Characterization of Aminoacyl-tRNA Synthetases in Chromerids
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31370303
PubMed Central
PMC6723311
DOI
10.3390/genes10080582
PII: genes10080582
Knihovny.cz E-zdroje
- Klíčová slova
- Aminoacyl tRNA synthetase (AaRS), Chromera velia, Vitrella brassicaformis, chloroplast, evolution, mitochondrion, nucleus, protein localization,
- MeSH
- Alveolata klasifikace enzymologie genetika MeSH
- aminoacyl-tRNA-synthetasy genetika MeSH
- fylogeneze MeSH
- protozoální proteiny genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- aminoacyl-tRNA-synthetasy MeSH
- protozoální proteiny MeSH
Aminoacyl-tRNA synthetases (AaRSs) are enzymes that catalyze the ligation of tRNAs to amino acids. There are AaRSs specific for each amino acid in the cell. Each cellular compartment in which translation takes place (the cytosol, mitochondria, and plastids in most cases), needs the full set of AaRSs; however, individual AaRSs can function in multiple compartments due to dual (or even multiple) targeting of nuclear-encoded proteins to various destinations in the cell. We searched the genomes of the chromerids, Chromera velia and Vitrella brassicaformis, for AaRS genes: 48 genes encoding AaRSs were identified in C. velia, while only 39 AaRS genes were found in V. brassicaformis. In the latter alga, ArgRS and GluRS were each encoded by a single gene occurring in a single copy; only PheRS was found in three genes, while the remaining AaRSs were encoded by two genes. In contrast, there were nine cases for which C. velia contained three genes of a given AaRS (45% of the AaRSs), all of them representing duplicated genes, except AsnRS and PheRS, which are more likely pseudoparalogs (acquired via horizontal or endosymbiotic gene transfer). Targeting predictions indicated that AaRSs are not (or not exclusively), in most cases, used in the cellular compartment from which their gene originates. The molecular phylogenies of the AaRSs are variable between the specific types, and similar between the two investigated chromerids. While genes with eukaryotic origin are more frequently retained, there is no clear pattern of orthologous pairs between C. velia and V. brassicaformis.
Faculty of Science University of South Bohemia 370 05 České Budějovice Czech Republic
Genetics Department Faculty of Agriculture Ain Shams University Cairo 11241 Egypt
Zobrazit více v PubMed
Moore R.B., Oborník M., Janouškovec J., Chrudimský T., Vancová M., Green D.H., Wright S.W., Davies N.W., Bolch C.J.S., Heimann K., et al. A photosynthetic alveolate closely related to apicomplexan parasites. Nature. 2008;451:959–963. doi: 10.1038/nature06635. PubMed DOI
Oborník M., Modrý D., Lukeš M., Černotíková-Stříbrná E., Cihlář J., Tesařová M., Kotabová E., Vancová M., Prášil O., Lukeš J. Morphology, Ultrastructure and Life Cycle of Vitrella brassicaformis n. sp., n. gen., a Novel Chromerid from the Great Barrier Reef. Protist. 2012;163:306–323. doi: 10.1016/j.protis.2011.09.001. PubMed DOI
Cumbo V.R., Baird A.H., Moore R.B., Negri A.P., Neilan B.A., Salih A., van Oppen M.J.H., Wang Y., Marquis C.P. Chromera velia is endosymbiotic in larvae of the reef corals Acropora digitifera and A. tenuis. Protist. 2013;164:237–244. doi: 10.1016/j.protis.2012.08.003. PubMed DOI
Janouškovec J., Horák A., Barott K.L., Rohwer F.L., Keeling P.J. Environmental distribution of coral-associated relatives of apicomplexan parasites. ISME J. 2013;7:444–447. doi: 10.1038/ismej.2012.129. PubMed DOI PMC
Füssy Z., Oborník M. Advances in Botanical Research. Volume 84. Academic Press; Cambridge, MA, USA: 2017. Chromerids and Their Plastids; pp. 187–218.
McFadden G.I., Waller R.F. Plastids in parasites of humans. Bioessays. 1997;19:1033–1040. doi: 10.1002/bies.950191114. PubMed DOI
Woo Y.H., Ansari H., Otto T.D., Linger C.M.K., Olisko M.K., Michálek J., Saxena A., Shanmugam D., Tayyrov A., Veluchamy A., et al. Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. eLife. 2015;4:e06974. doi: 10.7554/eLife.06974. PubMed DOI PMC
Flegontov P., Michálek J., Janouškovec J., Lai D.H., Jirků M., Hajdušková E., Tomčala A., Otto T.D., Keeling P.J., Pain A., et al. Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites. Mol. Biol. Evol. 2015;32:1115–1131. doi: 10.1093/molbev/msv021. PubMed DOI
Oborník M., Janouškovec J., Chrudimský T., Lukeš J. Evolution of the apicoplast and its hosts: From heterotrophy to autotrophy and back again. Int. J. Parasitol. 2009;39:1–12. doi: 10.1016/j.ijpara.2008.07.010. PubMed DOI
Oborník M., Lukeš J. The organellar genomes of Chromera and Vitrella, the phototrophic relatives of apicomplexan parasites. Annu. Rev. Microbiol. 2015;69:129–144. doi: 10.1146/annurev-micro-091014-104449. PubMed DOI
Oborník M., Lukeš J. International Review of Cell and Molecular Biology. Volume 306. Academic Press; Cambridge, MA, USA: 2013. Cell Biology of Chromerids: Autotrophic Relatives to Apicomplexan Parasites; pp. 333–369. PubMed
Oborník M., Kručinská J., Esson H. Life cycles of chromerids resemble those of colpodellids and apicomplexan parasites. Perspect. Phycol. 2016;3:21–27. doi: 10.1127/pip/2016/0038. DOI
Janouškovec J., Tikhonenkov D.V., Burki F., Howe A.T., Kolísko M., Mylnikov A.P., Keeling P.J. Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proc. Natl. Acad. Sci. USA. 2015;112:10200–10207. doi: 10.1073/pnas.1423790112. PubMed DOI PMC
Füssy Z., Oborník M. Evolutionary Biology: Self/Nonself Evolution, Species and Complex Traits Evolution, Methods and Concepts. Springer; Cham, Switzerland: 2017. Reductive Evolution of Apicomplexan Parasites from Phototrophic Ancestors; pp. 217–236.
Janouškovec J., Horák A., Oborník M., Lukeš J., Keeling P.J. A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc. Natl. Acad. Sci. USA. 2010;107:10949–10954. doi: 10.1073/pnas.1003335107. PubMed DOI PMC
Sobotka R., Esson H.J., Koník P., Trsková E., Moravcová L., Horák A., Dufková P., Oborník M. Extensive gain and loss of photosystem I subunits in chromerid algae, photosynthetic relatives of apicomplexans. Sci. Rep. 2017;7:13214. doi: 10.1038/s41598-017-13575-x. PubMed DOI PMC
Füssy Z., Faitová T., Oborník M. Subcellular compartments interplay for carbon and nitrogen allocation in Chromera velia and Vitrella brassicaformis. Genome Biol. Evol. 2019 doi: 10.1093/gbe/evz123. PubMed DOI PMC
Ševcíková T., Horák A., Klimeš V., Zbránková V., Demir-Hilton E., Sudek S., Jenkins J., Schmutz J., Pribyl P., Fousek J., et al. Updating algal evolutionary relationships through plastid genome sequencing: Did alveolate plastids emerge through endosymbiosis of an ochrophyte? Sci. Rep. 2015;5:10134. doi: 10.1038/srep10134. PubMed DOI PMC
Kořený L., Sobotka R., Janouškovec J., Keeling P.J., Oborník M. Tetrapyrrole Synthesis of Photosynthetic Chromerids Is Likely Homologous to the Unusual Pathway of Apicomplexan Parasites. Plant Cell. 2011;23:3454–3462. doi: 10.1105/tpc.111.089102. PubMed DOI PMC
van Dooren G.G., Kennedy A.T., McFadden G.I. The Use and Abuse of Heme in Apicomplexan Parasites. Antioxid. Redox Signal. 2012;17:634–656. doi: 10.1089/ars.2012.4539. PubMed DOI
Patron N.J., Waller R.F., Archibald J.M., Keeling P.J. Complex protein targeting to dinoflagellate plastids. J. Mol. Biol. 2005;348:1015–1024. doi: 10.1016/j.jmb.2005.03.030. PubMed DOI
Slamovits C.H., Saldarriaga J.F., Larocque A., Keeling P.J. The Highly Reduced and Fragmented Mitochondrial Genome of the Early-branching Dinoflagellate Oxyrrhis marina Shares Characteristics with both Apicomplexan and Dinoflagellate Mitochondrial Genomes. J. Mol. Biol. 2007;372:356–368. doi: 10.1016/j.jmb.2007.06.085. PubMed DOI
Nash E.A., Nisbet R.E.R., Barbrook A.C., Howe C.J. Dinoflagellates: A mitochondrial genome all at sea. Trends Genet. 2008;24:328–335. doi: 10.1016/j.tig.2008.04.001. PubMed DOI
Waller R.F., Jackson C.J. Dinoflagellate mitochondrial genomes: Stretching the rules of molecular biology. BioEssays. 2009;31:237–245. doi: 10.1002/bies.200800164. PubMed DOI
Waller R.F., Kořený L. Advances in Botanical Research. Volume 84. Academic Press; Cambridge, MA, USA: 2017. Plastid Complexity in Dinoflagellates: A Picture of Gains, Losses, Replacements and Revisions; pp. 105–143.
John U., Lu Y., Wohlrab S., Groth M., Janouškovec J., Kohli G.S., Mark F.C., Bickmeyer U., Farhat S., Felder M., et al. An aerobic eukaryotic parasite with functional mitochondria that likely lacks a mitochondrial genome. Sci. Adv. 2019;6:eaav1110. doi: 10.1126/sciadv.aav1110. PubMed DOI PMC
Zhou X.L., Du D.H., Tan M., Lei H.Y., Ruan L.L., Eriani G., Wang E.D. Role of tRNA amino acid-accepting end in aminoacylation and its quality control. Nucleic Acids Res. 2011;20:8857–8868. doi: 10.1093/nar/gkr595. PubMed DOI PMC
Chien C.-I., Chen Y.-W., Wu Y.-H., Chang C.-Y., Wang T.-L., Wang C.-C. Functional Substitution of a Eukaryotic Glycyl-tRNA Synthetase with an Evolutionarily Unrelated Bacterial Cognate Enzyme. PLoS ONE. 2014;9:e94659. doi: 10.1371/journal.pone.0094659. PubMed DOI PMC
Carter C.W., Jr. Cognition, mechanism, and evolutionary relationships in aminoacyl-tRNA synthetases. Annu. Rev. Biochem. 1993;62:715–748. doi: 10.1146/annurev.bi.62.070193.003435. PubMed DOI
Giege R., Sissler M., Florentz C. Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res. 1998;26:5017–5035. doi: 10.1093/nar/26.22.5017. PubMed DOI PMC
Schimmel P.R., Söll D. Aminoacyl-tRNA Synthetases: General Features and Recognition of Transfer RNAs. Annu. Rev. Biochem. 1979;48:601–648. doi: 10.1146/annurev.bi.48.070179.003125. PubMed DOI
Chaliotis A., Vlastaridis P., Mossialos D., Ibba M., Becker H.D., Stathopoulos C., Amoutzias G.D. The complex evolutionary history of aminoacyl-tRNA synthetases. Nucleic Acids Res. 2017;45:1059–1068. doi: 10.1093/nar/gkw1182. PubMed DOI PMC
Eriani G., Delarue M., Poch O., Gangloff J., Moras D. Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs. Nature. 1990;347:203–206. doi: 10.1038/347203a0. PubMed DOI
Ludmerer S.W., Schimmel P. Gene for yeast glutamine tRNA synthetase encodes a large amino-terminal extension and provides a strong confirmation of the signature sequence for a group of the aminoacyl-tRNA synthetases. J. Biol. Chem. 1987;262:10801–10806. PubMed
Mazauric M.H., Keith G., Logan D., Kreutzer R., Giegé R., Kern D. Glycyl-tRNA synthetase from Thermus thermophilus--wide structural divergence with other prokaryotic glycyl-tRNA synthetases and functional inter-relation with prokaryotic and eukaryotic glycylation systems. Eur. J. Biochem. 1998;251:744–757. doi: 10.1046/j.1432-1327.1998.2510744.x. PubMed DOI
Ostrem D.L., Berg P. Glycyl transfer ribonucleic acid synthetase from Escherichia coli: Purification, properties, and substrate binding. Biochemistry. 1974;13:1338–1348. doi: 10.1021/bi00704a006. PubMed DOI
Surguchov A.P., Surguchov I.G. Two Enzymically Active Forms of Glycyl-tRNA Synthetase from Bacillus brevis Purification and Properties. Eur. J. Biochem. 1975;54:175–184. doi: 10.1111/j.1432-1033.1975.tb04127.x. PubMed DOI
Kern D., Giegé R., Ebel J.P. Purification and some properties of alanyl- and leucyl-tRNA synthetases from baker’s yeast. BBA Sect. Nucleic Acids Protein Synth. 1981;653:83–90. doi: 10.1016/0005-2787(81)90106-4. PubMed DOI
Shiba K., Schimmel P., Motegi H., Noda T. Human glycyl-tRNA synthetase. Wide divergence of primary structure from bacterial counterpart and species-specific aminoacylation. J. Biol. Chem. 1994;269:30049–30055. PubMed
Curnow A.W., Hong K.W., Yuan R., Kim S.I., Martins O., Winkler W., Henkin T.M., Söll D. Glu-tRNAGln amidotransferase: A novel heterotrimeric enzyme required for correct decoding of glutamine codons during translation. Proc. Natl. Acad. Sci. USA. 1997;22:11819–11826. doi: 10.1073/pnas.94.22.11819. PubMed DOI PMC
Becker H.D., Kern D. Thermus thermophilus: A link in evolution of the tRNA-dependent amino acid amidation pathways. Proc. Natl. Acad. Sci. USA. 1998;22:12832–12837. doi: 10.1073/pnas.95.22.12832. PubMed DOI PMC
Ibba M., Curnow A.W., Söll D. Aminoacyl-tRNA synthesis: Divergent routes to a common goal. Trends Biochem. Sci. 1997;22:39–42. doi: 10.1016/S0968-0004(96)20033-7. PubMed DOI
Leinfelder W., Zehelein E., Mandrandberthelot M., Bock A. Gene for a novel tRNA species that accepts L-serine and cotranslationally inserts selenocysteine. Nature. 1988;331:723–725. doi: 10.1038/331723a0. PubMed DOI
Sauerwald A., Zhu W., Major T.A., Roy H., Palioura S., Jahn D., Whitman W.B., Yates J.R., Ibba M., Söll D. RNA-dependent cysteine biosynthesis in archaea. Science. 2005;307:1969–1972. doi: 10.1126/science.1108329. PubMed DOI
Sheppard K., Yuan J., Hohn M.J., Jester B., Devine K.M., Söll D. From one amino acid to another: tRNA-dependent amino acid biosynthesis. Nucleic Acids Res. 2008;36:1813–1825. doi: 10.1093/nar/gkn015. PubMed DOI PMC
Gile G.H., Moog D., Slamovits C.H., Maier U.G., Archibald J.M. Dual organellar targeting of aminoacyl-tRNA synthetases in diatoms and cryptophytes. Genome Biol. Evol. 2015;7:1728–1742. doi: 10.1093/gbe/evv095. PubMed DOI PMC
Warrenfeltz S., Basenko E.Y., Crouch K., Harb O.S., Kissinger J.C., Roos D.S., Shanmugasundram A., Silva-Franco F. Eukaryotic Genomic Databases. Volume 1757. Humana Press; New York, NY, USA: 2018. EuPathDB: The eukaryotic pathogen genomics database resource; pp. 69–113. PubMed PMC
Woese C.R., Olsen G.J., Ibba M., Soll D. Aminoacyl-tRNA Synthetases, the Genetic Code, and the Evolutionary Process. Microbiol. Mol. Biol. Rev. 2000;64:202–236. doi: 10.1128/MMBR.64.1.202-236.2000. PubMed DOI PMC
Brown J.R. Ancient horizontal gene transfer. Nat. Rev. Genet. 2003;4:121–132. doi: 10.1038/nrg1000. PubMed DOI
Bailey T.L., Johnson J., Grant C.E., Noble W.S. The MEME Suite. Nucleic Acids Res. 2015;43:39–49. doi: 10.1093/nar/gkv416. PubMed DOI PMC
Bendtsen J.D., Nielsen H., Von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004;340:783–795. doi: 10.1016/j.jmb.2004.05.028. PubMed DOI
Petersen T.N., Brunak S., von Heijne G., Nielsen H. SignalP 4.0: Discriminating signal peptides from transmembrane regions. Nat. Methods. 2011;8:785–786. doi: 10.1038/nmeth.1701. PubMed DOI
Gruber A., Rocap G., Kroth P.G., Armbrust E.V., Mock T. Plastid proteome prediction for diatoms and other algae with secondary plastids of the red lineage. Plant J. 2015;81:519–528. doi: 10.1111/tpj.12734. PubMed DOI PMC
Emanuelsson O., Brunak S., von Heijne G., Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007;2:953–971. doi: 10.1038/nprot.2007.131. PubMed DOI
Bannai H., Tamada Y., Maruyama O., Nakai K., Miyano S. Extensive feature detection of N-terminal protein sorting signals. Bioinformatics. 2002;18:298–305. doi: 10.1093/bioinformatics/18.2.298. PubMed DOI
Horton P., Park K.J., Obayashi T., Fujita N., Harada H., Adams-Collier C.J., Nakai K. WoLF PSORT: Protein localization predictor. Nucleic Acids Res. 2007;35:585–587. doi: 10.1093/nar/gkm259. PubMed DOI PMC
Claros M.G., Vincens P. Computational Method to Predict Mitochondrially Imported Proteins and their Targeting Sequences. Eur. J. Biochem. 1996;241:779–786. doi: 10.1111/j.1432-1033.1996.00779.x. PubMed DOI
Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Darriba D., Taboada G.L., Doallo R., Posada D. ProtTest-HPC: Fast selection of best-fit models of protein evolution. Bioinformatics. 2011;27:1164–1165. doi: 10.1093/bioinformatics/btr088. PubMed DOI PMC
de Juan D., Pazos F., Valencia A., Evaluation P.M., Rehbein P., Schwalbe H., Jones D.T., Buchan D.W.A., Cozzetto D., Pontil M., et al. ProtTest: Selection of best-fit models of protein evolution. Bioinformatics. 2015;21:2104–2105. PubMed
Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI
Stamatakis A., Ludwig T., Meier H. RAxML-III: A fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics. 2005;21:456–463. doi: 10.1093/bioinformatics/bti191. PubMed DOI
Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. PubMed DOI
Hopper A.K., Martinis S.A., Schimmel P., Kisselev L., Wolfson A., Melton D.A., De Robertis E.M., Cortese R., Popenko V.I., Wolfe C.L., et al. Nuclear functions charge ahead. Science. 1998;282:2003–2004. doi: 10.1126/science.282.5396.2003. PubMed DOI
Lund E. Proofreading and Aminoacylation of tRNAs Before Export from the Nucleus. Science. 1998;282:2082–2085. doi: 10.1126/science.282.5396.2082. PubMed DOI
Szymanski M., Deniziak M.A., Barciszewski J. Aminoacyl-tRNA synthetases database. Nucleic Acids Res. 2001;29:288–290. doi: 10.1093/nar/29.1.288. PubMed DOI PMC
Nathanson L., Deutscher M.P. Active aminoacyl-tRNA synthetases are present in nuclei as a high molecular weight multienzyme complex. J. Biol. Chem. 2000;275:31559–31562. doi: 10.1074/jbc.C000385200. PubMed DOI
Ko Y.G., Kang Y.S., Kim E.K., Park S.G., Kim S. Nucleolar localization of human methionyl-tRNA synthetase and its role in ribosomal RNA synthesis. J. Cell Biol. 2000;149:567–574. doi: 10.1083/jcb.149.3.567. PubMed DOI PMC
Kaminska M., Havrylenko S., Decottignies P., Le Maréchal P., Negrutskii B., Mirande M. Dynamic organization of aminoacyl-tRNA synthetase complexes in the cytoplasm of human cells. J. Biol. Chem. 2009;284:13746–13754. doi: 10.1074/jbc.M900480200. PubMed DOI PMC
Duchene A.-M., Giritch A., Hoffmann B., Cognat V., Lancelin D., Peeters N.M., Zaepfel M., Marechal-Drouard L., Small I.D. Dual targeting is the rule for organellar aminoacyl-tRNA synthetases in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 2005;102:16484–16489. doi: 10.1073/pnas.0504682102. PubMed DOI PMC
Ito J., Batth T.S., Petzold C.J., Redding-Johanson A.M., Mukhopadhyay A., Verboom R., Meyer E.H., Millar A.H., Heazlewood J.L. Analysis of the Arabidopsis cytosolic proteome highlights subcellular partitioning of central plant metabolism. J. Proteome Res. 2011;10:1571–1582. doi: 10.1021/pr1009433. PubMed DOI
Araiso Y., Huot J.L., Sekiguchi T., Frechin M., Fischer F., Enkler L., Senger B., Ishitani R., Becker H.D., Nureki O. Crystal structure of Saccharomyces cerevisiae mitochondrial GatFAB reveals a novel subunit assembly in tRNA-dependent amidotransferases. Nucleic Acids Res. 2014;42:6052–6063. doi: 10.1093/nar/gku234. PubMed DOI PMC
Frechin M., Duchêne A.-M., Becker H.D. Translating organellar glutamine codons: A case by case scenario? RNA Biol. 2009;6:31–34. doi: 10.4161/rna.6.1.7564. PubMed DOI
Freist W., Logan D.T., Gauss D.H. Glycyl-tRNA synthetase. Biol. Chem. Hoppe Seyler. 1996;377:343–356. PubMed
Hipps D., Shiba K., Henderson B., Schimmel P. Operational RNA code for amino acids: Species-specific aminoacylation of minihelices switched by a single nucleotide. Proc. Natl. Acad. Sci. USA. 1995;92:5550–5552. doi: 10.1073/pnas.92.12.5550. PubMed DOI PMC
Duchêne A.M., Peeters N., Dietrich A., Cosset A., Small I.D., Wintz H. Overlapping Destinations for Two Dual Targeted Glycyl-tRNA Synthetases in Arabidopsis thaliana and Phaseolus vulgaris. J. Biol. Chem. 2001;276:15275–15283. doi: 10.1074/jbc.M011525200. PubMed DOI
Halary S., McInerney J.O., Lopez P., Bapteste E. EGN: A wizard for construction of gene and genome similarity networks. BMC Evol. Biol. 2013;13:146. doi: 10.1186/1471-2148-13-146. PubMed DOI PMC
Brindefalk B., Viklund J., Larsson D., Thollesson M., Andersson S.G.E. Origin and evolution of the mitochondrial aminoacyl-tRNA synthetases. Mol. Biol. Evol. 2007;24:743–756. doi: 10.1093/molbev/msl202. PubMed DOI
Makarova K.S. Ancestral paralogs and pseudoparalogs and their role in the emergence of the eukaryotic cell. Nucleic Acids Res. 2005;33:4626–4638. doi: 10.1093/nar/gki775. PubMed DOI PMC
Ribas de Pouplana L., Brown J.R., Schimmel P. Structure-based phylogeny of class IIa tRNA synthetases in relation to an unusual biochemistry. J. Mol. Evol. 2001;53:261–268. doi: 10.1007/s002390010216. PubMed DOI
Roy H., Ling J., Alfonzo J., Ibba M. Loss of editing activity during the evolution of mitochondrial phenylalanyl-tRNA synthetase. J. Biol. Chem. 2005;280:38186–38192. doi: 10.1074/jbc.M508281200. PubMed DOI