Interdependence, reflexivity, fidelity, impedance matching, and the evolution of genetic coding

Show simple item record Carter, CW en Wills, Peter en 2018-12-02T21:51:34Z en 2017-10-24 en
dc.identifier.citation Molecular Biology and Evolution 35(2):269-286 Article number msx265 24 Oct 2017 en
dc.identifier.issn 0737-4038 en
dc.identifier.uri en
dc.description.abstract Genetic coding is generally thought to have required ribozymes whose functions were taken over by polypeptide aminoacyl-tRNA synthetases (aaRS). Two discoveries about aaRS and their interactions with tRNA substrates now furnish a unifying rationale for the opposite conclusion: that the key processes of the Central Dogma of molecular biology emerged simultaneously and naturally from simple origins in a peptide•RNA partnership, eliminating the epistemological utility of a prior RNA world. First, the two aaRS classes likely arose from opposite strands of the same ancestral gene, implying a simple genetic alphabet. The resulting inversion symmetries in aaRS structural biology would have stabilized the initial and subsequent differentiation of coding specificities, rapidly promoting diversity in the proteome. Second, amino acid physical chemistry maps onto tRNA identity elements, establishing reflexive, nanoenvironmental sensing in protein aaRS. Bootstrapping of increasingly detailed coding is thus intrinsic to polypeptide aaRS, but impossible in an RNA world. These notions underline the following concepts that contradict gradual replacement of ribozymal aaRS by polypeptide aaRS: (i) aaRS enzymes must be interdependent; (ii) reflexivity intrinsic to polypeptide aaRS production dynamics promotes bootstrapping; (iii) takeover of RNA-catalyzed aminoacylation by enzymes will necessarily degrade specificity; (iv) the Central Dogma’s emergence is most probable when replication and translation error rates remain comparable. These characteristics are necessary and sufficient for the essentially de novo emergence of a coupled gene-replicase-translatase system of genetic coding that would have continuously preserved the functional meaning of genetically encoded protein genes whose phylogenetic relationships match those observed today. en
dc.publisher Oxford University Press (OUP) en
dc.relation.ispartofseries Molecular Biology and Evolution en
dc.rights Items in ResearchSpace are protected by copyright, with all rights reserved, unless otherwise indicated. Previously published items are made available in accordance with the copyright policy of the publisher. en
dc.rights.uri en
dc.rights.uri en
dc.subject Aminoacyl-tRNA synthetases, Bootstrapping, Evolution of translation, Molecular Phylogeny en
dc.title Interdependence, reflexivity, fidelity, impedance matching, and the evolution of genetic coding en
dc.type Journal Article en
dc.identifier.doi 10.1093/molbev/msx265 en
pubs.issue 2 en
pubs.begin-page 269 en
pubs.volume 35 en
dc.rights.holder Copyright: The authors en
dc.identifier.pmid 29077934 en en
pubs.end-page 286 en
dc.rights.accessrights en
pubs.subtype Article en
pubs.elements-id 701665 en
dc.relation.isnodouble 1159399 * Science en Physics en
dc.identifier.eissn 1537-1719 en
pubs.record-created-at-source-date 2017-10-27 en 2017-10-24 en
pubs.dimensions-id 29077934 en

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