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Biogenesis of chloroplast outer envelope membrane proteins

  • Jonghak Kim
  • Yun Jeong Na
  • Soon Ju Park
  • So-Hyeon Baek
  • Dae Heon KimEmail author
Review article

Abstract

Most organisms on Earth use glucose, a photosynthetic product, as energy source. The chloroplast, the home of photosynthesis, is the most representative and characteristic organelle in plants and is enclosed by the outer envelope and inner envelope membranes. The chloroplast biogenesis and unique functions are very closely associated with proteins in the two envelope membranes of the chloroplast. Especially, the chloroplast outer envelope membrane proteins have important roles in signal transduction, protein import, lipid biosynthesis and remodeling, exchange of ions and numerous metabolites, plastid division, movement, and host defense. Therefore, biogenesis of these membrane proteins of chloroplast outer envelope membrane is very important for biogenesis of the entire chloroplast proteome as well as plant development. Most proteins among the outer envelope membrane proteins are encoded by the nuclear genome and are post-translationally targeted to the chloroplast outer envelope membrane. In this process, cytoplasmic receptor and import machineries are required for efficient and correct targeting of these membrane proteins. In this review, we have summarized recent advances on the sorting, targeting, and insertion mechanisms of the outer envelope membrane proteins of chloroplasts and also provide future direction of the study on these topics.

Keywords

Signal-anchored protein Tail-anchored protein β-Barrel protein Chloroplast outer envelope membrane protein Chloroplast AKR2 

Notes

Acknowledgements

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (2017R1A4A1015594, 2017R1C1B2009362).

Compliance with ethical standards

Conflict of interest

The authors declare no competing financial interests.

References

  1. 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 10:220–227CrossRefGoogle Scholar
  2. Baldwin AJ, Inoue K (2006) 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 273:1547–1555CrossRefGoogle Scholar
  3. Bauer J, Hiltbrunner A, Weibel P, Vidi PA, Alvarez-Huerta M, Smith MD, Schnell DJ, Kessler F (2002) Essential role of the G-domain in targeting of the protein import receptor atToc159 to the chloroplast outer membrane. J Cell Biol 159:845–854CrossRefGoogle Scholar
  4. Blobel G, Sabatini DD (1970) Controlled proteolysis of nascent polypeptides in rat liver cell fractions. I. Location of the polypeptides within ribosomes. J Cell Biol 45:130–145CrossRefGoogle Scholar
  5. Borgese N, Brambillasca S, Colombo S (2007) How tails guide tail-anchored proteins to their destinations. Curr Opin Cell Biol 19:368–375CrossRefGoogle Scholar
  6. Chartron JW, Clemons WM, Suloway CJM (2012) The complex process of GETting tail-anchored membrane proteins to the ER. Curr Opin Struc Biol 22:217–224CrossRefGoogle Scholar
  7. Cline K, Keegstra K (1983) Galactosyltransferases involved in galactolipid biosynthesis are located in the outer membrane of pea chloroplast envelopes. Plant Physiol 71(2):366–372CrossRefGoogle Scholar
  8. Court DA, Kleene R, Neupert W, Lill R (1996) Role of the N- and C-termini of porin in import into the outer membrane of Neurospora mitochondria. FEBS Lett 390:73–77CrossRefGoogle Scholar
  9. Dhanoa PK, Richardson LG, Smith MD, Gidda SK, Henderson MP, Adrews DW, Mullen RT (2010) Distinct pathways mediate the sorting of tail-anchored proteins to the plastid outer envelope. PLoS One 5(4):e10098CrossRefGoogle Scholar
  10. Dukanovic J, Rapaport D (2011) Multiple pathways in the integration of proteins into the mitochondrial outer membrane. Biochim Biophys Acta 1808:971–980CrossRefGoogle Scholar
  11. Ellis RJ, Minton AP (2006) Protein aggregation in crowded environments. Biol Chem 387:485–497CrossRefGoogle Scholar
  12. Flores-Pérez U, Jarvis P (2013) Molecular chaperone involvement in chloroplast protein import. Biochim Biophys Acta 1833:332–340CrossRefGoogle Scholar
  13. Formighieri C, Cazzaniga S, Kuras R, Bassi R (2013) Biogenesis of photosynthetic complexes in the chloroplast of Chlamydomonas reinhardtii requires ARSA1, a homolog of prokaryotic arsenite transporter and eukaryotic TRC40 for guided entry of tail-anchored proteins. Plant J 73:850–861CrossRefGoogle Scholar
  14. Hofmann NR, Theg SM (2005) Chloroplast outer membrane protein targeting and insertion. Trends Plant Sci 10:450–457CrossRefGoogle Scholar
  15. Hsu SC, Inoue K (2009) Two evolutionarily conserved essential β-barrel proteins in the chloroplast outer envelope membrane. Biosci Trends 3:168–178Google Scholar
  16. 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 78:147–158CrossRefGoogle Scholar
  17. Huang W, Ling Q, Bedard J, Lilley K, Jarvis P (2011) In vivo analyses of the roles of essential Omp85-related proteins in the chloroplast outer envelope membrane. Plant Physiol 157:147–159CrossRefGoogle Scholar
  18. Hwang YT, Pelitire SM, Henderson MP, Andrews DW, Dyer JM, Mullen RT (2004) Novel targeting signals mediate the sorting of different isoforms of the tail-anchored membrane protein cytochrome b5 to either endoplasmic reticulum or mitochondria. Plant Cell 16:3002–3019CrossRefGoogle Scholar
  19. Inoue K (2007) The chloroplast outer envelope membrane: The edge of light and excitement. J Integr Plant Biol 49(8):1100–1111CrossRefGoogle Scholar
  20. Inoue K (2011) Emerging roles of the chloroplast outer envelope membrane. Trends Plant Sci 16:550–557CrossRefGoogle Scholar
  21. 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 34:661–669CrossRefGoogle Scholar
  22. 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 171:425–430CrossRefGoogle Scholar
  23. Jaru-Ampornpan P, Shen K, Lam VQ, Ali M, Doniach S, Jia TZ, Shan S (2010) ATP-independent reversal of a membrane protein aggregate by a chloroplast SRP. Nat Struct Mol Biol 17(6):696–702CrossRefGoogle Scholar
  24. Kaufmann T, Schlipf S, Sanz J, Neubert K, Stein R, Borner C (2003) Characterization of the signal that directs Bcl-xL, but not Bcl-2, to the mitochondrial outer membrane. J Cell Biol 160:53–64CrossRefGoogle Scholar
  25. Keegstra K, Cline K (1999) Protein import and routing systems of chloroplasts. Plant Cell 11(4):557–570CrossRefGoogle Scholar
  26. Kessler F, Schnell D (2009) Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Curr Opin Cell Biol 21:494–500CrossRefGoogle Scholar
  27. Kim DH, Hwang I (2013) Direct targeting of proteins from the cytosol to organelles: the ER versus endosymbiotic organelles. Traffic 14(6):613–621CrossRefGoogle Scholar
  28. Kim DH, Xu Z-H, Na YJ, Yoo YJ, Lee J, Sohn EJ, Hwang I (2011) Small heat shock protein Hsp17.8 functions as an AKR2A cofactor in the targeting of chloroplast outer membrane proteins in Arabidopsis. Plant Physiol 157:132–146CrossRefGoogle Scholar
  29. Kim DH, Park MJ, Gwon GH, Silkov A, Xu ZY, Yang EC, Song S, Song K, Kim Y, Yoon HS, Honig B, Cho W, Cho Y, Hwang I (2014) An ankyrin repeat domain of AKR2 drives chloroplast targeting through coincident binding of two chloroplast lipids. Dev Cell 30(5):598–609CrossRefGoogle Scholar
  30. Kim DH, Lee JE, Xu ZY, Geem KR, Kwon Y, Park JW, Hwang I (2015) Cytosolic targeting factor AKR2A captures chloroplast outer membrane-localized client proteins at the ribosome during translation. Nat Commun 6:6843CrossRefGoogle Scholar
  31. Kriechbaumer V, Abell BM (2012) Chloroplast envelope protein targeting fidelity is independent of cytosolic components in dual organelle assays. Front Plant Sci 3:148CrossRefGoogle Scholar
  32. Lee DW, Hwang I (2018) Evolution and design principles of the diverse chloroplast transit peptides. Mol Cells 41:161–167Google Scholar
  33. 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 13:2175–2190CrossRefGoogle Scholar
  34. Lee YJ, Sohn EJ, Lee KH, Lee DW, Hwang I (2004) The transmembrane domain of AtToc64 and its C-terminal lysine-rich flanking region are targeting signals to the chloroplast outer envelope membrane [correction]. Mol Cells 17:281–291Google Scholar
  35. Lee DW, Lee S, Lee GJ, Lee KH, Kim S, Cheong GW, Hwang I (2006) Functional characterization of sequence motifs in the transit peptide of Arabidopsis small subunit of rubisco. Plant Physiol 140:466–483CrossRefGoogle Scholar
  36. Lee DW, Kim JK, Lee S, Choi S, Kim S, Hwang I (2008) Arabidopsis nuclear-encoded plastid transit peptides contain multiple sequence subgroups with distinctive chloroplast-targeting sequence motifs. Plant Cell 20:1603–1622CrossRefGoogle Scholar
  37. Lee J, Lee H, Kim J, Lee S, Kim DH, Kim S, Hwang I (2011) 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 23:1588–1607CrossRefGoogle Scholar
  38. Lee J, Kim DH, Hwang I (2014) Specific targeting of proteins to outer envelope membranes of endosymbiotic organelles, chloroplasts, and mitochondria. Front Plant Sci 5:1–11Google Scholar
  39. Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19:47–56CrossRefGoogle Scholar
  40. Li HM, Chiu CC (2010) Protein transport into chloroplasts. Ann Rev Plant Biol 61:157–180CrossRefGoogle Scholar
  41. Maestre-Reyna M, Wu SM, Chang YC, Chen CC, Maestre-Reyna A, Wang AH, Chang HY (2017) In search of tail-anchored protein machinery in plants: reevaluating the role of arsenite transporters. Sci Rep 7:46022CrossRefGoogle Scholar
  42. Margulis L (1981) Symbiosis in cell evolution. WH Freeman, New YorkGoogle Scholar
  43. Mereschkowsky C (1905) Über Natur und Ursprung der Chromatophoren im Pflanzenreiche. Biol Centralbl 25:593–604Google Scholar
  44. Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:226–228CrossRefGoogle Scholar
  45. 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 148:235–245CrossRefGoogle Scholar
  46. Qbadou S, Becker T, Bionda T, Reger K, Ruprecht M, Soll J, Schleiff E (2007) Toc64—a preprotein-receptor at the outer membrane with bipartide function. J Mol Biol 367(5):1330–1346CrossRefGoogle Scholar
  47. Rapaport D (2003) Finding the right organelle. Targeting signals in mitochondrial outer-membrane proteins. EMBO Rep 4:948–952CrossRefGoogle Scholar
  48. Rapaport D, Neupert W (1999) Biogenesis of Tom40, core component of the TOM complex of mitochondria. J Cell Biol 146:321–331CrossRefGoogle Scholar
  49. Reyes-Prieto A, Weber AP, Bhattacharya D (2007) The origin and establishment of the plastid in algae and plants. Annu Rev Genet 41:147–168CrossRefGoogle Scholar
  50. Schleiff E, Becker T (2011) Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat Rev Mol Cell Biol 12:48–59CrossRefGoogle Scholar
  51. Schleiff E, Soll J (2005) Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep 6:1023–1027CrossRefGoogle Scholar
  52. Schleiff E, Tien R, Salomon M, Soll J (2001) Lipid composition of outer leaflet of chloroplast outer envelope determines topology of OEP7. Mol Biol Cell 12(12):4090–4102CrossRefGoogle Scholar
  53. Schlünzen F, Wilson DN, Tian P, Harms JM, Mclnnes SJ, Hansen HA, Albrecht R, Buerger J, Wilbanks SM, Fucini P (2005) The binding mode of the trigger factor on the ribosome: implications for protein folding and SRP interaction. Structure 13(11):1685–1694CrossRefGoogle Scholar
  54. Shipman RL, Inoue K (2009) Suborganellar localization of plastidic type I signal peptidase 1 depends on chloroplast development. FEBS Lett 583:938–942CrossRefGoogle Scholar
  55. Simm S, Papasotiriou DG, Ibrahim M, Leisegang MS, Müller B, Schorge T, Karas M, Mirus O, Sommer MS, Schleiff E (2013) Defining the core proteome of the chloroplast envelope membranes. Front Plant Sci 4:11CrossRefGoogle Scholar
  56. Smith MD, Hiltbrunner A, Kessler F, Schnell DJ (2002) The targeting of the atToc159 preprotein receptor to the chloroplast outer membrane is mediated by its GTPase domain and is regulated by GTP. J Cell Biol 159:833–843CrossRefGoogle Scholar
  57. Sohrt K, Soll J (2000) Toc64, a new component of the protein translocon of chloroplasts. J Cell Biol 148(6):1213–1221CrossRefGoogle Scholar
  58. Spreter T, Pech M, Beatrix B (2005) The crystal structure of archaeal nascent polypeptide-associated complex (NAC) reveals a unique fold and the presence of a ubiquitin-associated domain. J Biol Chem 280(16):15849–15854CrossRefGoogle Scholar
  59. Stefanovic S, Hegde RS (2007) Identification of a targeting factor for posttranslational membrane protein insertion into the ER. Cell 128(6):1147–1159CrossRefGoogle Scholar
  60. Tranel PJ, Keegstra K (1996) A novel, bipartite transit peptide targets OEP75 to the outer membrane of the chloroplastic envelope. Plant Cell 8:2093–2104CrossRefGoogle Scholar
  61. 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 atToc75. Plant Cell 16:2078–2088CrossRefGoogle Scholar
  62. Ullers RS, Houben EN, Raine A, ten Hagen-Jongman CM, Ehrenberg M, Brunner J, Oudega B, Harms N, Luirink J (2003) Interplay of signal recognition particle and trigger factor at L23 near the nascent chain exit site on the Escherichia coli ribosome. J Cell Biol 161(4):679–684CrossRefGoogle Scholar
  63. von Heijne G (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225:487–494CrossRefGoogle Scholar
  64. Walther DM, Rapaport D, Tommassen J (2009) Biogenesis of beta-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell Mol Life Sci 66:2789–2804CrossRefGoogle Scholar
  65. Whatley JM (1978) A suggested cycle of plastid developmental interrelationships. New Phytol 80:489–502CrossRefGoogle Scholar
  66. Xing S, Mehlhorn DG, Wallmeroth N, Asseck LY, Kar R, Voss A, Denninger P, Schmidt VA, Schwarzländer M, Stierhof YD, Grossmann G, Grefen C (2017) Loss of GET pathway orthologs in Arabidopsis thaliana causes root hair growth defects and affects SNARE abundance. Proc Natl Acad Sci USA 114(8):E1544–E1553CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of BiologySunchon National UniversitySunchonSouth Korea
  2. 2.Biological Sciences and Research Institute for Basic ScienceWonkwang UniversityIksanSouth Korea
  3. 3.Department of Well-being ResourcesSunchon National UniversitySunchonSouth Korea

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