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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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Plot of the pseudo-step function φ for calculating protein fitness.The function (see equation {3}) ensures infertility of coding systems producing protein sequences that are less than 70% identical to the reference sequence.
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pone-0005708-g005: Plot of the pseudo-step function φ for calculating protein fitness.The function (see equation {3}) ensures infertility of coding systems producing protein sequences that are less than 70% identical to the reference sequence.

Mentions: The protein fitness function φ for coding system χi is based on the score of the alignment of protein sequence πi produced by coding system χi with the sequence of the reference protein π0. For simplicity, we model evolution under purifying selection, as most housekeeping proteins which encode genes evolve under strong purifying selection [63]. Hence, we consider any deviations of protein πi from π0 to be deleterious, independent of the position where the changes between the two protein sequences occur. Therefore, the fitness function can be represented as an increasing function of a protein alignment score. It is reasonable to assume that a certain number of changes in a protein sequence should result in a complete loss of protein function and therefore in the coding system being unable to reproduce. We decided to set this limit to 0.7 (70% identity), where φ(π0) = 1, as this is a much higher level of similarity than what can be observed between distant homologs that retain the same functionality. We also assumed that a small number of sequence changes should affect the fitness function insignificantly. These considerations result in a behavior that is illustrated with the plot in the Figure 5. Using this curve as a target, we estimated the parameters of a protein fitness function φ that would yield the appropriate behavior; the resulting function is shown below.(3)where ζ is the alignment score (see “Alignment” subsection below).


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

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

Plot of the pseudo-step function φ for calculating protein fitness.The function (see equation {3}) ensures infertility of coding systems producing protein sequences that are less than 70% identical to the reference sequence.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2682656&req=5

pone-0005708-g005: Plot of the pseudo-step function φ for calculating protein fitness.The function (see equation {3}) ensures infertility of coding systems producing protein sequences that are less than 70% identical to the reference sequence.
Mentions: The protein fitness function φ for coding system χi is based on the score of the alignment of protein sequence πi produced by coding system χi with the sequence of the reference protein π0. For simplicity, we model evolution under purifying selection, as most housekeeping proteins which encode genes evolve under strong purifying selection [63]. Hence, we consider any deviations of protein πi from π0 to be deleterious, independent of the position where the changes between the two protein sequences occur. Therefore, the fitness function can be represented as an increasing function of a protein alignment score. It is reasonable to assume that a certain number of changes in a protein sequence should result in a complete loss of protein function and therefore in the coding system being unable to reproduce. We decided to set this limit to 0.7 (70% identity), where φ(π0) = 1, as this is a much higher level of similarity than what can be observed between distant homologs that retain the same functionality. We also assumed that a small number of sequence changes should affect the fitness function insignificantly. These considerations result in a behavior that is illustrated with the plot in the Figure 5. Using this curve as a target, we estimated the parameters of a protein fitness function φ that would yield the appropriate behavior; the resulting function is shown below.(3)where ζ is the alignment score (see “Alignment” subsection below).

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
Related in: MedlinePlus