Fates of Sec, Tat, and YidC Translocases in Mitochondria and Other Eukaryotic Compartments
Jazyk angličtina Země Spojené státy americké Médium print
Typ dokumentu časopisecké články, práce podpořená grantem, přehledy
PubMed
34436602
PubMed Central
PMC8662606
DOI
10.1093/molbev/msab253
PII: 6358141
Knihovny.cz E-zdroje
- Klíčová slova
- eukaryogenesis, membrane trafficking, neofunctionalization, protein targeting,
- MeSH
- Eukaryota * genetika metabolismus MeSH
- membránové transportní proteiny genetika metabolismus MeSH
- mitochondriální proteiny genetika metabolismus MeSH
- mitochondrie genetika metabolismus MeSH
- molekulární evoluce MeSH
- proteiny z Escherichia coli * genetika MeSH
- transport proteinů MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- membránové transportní proteiny MeSH
- mitochondriální proteiny MeSH
- proteiny z Escherichia coli * MeSH
Formation of mitochondria by the conversion of a bacterial endosymbiont was a key moment in the evolution of eukaryotes. It was made possible by outsourcing the endosymbiont's genetic control to the host nucleus, while developing the import machinery for proteins synthesized on cytosolic ribosomes. The original protein export machines of the nascent organelle remained to be repurposed or were completely abandoned. This review follows the evolutionary fates of three prokaryotic inner membrane translocases Sec, Tat, and YidC. Homologs of all three translocases can still be found in current mitochondria, but with different importance for mitochondrial function. Although the mitochondrial YidC homolog, Oxa1, became an omnipresent independent insertase, the other two remained only sporadically present in mitochondria. Only a single substrate is known for the mitochondrial Tat and no function has yet been assigned for the mitochondrial Sec. Finally, this review compares these ancestral mitochondrial proteins with their paralogs operating in the plastids and the endomembrane system.
Zobrazit více v PubMed
Akimaru J, Matsuyama S, Tokuda H, Mizushima S.. 1991. Reconstitution of a protein translocation system containing purified SecY, SecE, and SecA from Escherichia coli. Proc Natl Acad Sci USA. 88(15):6545–6549. PubMed PMC
Alami M, Lüke I, Deitermann S, Eisner G, Koch H-G, Brunner J, Müller M.. 2003. Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol Cell. 12(4):937–946. PubMed
Albiniak AM, Baglieri J, Robinson C.. 2012. Targeting of lumenal proteins across the thylakoid membrane. J Exp Bot. 63(4):1689–1698. PubMed
Alcock F, Stansfeld PJ, Basit H, Habersetzer J, Baker MA, Palmer T, Wallace MI, Berks BC.. 2016. Assembling the Tat protein translocase. Elife 5:1–28. PubMed PMC
Alder NN, Jensen RE, Johnson AE.. 2008. Fluorescence mapping of mitochondrial TIM23 complex reveals a water-facing, substrate-interacting helix surface. Cell 134(3):439–450. PubMed
Andersson SGE, Zomorodipour A, Andersson JO, Sicheritz-Pontén T, Alsmark UCM, Podowski RM, Näslund AK, Eriksson AS, Winkler HH, Kurland CG.. 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396(6707):133–140. PubMed
Angelini S, Deitermann S, Koch HG.. 2005. FtsY, the bacterial signal-recognition particle receptor, interacts functionally and physically with the SecYEG translocon. EMBO Rep. 6(5):476–481. PubMed PMC
Anghel SA, McGilvray PT, Hegde RS, Keenan RJ.. 2017. Identification of Oxa1 homologs operating in the eukaryotic endoplasmic reticulum. Cell Rep. 21(13):3708–3716. PubMed PMC
Aschtgen MS, Zoued A, Lloubès R, Journet L, Cascales E.. 2012. The C-tail anchored TssL subunit, an essential protein of the enteroaggregative Escherichia coli Sci-1 Type VI secretion system, is inserted by YidC. Microbiologyopen 1(1):71–82. PubMed PMC
Belin D, Plaia G, Boulfekhar Y, Silva F.. 2015. Escherichia coli SecG is required for residual export mediated by mutant signal sequences and for SecY-SecE complex stability. J Bacteriol. 197(3):542–552. PubMed PMC
Benz M, Bals T, Gügel IL, Piotrowski M, Kuhn A, Schünemann D, Soll J, Ankele E.. 2009. Alb4 of Arabidopsis promotes assembly and atabilization of a non chlorophyll-binding photosynthetic complex, the CF1CF0–ATP synthase. Mol Plant. 2(6):1410–1424. PubMed
Berks BC. 1996. A common export pathway for proteins binding complex redox cofactors? Mol Microbiol. 22(3):393–404. PubMed
Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, et al.2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res. 42(Web Server issue):W252–W258. PubMed PMC
Bieker KL, Phillips GJ, Silhavy TJ.. 1990. The sec and prl genes of Escherichia coli. J Bioenerg Biomembr. 22(3):291–310. PubMed
Blobel G, Dobberstein B.. 1975. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol. 67(3):835–851. PubMed PMC
Bolhuis A, Mathers JE, Thomas JD, Barrett CM, Robinson C.. 2001. TatB and TatC form a functional and structural unit of the twin-arginine translocase from Escherichia coli. J Biol Chem. 276(23):20213–20219. PubMed
Bonnefoy N, Chalvet F, Hamel P, Slonimski PP, Dujardin G.. 1994. OXA1, a Saccharomyces cerevisiae nuclear gene whose sequence is conserved from prokaryotes to eukaryotes controls cytochrome oxidase biogenesis. J Mol Biol. 239(2):201–212. PubMed
Bonnefoy N, Fiumera HL, Dujardin G, Fox TD.. 2009. Roles of Oxa1-related inner-membrane translocases in assembly of respiratory chain complexes. Biochim Biophys Acta. 1793(1):60–70. PubMed PMC
Borowska MT, Dominik PK, Anghel SA, Kossiakoff AA, Keenan RJ.. 2015. A YidC-like protein in the archaeal plasma membrane. Structure 23(9):1715–1724. PubMed PMC
Burger G, Gray MW, Forget L, Lang BF.. 2013. Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biol Evol. 5(2):418–438. PubMed PMC
Calvo SE, Clauser KR, Mootha VK.. 2016. MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins. Nucleic Acids Res. 44(D1):D1251–D1257. PubMed PMC
Cannon KS, Or E, Clemons WM, Shibata Y, Rapoport TA.. 2005. Disulfide bridge formation between SecY and a translocating polypeptide localizes the translocation pore to the center of SecY. J Cell Biol. 169(2):219–225. PubMed PMC
Cao TB, Saier MH.. 2003. The general protein secretory pathway: phylogenetic analyses leading to evolutionary conclusions. Biochim Biophys Acta Biomembr. 1609(1):115–125. PubMed
Carrie C, Weißenberger S, Soll J.. 2016. Plant mitochondria contain the protein translocase subunits TatB and TatC. J Cell Sci. 129(20):3935–3947. PubMed
Cavalier-Smith T, Lee JJ.. 1985. Protozoa as hosts for endosymbioses and the conversion of symbionts into organelles. J Protozool. 32(3):376–379.
Celedon JM, Cline K.. 2013. Intra-plastid protein trafficking: how plant cells adapted prokaryotic mechanisms to the eukaryotic condition. Biochim Biophys Acta. 1833(2):341–351. PubMed PMC
Chacinska A, Pfannschmidt S, Wiedemann N, Kozjak V, Sanjuán Szklarz LK, Schulze-Specking A, Truscott KN, Guiard B, Meisinger C, Pfanner N.. 2004. Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO J. 23(19):3735–3746. PubMed PMC
Chen Y, Dalbey RE.. 2018. Oxa1 superfamily: new members found in the ER. Trends Biochem Sci. 43(3):151–153. PubMed
Cline K, Dabney-Smith C.. 2008. Plastid protein import and sorting: different paths to the same compartments. Curr Opin Plant Biol. 11(6):585–592. PubMed PMC
Costa TRD, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, Waksman G.. 2015. Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol. 13(6):343–359. PubMed
Daley DO, Adams KL, Clifton R, Qualmann S, Millar AH, Palmer JD, Pratje E, Whelan J.. 2002. Gene transfer from mitochondrion to nucleus: novel mechanisms for gene activation from Cox2. Plant J. 30(1):11–21. PubMed
de Leeuw E, Granjon T, Porcelli I, Alami M, Carr SB, Müller M, Sargent F, Palmer T, Berks BC.. 2002. Oligomeric properties and signal peptide binding by Escherichia coli Tat protein transport complexes. J Mol Biol. 322(5):1135–1146. PubMed
Denks K, Vogt A, Sachelaru I, Petriman N-A, Kudva R, Koch H-G.. 2014. The Sec translocon mediated protein transport in prokaryotes and eukaryotes. Mol Membr Biol. 31(2–3):58–84. PubMed
Dilks K, Rose RW, Hartmann E, Pohlschröder M.. 2003. Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J Bacteriol. 185(4):1478–1483. PubMed PMC
Dolezal P, Likic V, Tachezy J, Lithgow T.. 2006. Evolution of the molecular machines for protein import into mitochondria. Science 313(5785):314–318. PubMed
Dolezal P, Makki A, Dyall SD.. 2019. Protein import into hydrogenosomes and mitosomes. In: Tachezy J, editor. Hydrogenosomes and mitosomes: mitochondria of anaerobic eukaryotes. Microbiology monographs. Cham: Springer. p. 31–84.
Driessen AJM, Nouwen N.. 2008. Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem. 77:643–667. PubMed
Du Plessis DJF, Nouwen N, Driessen AJM.. 2006. Subunit A of cytochrome o oxidase requires both YidC and SecYEG for membrane insertion. J Biol Chem. 281(18):12248–12252. PubMed
Eichler J, Moll R.. 2001. The signal recognition particle of Archaea. Trends Microbiol. 9(3):130–136. PubMed
Elliott LE, Saracco SA, Fox TD.. 2012. Multiple roles of the Cox20 chaperone in assembly of saccharomyces cerevisiae cytochrome C oxidase. Genetics 190(2):559–567. PubMed PMC
Endo T, Yamano K.. 2010. Transport of proteins across or into the mitochondrial outer membrane. Biochim Biophys Acta. 1803(6):706–714. PubMed
Ernster L, Schatz G.. 1981. Mitochondria: a historical review. J Cell Biol. 91(3 Pt 2):227s–255s. PubMed PMC
Esser K, Jan PS, Pratje E, Michaelis G.. 2004. The mitochondrial IMP peptidase of yeast: functional analysis of domains and identification of Gut2 as a new natural substrate. Mol Genet Genomics. 271(5):616–626. PubMed
Facey SJ, Neugebauer SA, Krauss S, Kuhn A.. 2007. The mechanosensitive channel protein MscL is targeted by the SRP to the novel YidC membrane insertion pathway of Escherichia coli. J Mol Biol. 365(4):995–1004. PubMed
Frain KM, Robinson C, van Dijl JM.. 2019. Transport of folded proteins by the Tat System. Protein J. 38(4):377–388. PubMed PMC
Fukasawa Y, Oda T, Tomii K, Imai K.. 2017. Origin and evolutionary alteration of the mitochondrial import system in eukaryotic lineages. Mol Biol Evol. 34(7):1574–1586. PubMed PMC
Funes S, Nargang FE, Neupert W, Herrmann JM.. 2004. The Oxa2 protein of Neurospora crassa plays a critical role in the biogenesis of cytochrome oxidase and defines a ubiquitous subbranch of the Oxa1/YidC/Alb3 protein family. Mol Biol Cell. 15(4):1853–1861. PubMed PMC
Gabaldón T, Huynen MA.. 2007. From endosymbiont to host-controlled organelle: the hijacking of mitochondrial protein synthesis and metabolism. PLoS Comput. Biol. 3:2209–2218. PubMed PMC
Gabaldón T, Snel B, van Zimmeren F, Hemrika W, Tabak H, Huynen MA.. 2006. Origin and evolution of the peroxisomal proteome. Biol Direct. 1:8. PubMed PMC
Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, et al.2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419(6906):498–511. PubMed PMC
Gentle I, Gabriel K, Beech P, Waller R, Lithgow T.. 2004. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol. 164(1):19–24. PubMed PMC
Gerdes L, Bals T, Klostermann E, Karl M, Philippar K, Hünken M, Soll J, Schünemann D.. 2006. A second thylakoid membrane-localized Alb3/OxaI/YidC homologue is involved in proper chloroplast biogenesis in Arabidopsis thaliana. J Biol Chem. 281(24):16632–16642. PubMed
Ghaemmaghami S, Huh W-K, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS.. 2003. Global analysis of protein expression in yeast. Nature 425(6959):737–741. PubMed
Gillespie JJ, Kaur SJ, S, Rahman M, Rennoll-Bankert K, Sears KT, Beier-Sexton M, Azad AF.. 2015. Secretome of obligate intracellular Rickettsia. FEMS Microbiol Rev. 39(1):47–80. PubMed PMC
Gray MW. 2015. Mosaic nature of the mitochondrial proteome: implications for the origin and evolution of mitochondria. Proc Natl Acad Sci USA. 112(33):10133–10138. PubMed PMC
Gray MW, Lang BF, Burger G.. 2004. Mitochondria of protists. Annu Rev Genet. 38:477–524. PubMed
Guna A, Volkmar N, Christianson JC, Hegde RS.. 2018. The ER membrane protein complex is a transmembrane domain insertase. Science 359(6374):470–473. PubMed PMC
Hamsanathan S, Musser SM.. 2018. The Tat protein transport system: intriguing questions and conundrums. FEMS Microbiol. Lett. 365: 1–11. PubMed PMC
Haque ME, Elmore KB, Tripathy A, Koc H, Koc EC, Spremulli LL.. 2010. Properties of the C-terminal tail of human mitochondrial inner membrane protein Oxa1L and its interactions with mammalian mitochondrial ribosomes. J Biol Chem. 285(36):28353–28362. PubMed PMC
Hell K, Neupert W, Stuart RA.. 2001. Oxa1p acts as a general membrane insertion machinery for proteins encoded by mitochondrial DNA. EMBO J. 20(6):1281–1288. PubMed PMC
Hempel J, Zehner S, Göttfert M, Patschkowski T.. 2009. Analysis of the secretome of the soybean symbiont Bradyrhizobium japonicum. J Biotechnol. 140(1–2):51–58. PubMed
Hill K, Model K, Ryan MT, Dietmeier K, Martin F, Wagner R, Pfanner N.. 1998. Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature 395(6701):516–521. PubMed
Horváthová L, Žárský V, Pánek T, Derelle R, Pyrih J, Motyčková A, Klápšťová V, Vinopalová M, Marková L, Voleman L, et al.2021. Analysis of diverse eukaryotes suggests the existence of an ancestral mitochondrial apparatus derived from the bacterial type II secretion system. Nat Commun. 12(1):2947. PubMed PMC
Hou B, Heidrich ES, Mehner-Breitfeld D, Brüser T.. 2018. The TatA component of the twin-arginine translocation system locally weakens the cytoplasmic membrane of Escherichia coli upon protein substrate binding. J Biol Chem. 293(20):7592–7605. PubMed PMC
Husnik F, Keeling PJ.. 2019. The fate of obligate endosymbionts: reduction, integration, or extinction. Curr Opin Genet Dev. 58-59:1–8. PubMed
Jacob F. 1977. Evolution and tinkering. Science 196(4295):1161–1166. PubMed
Jiang F, Chen M, Yi L, de Gier J-W, Kuhn A, Dalbey RE.. 2003. Defining the regions of Escherichia coli YidC that contribute to activity. J Biol Chem. 278(49):48965–48972. PubMed
Karamanou S, Gouridis G, Papanikou E, Sianidis G, Gelis I, Keramisanou D, Vrontou E, Kalodimos CG, Economou A.. 2007. Preprotein-controlled catalysis in the helicase motor of SecA. EMBO J. 26(12):2904–2914. PubMed PMC
Kiefer D, Kuhn A.. 2018. YidC-mediated membrane insertion. FEMS Microbiol Lett. 365(12):1–6. PubMed
Kohler R, Boehringer D, Greber B, Bingel-Erlenmeyer R, Collinson I, Schaffitzel C, Ban N.. 2009. YidC and Oxa1 form dimeric insertion pores on the translating ribosome. Mol Cell. 34(3):344–353. PubMed
Kol S, Majczak W, Heerlien R, van der Berg JP, Nouwen N, Driessen AJM.. 2009. Subunit A of the F1FO ATP synthase requires YidC and SecYEG for membrane insertion. J Mol Biol. 390(5):893–901. PubMed
Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N.. 2003. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem. 278(49):48520–48523. PubMed
Kumazaki K, Kishimoto T, Furukawa A, Mori H, Tanaka Y, Dohmae N, Ishitani R, Tsukazaki T, Nureki O.. 2014. Crystal structure of Escherichia coli YidC, a membrane protein chaperone and insertase. Sci Rep. 4:7299. PubMed PMC
Lang BF, Burger G, O’Kelly CJ, Cedergren R, Golding GB, Lemieux C, Sankoff D, Turmel M, Gray MW.. 1997. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387(6632):493–497. PubMed
Lewis AJO, Hegde RS.. 2021. A unified evolutionary origin for SecY and YidC. bioRxiv. doi:10.1101/2020.12.20.422553. PubMed PMC
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(4):2121–2137. PubMed PMC
Makki A, Rada P, Žárský V, Kereïche S, Kováčik L, Novotný M, Jores T, Rapaport D, Tachezy J.. 2019. Triplet-pore structure of a highly divergent TOM complex of hydrogenosomes in Trichomonas vaginalis. PLoS Biol. 17(1):e3000098. PubMed PMC
Mani J, Meisinger C, Schneider A.. 2016. Peeping at TOMs—diverse entry gates to mitochondria provide insights into the evolution of eukaryotes. Mol Biol Evol. 33(2):337–351. PubMed
Martijn J, Vosseberg J, Guy L, Offre P, Ettema TJG.. 2018. Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature 557(7703):101–105. PubMed
Martin WF, Garg S, Zimorski V.. 2015. Endosymbiotic theories for eukaryote origin. Philos Trans R Soc Lond B Biol Sci. 370(1678):20140330. PubMed PMC
McCutcheon JP. 2016. From microbiology to cell biology: when an intracellular bacterium becomes part of its host cell. Curr Opin Cell Biol. 41:132–136. PubMed PMC
McGilvray PT, Anghel SA, Sundaram A, Zhong F, Trnka MJ, Fuller JR, Hu H, Burlingame AL, Keenan RJ.. 2020. An ER translocon for multi-pass membrane protein biogenesis. Elife 9:1–43. PubMed PMC
Meinecke M, Wagner R, Kovermann P, Guiard B, Mick DU, Hutu DP, Voos W, Truscott KN, Chacinska A, Pfanner N, et al.2006. Tim50 maintains the permeability barrier of the mitochondrial inner membrane. Science 312(5779):1523–1526. PubMed
Ménétret J-F, Schaletzky J, Clemons WM, Osborne AR, Skånland SS, Denison C, Gygi SP, Kirkpatrick DS, Park E, Ludtke SJ, et al.2007. Ribosome binding of a Single copy of the SecY complex: implications for protein translocation. Mol Cell. 28(6):1083–1092. PubMed
Mokranjac D. 2020. How to get to the other side of the mitochondrial inner membrane – the protein import motor. Biol Chem. 401(6–7):723–736. PubMed
Molik S, Karnauchov I, Weidlich C, Herrmann RG, Klösgen RB.. 2001. The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J Biol Chem. 276(46):42761–42766. PubMed
Moore M, Harrison MS, Peterson EC, Henry R.. 2000. Chloroplast Oxa1p homolog albino3 is required for post-translational integration of the light harvesting chlorophyll-binding protein into thylakoid membranes. J Biol Chem. 275(3):1529–1532. PubMed
Morgenstern M, Stiller SB, Lübbert P, Peikert CD, Dannenmaier S, Drepper F, Weill U, Höß P, Feuerstein R, Gebert M, et al.2017. Definition of a high-confidence mitochondrial proteome at quantitative scale. Cell Rep. 19(13):2836–2852. PubMed PMC
Natale P, Brüser T, Driessen AJM.. 2008. Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane—distinct translocases and mechanisms. Biochim Biophys Acta. 1778(9):1735–1756. PubMed
Nishiyama K, Hanada M, Tokuda H.. 1994. Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Escherichia coli at low temperature. EMBO J. 13(14):3272–3277. PubMed PMC
Orfanoudaki G, Economou A.. 2014. Proteome-wide subcellular topologies of E. coli polypeptides database (STEPdb). Mol Cell Proteomics. 13(12):3674–3687. PubMed PMC
Orriss GL, Tarry MJ, Ize B, Sargent F, Lea SM, Palmer T, Berks BC.. 2007. TatBC, TatB, and TatC form structurally autonomous units within the twin arginine protein transport system of Escherichia coli. FEBS Lett. 581(21):4091–4097. PubMed PMC
Ott M, Prestele M, Bauerschmitt H, Funes S, Bonnefoy N, Herrmann JM.. 2006. Mba1, a membrane-associated ribosome receptor in mitochondria. EMBO J. 25(8):1603–1610. PubMed PMC
Owji H, Nezafat N, Negahdaripour M, Hajiebrahimi A, Ghasemi Y.. 2018. A comprehensive review of signal peptides: structure, roles, and applications. Eur J Cell Biol. 97(6):422–441. PubMed
Palmer T, Berks BC.. 2012. The twin-arginine translocation (Tat) protein export pathway. Nat Rev Microbiol. 10(7):483–496. PubMed
Palmer T, Stansfeld PJ.. 2020. Targeting of proteins to the twin‐arginine translocation pathway. Mol Microbiol. 113(5):861–871. PubMed PMC
Panigrahi AK, Ogata Y, Zíková A, Anupama A, Dalley RA, Acestor N, Myler PJ, Stuart KD.. 2009. A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 9(2):434–450. PubMed PMC
Park E, Rapoport TA.. 2012. Bacterial protein translocation requires only one copy of the SecY complex in vivo. J Cell Biol. 198(5):881–893. PubMed PMC
Peltier J-B, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Söderberg L, Roepstorff P, von Heijne G, et al.2002. Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14(1):211–236. PubMed PMC
Perry AJ, Hulett JM, Likić VA, Lithgow T, Gooley PR.. 2006. Convergent evolution of receptors for protein import into mitochondria. Curr Biol. 16(3):221–229. PubMed
Petrů M, Wideman J, Moore K, Alcock F, Palmer T, Doležal P.. 2018. Evolution of mitochondrial TAT translocases illustrates the loss of bacterial protein transport machines in mitochondria. BMC Biol. 16(1):141. PubMed PMC
Pett W, Lavrov DV.. 2013. The twin-arginine subunit C in Oscarella: origin, evolution, and potential functional significance. Integr Comp Biol. 53(3):495–502. PubMed
Poueymiro M, Genin S.. 2009. Secreted proteins from Ralstonia solanacearum: a hundred tricks to kill a plant. Curr Opin Microbiol. 12(1):44–52. PubMed
Price CE, Driessen AJM.. 2010. Conserved negative charges in the transmembrane segments of subunit K of the NADH:ubiquinone oxidoreductase determine its dependence on YidC for membrane insertion. J Biol Chem. 285(6):3575–3581. PubMed PMC
Pyrih J, Pánek T, Durante IM, Rašková V, Cimrhanzlová K, Kriegová E, Tsaousis AD, Eliáš M, Lukeš J.. 2021. Vestiges of the bacterial signal recognition particle-based protein targeting in mitochondria. Mol Biol Evol. 38(8):3170–3187. PubMed PMC
Rapoport TA. 2008. Protein transport across the endoplasmic reticulum membrane. FEBS J. 275(18):4471–4478. PubMed
Richardson LGL, Singhal R, Schnell DJ.. 2017. The integration of chloroplast protein targeting with plant developmental and stress responses. BMC Biol. 15(1):118. PubMed PMC
Rissler M, Wiedemann N, Pfannschmidt S, Gabriel K, Guiard B, Pfanner N, Chacinska A.. 2005. The essential mitochondrial protein Erv1 cooperates with Mia40 in biogenesis of intermembrane space proteins. J Mol Biol. 353(3):485–492. PubMed
Roger AJ, Muñoz-Gómez SA, Kamikawa R.. 2017. The origin and diversification of mitochondria. Curr Biol. 27(21):R1177–R1192. PubMed
Rout S, Oeljeklaus S, Makki A, Tachezy J, Warscheid B, Schneider A.. 2021. Determinism and contingencies shaped the evolution of mitochondrial protein import. Proc Natl Acad Sci USA. 118:e2017774118. PubMed PMC
Sääf A, Monné M, de Gier JW, von Heijne G.. 1998. Membrane topology of the 60-kDa Oxa1p homologue from Escherichia coli. J Biol Chem. 273(46):30415–30418. PubMed
Samuelson JC, Chen M, Jiang F, Möller I, Wiedmann M, Kuhn A, Phillips GJ, Dalbey RE.. 2000. YidC mediates membrane protein insertion in bacteria. Nature 406(6796):637–641. PubMed
Saracco SA, Fox TD.. 2002. Cox18p is required for export of the mitochondrially encoded Saccharomyces cerevisiae Cox2p C-tail and interacts with Pnt1p and Mss2p in the inner membrane. Mol Biol Cell. 13(4):1122–1131. PubMed PMC
Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C, Berks BC, Palmer T.. 1998. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17(13):3640–3650. PubMed PMC
Schäfer K, Künzler P, Schneider K, Klingl A, Eubel H, Carrie C.. 2020. The plant mitochondrial TAT pathway is essential for complex III biogenesis. Curr Biol. 30(5):840–853.e5. PubMed
Schatz PJ, Beckwith J.. 1990. Genetic analysis of protein export in Escherichia coli. Annu Rev Genet. 24:215–248. PubMed
Schlacht A, Herman EK, Klute MJ, Field MC, Dacks JB.. 2014. Missing pieces of an ancient puzzle: evolution of the eukaryotic membrane-trafficking system. Cold Spring Harb Perspect Biol. 6(10):a016048. PubMed PMC
Schneider A, Behrens M, Scherer P, Pratje E, Michaelis G, Schatz G.. 1991. Inner membrane protease I, an enzyme mediating intramitochondrial protein sorting in yeast. EMBO J. 10(2):247–254. PubMed PMC
Schuldiner M, Metz J, Schmid V, Denic V, Rakwalska M, Schmitt HD, Schwappach B, Weissman JS.. 2008. The GET complex mediates insertion of tail-anchored proteins into the ER membrane. Cell 134(4):634–645. PubMed PMC
Settles AM, Yonetani A, Baron A, Bush DR, Cline K, Martienssen R.. 1997. Sec-independent protein translocation by the maize Hcf106 protein. Science 278(5342):1467–1470. PubMed
Shanmugam SK, Dalbey RE.. 2019. The conserved role of YidC in membrane protein biogenesis. Protein Secret Bact. 7:43–51. PubMed PMC
Shimokawa-Chiba N, Kumazaki K, Tsukazaki T, Nureki O, Ito K, Chiba S.. 2015. Hydrophilic microenvironment required for the channel-independent insertase function of YidC protein. Proc Natl Acad Sci USA. 112(16):5063–5068. PubMed PMC
Sibbald SJ, Archibald JM.. 2020. Genomic insights into plastid evolution. Genome Biol Evol. 12(7):978–990. PubMed PMC
Skalitzky CA, Martin JR, Harwood JH, Beirne JJ, Adamczyk BJ, Heck GR, Cline K, Fernandez DE.. 2011. Plastids contain a second sec translocase system with essential functions. Plant Physiol. 155(1):354–369. PubMed PMC
Škodová-Sveráková I, Záhonová K, Bučková B, Füssy Z, Yurchenko V, Lukeš J.. 2020. Catalase and ascorbate peroxidase in euglenozoan protists. Pathogens 9:317. PubMed PMC
Smets D, Loos MS, Karamanou S, Economou A.. 2019. Protein transport across the bacterial plasma membrane by the Sec pathway. Protein J. 38(3):262–273. PubMed
Stiller SB, Höpker J, Oeljeklaus S, Schütze C, Schrempp SG, Vent-Schmidt J, Horvath SE, Frazier AE, Gebert N, van der Laan M, et al.2016. Mitochondrial OXA translocase plays a major role in biogenesis of inner-membrane proteins. Cell Metab. 23(5):901–908. PubMed PMC
Summer EJ, Mori H, Settles AM, Cline K.. 2000. The thylakoid ΔpH-dependent pathway machinery facilitates RR-independent N-tail protein integration. J Biol Chem. 275(31):23483–23490. PubMed
Supekova L, Supek F, Greer JE, Schultz PG.. 2010. A single mutation in the first transmembrane domain of yeast COX2 enables its allotopic expression. Proc Natl Acad Sci USA. 107(11):5047–5052. PubMed PMC
Tarry MJ, Schäfer E, Chen S, Buchanan G, Greene NP, Lea SM, Palmer T, Saibil HR, Berks BC.. 2009. Structural analysis of substrate binding by the TatBC component of the twin-arginine protein transport system. Proc Natl Acad Sci USA. 106(32):13284–13289. PubMed PMC
Timón-Gómez A, Nývltová E, Abriata LA, Vila AJ, Hosler J, Barrientos A.. 2018. Mitochondrial cytochrome c oxidase biogenesis: recent developments. Semin Cell Dev Biol. 76:163–178. PubMed PMC
Tong J, Dolezal P, Selkrig J, Crawford S, Simpson AGB, Noinaj N, Buchanan SK, Gabriel K, Lithgow T.. 2011. Ancestral and derived protein import pathways in the mitochondrion of Reclinomonas americana. Mol Biol Evol. 28(5):1581–1591. PubMed PMC
Tsirigotaki A, De Geyter J, Šoštarić N, Economou A, Karamanou S.. 2017. Protein export through the bacterial Sec pathway. Nat Rev Microbiol. 15(1):21–36. PubMed
Valentin K. 1993. SecA is plastid-encoded in a red alga: implications for the evolution of plastid genomes and the thylakoid protein import apparatus. Mol Gen Genet. 236(2–3):245–250. PubMed
van den Berg B, Clemons WM, Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA.. 2004. X-ray structure of a protein-conducting channel. Nature 427(6969):36–44. PubMed
von Heijne G. 1990. Protein targeting signals. Curr Opin Cell Biol. 2(4):604–608. PubMed
von Heijne G. 2006. Membrane-protein topology. Nat Rev Mol Cell Biol. 7(12):909–918. PubMed
Vosseberg J, van Hooff JJE, Marcet-Houben M, van Vlimmeren A, van Wijk LM, Gabaldón T, Snel B.. 2021. Timing the origin of eukaryotic cellular complexity with ancient duplications. Nat Ecol Evol. 5(1):92–100. PubMed PMC
Vothknecht UC, Westhoff P.. 2001. Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta Mol Cell Res. 1541(1–2):91–101. PubMed
Wagener N, Ackermann M, Funes S, Neupert W.. 2011. A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol Cell. 44(2):191–202. PubMed
Waller RF, Keeling PJ.. 2006. Alveolate and chlorophycean mitochondrial cox2 genes split twice independently. Gene 383:33–37. PubMed
Wente SR, Rout MP.. 2010. The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol. 2(10):a000562. PubMed PMC
Wiedemann N, Pfanner N.. 2017. Mitochondrial machineries for protein import and assembly. Annu Rev Biochem. 86:685–714. PubMed
Yahr TL, Wickner WT.. 2001. Functional reconstitution of bacterial Tat translocation in vitro. EMBO J. 20(10):2472–2479. PubMed PMC
Yang D, , OyaizuY, , OyaizuH, , OlsenGJ, , Woese CR.. 1985. Mitochondrial origins. Proc Natl Acad Sci U S A. 82(13):4443–4447. PubMed PMC
Yen MR, Harley KT, Tseng YH, Saier MH.. 2001. Phylogenetic and structural analyses of the oxa1 family of protein translocases. FEMS Microbiol Lett. 204(2):223–231. PubMed
Yi L, Celebi N, Chen M, Dalbey RE.. 2004. Sec/SRP requirements and energetics of membrane insertion of subunits a, b, and c of the Escherichia coli F1F0 ATP synthase. J Biol Chem. 279(38):39260–39267. PubMed
Žárský V, Doležal P.. 2016. Evolution of the Tim17 protein family. Biol Direct. 11(1):54. PubMed PMC
Zhang Y-J, Tian H-F, Wen J-F.. 2009. The evolution of YidC/Oxa/Alb3 family in the three domains of life: a phylogenomic analysis. BMC Evol Biol. 9:137. PubMed PMC
Zhu L, Klenner C, Kuhn A, Dalbey RE.. 2012. Both yidc and SecYEG are required for translocation of the periplasmic loops 1 and 2 of the multispanning membrane protein tatC. J Mol Biol. 424(5):354–367. PubMed
Reconstructing the last common ancestor of all eukaryotes
Bacterial Type II Secretion System and Its Mitochondrial Counterpart