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Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution

The integration of individually replicating genes into a primitive chromosome is a key evolutionary transition in the development of life, allowing the simultaneous inheritance of genes. However, how this transition occurred is unclear because the extended size of primitive chromosomes replicate slo...

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Detalles Bibliográficos
Autores principales: Ueda, Kensuke, Mizuuchi, Ryo, Ichihashi, Norikazu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10431678/
https://www.ncbi.nlm.nih.gov/pubmed/37540715
http://dx.doi.org/10.1371/journal.pgen.1010471
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author Ueda, Kensuke
Mizuuchi, Ryo
Ichihashi, Norikazu
author_facet Ueda, Kensuke
Mizuuchi, Ryo
Ichihashi, Norikazu
author_sort Ueda, Kensuke
collection PubMed
description The integration of individually replicating genes into a primitive chromosome is a key evolutionary transition in the development of life, allowing the simultaneous inheritance of genes. However, how this transition occurred is unclear because the extended size of primitive chromosomes replicate slower than unlinked genes. Theoretical studies have suggested that a primitive chromosome can evolve in the presence of cell-like compartments, as the physical linkage prevents the stochastic loss of essential genes upon division, but experimental support for this is lacking. Here, we demonstrate the evolution of a chromosome-like RNA from two cooperative RNA replicators encoding replication and metabolic enzymes. Through their long-term replication in cell-like compartments, linked RNAs emerged with the two cooperative RNAs connected end-to-end. The linked RNAs had different mutation patterns than the two unlinked RNAs, suggesting that they were maintained as partially distinct lineages in the population. Our results provide experimental evidence supporting the plausibility of the evolution of a primitive chromosome from unlinked gene fragments, an important step in the emergence of complex biological systems.
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spelling pubmed-104316782023-08-17 Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution Ueda, Kensuke Mizuuchi, Ryo Ichihashi, Norikazu PLoS Genet Research Article The integration of individually replicating genes into a primitive chromosome is a key evolutionary transition in the development of life, allowing the simultaneous inheritance of genes. However, how this transition occurred is unclear because the extended size of primitive chromosomes replicate slower than unlinked genes. Theoretical studies have suggested that a primitive chromosome can evolve in the presence of cell-like compartments, as the physical linkage prevents the stochastic loss of essential genes upon division, but experimental support for this is lacking. Here, we demonstrate the evolution of a chromosome-like RNA from two cooperative RNA replicators encoding replication and metabolic enzymes. Through their long-term replication in cell-like compartments, linked RNAs emerged with the two cooperative RNAs connected end-to-end. The linked RNAs had different mutation patterns than the two unlinked RNAs, suggesting that they were maintained as partially distinct lineages in the population. Our results provide experimental evidence supporting the plausibility of the evolution of a primitive chromosome from unlinked gene fragments, an important step in the emergence of complex biological systems. Public Library of Science 2023-08-04 /pmc/articles/PMC10431678/ /pubmed/37540715 http://dx.doi.org/10.1371/journal.pgen.1010471 Text en © 2023 Ueda et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Ueda, Kensuke
Mizuuchi, Ryo
Ichihashi, Norikazu
Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution
title Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution
title_full Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution
title_fullStr Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution
title_full_unstemmed Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution
title_short Emergence of linkage between cooperative RNA replicators encoding replication and metabolic enzymes through experimental evolution
title_sort emergence of linkage between cooperative rna replicators encoding replication and metabolic enzymes through experimental evolution
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10431678/
https://www.ncbi.nlm.nih.gov/pubmed/37540715
http://dx.doi.org/10.1371/journal.pgen.1010471
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