Cited by 36Origins and Evolution of LifeRNA and protein synthesis mechanismsEvolution and Genetic Dynamics

Evolution of the division of labor between genes and enzymes in the RNA world

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Boza, Gergely, Szilágyi, András, Kun, Ádám, Santos, Mauro, Szathmáry, Eörs·2014·PLoS Computational Biology

Abstract

The RNA world is a very likely interim stage of the evolution after the first replicators and before the advent of the genetic code and translated proteins. Ribozymes are known to be able to catalyze many reaction types, including cofactor-aided metabolic transformations. In a metabolically complex RNA world, early division of labor between genes and enzymes could have evolved, where the ribozymes would have been transcribed from the genes more often than the other way round, benefiting the encapsulating cells through this dosage effect. Here we show, by computer simulations of protocells harboring unlinked RNA replicators, that the origin of replicational asymmetry producing more ribozymes from a gene template than gene strands from a ribozyme template is feasible and robust. Enzymatic activities of the two modeled ribozymes are in trade-off with their replication rates, and the relative replication rates compared to those of complementary strands are evolvable traits of the ribozymes. The degree of trade-off is shown to have the strongest effect in favor of the division of labor. Although some asymmetry between gene and enzymatic strands could have evolved even in earlier, surface-bound systems, the shown mechanism in protocells seems inevitable and under strong positive selection. This could have preadapted the genetic system for transcription after the subsequent origin of chromosomes and DNA.

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Crossref · 10.1371/journal.pcbi.1003936

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  • There is an antagonism between an RNA sequence's ability to fold into a defined three-dimensional structure to encode function and the ease with which it can be replicated.

    “The strong inhibitory role of this central feature of RNA leads to an antagonism between the degree to which an RNA sequence is able to fold into a defined three-dimensional structure to encode function (such as catalysis) and the ease with which it can be replicated (Boza et al., 2014).”

    From Ribozyme-catalysed RNA synthesis using triplet building blocks (2018) · cites this paper as Boza et al., 2014

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  1. [12]Maynard Smith J, Szathmáry E (1995) The Major Transition in Evolution. Oxford, UK: W.H. Freeman.

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Authors
Boza, G., Szilágyi, A., Kun, Á., Santos, M., & Szathmáry, E.
Affiliations
Eötvös Loránd University (HU)
Corresponding author
Szathmáry, Eörs
Venue
PLoS Computational Biology
Published
2014-12-04
Volume
10
Issue
12
Pages
e1003936
ISSN
  • 1553-734X (ISSN-L)
  • 1553-7358
OpenAlex
W2053806202
Cited by
36
References
37
Citations by year
2025: 1 · 2024: 2 · 2023: 1 · 2022: 16 · 2021: 1 · 2020: 3 · 2018: 4 · 2017: 2 · 2016: 1 · 2015: 4 · 2014: 1
FWCI
1.44
Type
journal article
Language
en
Open access
Locations
  • PLoS Computational Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
  • Dipòsit Digital de Documents de la UAB (Universitat Autònoma de Barcelona) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • ELTE Digital Institutional Repository (EDIT) (Eötvös Loránd University) (submittedVersion, cc-by)
Funders
  • European Commission (TAMOP 4.2.1/B-09/1/KMR-2010-0003, CM1304, KMR-2010-0003, 2007–2013, FP7 2007-2013, 294332, FP7/2007, 4.2.1/B-09/1/KMR-2010-0003)
  • Hungarian Scientific Research Fund (K100299, KMR-2010-0003, NAP 2005/KCKHA005, 4.2.1/B-09/1/KMR-2010-0003)
  • Institució Catalana de Recerca i Estudis Avançats
  • Magyar Tudományos Akadémia
  • Nemzeti Kutatási és Technológiai Hivatal (KCKHA005, NAP 2005/KCKHA005)
  • European Social Fund (2007–2013, FP7/2007-2013, KMR-2010-0003)
  • FP7 Ideas: European Research Council (294332)
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
RNA world, origin of life, division of labor, ribozymes, protocells, replication rate, transcription, origin of the genetic code, positive selection
MeSH terms
DNA Replication, Biological Evolution, Models, Genetic, RNA, RNA, Catalytic, Computational Biology

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