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The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA

In the early ‘RNA world’ stage of life, RNA stored genetic information and catalyzed chemical reactions. However, the RNA world eventually gave rise to the DNA–RNA–protein world, and this transition included the ‘genetic takeover’ of information storage by DNA. We investigated evolutionary advantage...

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Autores principales: Leu, Kevin, Obermayer, Benedikt, Rajamani, Sudha, Gerland, Ulrich, Chen, Irene A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2011
Materias:
RNA
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3185426/
https://www.ncbi.nlm.nih.gov/pubmed/21724606
http://dx.doi.org/10.1093/nar/gkr525
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author Leu, Kevin
Obermayer, Benedikt
Rajamani, Sudha
Gerland, Ulrich
Chen, Irene A.
author_facet Leu, Kevin
Obermayer, Benedikt
Rajamani, Sudha
Gerland, Ulrich
Chen, Irene A.
author_sort Leu, Kevin
collection PubMed
description In the early ‘RNA world’ stage of life, RNA stored genetic information and catalyzed chemical reactions. However, the RNA world eventually gave rise to the DNA–RNA–protein world, and this transition included the ‘genetic takeover’ of information storage by DNA. We investigated evolutionary advantages for using DNA as the genetic material. The error rate of replication imposes a fundamental limit on the amount of information that can be stored in the genome, as mutations degrade information. We compared misincorporation rates of RNA and DNA in experimental non-enzymatic polymerization and calculated the lowest possible error rates from a thermodynamic model. Both analyses found that RNA replication was intrinsically error-prone compared to DNA, suggesting that total genomic information could increase after the transition to DNA. Analysis of the transitional RNA/DNA hybrid duplexes showed that copying RNA into DNA had similar fidelity to RNA replication, so information could be maintained during the genetic takeover. However, copying DNA into RNA was very error-prone, suggesting that attempts to return to the RNA world would result in a considerable loss of information. Therefore, the genetic takeover may have been driven by a combination of increased chemical stability, increased genome size and irreversibility.
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spelling pubmed-31854262011-10-04 The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA Leu, Kevin Obermayer, Benedikt Rajamani, Sudha Gerland, Ulrich Chen, Irene A. Nucleic Acids Res RNA In the early ‘RNA world’ stage of life, RNA stored genetic information and catalyzed chemical reactions. However, the RNA world eventually gave rise to the DNA–RNA–protein world, and this transition included the ‘genetic takeover’ of information storage by DNA. We investigated evolutionary advantages for using DNA as the genetic material. The error rate of replication imposes a fundamental limit on the amount of information that can be stored in the genome, as mutations degrade information. We compared misincorporation rates of RNA and DNA in experimental non-enzymatic polymerization and calculated the lowest possible error rates from a thermodynamic model. Both analyses found that RNA replication was intrinsically error-prone compared to DNA, suggesting that total genomic information could increase after the transition to DNA. Analysis of the transitional RNA/DNA hybrid duplexes showed that copying RNA into DNA had similar fidelity to RNA replication, so information could be maintained during the genetic takeover. However, copying DNA into RNA was very error-prone, suggesting that attempts to return to the RNA world would result in a considerable loss of information. Therefore, the genetic takeover may have been driven by a combination of increased chemical stability, increased genome size and irreversibility. Oxford University Press 2011-10 2011-06-30 /pmc/articles/PMC3185426/ /pubmed/21724606 http://dx.doi.org/10.1093/nar/gkr525 Text en © The Author(s) 2011. Published by Oxford University Press. http://creativecommons.org/licenses/by-nc/3.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle RNA
Leu, Kevin
Obermayer, Benedikt
Rajamani, Sudha
Gerland, Ulrich
Chen, Irene A.
The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA
title The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA
title_full The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA
title_fullStr The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA
title_full_unstemmed The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA
title_short The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA
title_sort prebiotic evolutionary advantage of transferring genetic information from rna to dna
topic RNA
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3185426/
https://www.ncbi.nlm.nih.gov/pubmed/21724606
http://dx.doi.org/10.1093/nar/gkr525
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