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What RNA World? Why a Peptide/RNA Partnership Merits Renewed Experimental Attention.

Carter CW - Life (Basel) (2015)

Bottom Line: We review arguments that biology emerged from a reciprocal partnership in which small ancestral oligopeptides and oligonucleotides initially both contributed rudimentary information coding and catalytic rate accelerations, and that the superior information-bearing qualities of RNA and the superior catalytic potential of proteins emerged from such complexes only with the gradual invention of the genetic code.Parallel hierarchical catalytic repertoires for increasingly highly conserved sequences from the two synthetase classes now increase the likelihood that they arose as translation products from opposite strands of a single gene.Sense/antisense coding affords a new bioinformatic metric for phylogenetic relationships much more distant than can be reconstructed from multiple sequence alignments of a single superfamily.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7260, USA. carter@med.unc.edu.

ABSTRACT
We review arguments that biology emerged from a reciprocal partnership in which small ancestral oligopeptides and oligonucleotides initially both contributed rudimentary information coding and catalytic rate accelerations, and that the superior information-bearing qualities of RNA and the superior catalytic potential of proteins emerged from such complexes only with the gradual invention of the genetic code. A coherent structural basis for that scenario was articulated nearly a decade before the demonstration of catalytic RNA. Parallel hierarchical catalytic repertoires for increasingly highly conserved sequences from the two synthetase classes now increase the likelihood that they arose as translation products from opposite strands of a single gene. Sense/antisense coding affords a new bioinformatic metric for phylogenetic relationships much more distant than can be reconstructed from multiple sequence alignments of a single superfamily. Evidence for distinct coding properties in tRNA acceptor stems and anticodons, and experimental demonstration that the two synthetase family ATP binding sites can indeed be coded by opposite strands of the same gene supplement these biochemical and bioinformatic data, establishing a solid basis for key intermediates on a path from simple, stereochemically coded, reciprocally catalytic peptide/RNA complexes through the earliest peptide catalysts to contemporary aminoacyl-tRNA synthetases. That scenario documents a path to increasing complexity that obviates the need for a single polymer to act both catalytically and as an informational molecule.

No MeSH data available.


Related in: MedlinePlus

Possible relevance of mass, β-branching, and carboxylates to the operational RNA code (adapted from [56]). For ancient β-hairpins to interact with double-stranded RNA as envisioned by Carter and Kraut [1], large side chains would necessarily have faced away from the RNA minor groove. β-branched side chains on either face (re-entrant angles; green; threonine, valine on the inward face; isoleucine on the outer face) enhance β-structure formation. Carboxylate side chains in outward facing positions (red) could enhance solubility [58,59] and coordinate catalytic divalent metals, either for catalysis or to protect against RNA degradation [60].
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life-05-00294-f009: Possible relevance of mass, β-branching, and carboxylates to the operational RNA code (adapted from [56]). For ancient β-hairpins to interact with double-stranded RNA as envisioned by Carter and Kraut [1], large side chains would necessarily have faced away from the RNA minor groove. β-branched side chains on either face (re-entrant angles; green; threonine, valine on the inward face; isoleucine on the outer face) enhance β-structure formation. Carboxylate side chains in outward facing positions (red) could enhance solubility [58,59] and coordinate catalytic divalent metals, either for catalysis or to protect against RNA degradation [60].

Mentions: Binding pockets of the Carter and Kraut model in Figure 2 establish symmetry between the mechanism for choosing incoming amino acid and nucleotide precursors. Incoming inward-facing amino acids of the appropriate chirality are determined chiefly by the templating peptide strand and the base of the corresponding polynucleotide strand. The proposal of Carter & Kraut thus actually implements a rudimentary sense/antisense coding in which each base in an RNA duplex codes for two amino acids, and vice versa each dipeptide specifies a corresponding base (Figure 1 and Figure 9). Functionalities emerging from such a primitive coding system would tend to persist and lend a selective advantage to any successive genetic coding that would preserve the ability of peptides to interact with RNA in this fashion. It is within the realm of possibility that this stereochemical coding might generate peptides (and corresponding RNA “genes”) as long and functional as the 23mer system illustrated in Figure 7. Furthermore, such a gene would have the length of a tRNA gene (~72 bases). Such an evolutionary intermediate might be expected also to preserve sense/antisense coding, consistent with the vestigial traces of such coding in the contemporary aaRS genes.


What RNA World? Why a Peptide/RNA Partnership Merits Renewed Experimental Attention.

Carter CW - Life (Basel) (2015)

Possible relevance of mass, β-branching, and carboxylates to the operational RNA code (adapted from [56]). For ancient β-hairpins to interact with double-stranded RNA as envisioned by Carter and Kraut [1], large side chains would necessarily have faced away from the RNA minor groove. β-branched side chains on either face (re-entrant angles; green; threonine, valine on the inward face; isoleucine on the outer face) enhance β-structure formation. Carboxylate side chains in outward facing positions (red) could enhance solubility [58,59] and coordinate catalytic divalent metals, either for catalysis or to protect against RNA degradation [60].
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4390853&req=5

life-05-00294-f009: Possible relevance of mass, β-branching, and carboxylates to the operational RNA code (adapted from [56]). For ancient β-hairpins to interact with double-stranded RNA as envisioned by Carter and Kraut [1], large side chains would necessarily have faced away from the RNA minor groove. β-branched side chains on either face (re-entrant angles; green; threonine, valine on the inward face; isoleucine on the outer face) enhance β-structure formation. Carboxylate side chains in outward facing positions (red) could enhance solubility [58,59] and coordinate catalytic divalent metals, either for catalysis or to protect against RNA degradation [60].
Mentions: Binding pockets of the Carter and Kraut model in Figure 2 establish symmetry between the mechanism for choosing incoming amino acid and nucleotide precursors. Incoming inward-facing amino acids of the appropriate chirality are determined chiefly by the templating peptide strand and the base of the corresponding polynucleotide strand. The proposal of Carter & Kraut thus actually implements a rudimentary sense/antisense coding in which each base in an RNA duplex codes for two amino acids, and vice versa each dipeptide specifies a corresponding base (Figure 1 and Figure 9). Functionalities emerging from such a primitive coding system would tend to persist and lend a selective advantage to any successive genetic coding that would preserve the ability of peptides to interact with RNA in this fashion. It is within the realm of possibility that this stereochemical coding might generate peptides (and corresponding RNA “genes”) as long and functional as the 23mer system illustrated in Figure 7. Furthermore, such a gene would have the length of a tRNA gene (~72 bases). Such an evolutionary intermediate might be expected also to preserve sense/antisense coding, consistent with the vestigial traces of such coding in the contemporary aaRS genes.

Bottom Line: We review arguments that biology emerged from a reciprocal partnership in which small ancestral oligopeptides and oligonucleotides initially both contributed rudimentary information coding and catalytic rate accelerations, and that the superior information-bearing qualities of RNA and the superior catalytic potential of proteins emerged from such complexes only with the gradual invention of the genetic code.Parallel hierarchical catalytic repertoires for increasingly highly conserved sequences from the two synthetase classes now increase the likelihood that they arose as translation products from opposite strands of a single gene.Sense/antisense coding affords a new bioinformatic metric for phylogenetic relationships much more distant than can be reconstructed from multiple sequence alignments of a single superfamily.

View Article: PubMed Central - PubMed

Affiliation: Department of Biochemistry and Biophysics, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7260, USA. carter@med.unc.edu.

ABSTRACT
We review arguments that biology emerged from a reciprocal partnership in which small ancestral oligopeptides and oligonucleotides initially both contributed rudimentary information coding and catalytic rate accelerations, and that the superior information-bearing qualities of RNA and the superior catalytic potential of proteins emerged from such complexes only with the gradual invention of the genetic code. A coherent structural basis for that scenario was articulated nearly a decade before the demonstration of catalytic RNA. Parallel hierarchical catalytic repertoires for increasingly highly conserved sequences from the two synthetase classes now increase the likelihood that they arose as translation products from opposite strands of a single gene. Sense/antisense coding affords a new bioinformatic metric for phylogenetic relationships much more distant than can be reconstructed from multiple sequence alignments of a single superfamily. Evidence for distinct coding properties in tRNA acceptor stems and anticodons, and experimental demonstration that the two synthetase family ATP binding sites can indeed be coded by opposite strands of the same gene supplement these biochemical and bioinformatic data, establishing a solid basis for key intermediates on a path from simple, stereochemically coded, reciprocally catalytic peptide/RNA complexes through the earliest peptide catalysts to contemporary aminoacyl-tRNA synthetases. That scenario documents a path to increasing complexity that obviates the need for a single polymer to act both catalytically and as an informational molecule.

No MeSH data available.


Related in: MedlinePlus