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Cited by 274Origins and Evolution of LifeRNA and protein synthesis mechanismsEvolution and Genetic Dynamics

The Path from the RNA World

Poole, Anthony M., Jeffares, Daniel C., Penny, David·1998·Journal of Molecular Evolution
DOI 10.1007/pl00006275
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Abstract

We describe a sequential (step by step) Darwinian model for the evolution of life from the late stages of the RNA world through to the emergence of eukaryotes and prokaryotes. The starting point is our model, derived from current RNA activity, of the RNA world just prior to the advent of genetically-encoded protein synthesis. By focusing on the function of the protoribosome we develop a plausible model for the evolution of a protein-synthesizing ribosome from a high-fidelity RNA polymerase that incorporated triplets of oligonucleotides. With the standard assumption that during the evolution of enzymatic activity, catalysis is transferred from RNA --> RNP --> protein, the first proteins in the "breakthrough organism" (the first to have encoded protein synthesis) would be nonspecific chaperone-like proteins rather than catalytic. Moreover, because some RNA molecules that pre-date protein synthesis under this model now occur as introns in some of the very earliest proteins, the model predicts these particular introns are older than the exons surrounding them, the "introns-first" theory. Many features of the model for the genome organization in the final RNA world ribo-organism are more prevalent in the eukaryotic genome and we suggest that the prokaryotic genome organization (a single, circular genome with one center of replication) was derived from a "eukaryotic-like" genome organization (a fragmented linear genome with multiple centers of replication). The steps from the proposed ribo-organism RNA genome --> eukaryotic-like DNA genome --> prokaryotic-like DNA genome are all relatively straightforward, whereas the transition prokaryotic-like genome --> eukaryotic-like genome appears impossible under a Darwinian mechanism of evolution, given the assumption of the transition RNA --> RNP --> protein. A likely molecular mechanism, "plasmid transfer," is available for the origin of prokaryotic-type genomes from an eukaryotic-like architecture. Under this model prokaryotes are considered specialized and derived with reduced dependence on ssRNA biochemistry. A functional explanation is that prokaryote ancestors underwent selection for thermophily (high temperature) and/or for rapid reproduction (r selection) at least once in their history.

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  • The earliest ribozymes may have been short and simple, in part due to the availability of prebiotic chemicals and the probably lower fidelity of early RNA replication systems.

    “The earliest ribozymes may have been short and simple, in part due to the availability of prebiotic chemicals (Akoopie and Müller 2016) as well as the fidelity of early RNA replication systems, which was probably lower (Poole et al. 1998).”

    From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Poole et al. 1998

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Authors
Poole, A. M., Jeffares, D. C., & Penny, D.
Affiliations
Massey University (NZ)
ORCID
Venue
Journal of Molecular Evolution
Publisher
Springer Science and Business Media LLC
Published
1998-01
Volume
46
Issue
1
Pages
1-17
ISSN
0022-2844 (ISSN-L)
DOI
10.1007/pl00006275
OpenAlex
W2085720218
Cited by
274
References
109
Citations by year
2026: 6 · 2025: 4 · 2024: 9 · 2023: 5 · 2022: 3 · 2021: 12 · 2020: 7 · 2019: 6 · 2018: 11 · 2017: 6 · 2016: 6 · 2015: 9 · 2014: 8 · 2013: 13 · 2012: 16
FWCI
8.12
Type
journal article
Language
en
Open access
closed
Licence
www.springer.com/tdm (tdm)
Locations
  • Journal of Molecular Evolution (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
origin of life, RNA world, ribosome evolution, protein synthesis, RNA polymerase, genome organization, eukaryotic genomes, plasmid transfer, Darwinian evolution, thermophily, r-selection, chaperone-like protein
MeSH terms
Archaea, Bacteria, Eukaryotic Cells, Biological Evolution, Introns, Models, Biological, Plasmids, Prokaryotic Cells, Proteins, Ribosomes, RNA, RNA Processing, Post-Transcriptional, RNA Splicing, RNA, Messenger, RNA, Ribosomal, Protein Biosynthesis, Genome

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