Three old and one new: Protein import into red algal-derived plastids surrounded by four membranes

Protoplasma

Volumn 250, Issue 5, 2013, Pages 1013-1023

  Stork, Simone ^a   Lau, Julia ^a   Moog, Daniel ^a   Maier, Uwe G ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Apicomplexans; Complex plastid; Diatom; Periplastidal membrane; Protein import; Secondary endosymbiosis; SELMA

Indexed keywords

ALGAE; APICOMPLEXA; BACILLARIOPHYTA; CHLOROPHYTA; CRYPTOPHYTA; EUKARYOTA; HAPTOPHYCEAE;

EVOLUTION; METABOLISM; PLASTID; PROTEIN TRANSPORT; RED ALGA; REVIEW;

BIOLOGICAL EVOLUTION; PLASTIDS; PROTEIN TRANSPORT; RHODOPHYTA;

EID: 84884909507     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-013-0498-7     Document Type: Review

References (95)

1. Agrawal S, van Dooren GG, Beatty WL, Striepen B (2009) Genetic evidence that an endosymbiont-derived endoplasmic reticulum-associated protein degradation (ERAD) system functions in import of apicoplast proteins. J Biol Chem 284: 33683-33691. doi: 10. 1074/jbc. M109. 044024.
2. Allen MD, Buchberger A, Bycroft M (2006) The PUB domain functions as a p97 binding module in human peptide N-glycanase. J Biol Chem 281: 25502-25508. doi: 10. 1074/jbc. M601173200.
3. Apt KE, Zaslavkaia L, Lippmeier JC, Lang M, Kilian O, Wetherbee R, Grossman AR, Kroth PG (2002) In vivo characterization of diatom multipartite plastid targeting signals. J Cell Sci 115: 4061-4069. doi: 10. 1242/jcs. 00092.
4. Armbrust EV, Berges JA, Bowler C, Green BR (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306(5693): 79-86. doi: 10. 1126/science. 1101156.
5. Baek GH, Kim I, Rao H (2011) The Cdc48 ATPase modulates the interaction between two proteolytic factors Ufd2 and Rad23. Proc Natl Acad Sci U S A. doi: 10. 1073/pnas. 1104051108.
6. Bagola K, Mehnert M, Jarosch E, Sommer T (2011) Protein dislocation from the ER. Biochim Biophys Acta 1808(3): 925-936. doi: 10. 1016/j. bbamem. 2010. 06. 025.
7. Bhaya D, Grossman A (1991) Targeting proteins to diatom plastids involves transport through an endoplasmic reticulum. Mol Gen Genet 229: 400-404. doi: 10. 1007/BF00267462.
8. Bodył A, Mackiewicz P, Gagat P (2012) Organelle evolution: Paulinella breaks a paradigm. Curr Biol 22(9): R304-R306. doi: 10. 1016/j. cub. 2012. 03. 020.
9. Bolte K, Bullmann L, Hempel F, Bozarth A, Zauner S, Maier U-G (2009) Protein targeting into secondary plastids. J Eukaryot Microbiol 56: 9-15. doi: 10. 1111/j. 1550-7408. 2008. 00370. x.
10. Borgese N, Fasana E (2011) Targeting pathways of C-tail-anchored proteins. Biochim Biophys Acta 1808(3): 937-946. doi: 10. 1016/j. bbamem. 2010. 07. 010.
11. Bullmann L, Haarmann R, Mirus O, Bredemeier R, Hempel F, Maier UG, Schleiff E (2010) Filling the gap, evolutionarily conserved Omp85 in plastids of chromalveolates. J Biol Chem 285: 6848-6856. doi: 10. 1074/jbc. M109. 074807.
12. Carvalho P, Goder V, Rapoport TA (2006) Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126(2): 361-373. doi: 10. 1016/j. cell. 2006. 05. 043.
13. Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J Eukaryot Microbiol 46(4): 347-366. doi: 10. 1111/j. 1550-7408. 1999. tb04614. x.
14. Cavalier-Smith T (2003) Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). Philos Trans R Soc Lond B Biol Sci 358: 109. doi: 10. 1098/rstb. 2002. 1194.
15. Curtis BA, Tanifuji G, Burki F et al (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492(7427): 59-65. doi: 10. 1038/nature11681.
16. DeRocher A, Hagen CB, Froehlich JE, Feagin JE, Parsons M (2000) Analysis of targeting sequences demonstrates that trafficking to the Toxoplasma gondii plastid branches off the secretory system. J Cell Sci 113(22): 3969-3977.
17. Deschamps P, Moreira D (2012) Re-evaluating the green contribution to diatom genomes. Genome Biol Evol 4(7): 683-688. doi: 10. 1093/gbe/evs053.
18. Douglas S, Zauner S, Fraunholz M et al (2001) The highly reduced genome of an enslaved algal nucleus. Nature 410: 1091-1096. doi: 10. 1038/35074092.
19. Felsner G, Sommer MS, Maier UG (2010) The physical and functional borders of transit peptide-like sequences in secondary endosymbionts. BMC Plant Biol 10: 223. doi: 10. 1186/1471-2229-10-223.
20. Felsner G, Sommer MS, Gruenheit N, Hempel F, Moog D, Zauner S, Martin W, Maier UG (2011) ERAD components in organisms with complex red plastids suggest recruitment of a preexisting protein transport pathway for the periplastid membrane. Genome Biol Evol 3: 140-150. doi: 10. 1093/gbe/evq074.
21. Finley D (2009) Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 78: 477-513. doi: 10. 1146/annurev. biochem. 78. 081507. 101607.
22. Forouzan D, Ammelburg M, Hobel CF, Ströh LJ, Sessler N, Martin J, Lupas AN (2012) The archaeal proteasome is regulated by a network of AAA ATPases. J Biol Chem. doi: 10. 1074/jbc. M112. 386458.
23. Foth BJ, Ralph SA, Tonkin CJ, Struck NS, Fraunholz M, Roos DS, Cowman AF, McFadden GI (2003) Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science 299(5607): 705-708. doi: 10. 1126/science. 1078599.
24. Funakoshi M, Sasaki T, Nishimoto T, Kobayashi H (2002) Budding yeast Dsk2p is a polyubiquitin-binding protein that can interact with the proteasome. Proc Natl Acad Sci U S A 99: 745-750. doi: 10. 1073/pnas. 012585199.
25. Gentle IE, Burri L, Lithgow T (2005) Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58(5): 1216-1225. doi: 10. 1111/j. 1365-2958. 2005. 04906. x.
26. 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(47): 39505-39512. doi: 10. 1074/jbc. M112. 405100.
27. Gould SB, Sommer MS, Kroth PG, Gile GH, Keeling PJ, Maier UG (2006) Nucleus-to-nucleus gene transfer and protein retargeting into a remnant cytoplasm of cryptophytes and diatoms. Mol Biol Evol 23(12): 2413-2422. doi: 10. 1093/molbev/msl113.
28. Gould SB, Fan E, Hempel F, Maier UG, Klosgen RB (2007) Translocation of a phycoerythrin alpha subunit across five biological membranes. J Biol Chem 282: 30295-30302. doi: 10. 1074/jbc. M701869200.
29. Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59: 491-517. doi: 10. 1146/annurev. arplant. 59. 032607. 092915.
30. Gray MW (2012) Mitochondrial evolution. Cold Spring Harb Perspect Biol 4(9). doi: 10. 1101/cshperspect. a011403.
31. Gruber A, Vugrinec S, Hempel F, Gould SB, Maier U-G, Kroth PG (2007) Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif. Plant Mol Biol 64: 519-530. doi: 10. 1007/s11103-007-9171-x.
32. Hampton RY, Sommer T (2012) Finding the will and the way of ERAD substrate retrotranslocation. Curr Opin Cell Biol 24(4): 460-466. doi: 10. 1016/j. ceb. 2012. 05. 010.
33. Hänzelmann P, Stingele J, Hofmann K, Schindelin H, Raasi S (2010) The yeast E4 ubiquitin ligase Ufd2 interacts with the ubiquitin-like domains of Rad23 and Dsk2 via a novel and distinct ubiquitin-like binding domain. J Biol Chem 285: 20390-20398. doi: 10. 1074/jbc. M110. 112532.
34. Hempel F, Bullmann L, Lau J, Zauner S, Maier UG (2009) ERAD-derived preprotein transport across the second outermost plastid membrane of diatoms. Mol Biol Evol 26: 1781-1790. doi: 10. 1093/molbev/msp079.
35. Hempel F, Felsner G, Maier UG (2010) New mechanistic insights into pre-protein transport across the second outermost plastid membrane of diatoms. Mol Microbiol 76: 793-801. doi: 10. 1111/j. 1365-2958. 2010. 07142. x.
36. Hirakawa Y, Burki F, Keeling PJ (2012) Genome-based reconstruction of the protein import machinery in the secondary plastid of a chlorarachniophyte alga. Eukaryot Cell 11(3): 324-333. doi: 10. 1128/EC. 05264-11.
37. Howe CJ, Barbrook AC, Nisbet RER, Lockhart PJ, Larkum AWD (2008) The origin of plastids. Philos Trans R Soc Lond B Biol Sci 363(1504): 2675-2685. doi: 10. 1098/rstb. 2008. 0050.
38. Izawa T, Nagai H, Endo T, Nishikawa S (2012) Yos9p and Hrd1p mediate ER retention of misfolded proteins for ER-associated degradation. Mol Biol Cell 23(7): 1283-1293. doi: 10. 1091/mbc. E11-08-0722.
39. Jarosch E, Taxis C, Volkwein C, Bordallo J, Finley D, Wolf DH, Sommer T (2002) Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nat Cell Biol 4: 134-139. doi: 10. 1016/j. bbamem. 2010. 06. 025.
40. Kalanon M, Tonkin C, McFadden G (2009) Characterization of two putative protein translocation components in the apicoplast of Plasmodium falciparum. Eukaryot Cell 8: 1146-1154. doi: 10. 1128/EC. 00061-09.
41. Karnataki A, DeRocher A, Coppens I, Nash C, Feagin JE, Parsons M (2007a) Cell cycle-regulated vesicular trafficking of Toxoplasma APT1, a protein localized to multiple apicoplast membranes. Mol Microbiol 63(6): 1653-1668. doi: 10. 1111/j. 1365-2958. 2007. 05619. x.
42. Karnataki A, DeRocher AE, Coppens I, Feagin JE, Parsons M (2007b) A membrane protease is targeted to the relict plastid of Toxoplasma via an internal signal sequence. Traffic 8(11): 1543-1553. doi: 10. 1111/j. 1600-0854. 2007. 00637. x.
43. Keeling PJ (2009) Chromalveolates and the evolution of plastids by secondary endosymbiosis. J Eukaryot Microbiol 56(1): 1-8. doi: 10. 1111/j. 1550-7408. 2008. 00371. x.
44. Keeling PJ (2013) The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu Rev Plant Biol 64(1): null. doi: 10. 1146/annurev-arplant-050312-120144.
45. Kessler F, Blobel G, Patel HA, Schnell DJ (1994) Identification of two GTP-binding proteins in the chloroplast protein import machinery. Science 266(5187): 1035-1039. doi: 10. 1126/science. 7973656.
46. Kilian O, Kroth PG (2005) Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J 41: 175-183. doi: 10. 1111/j. 1365-313X. 2004. 02294. x.
47. Kim I, Ahn J, Liu C, Tanabe K, Apodaca J, Suzuki T, Rao H (2006) The Png1-Rad23 complex regulates glycoprotein turnover. J Cell Biol 172(2): 211-219. doi: 10. 1083/jcb. 200507149.
48. Lang M, Apt KE, Kroth PG (1998) Protein transport into "complex" diatom plastids utilizes two different targeting signals. J Biol Chem 273: 30973-30978. doi: 10. 1074/jbc. 273. 47. 30973.
49. Lemgruber L, Kudryashev M, Dekiwadia C, Riglar DT, Baum J, Stahlberg H, Ralph SA, Frischknecht F (2013) Cryo-electron tomography reveals four-membrane architecture of the Plasmodium apicoplast. Malar J 12(1): 25. doi: 10. 1186/1475-2875-12-25.
50. Lim PJ, Danner R, Liang J et al (2009) Ubiquilin and p97/VCP bind erasin, forming a complex involved in ERAD. J Cell Biol 187: 201-217. doi: 10. 1083/jcb. 200903024.
51. Madsen L, Seeger M, Semple CA, Hartmann-Petersen R (2009) New ATPase regulators-p97 goes to the PUB. Int J Biochem Cell Biol 41: 2380-2388. doi: 10. 1016/j. biocel. 2009. 05. 017.
52. Maier UG, Douglas SE, Cavalier-Smith T (2000) The nucleomorph genomes of cryptophytes and chlorarachniophytes. Protist 151: 103. doi: 10. 1078/1434-4610-00011.
53. Martin W (2010) Evolutionary origins of metabolic compartmentalization in eukaryotes. Philos Trans R Soc Lond B Biol Sci 365(1541): 847-855. doi: 10. 1098/rstb. 2009. 0252.
54. Martinez Benitez E, Stolz A, Wolf DH (2011) Yos9, a control protein for misfolded glycosylated and non-glycosylated proteins in ERAD. FEBS Lett 585(19): 3015-3019. doi: 10. 1016/j. febslet. 2011. 08. 021.
55. McFadden GI, van Dooren GG (2004) Evolution: red algal genome affirms a common origin of all plastids. Curr Biol 14(13): R514-R516. doi: 10. 1016/j. cub. 2004. 06. 041.
56. Melkonian M (2001) Systematics and evolution of the algae. I. Genomics meets phylogeny. Vol 62. In: Progress in botany. Springer, Berlin, pp 340-382.
57. Moog D, Stork S, Zauner S, Maier U-G (2011) In silico and in vivo investigations of proteins of a minimized eukaryotic cytoplasm. Genome Biol Evol 3: 375-382. doi: 10. 1093/gbe/evr031.
58. Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D (2009) Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324(5935): 1724-1726. doi: 10. 1126/science. 1172983.
59. Müller M, Mentel M, van Hellemond JJ et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76(2): 444-495. doi: 10. 1128/mmbr. 05024-11.
60. Mullin KA, Lim L, Ralph SA, Spurck TP, Handman E, McFadden GI (2006) Membrane transporters in the relict plastid of malaria parasites. Proc Natl Acad Sci U S A 103(25): 9572-9577. doi: 10. 1073/pnas. 0602293103.
61. Nassoury N, Cappadocia M, Morse D (2003) Plastid ultrastructure defines the protein import pathway in dinoflagellates. J Cell Sci 116(Pt 14): 2867-2874. doi: 10. 1242/jcs. 00517.
62. Nathan JA, Tae Kim H, Ting L, Gygi SP, Goldberg AL (2013) Why do cellular proteins linked to K63-polyubiquitin chains not associate with proteasomes? EMBO J. doi: 10. 1038/emboj. 2012. 354.
63. Neuber O, Jarosch E, Volkwein C, Walter J, Sommer T (2005) Ubx2 links the Cdc48 complex to ER-associated protein degradation. Nat Cell Biol 7: 993-998. doi: 10. 1038/ncb1298.
64. Patron NJ, Waller RF (2007) Transit peptide diversity and divergence: a global analysis of plastid targeting signals. Bioessays 29: 1048-1058. doi: 10. 1002/bies. 20638.
65. Patron NJ, Waller RF, Keeling PJ (2006) A tertiary plastid uses genes from two endosymbionts. J Mol Biol 357(5): 1373-1382. doi: 10. 1016/j. jmb. 2006. 01. 084.
66. Pick E, Berman TS (2013) Formation of alternative proteasomes: same lady, different cap? FEBS Lett (0). doi: 10. 1016/j. febslet. 2013. 01. 014.
67. Pieuchot L, Jedd G (2012) Peroxisome assembly and functional diversity in eukaryotic microorganisms. Annu Rev Microbiol 66(1): 237-263. doi: 10. 1146/annurev-micro-092611-150126.
68. Ralph SA, Foth BJ, Hall N, McFadden GI (2004) Evolutionary pressures on apicoplast transit peptides. Mol Biol Evol 21(12): 2183-2194. doi: 10. 1093/molbev/msh233.
69. Rosenzweig R, Bronner V, Zhang D, Fushman D, Glickman MH (2012) Rpn1 and Rpn2 coordinate ubiquitin processing factors at the proteasome. J Biol Chem. doi: 10. 1074/jbc. M111. 316323.
70. Rubenstein EM, Kreft SG, Greenblatt W, Swanson R, Hochstrasser M (2012) Aberrant substrate engagement of the ER translocon triggers degradation by the Hrd1 ubiquitin ligase. J Cell Biol 197(6): 761-773. doi: 10. 1083/jcb. 201203061.
71. Sanchez-Pulido L, Devos D, Genevrois S, Vicente M, Valencia A (2003) POTRA: a conserved domain in the FtsQ family and a class of beta-barrel outer membrane proteins. Trends Biochem Sci 28(10): 523-526. doi: 10. 1016/j. tibs. 2003. 08. 003.
72. Sato S (2011) The apicomplexan plastid and its evolution. Cell Mol Life Sci 68(8): 1285-1296. doi: 10. 1007/s00018-011-0646-1.
73. Schäfer A, Wolf D (2009) Sec61p is part of the endoplasmic reticulum-associated degradation machinery. EMBO J 28: 2874-2884. doi: 10. 1038/emboj. 2009. 231.
74. Schleiff E, Becker T (2011) Common ground for protein translocation: access control for mitochondria and chloroplasts. Nat Rev Mol Cell Biol 12(1): 48-59. doi: 10. 1038/nrm3027.
75. Schnell DJ, Kessler F, Blobel G (1994) Isolation of components of the chloroplast protein import machinery. Science 266(5187): 1007-1012. doi: 10. 1126/science. 7973649.
76. Schuberth C, Buchberger A (2005) Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation. Nat Cell Biol 7: 999-1006. doi: 10. 1038/ncb1299.
77. Sheiner L, Demerly JL, Poulsen N, Beatty WL, Lucas O, Behnke MS, White MW, Striepen B (2011) A systematic screen to discover and analyze apicoplast proteins identifies a conserved and essential protein import factor. PLoS Pathog 7: e1002392. doi: 10. 1371/journal. ppat. 1002392.
78. Smith MH, Ploegh HL, Weissman JS (2011) Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334: 1086-1090. doi: 10. 1126/science. 1209235.
79. Sommer MS, Gould SB, Lehmann P, Gruber A, Przyborski JM, Maier U-G (2007) Der1-mediated preprotein import into the periplastid compartment of chromalveolates? Mol Biol Evol 24: 918-928. doi: 10. 1093/molbev/msm008.
80. Sommer MS, Daum B, Gross LE, Weis BL, Mirus O, Abram L, Maier UG, Kuhlbrandt W, Schleiff E (2011) Chloroplast Omp85 proteins change orientation during evolution. Proc Natl Acad Sci U S A 108(33): 13841-13846. doi: 10. 1073/pnas. 1108626108.
81. Spork S, Hiss JA, Mandel K, Sommer M, Kooij TWA, Chu T, Schneider G, Maier UG, Przyborski JM (2009) An unusual ERAD-like complex is targeted to the apicoplast of Plasmodium falciparum. Eukaryot Cell 8: 1134-1145. doi: 10. 1128/EC. 00083-09.
82. Stolz A, Hilt W, Buchberger A, Wolf DH (2011) Cdc48: a power machine in protein degradation. Trends Biochem Sci 36(10): 515-523. doi: 10. 1016/j. tibs. 2011. 06. 001.
83. Stork S, Moog D, Przyborski JM, Wilhelmi I, Zauner S, Maier UG (2012) Distribution of the SELMA translocon in secondary plastids of red algal origin and predicted uncoupling of ubiquitin-dependent translocation from degradation. Eukaryot Cell 11(12): 1472-1481. doi: 10. 1128/ec. 00183-12.
84. Suzuki T, Park H, Anderson Till E, Lennarz WJ (2001) The PUB domain: a putative protein-protein interaction domain implicated in the ubiquitin-proteasome pathway. Biochem Biophys Res Commun 287: 1083-1087. doi: 10. 1006/bbrc. 2001. 5688.
85. Theissen U, Martin W (2006) The difference between organelles and endosymbionts. Curr Biol CB 16(24): R1016-R1017. doi: 10. 1016/j. cub. 2006. 11. 020.
86. Thrower JS, Hoffman L, Rechsteiner M, Pickart CM (2000) Recognition of the polyubiquitin proteolytic signal. EMBO J 19: 94-102. doi: 10. 1093/emboj/19. 1. 94.
87. Tonkin CJ, Roos DS, McFadden GI (2006a) N-terminal positively charged amino acids, but not their exact position, are important for apicoplast transit peptide fidelity in Toxoplasma gondii. Mol Biochem Parasitol 150(2): 192-200. doi: 10. 1016/j. molbiopara. 2006. 08. 001.
88. Tonkin CJ, Struck NS, Mullin KA, Stimmler LM, McFadden GI (2006b) Evidence for Golgi-independent transport from the early secretory pathway to the plastid in malaria parasites. Mol Microbiol 61(3): 614-630. doi: 10. 1111/j. 1365-2958. 2006. 05244. x.
89. Trempe J-F (2011) Reading the ubiquitin postal code. Curr Opin Struct Biol 21: 792-801. doi: 10. 1016/j. sbi. 2011. 09. 009.
90. van Dooren GG, Tomova C, Agrawal S, Humbel BM, Striepen B (2008) Toxoplasma gondii Tic20 is essential for apicoplast protein import. Proc Natl Acad Sci U S A 105: 13574-13579. doi: 10. 1073/pnas. 0803862105.
91. Waller RF, Keeling PJ, Donald RGK et al (1998) Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc Natl Acad Sci U S A 95(21): 12352-12357. doi: 10. 1073/pnas. 95. 21. 12352.
92. Waller RF, Reed MB, Cowman AF, McFadden GI (2000) Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway. EMBO J 19(8): 1794-1802. doi: 10. 1093/emboj/19. 8. 1794.
93. Willer M, Forte GMA, Stirling CJ (2008) Sec61p is required for ERAD-L: genetic dissection of the translocation and ERAD-L functions of Sec61p using novel derivatives of CPY. J Biol Chem 283(49): 33883-33888. doi: 10. 1074/jbc. M803054200.
94. Woehle C, Dagan T, Martin WF, Gould SB (2011) Red and problematic green phylogenetic signals among thousands of nuclear genes from the photosynthetic and apicomplexa-related Chromera velia. Genome Biol Evol 3: 1220-1230. doi: 10. 1093/gbe/evr100.
95. Wunder T, Martin R, Loffelhardt W, Schleiff E, Steiner JM (2007) The invariant phenylalanine of precursor proteins discloses the importance of Omp85 for protein translocation into cyanelles. BMC Evol Biol 7: 236. doi: 10. 1186/1471-2148-7-236.