Abstract
Chloroplasts are descendants of an ancient endosymbiotic cyanobacterium that lived inside a eukaryotic cell. They inherited the prokaryotic double membrane envelope from cyanobacteria. This envelope contains prokaryotic protein sorting machineries including a Sec translocase and relatives of the central component of the bacterial outer membrane β-barrel assembly module. As the endosymbiont was integrated with the rest of the cell, the synthesis of most of its proteins shifted from the stroma to the host cytosol. This included nearly all the envelope proteins identified so far. Consequently, the overall biogenesis of the chloroplast envelope must be distinct from cyanobacteria. Envelope proteins initially approach their functional locations from the exterior rather than the interior. In many cases, they have been shown to use components of the general import pathway that also serves the stroma and thylakoids. If the ancient prokaryotic protein sorting machineries are still used for chloroplast envelope proteins, their activities must have been modified or combined with the general import pathway. In this review, we analyze the current knowledge pertaining to chloroplast envelope biogenesis and compare this to bacteria.
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Bae W, Lee YJ, Kim DH, Lee J, Kim S, Sohn EJ, Hwang I (2008) AKR2A-mediated import of chloroplast outer membrane proteins is essential for chloroplast biogenesis. Nat Cell Biol 10:220–227. https://doi.org/10.1038/ncb1683
Baldwin AJ, Wardle A, Patel R, Dudley P, Park SK, Twell D, Inoue K, Jarvis P (2005) A molecular-genetic study of the Arabidopsis Toc75 gene family. Plant Physiol 138:715–733. https://doi.org/10.1104/pp.105.063289
Bolter B, Soll J (2016) Once upon a time—chloroplast protein import research from infancy to future. Chall Mol Plant 9:798–812. https://doi.org/10.1016/j.molp.2016.04.014
Bolter B, Soll J, Schulz A, Hinnah S, Wagner R (1998) Origin of a chloroplast protein importer. Proc Natl Acad Sci USA 95:15831–15836
Bolter B, Soll J, Hill K, Hemmler R, Wagner R (1999) A rectifying ATP-regulated solute channel in the chloroplastic outer envelope from pea. EMBO J 18:5505–5516. https://doi.org/10.1093/emboj/18.20.5505
Breuers FK, Brautigam A, Weber AP (2011) The plastid outer envelope—a highly dynamic interface between plastid and cytoplasm. Front Plant Sci 2:97. https://doi.org/10.3389/fpls.2011.00097
Brink S, Fischer K, Klosgen RB, Flugge UI (1995) Sorting of nuclear-encoded chloroplast membrane proteins to the envelope and the thylakoid membrane. J Biol Chem 270:20808–20815
Celedon JM, Cline K (2013) Intra-plastid protein trafficking: how plant cells adapted prokaryotic mechanisms to the eukaryotic condition. Biochim Biophys Acta 1833:341–351. https://doi.org/10.1016/j.bbamcr.2012.06.028
Chen YL, Chen LJ, Li HM (2016) Polypeptide transport-associated domains of the Toc75 channel protein are located in the intermembrane space of chloroplasts. Plant Physiol 172:235–243. https://doi.org/10.1104/pp.16.00919
Day PM, Potter D, Inoue K (2014) Evolution and targeting of Omp85 homologs in the chloroplast outer envelope membrane. Front Plant Sci 5:535. https://doi.org/10.3389/fpls.2014.00535
Dhanoa PK, Richardson LG, Smith MD, Gidda SK, Henderson MP, Andrews DW, Mullen RT (2010) Distinct pathways mediate the sorting of tail-anchored proteins to the plastid outer envelope. PLoS ONE 5:e10098. https://doi.org/10.1371/journal.pone.0010098
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. https://doi.org/10.1093/embo-reports/kvf110
Endow JK, Singhal R, Fernandez DE, Inoue K (2015) Chaperone-assisted post-translational transport of plastidic type i signal peptidase 1. J Biol Chem 290:28778–28791. https://doi.org/10.1074/jbc.M115.684829
Endow JK, Rocha AG, Baldwin AJ, Roston RL, Yamaguchi T, Kamikubo H, Inoue K (2016) Polyglycine acts as a rejection signal for protein transport at the chloroplast envelope. PLoS ONE 11:e0167802. https://doi.org/10.1371/journal.pone.0167802
Facchinelli F, Weber AP (2011) The metabolite transporters of the plastid envelope: an update. Front Plant Sci 2:50. https://doi.org/10.3389/fpls.2011.00050
Fernandez DE (2018) Two paths diverged in the stroma: targeting to dual SEC translocase systems in chloroplasts. Photosynth Res. https://doi.org/10.1007/s11120-018-0541-9
Firlej-Kwoka E, Strittmatter P, Soll J, Bolter B (2008) Import of preproteins into the chloroplast inner envelope membrane. Plant Mol Biol 68:505–519. https://doi.org/10.1007/s11103-008-9387-4
Frain KM, Gangl D, Jones A, Zedler JA, Robinson C (2016) Protein translocation and thylakoid biogenesis in cyanobacteria. Biochim Biophys Acta 1857:266–273. https://doi.org/10.1016/j.bbabio.2015.08.010
Froehlich JE, Keegstra K (2011) The role of the transmembrane domain in determining the targeting of membrane proteins to either the inner envelope or thylakoid membrane. Plant J 68:844–856. https://doi.org/10.1111/j.1365-313X.2011.04735.x
Glaser S, van Dooren GG, Agrawal S, Brooks CF, McFadden GI, Striepen B, Higgins MK (2012) Tic22 is an essential chaperone required for protein import into the apicoplast. J Biol Chem 287:39505–39512. https://doi.org/10.1074/jbc.M112.405100
Goetze TA, Philippar K, Ilkavets I, Soll J, Wagner R (2006) OEP37 is a new member of the chloroplast outer membrane ion channels. J Biol Chem 281:17989–17998. https://doi.org/10.1074/jbc.M600700200
Harsman A et al (2016) OEP40, a regulated glucose-permeable beta-barrel solute channel in the chloroplast outer envelope membrane. J Biol Chem 291:17848–17860. https://doi.org/10.1074/jbc.M115.712398
Heinz E, Selkrig J, Belousoff MJ, Lithgow T (2015) Evolution of the translocation and assembly module (TAM). Genome Biol Evol 7:1628–1643. https://doi.org/10.1093/gbe/evv097
Hirano T et al (2016) Moss chloroplasts are surrounded by a peptidoglycan wall containing D-amino acids. Plant Cell 28:1521–1532. https://doi.org/10.1105/tpc.16.00104
Hofmann NR, Theg SM (2005a) Chloroplast outer membrane protein targeting and insertion. Trends Plant Sci 10:450–457. https://doi.org/10.1016/j.tplants.2005.07.009
Hofmann NR, Theg SM (2005b) Protein- and energy-mediated targeting of chloroplast outer envelope membrane proteins. Plant J 44:917–927. https://doi.org/10.1111/j.1365-313X.2005.02571.x
Hoiczyk E, Hansel A (2000) Cyanobacterial cell walls: news from an unusual prokaryotic envelope. J Bacteriol 182:1191–1199
Hsu SC, Belmonte MF, Harada JJ, Inoue K (2010) Indispensable roles of plastids in Arabidopsis thaliana embryogenesis. Curr Genom 11:338–349. https://doi.org/10.2174/138920210791616716
Hsu SC, Nafati M, Inoue K (2012) 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 78:147–158. https://doi.org/10.1007/s11103-011-9853-2
Hsueh YC, Flinner N, Gross LE, Haarmann R, Mirus O, Sommer MS, Schleiff E (2014) Chloroplast outer envelope protein P39 in Arabidopsis thaliana belongs to the Omp85 protein family. Proteins 85:1391–1401. https://doi.org/10.1002/prot.24725
Hurlock AK, Roston RL, Wang K, Benning C (2014) Lipid trafficking in plant cells. Traffic 15:915–932. https://doi.org/10.1111/tra.12187
Inoue K (2011) Emerging roles of the chloroplast outer envelope membrane. Trends Plant Sci 16:550–557. https://doi.org/10.1016/j.tplants.2011.06.005
Inoue K, Keegstra K (2003) A polyglycine stretch is necessary for proper targeting of the protein translocation channel precursor to the outer envelope membrane of chloroplasts. Plant J 34:661–669
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. https://doi.org/10.1111/j.1365-313X.2004.02135.x
Inoue K, Baldwin AJ, Shipman RL, Matsui K, Theg SM, Ohme-Takagi M (2005) Complete maturation of the plastid protein translocation channel requires a type I signal peptidase. J Cell Biol 171:425–430. https://doi.org/10.1083/jcb.200506171
Iqbal H, Kenedy MR, Lybecker M, Akins DR (2016) The TamB ortholog of Borrelia burgdorferi interacts with the beta-barrel assembly machine (BAM) complex protein BamA. Mol Microbiol 102:757–774. https://doi.org/10.1111/mmi.13492
Kessler F, Blobel G, Patel HA, Schnell DJ (1994) Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 266:1035–1039
Kikuchi S et al (2013) Uncovering the protein translocon at the chloroplast inner envelope membrane. Science 339:571–574. https://doi.org/10.1126/science.1229262
Kim DH et al (2014) An ankyrin repeat domain of AKR2 drives chloroplast targeting through coincident binding of two chloroplast lipids. Dev Cell 30:598–609. https://doi.org/10.1016/j.devcel.2014.07.026
Kirchberger S, Tjaden J, Neuhaus HE (2008) Characterization of the Arabidopsis Brittle1 transport protein and impact of reduced activity on plant metabolism. Plant J 56:51–63. https://doi.org/10.1111/j.1365-313X.2008.03583.x
Klasek L, Inoue K (2016) Dual protein localization to the envelope and thylakoid membranes within the chloroplast. Int Rev Cell Mol Biol 323:231–263. https://doi.org/10.1016/bs.ircmb.2015.12.008
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 7:1421–1432. https://doi.org/10.1105/tpc.7.9.1421
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
Kouranov A, Wang H, Schnell DJ (1999) Tic22 is targeted to the intermembrane space of chloroplasts by a novel pathway. J Biol Chem 274:25181–25186
Kuhn A, Koch HG, Dalbey RE (2017) Targeting and insertion of membrane proteins. EcoSal Plus. https://doi.org/10.1128/ecosalplus.ESP-0012-2016
Lee DW, Hwang I (2018) Evolution and design principles of the diverse chloroplast transit peptides. Mol Cells 41:161–167. https://doi.org/10.14348/molcells.2018.0033
Lee YJ, Kim DH, Kim YW, Hwang I (2001) Identification of a signal that distinguishes between the chloroplast outer envelope membrane and the endomembrane system in vivo. Plant Cell 13:2175–2190
Lee J, Kim DH, Hwang I (2014) Specific targeting of proteins to outer envelope membranes of endosymbiotic organelles, chloroplasts, and mitochondria. Front Plant Sci 5:173. https://doi.org/10.3389/fpls.2014.00173
Li HM, Chen LJ (1996) Protein targeting and integration signal for the chloroplastic outer envelope membrane. Plant Cell 8:2117–2126
Li H, Chen LJ (1997) A novel chloroplastic outer membrane-targeting signal that functions at both termini of passenger polypeptides. J Biol Chem 272:10968–10974
Li M, Schnell DJ (2006) Reconstitution of protein targeting to the inner envelope membrane of chloroplasts. J Cell Biol 175:249–259. https://doi.org/10.1083/jcb.200605162
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 3:709–717
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 267:18999–19004
Li Y, Singhal R, Taylor IW, McMinn PH, Chua XY, Cline K, Fernandez DE (2015) The Sec2 translocase of the chloroplast inner envelope contains a unique and dedicated SECE2 component. Plant J 84:647–658. https://doi.org/10.1111/tpj.13028
Li Y, Martin JR, Aldama GA, Fernandez DE, Cline K (2017) Identification of putative substrates of SEC2, a chloroplast inner envelope translocase. Plant Physiol 173:2121–2137. https://doi.org/10.1104/pp.17.00012
Lubeck J, Heins L, Soll J (1997) A nuclear-coded chloroplastic inner envelope membrane protein uses a soluble sorting intermediate upon import into the organelle. J Cell Biol 137:1279–1286
Matsushima R, Maekawa M, Kusano M, Kondo H, Fujita N, Kawagoe Y, Sakamoto W (2014) Amyloplast-localized SUBSTANDARD STARCH GRAIN4 protein influences the size of starch grains in rice endosperm. Plant Physiol 164:623–636. https://doi.org/10.1104/pp.113.229591
Miege C et al (1999) Biochemical and topological properties of type A MGDG synthase, a spinach chloroplast envelope enzyme catalyzing the synthesis of both prokaryotic and eukaryotic MGDG. Eur J Biochem 265:990–1001
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 269:31338–31341
Nishimura K, Kato Y, Sakamoto W (2016) Chloroplast proteases: updates on proteolysis within and across suborganellar compartments. Plant Physiol 171:2280–2293. https://doi.org/10.1104/pp.16.00330
Okawa K et al (2014) Targeting of a polytopic membrane protein to the inner envelope membrane of chloroplasts in vivo involves multiple transmembrane segments. J Exp Bot 65:5257–5265. https://doi.org/10.1093/jxb/eru290
Osteryoung KW, Pyke KA (2014) Division and dynamic morphology of plastids. Annu Rev Plant Biol 65:443–472. https://doi.org/10.1146/annurev-arplant-050213-035748
Paila YD, Richardson LG, Inoue H, Parks ES, McMahon J, Inoue K, Schnell DJ (2016) Multi-functional roles for the polypeptide transport associated domains of Toc75 in chloroplast protein import. Elife. https://doi.org/10.7554/eLife.12631
Patel R, Hsu SC, Bedard 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. https://doi.org/10.1104/pp.108.122754
Pohlmeyer K, Soll J, Grimm R, Hill K, Wagner R (1998) A high-conductance solute channel in the chloroplastic outer envelope from pea. Plant Cell 10:1207–1216
Reumann S, Keegstra K (1999) The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci 4:302–307
Reumann S, Davila-Aponte J, Keegstra K (1999) The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proc Natl Acad Sci USA 96:784–789
Reumann S, Inoue K, Keegstra K (2005) Evolution of the general protein import pathway of plastids (review). Mol Membr Biol 22:73–86
Rollauer SE, Sooreshjani MA, Noinaj N, Buchanan SK (2015) Outer membrane protein biogenesis in Gram-negative bacteria Philos Trans R Soc Lond B. https://doi.org/10.1098/rstb.2015.0023
Roston RL, Wang K, Kuhn LA, Benning C (2014) Structural determinants allowing transferase activity in SENSITIVE TO FREEZING 2, classified as a family I glycosyl hydrolase. J Biol Chem 289:26089–26106. https://doi.org/10.1074/jbc.M114.576694
Schleiff E, Eichacker LA, Eckart K, Becker T, Mirus O, Stahl T, Soll J (2003) Prediction of the plant beta-barrel proteome: a case study of the chloroplast outer envelope. Protein Sci 12:748–759. https://doi.org/10.1110/ps.0237503
Schnell DJ, Kessler F, Blobel G (1994) Isolation of components of the chloroplast protein import machinery. Science 266:1007–1012
Seedorf M, Waegemann K, Soll J (1995) A constituent of the chloroplast import complex represents a new type of GTP-binding protein. Plant J 7:401–411
Selkrig J et al (2012) Discovery of an archetypal protein transport system in bacterial outer membranes. Nat Struct Mol Biol 19:506–510, S501. https://doi.org/10.1038/nsmb.2261
Shi LX, Theg SM (2013) The chloroplast protein import system: from algae to trees. Biochim Biophys Acta 1833:314–331. https://doi.org/10.1016/j.bbamcr.2012.10.002
Singhal R, Fernandez DE (2017) Sorting of SEC translocase SCY components to different membranes in chloroplasts. J Exp Bot. https://doi.org/10.1093/jxb/erx318
Skalitzky CA et al (2011) Plastids contain a second sec translocase system with essential functions. Plant Physiol 155:354–369. https://doi.org/10.1104/pp.110.166546
Sommer MS et al (2011) Chloroplast Omp85 proteins change orientation during evolution. Proc Natl Acad Sci USA 108:13841–13846. https://doi.org/10.1073/pnas.1108626108
Topel M, Ling Q, Jarvis P (2012) Neofunctionalization within the Omp85 protein superfamily during chloroplast evolution. Plant Signal Behav 7:161–164. https://doi.org/10.4161/psb.18677
Tranel PJ, Keegstra K (1996) A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope. Plant Cell 8:2093–2104. https://doi.org/10.1105/tpc.8.11.2093
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
Tripp J, Inoue K, Keegstra K, Froehlich JE (2007) 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 52:824–838. https://doi.org/10.1111/j.1365-313X.2007.03279.x
Tripp J et al (2012) Structure and conservation of the periplasmic targeting factor Tic22 protein from plants and cyanobacteria. J Biol Chem 287:24164–24173. https://doi.org/10.1074/jbc.M112.341644
Tsai LY, Tu SL, Li HM (1999) Insertion of at Toc34 into the chloroplastic outer membrane is assisted by at least two proteinaceous components in the import system. J Biol Chem 274:18735–18740
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 Toc 75. Plant Cell 16:2078–2088. https://doi.org/10.1105/tpc.104.023952
Tyra HM, Linka M, Weber AP, Bhattacharya D (2007) Host origin of plastid solute transporters in the first photosynthetic eukaryotes. Genome Biol 8:R212. https://doi.org/10.1186/gb-2007-8-10-r212
Tzafrir I et al (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135:1206–1220. https://doi.org/10.1104/pp.104.045179
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 92:7177–7181
Viana AA, Li M, Schnell DJ (2010) Determinants for stop-transfer and post-import pathways for protein targeting to the chloroplast inner envelope membrane. J Biol Chem 285:12948–12960. https://doi.org/10.1074/jbc.M110.109744
Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn 2. Plant Cell 15:1918–1933
Vojta L, Soll J, Bolter B (2007) Protein transport in chloroplasts—targeting to the intermembrane space. FEBS J 274:5043–5054. https://doi.org/10.1111/j.1742-4658.2007.06023.x
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. https://doi.org/10.1074/jbc.M307873200
Wang Z, Xu C, Benning C (2012) TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. Plant J 70:614–623. https://doi.org/10.1111/j.1365-313X.2012.04900.x
Webb CT, Heinz E, Lithgow T (2012) Evolution of the beta-barrel assembly machinery. Trends Microbiol 20:612–620. https://doi.org/10.1016/j.tim.2012.08.006
Wu C, Ko K (1993) Identification of an uncleavable targeting signal in the 70-kilodalton spinach chloroplast outer envelope membrane protein. J Biol Chem 268:19384–19391
Yuan J, Henry R, McCaffery M, Cline K (1994) SecA homolog in protein transport within chloroplasts: evidence for endosymbiont-derived sorting. Science 266:796–798
Yuzawa Y et al (2012) Phylogeny of galactolipid synthase homologs together with their enzymatic analyses revealed a possible origin and divergence time for photosynthetic membrane biogenesis. DNA Res 19:91–102. https://doi.org/10.1093/dnares/dsr044
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Day, P.M., Theg, S.M. Evolution of protein transport to the chloroplast envelope membranes. Photosynth Res 138, 315–326 (2018). https://doi.org/10.1007/s11120-018-0540-x
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DOI: https://doi.org/10.1007/s11120-018-0540-x