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 ev...

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Bibliographic Details
Published in:Nucleic acids research 2011-10, Vol.39 (18), p.8135-8147
Main Authors: Leu, Kevin, Obermayer, Benedikt, Rajamani, Sudha, Gerland, Ulrich, Chen, Irene A.
Format: Article
Language:English
Subjects:
DNA
DNA - chemistry
DNA Replication
Evolution
Evolution, Molecular
Fidelity
Genomes
genomics
Hybrids
Mutation
Nucleotides - analysis
Polymerization
Replication
RNA
RNA - biosynthesis
RNA - chemistry
RNA, Catalytic - metabolism
Thermodynamics
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Summary: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.
ISSN:0305-1048
1362-4962
DOI:10.1093/nar/gkr525