Cell Biol. 5:444-47
88. Theg SM, Scott SV. 1993. Protein import into chloroplasts. Trends Cell Biol. 3:186-90
89. 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(11):2436-46
90. + reductase upon its import into chloroplasts. FEBS Lett. 320(3):198-202
91. VanderVere PS, Bennett TM, Oblong JE, Lamppa GK. 1995. A chloroplast processing enzyme involved in precursor maturation shares a zinc-binding motif with a recently recognized family of metalloendopeptidases. Proc. Natl. Acad. Sci. USA 92:7177-81
92. van't Hof R, van Klompenburg W, Pilon M, Kozubek A, de Korte-Kool G, et al. 1993. The transit sequence mediates the specific interaction of the precursor of ferredoxin with chloroplast envelope membrane lipids. J. Biol. Chem. 268(6):4037-42
93. Viitanen PV, Doran ER, Dunsmuir P. 1988. What is the role of the transit peptide in thylakoid integration of the light-harvesting chlorophyll a/b protein? J. Biol. Chem. 263:15000-7
94. Voelker R, Barkan A. 1995. Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. EMBO J. 14(16):3905-14
95. von Heijne G, Nishikawa K. 1991. Chloroplast transit peptides: the perfect random coil? FEBS Lett. 278(1):1-3
96. von Heijne G, Steppuhn J, Herrmann RG. 1989. Domain structure of mitochondrial and chloroplast targeting peptides. Eur. J. Biochem. 180:535-45
97. Waegemann K, Soll J. 1991. Characterization of the protein import apparatus in isolated outer envelopes of chloroplasts. Plant J. 1(2):149-58
98. Walter P, Johnson AE. 1994. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 10:87-119
99. Whatley JM, Hawes CR, Horne JC, Kerr JDA. 1982. The establishment of the plastid thylakoid system. New Phytol. 90:619-29
100. Wickner WT. 1994. How ATP drives proteins across membranes. Science 266:1197-98
101. Wu C, Seibert FS, Ko K. 1994. Identification of chloroplast envelope proteins in close physical proximity to a partially translocated chimeric precursor protein. J. Biol. Chem. 269(51):32264-71
102. Yuan J, Cline K. 1994. Plastocyanin and the 33-kDa subunit of the oxygen-evolving complex are transported into thylakoids with similar requirements as predicted from pathway specificity. J. Biol. Chem. 269(28):18463-67
103. Yuan J, Henry R, Cline K. 1993. Stromal factor plays an essential role in protein integration into thylakoids that cannot be replaced by unfolding or by heat shock protein Hsp70. Proc. Natl. Acad. Sci. USA 90:8552-56
104. Yuan J, Henry R, McCaffery M, Cline K. 1994. SecA homolog in protein transport within chloroplasts: evidence for endosymbiont-derived sorting. Science 266:796-98