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. 1998 Sep 15;95(19):11295-300.
doi: 10.1073/pnas.95.19.11295.

Genetic code origins: tRNAs older than their synthetases?

L Ribas de Pouplana  1 , R J Turner, B A Steer, P Schimmel
Affiliations

Genetic code origins: tRNAs older than their synthetases?

L Ribas de Pouplana et al. Proc Natl Acad Sci U S A. .

Abstract

We present a phylogenetic analysis to determine whether a given tRNA molecule was established in evolution before its cognate aminoacyl-tRNA synthetase. The earlier appearance of tRNA versus their metabolically related enzymes is a prediction of the RNA world theory, but the available synthetase and tRNA sequences previously had not allowed a formal comparison of their relative time of appearance. Using data recently obtained from the emerging genome projects, our analysis points to the extant forms of lysyl-tRNA synthetase being preceded in evolution by the establishment of the identity of lysine tRNA.

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Figures

Figure 1
Figure 1
(Left) The three possible schemes that may have given rise to the extant distribution of class I LysRS enzymes within the phylogenetic tree. (Right) The predicted phylogenetic relationships that would be expected between class I LysRS sequences and their closest class I aaRSs. (Top) A late duplication event followed by horizontal transfer. (Middle) Two independent duplication and gene replacement events. (Bottom) Two ancestral enzymes coexist initially, and they displace each other in different groups. ○, Class II LysRS. •, Class I LysRS. ▴ ■, Class I synthetases closest to class I LysRS. ⊗, Displacement of class II LysRS.
Figure 2
Figure 2
Evolutionary relationships obtained for class I LysRS in the context of the sequences of all other class I aaRS. The analyses of five species that contain a class I lysS gene are shown. Numbers at branches correspond to bootstrap frequencies obtained from 100 replicates. (Top) Tree obtained with A. fulgidus class I aaRS sequences. (Middle) Tree obtained with class I aaRS sequences from B. burgdorferi, T. pallidum, and P. horikoshii (bootstrap frequencies correspond to the tree obtained with T. pallidum sequences). (Bottom) Tree obtained with M. jannaschii class I aaRS sequences.
Figure 3
Figure 3
Unrooted maximum parsimony tree for all known class I LysRS sequences in the context of the sequences of CysRS, ArgRS, GluRS, and GlnRS from several bacterial, archaeal, and eukaryotic organisms. Numbers at nodes correspond to bootstrapping frequencies for 100 different trees. AF, A. fulgidus; BB, B. burgdorferi; TP, T. pallidum; MJ, M. jannaschii; MT, M. thermoautotrophicum.
Figure 4
Figure 4
Unrooted maximum parsimony tree of several archaeal and bacterial tRNALys sequences, in the context of sequences from all 20 tRNA types from E. coli, aligned without their anticodon triplets (tRNAs other than tRNALys are indicated by the three-letter code of their corresponding amino acid). Numbers at nodes of the tRNALys branches correspond to bootstrapping frequencies for the branch closest to the number (calculated from 100 different trees). The tRNALys sequences, charged by class I or II LysRS, are boxed, and those known to be charged by a class I LysRS are marked (I). S. aureus, Staphylococcus aureus; B. subtilis, Bacillus subtilis; H. influenzae, Haemophilus influenzae; H. volcanii, Halobacterium volcanii; M. kandleri, Methanopyrus kandleri; M. thermo., Methanobacterium thermoautotrophicum; M. fervidus, Methanothermus fervidus; M. voltae, Methanococcus voltae; M. vannielii, Methanococcus vannielii.
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