Targeting and biogenesis of transporters and channels in chloroplast envelope membranes: Unsolved questions

Cell Calcium

Volumn 58, Issue 1, 2015, Pages 122-130

  Oh, Young Jun ^a   Hwang, Inhwan ^a  

^a Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

Biogenesis; Chloroplasts; Molecular machinery for biogenesis; Outer and inner envelope membranes; Targeting signals; Transporters and channels

Indexed keywords

BETA BARREL PROTEIN; CHANNEL PROTEIN; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; TRANSPORTER; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; CALCIUM; CARRIER PROTEIN;

AMINO ACID SEQUENCE; BIOGENESIS; CHLOROPLAST; CHLOROPLAST ENVELOPE MEMBRANE; CHLOROPLAST MEMBRANE; CYTOSOL; ENDOPLASMIC RETICULUM; INNER MEMBRANE; MITOCHONDRION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; QUALITY CONTROL; REVIEW; SIGNAL TRANSDUCTION; ARABIDOPSIS; CHEMISTRY; ION TRANSPORT; METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM; CHLOROPLASTS; ION TRANSPORT; MEMBRANE TRANSPORT PROTEINS;

EID: 84930526400     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.10.012     Document Type: Review

References (94)

1. Neuhaus H.E., Wagner R. Solute pores, ion channels, and metabolite transporters in the outer and inner envelope membranes of higher plant plastids. Biochim. Biophys. Acta 2000, 1465:307-323.
2. Facchinelli F., Weber A.P. The metabolite transporters of the plastid envelope: an update. Front. Plant Sci. 2011, 2:50.
3. 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.
4. 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.
5. Jarvis P., Robinson C. Mechanisms of protein import and routing in chloroplasts. Curr. Biol. 2004, 14:1064-1077.
6. Cline K., Dabney-Smith C. Plastid protein import and sorting: different paths to the same compartments. Curr. Opin. Plant Biol. 2008, 11:585-592.
7. Lee J., Kim D.H., Hwang I. Specific targeting of proteins to outer envelope membranes of endosymbiotic organelles, chloroplasts, and mitochondria. Front. Plant Sci. 2014, 5:173.
8. Flugge U.I. Transport in and out of plastids: does the outer envelope membrane control the flow?. Trends Plant Sci. 2000, 5:135-137.
9. Weber A.P., Schwacke R., Flugge U.I. Solute transporters of the plastid envelope membrane. Annu. Rev. Plant Biol. 2005, 56:133-164.
10. Block M.A., Douce R., Joyard J., Rolland N. Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol. Photosynth. Res. 2007, 92:225-244.
11. Bolter B., Soll J., Hill K., Hemmler R., Wagner R. A rectifying ATP-regulated solute channel in the chloroplastic outer envelope from pea. EMBO J. 1999, 18:5505-5516.
12. Pohlmeyer K., Soll J., Grimm R., Hill K., Wagner R. A high-conductance solute channel in the chloroplastic outer envelope from pea. Plant Cell 1998, 10:1207-1216.
13. Reinbothe S., Quigley F., Springer A., Schemenewitz A., Reinbothe C. The outer plastid envelope protein Oep16: role as precursor translocase in import of protochlorophyllide oxidoreductase A. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:2203-2208.
14. Goetze T.A., Philippar K., Ilkavets I., Soll J., Wagner R. OEP37 is a new member of the chloroplast outer membrane ion channels. J. Biol. Chem. 2006, 281:17989-17998.
15. Hemmler R., Becker T., Schleiff E., Bolter B., Stahl T., Soll J., Gotze T.A., Braams S., Wagner R. Molecular properties of Oep21, an ATP-regulated anion-selective solute channel from the outer chloroplast membrane. J. Biol. Chem. 2006, 281:12020-12029.
16. Pudelski B., Schock A., Hoth S., Radchuk R., Weber H., Hofmann J., Sonnewald U., Soll J., Philippar K. The plastid outer envelope protein OEP16 affects metabolic fluxes during ABA-controlled seed development and germination. J. Exp. Bot. 2012, 63:1919-1936.
17. Steinkamp T., Hill K., Hinnah S.C., Wagner R., Rohl T., Pohlmeyer K., Soll J. Identification of the pore-forming region of the outer chloroplast envelope protein OEP16. J. Biol. Chem. 2000, 275:11758-11764.
18. 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.
19. 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.
20. 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.
21. 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.
22. Pfeil B.E., Schoefs B., Spetea C. Function and evolution of channels and transporters in photosynthetic membranes. Cell Mol. Life Sci. 2014, 71:979-998.
23. Ludewig F., Flugge U.I. Role of metabolite transporters in source-sink carbon allocation. Front. Plant Sci. 2013, 4:231.
24. Gigolashvili T., Yatusevich R., Rollwitz I., Humphry M., Gershenzon J., Flugge U.I. The plastidic bile acid transporter 5 is required for the biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana. Plant Cell 2009, 21:1813-1829.
25. Sawada Y., Toyooka K., Kuwahara A., Sakata A., Nagano M., Saito K., Hirai M.Y. Arabidopsis bile acid: sodium symporter family protein 5 is involved in methionine-derived glucosinolate biosynthesis. Plant Cell Physiol. 2009, 50:1579-1586.
26. Klaus S.M., Kunji E.R., Bozzo G.G., Noiriel A., de la Garza R.D., Basset G.J., Ravanel S., Rebeille F., Gregory J.F., Hanson A.D. Higher plant plastids and cyanobacteria have folate carriers related to those of trypanosomatids. J. Biol. Chem. 2005, 280:38457-38463.
27. Saier M.H., Tran C.V., Barabote R.D. TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res. 2006, 34:D181-D186.
28. Kinoshita H., Nagasaki J., Yoshikawa N., Yamamoto A., Takito S., Kawasaki M., Sugiyama T., Miyake H., Weber A.P., Taniguchi M. The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism. Plant J. 2011, 65:15-26.
29. Roston R.L., Gao J., Murcha M.W., Whelan J., Benning C. TGD1, -2, and -3 proteins involved in lipid trafficking form ATP-binding cassette (ABC) transporter with multiple substrate-binding proteins. J. Biol. Chem. 2012, 287:21406-21415.
30. Conte S.S., Lloyd A.M. The MAR1 transporter is an opportunistic entry point for antibiotics. Plant Signal. Behav. 2010, 5:49-52.
31. Kunz H.H., Gierth M., Herdean A., Satoh-Cruz M., Kramer D.M., Spetea C., Schroeder J.I. Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:7480-7485.
32. Block M.A., Dorne A.J., Joyard J., Douce R. 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.
33. 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.
34. 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.
35. 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.
36. Halic M., Beckmann R. The signal recognition particle and its interactions during protein targeting. Curr. Opin. Struct. Biol. 2005, 15:116-125.
37. Janda C.Y., Li J., Oubridge C., Hernandez H., Robinson C.V., Nagai K. Recognition of a signal peptide by the signal recognition particle. Nature 2010, 465:507-510.
38. Lee D.W., Jung C., Hwang I. Cytosolic events involved in chloroplast protein targeting. Biochim. Biophys. Acta 2013, 1833:245-252.
39. Jarvis P., Lopez-Juez E. Biogenesis and homeostasis of chloroplasts and other plastids. Mol. Cell Biol. 2013, 14:787-802.
40. Wang Z., Xu C., Benning C. TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. Plant J. 2012, 70:614-623.
41. Wang Z., Anderson N.S., Benning C. The phosphatidic acid binding site of the Arabidopsis trigalactosyldiacylglycerol 4 (TGD4) protein required for lipid import into chloroplasts. J. Biol. Chem. 2013, 288:4763-4771.
42. 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. Mol. Cells 2004, 17:281-291.
43. Lee J., Lee H., Kim J., Lee S., Kim D.H., Kim S., Hwang I. Both the hydrophobicity and a positively charged region flanking the C-terminal region of the transmembrane domain of signal-anchored proteins play critical roles in determining their targeting specificity to the endoplasmic reticulum or endosymbiotic organelles in Arabidopsis cells. Plant Cell 2011, 23:1588-1607.
44. Walther D.M., Papic D., Bos M.P., Tommassen J., Rapaport D. Signals in bacterial beta-barrel proteins are functional in eukaryotic cells for targeting to and assembly in mitochondria. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:2531-2536.
45. Rapaport D., Neupert W. Biogenesis of Tom40, core component of the TOM complex of mitochondria. J. Cell Biol. 1999, 146:321-331.
46. Humphries A.D., Streimann I.C., Stojanovski D., Johnston A.J., Yano M., Hoogenraad N.J., Ryan M.T. Dissection of the mitochondrial import and assembly pathway for human Tom40. J. Biol. Chem. 2005, 280:11535-11543.
47. Ulrich T., Gross L.E., Sommer M.S., Schleiff E., Rapaport D. Chloroplast beta-barrel proteins are assembled into the mitochondrial outer membrane in a process that depends on the TOM and TOB complexes. J. Biol. Chem. 2012, 287:27467-27479.
48. Li M., Schnell D.J. Reconstitution of protein targeting to the inner envelope membrane of chloroplasts. J. Cell Biol. 2006, 175:249-259.
49. 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.
50. 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.
51. Perry S.E., Keegstra K. Envelope membrane proteins that interact with chloroplastic precursor proteins. Plant Cell 1994, 6:93-105.
52. Schnell D.J., Kessler F., Blobel G. Isolation of components of the chloroplast protein import machinery. Science 1994, 266:1007-1012.
53. 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.
54. 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.
55. Viana A.A., Li M., Schnell D.J. Determinants for stop-transfer and post-import pathways for protein targeting to the chloroplast inner envelope membrane. J. Biol. Chem. 2010, 285:12948-12960.
56. Sommer M., Rudolf M., Tillmann B., Tripp J., Sommer M.S., Schleiff E. Toc33 and Toc64-III cooperate in precursor protein import into the chloroplasts of Arabidopsis thaliana. Plant Cell Environ. 2013, 36:970-983.
57. Shamu C.E., Cox J.S., Walter P. The unfolded-protein-response pathway in yeast. Trends Cell Biol. 1994, 4:56-60.
58. Niittyla T., Messerli G., Trevisan M., Chen J., Smith A.M., Zeeman S.C. A previously unknown maltose transporter essential for starch degradation in leaves. Science 2004, 303:87-89.
59. Dyall S.D., Brown M.T., Johnson P.J. Ancient invasions: from endosymbionts to organelles. Science 2004, 304:253-257.
60. Sickmann A., Reinders J., Wagner Y., Joppich C., Zahedi R., Meyer H.E., Schonfisch B., Perschil I., Chacinska A., Guiard B., Rehling P., Pfanner N., Meisinger C. The proteome of Saccharomyces cerevisiae mitochondria. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13207-13212.
61. Walter P., Johnson A.E. Signal sequence recognition and protein targeting to the endoplasmic reticulum membrane. Annu. Rev. Cell Biol. 1994, 10:87-119.
62. Kotak S., Larkindale J., Lee U., von Koskull-Doring P., Vierling E., Scharf K.D. Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 2007, 10:310-316.
63. Buchberger A., Bukau B., Sommer T. Protein quality control in the cytosol and the endoplasmic reticulum: brothers in arms. Mol. Cell 2010, 40:238-252.
64. Xu Z.S., Li Z.Y., Chen Y., Chen M., Li L.C., Ma Y.Z. Heat shock protein 90 in plants: molecular mechanisms and roles in stress responses. Int. J. Mol. Sci. 2012, 13:15706-15723.
65. Lee S., Lee D.W., Lee Y., Mayer U., Stierhof Y.D., Lee S., Jurgens G., Hwang I. Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. Plant Cell 2009, 21:3984-4001.
66. Flores-Perez U., Jarvis P. Molecular chaperone involvement in chloroplast protein import. Biochim. Biophys. Acta 2013, 1833:332-340.
67. May T., Soll J. 14-3-3 proteins form a guidance complex with chloroplast precursor proteins in plants. Plant Cell 2000, 12:53-64.
68. Lee D.W., Lee S., Lee G.J., Lee K.H., Kim S., Cheong G.W., Hwang I. Functional characterization of sequence motifs in the transit peptide of Arabidopsis small subunit of rubisco. Plant Physiol. 2006, 140:466-483.
69. Lee D.W., Kim J.K., Lee S., Choi S., Kim S., Hwang I. Arabidopsis nuclear-encoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 2008, 20:1603-1622.
70. Bae W., Lee Y.J., Kim D.H., Lee J., Kim S., Sohn E.J., Hwang I. AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nature Cell Biol. 2008, 10:220-227.
71. Lee Y.J., Kim D.H., Kim Y.W., Hwang I. Identification of a signal that distinguishes between the chloroplast outer envelope membrane and the endomembrane system in vivo. Plant Cell 2001, 13:2175-2190.
72. Macasev D., Newbigin E., Whelan J., Lithgow T. How do plant mitochondria avoid importing chloroplast proteins? Components of the import apparatus Tom20 and Tom22 from Arabidopsis differ from their fungal counterparts. Plant Physiol. 2000, 123:811-816.
73. 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.
74. Peeters N., Small I. Dual targeting to mitochondria and chloroplasts. Biochim. Biophys. Acta 2001, 1541:54-63.
75. Pinnaduwage P., Bruce B.D. In vitro interaction between a chloroplast transit peptide and chloroplast outer envelope lipids is sequence-specific and lipid class-dependent. J. Biol. Chem. 1996, 271:32907-32915.
76. Carrie C., Giraud E., Whelan J. Protein transport in organelles: dual targeting of proteins to mitochondria and chloroplasts. FEBS J. 2009, 276:1187-1195.
77. 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.
78. Walther D.M., Rapaport D., Tommassen J. Biogenesis of beta-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell. Mol. Life Sci. 2009, 66:2789-2804.
79. 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.
80. Richardson L.G., Paila Y.D., Siman S.R., Chen Y., Smith M.D., Schnell D.J. Targeting and assembly of components of the TOC protein import complex at the chloroplast outer envelope membrane. Front. Plant Sci. 2014, 5:269.
81. Paschen S.A., Waizenegger T., Stan T., Preuss M., Cyrklaff M., Hell K., Rapaport D., Neupert W. Evolutionary conservation of biogenesis of beta-barrel membrane proteins. Nature 2003, 426:862-866.
82. Paschen S.A., Neupert W., Rapaport D. Biogenesis of beta-barrel membrane proteins of mitochondria. Trends Biochem. Sci. 2005, 30:575-582.
83. Jiang J.H., Tong J., Tan K.S., Gabriel K. From evolution to pathogenesis: the link between beta-barrel assembly machineries in the outer membrane of mitochondria and gram-negative bacteria. Int. J. Mol. Sci. 2012, 13:8038-8050.
84. Knowles T.J., Scott-Tucker A., Overduin M., Henderson I.R. Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nature Rev. Microbiol. 2009, 7:206-214.
85. Dalbey R.E., Wang P., Kuhn A. Assembly of bacterial inner membrane proteins. Annu. Rev. Biochem. 2011, 80:161-187.
86. Noinaj N., Kuszak A.J., Gumbart J.C., Lukacik P., Chang H., Easley N.C., Lithgow T., Buchanan S.K. Structural insight into the biogenesis of beta-barrel membrane proteins. Nature 2013, 501:385-390.
87. Hofmann N.R., Theg S.M. Chloroplast outer membrane protein targeting and insertion. Trends Plant Sci. 2005, 10:450-457.
88. Knight J.S., Gray J.C. The N-terminal hydrophobic region of the mature phosphate translocator is sufficient for targeting to the chloroplast inner envelope membrane. Plant Cell 1995, 7:1421-1432.
89. Okawa K., Inoue H., Adachi F., Nakayama K., Ito-Inaba Y., Schnell D.J., Uehara S., Inaba T. Targeting of a polytopic membrane protein to the inner envelope membrane of chloroplasts in vivo involves multiple transmembrane segments. J. Exp. Bot. 2014, 65(18):5257-5265.
90. Brink S., Fischer K., Klosgen R.B., Flugge U.I. Sorting of nuclear-encoded chloroplast membrane proteins to the envelope and the thylakoid membrane. J. Biol. Chem. 1995, 270:20808-20815.
91. 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.
92. Vojta L., Soll J., Bolter B. Requirements for a conservative protein translocation pathway in chloroplasts. FEBS Lett. 2007, 581:2621-2624.
93. Neupert W., Herrmann J.M. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 2007, 76:723-749.
94. Bolender N., Sickmann A., Wagner R., Meisinger C., Pfanner N. Multiple pathways for sorting mitochondrial precursor proteins. EMBO Rep. 2008, 9:42-49.