The evolution of strand preference in simulated RNA replicators with strand displacement: Implications for the origin of transcriptionReport as inadecuate

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Biology Direct

, 3:33

Origin and early evolution of life


BackgroundThe simplest conceivable example of evolving systems is RNA molecules that can replicate themselves. Since replication produces a new RNA strand complementary to a template, all templates would eventually become double-stranded and, hence, become unavailable for replication. Thus the problem of how to separate the two strands is considered a major issue for the early evolution of self-replicating RNA. One biologically plausible way to copy a double-stranded RNA is to displace a preexisting strand by a newly synthesized strand. Such copying can in principle be initiated from either the + or - strand of a double-stranded RNA. Assuming that only one of them, say +, can act as replicase when single-stranded, strand displacement produces a new replicase if the - strand is the template. If, however, the + strand is the template, it produces a new template but no replicase. Modern transcription exhibits extreme strand preference wherein anti-sense strands are always the template. Likewise, replication by strand displacement seems optimal if it also exhibits extreme strand preference wherein - strands are always the template, favoring replicase production. Here we investigate whether such strand preference can evolve in a simple RNA replicator system with strand displacement.

ResultsWe first studied a simple mathematical model of the replicator dynamics. Our results indicated that if the system is well-mixed, there is no selective force acting upon strand preference per se. Next, we studied an individual-based simulation model to investigate the evolution of strand preference under finite diffusion. Interestingly, the results showed that selective forces -emerge- because of finite diffusion. Strikingly, the direction of the strand preference that evolves i.e. + or - strand excess is a complex non-monotonic function of the diffusion intensity. The mechanism underlying this behavior is elucidated. Furthermore, a speciation-like phenomenon is observed under certain conditions: two extreme replication strategies, namely replicase producers and template producers, emerge and coexist among competing replicators.

ConclusionFinite diffusion enables the evolution of strand preference, the direction of which is a non-monotonic function of the diffusion intensity. By identifying the conditions under which strand preference evolves, this study provides an insight into how a rudimentary transcription-like pattern might have emerged in an RNA-based replicator system.

ReviewersThis article was reviewed by Eugene V Koonin, Rob Kinght and István Scheuring nominated by David H Ardell. For the full reviews, please go to the Reviewers- comments section.

Electronic supplementary materialThe online version of this article doi:10.1186-1745-6150-3-33 contains supplementary material, which is available to authorized users.

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Author: Nobuto Takeuchi - Laura Salazar - Anthony M Poole - Paulien Hogeweg


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