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Meiotic recombination counteracts male-biased mutation (male-driven evolution).

ABSTRACT: Meiotic recombination is believed to produce greater genetic variation despite the fact that deoxyribonucleic acid (DNA)-replication errors are a major source of mutations. In some vertebrates, mutation rates are higher in males than in females, which developed the theory of male-driven evolution (male-biased mutation). However, there is little molecular evidence regarding the relationships between meiotic recombination and male-biased mutation. Here we tested the theory using the frog Rana rugosa, which has both XX/XY- and ZZ/ZW-type sex-determining systems within the species. The male-to-female mutation-rate ratio (?) was calculated from homologous sequences on the X/Y or Z/W sex chromosomes, which supported male-driven evolution. Surprisingly, each ? value was notably higher in the XX/XY-type group than in the ZZ/ZW-type group, although ? should have similar values within a species. Interestingly, meiotic recombination between homologous chromosomes did not occur except at terminal regions in males of this species. Then, by subdividing ? into two new factors, a replication-based male-to-female mutation-rate ratio (?) and a meiotic recombination-based XX-to-XY/ZZ-to-ZW mutation-rate ratio (?), we constructed a formula describing the relationship among a nucleotide-substitution rate and the two factors, ? and ?. Intriguingly, the ?- and ?-values were larger and smaller than 1, respectively, indicating that meiotic recombination might reduce male-biased mutations.

SUBMITTER: Mawaribuchi S

PROVIDER: S-EPMC4795034 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Meiotic recombination counteracts male-biased mutation (male-driven evolution).

Mawaribuchi Shuuji S Ito Michihiko M Ogata Mitsuaki M Oota Hiroki H Katsumura Takafumi T Takamatsu Nobuhiko N Miura Ikuo I

Proceedings. Biological sciences 20160101 1823

Meiotic recombination is believed to produce greater genetic variation despite the fact that deoxyribonucleic acid (DNA)-replication errors are a major source of mutations. In some vertebrates, mutation rates are higher in males than in females, which developed the theory of male-driven evolution (male-biased mutation). However, there is little molecular evidence regarding the relationships between meiotic recombination and male-biased mutation. Here we tested the theory using the frog Rana rugo ...[more]

PMID: 26791621

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Project description:Template-dependent RNA replication mechanisms render picornaviruses susceptible to error catastrophe, an overwhelming accumulation of mutations incompatible with viability. Viral RNA recombination, in theory, provides a mechanism for viruses to counteract error catastrophe. We tested this theory by exploiting well-defined mutations in the poliovirus RNA-dependent RNA polymerase (RDRP), namely, a G64S mutation and an L420A mutation. Our data reveal two distinct mechanisms by which picornaviral RDRPs influence error catastrophe: fidelity of RNA synthesis and RNA recombination. A G64S mutation increased the fidelity of the viral polymerase and rendered the virus resistant to ribavirin-induced error catastrophe, but only when RNA recombination was at wild-type levels. An L420A mutation in the viral polymerase inhibited RNA recombination and exacerbated ribavirin-induced error catastrophe. Furthermore, when RNA recombination was substantially reduced by an L420A mutation, a high-fidelity G64S polymerase failed to make the virus resistant to ribavirin. These data indicate that viral RNA recombination is required for poliovirus to evade ribavirin-induced error catastrophe. The conserved nature of L420 within RDRPs suggests that RNA recombination is a common mechanism for picornaviruses to counteract and avoid error catastrophe.IMPORTANCE Positive-strand RNA viruses produce vast amounts of progeny in very short periods of time via template-dependent RNA replication mechanisms. Template-dependent RNA replication, while efficient, can be disadvantageous due to error-prone viral polymerases. The accumulation of mutations in viral RNA genomes leads to error catastrophe. In this study, we substantiate long-held theories regarding the advantages and disadvantages of asexual and sexual replication strategies among RNA viruses. In particular, we show that picornavirus RNA recombination counteracts the negative consequences of asexual template-dependent RNA replication mechanisms, namely, error catastrophe.

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Meiotic recombination counteracts male-biased mutation (male-driven evolution).

Publications

Meiotic recombination counteracts male-biased mutation (male-driven evolution).

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