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Codon size reduction as the origin of the triplet genetic code.

Baranov PV, Venin M, Provan G - PLoS ONE (2009)

Bottom Line: The apparent impossibility of transitions between codon sizes in a discontinuous manner during evolution has resulted in an unbending view that the genetic code was always triplet.Computer simulations based on our model show that decoding systems with codons of length greater than three spontaneously evolve into predominantly triplet decoding systems.This scenario suggests an explanation of how protein synthesis could be accomplished by means of long RNA-RNA interactions prior to the emergence of the complex decoding machinery, such as the ribosome, that is required for stabilization and discrimination of otherwise weak triplet codon-anticodon interactions.

View Article: PubMed Central - PubMed

Affiliation: Biochemistry Department, University College Cork, Cork, Ireland. p.baranov@ucc.ie

ABSTRACT
The genetic code appears to be optimized in its robustness to missense errors and frameshift errors. In addition, the genetic code is near-optimal in terms of its ability to carry information in addition to the sequences of encoded proteins. As evolution has no foresight, optimality of the modern genetic code suggests that it evolved from less optimal code variants. The length of codons in the genetic code is also optimal, as three is the minimal nucleotide combination that can encode the twenty standard amino acids. The apparent impossibility of transitions between codon sizes in a discontinuous manner during evolution has resulted in an unbending view that the genetic code was always triplet. Yet, recent experimental evidence on quadruplet decoding, as well as the discovery of organisms with ambiguous and dual decoding, suggest that the possibility of the evolution of triplet decoding from living systems with non-triplet decoding merits reconsideration and further exploration. To explore this possibility we designed a mathematical model of the evolution of primitive digital coding systems which can decode nucleotide sequences into protein sequences. These coding systems can evolve their nucleotide sequences via genetic events of Darwinian evolution, such as point-mutations. The replication rates of such coding systems depend on the accuracy of the generated protein sequences. Computer simulations based on our model show that decoding systems with codons of length greater than three spontaneously evolve into predominantly triplet decoding systems. Our findings suggest a plausible scenario for the evolution of the triplet genetic code in a continuous manner. This scenario suggests an explanation of how protein synthesis could be accomplished by means of long RNA-RNA interactions prior to the emergence of the complex decoding machinery, such as the ribosome, that is required for stabilization and discrimination of otherwise weak triplet codon-anticodon interactions.

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An outline of the Codonevo simulations.A. Population dynamics. During each cycle a population of coding systems undergo two stages, birth (where a number of coding system copies are created according to a replication function ρ) and death (where coding systems are randomly destroyed until their number reaches a certain constant limit O). B. Obtaining the replication function ρ for each coding system. A coding system consists of a single mRNA sequence and a set of tRNA rules that are used to produce a protein sequence. The protein sequence πi is aligned to the reference protein sequence π0, and a replication function ρ is calculated based on the score of the alignment and the deviation of the coding system size from the average coding system size in the population. See section Methods for details.
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pone-0005708-g001: An outline of the Codonevo simulations.A. Population dynamics. During each cycle a population of coding systems undergo two stages, birth (where a number of coding system copies are created according to a replication function ρ) and death (where coding systems are randomly destroyed until their number reaches a certain constant limit O). B. Obtaining the replication function ρ for each coding system. A coding system consists of a single mRNA sequence and a set of tRNA rules that are used to produce a protein sequence. The protein sequence πi is aligned to the reference protein sequence π0, and a replication function ρ is calculated based on the score of the alignment and the deviation of the coding system size from the average coding system size in the population. See section Methods for details.

Mentions: The overall scheme of the model is outlined in Figure 1. In brief, a population consists of a set of digital coding systems X evolving through alternate birth and death cycles. During a birth cycle, a population is increased by a number of coding systems produced according to a replication rate function ρ, which is proportional to the products of (a) the fitness φ of a protein molecule πi produced by coding system χi, and (b) the difference in size of coding system χi from the average coding system size. System size is the sum of the “nucleotide sequences” (each coding system consists of a single “mRNA” and a set of “tRNA rules” that specifies associations between a combination of nucleotides and a single amino acid). During the death cycle, coding systems are destroyed randomly until their number reaches a certain constant limit. This restriction reflects the limited availability of energy and food resources. For simplicity we consider that the supply of energy and food resources remains constant over time.


Codon size reduction as the origin of the triplet genetic code.

Baranov PV, Venin M, Provan G - PLoS ONE (2009)

An outline of the Codonevo simulations.A. Population dynamics. During each cycle a population of coding systems undergo two stages, birth (where a number of coding system copies are created according to a replication function ρ) and death (where coding systems are randomly destroyed until their number reaches a certain constant limit O). B. Obtaining the replication function ρ for each coding system. A coding system consists of a single mRNA sequence and a set of tRNA rules that are used to produce a protein sequence. The protein sequence πi is aligned to the reference protein sequence π0, and a replication function ρ is calculated based on the score of the alignment and the deviation of the coding system size from the average coding system size in the population. See section Methods for details.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2682656&req=5

pone-0005708-g001: An outline of the Codonevo simulations.A. Population dynamics. During each cycle a population of coding systems undergo two stages, birth (where a number of coding system copies are created according to a replication function ρ) and death (where coding systems are randomly destroyed until their number reaches a certain constant limit O). B. Obtaining the replication function ρ for each coding system. A coding system consists of a single mRNA sequence and a set of tRNA rules that are used to produce a protein sequence. The protein sequence πi is aligned to the reference protein sequence π0, and a replication function ρ is calculated based on the score of the alignment and the deviation of the coding system size from the average coding system size in the population. See section Methods for details.
Mentions: The overall scheme of the model is outlined in Figure 1. In brief, a population consists of a set of digital coding systems X evolving through alternate birth and death cycles. During a birth cycle, a population is increased by a number of coding systems produced according to a replication rate function ρ, which is proportional to the products of (a) the fitness φ of a protein molecule πi produced by coding system χi, and (b) the difference in size of coding system χi from the average coding system size. System size is the sum of the “nucleotide sequences” (each coding system consists of a single “mRNA” and a set of “tRNA rules” that specifies associations between a combination of nucleotides and a single amino acid). During the death cycle, coding systems are destroyed randomly until their number reaches a certain constant limit. This restriction reflects the limited availability of energy and food resources. For simplicity we consider that the supply of energy and food resources remains constant over time.

Bottom Line: The apparent impossibility of transitions between codon sizes in a discontinuous manner during evolution has resulted in an unbending view that the genetic code was always triplet.Computer simulations based on our model show that decoding systems with codons of length greater than three spontaneously evolve into predominantly triplet decoding systems.This scenario suggests an explanation of how protein synthesis could be accomplished by means of long RNA-RNA interactions prior to the emergence of the complex decoding machinery, such as the ribosome, that is required for stabilization and discrimination of otherwise weak triplet codon-anticodon interactions.

View Article: PubMed Central - PubMed

Affiliation: Biochemistry Department, University College Cork, Cork, Ireland. p.baranov@ucc.ie

ABSTRACT
The genetic code appears to be optimized in its robustness to missense errors and frameshift errors. In addition, the genetic code is near-optimal in terms of its ability to carry information in addition to the sequences of encoded proteins. As evolution has no foresight, optimality of the modern genetic code suggests that it evolved from less optimal code variants. The length of codons in the genetic code is also optimal, as three is the minimal nucleotide combination that can encode the twenty standard amino acids. The apparent impossibility of transitions between codon sizes in a discontinuous manner during evolution has resulted in an unbending view that the genetic code was always triplet. Yet, recent experimental evidence on quadruplet decoding, as well as the discovery of organisms with ambiguous and dual decoding, suggest that the possibility of the evolution of triplet decoding from living systems with non-triplet decoding merits reconsideration and further exploration. To explore this possibility we designed a mathematical model of the evolution of primitive digital coding systems which can decode nucleotide sequences into protein sequences. These coding systems can evolve their nucleotide sequences via genetic events of Darwinian evolution, such as point-mutations. The replication rates of such coding systems depend on the accuracy of the generated protein sequences. Computer simulations based on our model show that decoding systems with codons of length greater than three spontaneously evolve into predominantly triplet decoding systems. Our findings suggest a plausible scenario for the evolution of the triplet genetic code in a continuous manner. This scenario suggests an explanation of how protein synthesis could be accomplished by means of long RNA-RNA interactions prior to the emergence of the complex decoding machinery, such as the ribosome, that is required for stabilization and discrimination of otherwise weak triplet codon-anticodon interactions.

Show MeSH