Interdependence, Reflexivity, Fidelity, Impedance Matching, and the Evolution of Genetic Coding

被引:35
作者
Carter, Charles W., Jr. [1 ]
Wills, Peter R. [2 ]
机构
[1] Univ North Carolina Chapel Hill, Dept Biochem & Biophys, Chapel Hill, NC 27514 USA
[2] Univ Auckland, Dept Phys, Auckland, New Zealand
关键词
aminoacyl-tRNA synthetases; bootstrapping; evolution of translation; molecular phylogeny; TRANSFER-RNA SYNTHETASES; RODIN-OHNO HYPOTHESIS; AMINO-ACIDS; CLASS-I; MOLECULAR EVOLUTION; SELF-ORGANIZATION; ACCEPTOR-STEM; PEPTIDYL TRANSFERASE; AUTOCATALYTIC SETS; COEVOLUTION THEORY;
D O I
10.1093/molbev/msx265
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
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: 1) aaRS enzymes must be interdependent; 2) reflexivity intrinsic to polypeptide aaRS production dynamics promotes bootstrapping; 3) takeover of RNA-catalyzed aminoacylation by enzymes will necessarily degrade specificity; and 4) 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 genereplicase- 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.
引用
收藏
页码:269 / 286
页数:18
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