Sex as a response to oxidative DNA damage

Berstein, Carol; Johns, Virginia

doi:10.1016/0891-5849(90)90335-g

Cited by 6 publications

(13 citation statements)

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“…The idea emerged that meiosis could be a repair mechanism of DNA double strand breaks [18], for which a homologous chromosome is needed as template. Later, this idea was linked up to oxidative DNA damage [19][20]. However, since many other DNA repair mechanisms exist, and since permanent diploidy would also serve for DNA repair, the theory was not broadly accepted by evolutionary biologists [11].…”

Section: The Origin Of Eukaryotic Life Oxidative Stress and Dna Damagementioning

confidence: 99%

“…Carol and Harris Bernstein [18][19][20] and coworkers were the first to propose a consistent hypothesis that crossing over at meiosis might have evolved as a repair mechanism of oxidative double strand DNA damage. Their ideas stemmed from observations that, in fact, meiosis is not at all optimized to create new gene combinations, as Holliday junctions can be resolved with and without cross-over.…”

Section: The Origin Of Eukaryotic Life Oxidative Stress and Dna Damagementioning

confidence: 99%

“…Initially, double strand breaks caused by oxidative damage could have been the primary trigger for the onset of meiosis. Carol Bernstein [20] summarized the main requirements for oxidative damage being a selective pressure for the maintenance of meiosis as a DNA repair mechanism in eukaryotes. To maintain meiosis by selection for DNA repair caused by oxidative damage, the following conditions must be fulfilled: (1) Oxidative damage is deleterious to cell function; (2) oxidative damage accumulates in somatic cells; (3) oxidative damage should be repairable by recombinational repair during meiosis; (4) the mechanisms of recombination enzymes should be more adapted to DNA repair than to simple random genetic exchange.…”

Section: Homologous Recombinational Dna Repair Of Oxidative Damagementioning

confidence: 99%

“…Oxidative DNA damages in somatic cells are by far the most frequent ones in mammals. Around 130,000 endogenous damages of DNA occur per cell per day for rats, whereby 86,000 are due to oxidative damage [20]. Oxidative damage may accumulate in the following way: free radicals first cause mutations of mitochondrial (mt) DNA, which, in turn, affects structure and function of mt proteins.…”

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confidence: 99%

“…Most damages affect just single strands of DNA, and repair can be conducted by the complementary strand which stores redundant sequence information for re-synthesis. Double-strand breaks and DNA cross-links cannot be easily repaired this way, and these damages require information from a second, undamaged homologous DNA molecule by recombinational repair [20].…”

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confidence: 99%

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Meiosis and the Paradox of Sex in Nature

Hörandl¹

2013

Meiosis

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Section: The Origin Of Eukaryotic Life Oxidative Stress and Dna Damagementioning

confidence: 99%

Section: The Origin Of Eukaryotic Life Oxidative Stress and Dna Damagementioning

confidence: 99%

Section: Homologous Recombinational Dna Repair Of Oxidative Damagementioning

confidence: 99%

mentioning

confidence: 99%

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confidence: 99%

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Meiosis and the Paradox of Sex in Nature

Hörandl¹

2013

Meiosis

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The oxidative damage initiation hypothesis for meiosis

Hörandl

Hadaček

2013

Plant Reprod

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The maintenance of sexual reproduction in eukaryotes is still a major enigma in evolutionary biology. Meiosis represents the only common feature of sex in all eukaryotic kingdoms, and thus, we regard it a key issue for discussing its function. Almost all asexuality modes maintain meiosis either in a modified form or as an alternative pathway, and facultatively apomictic plants increase frequencies of sexuality relative to apomixis after abiotic stress. On the physiological level, abiotic stress causes oxidative stress. We hypothesize that repair of oxidative damage on nuclear DNA could be a major driving force in the evolution of meiosis. We present a hypothetical model for the possible redox chemistry that underlies the binding of the meiosis-specific protein Spo11 to DNA. During prophase of meiosis I, oxidized sites at the DNA molecule are being targeted by the catalytic tyrosine moieties of Spo11 protein, which acts like an antioxidant reducing the oxidized target. The oxidized tyrosine residues, tyrosyl radicals, attack the phosphodiester bonds of the DNA backbone causing DNA double strand breaks that can be repaired by various mechanisms. Polyploidy in apomictic plants could mitigate oxidative DNA damage and decrease Spo11 activation. Our hypothesis may contribute to explaining various enigmatic phenomena: first, DSB formation outnumbers crossovers and, thus, effective recombination events by far because the target of meiosis may be the removal of oxidative lesions; second, it offers an argument for why expression of sexuality is responsive to stress in many eukaryotes; and third, repair of oxidative DNA damage turns meiosis into an essential characteristic of eukaryotic reproduction.

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A combinational theory for maintenance of sex

Hörandl

2009

Heredity

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Sexual reproduction implies high costs, but it is difficult to give evidence for evolutionary advantages that would explain the predominance of meiotic sex in eukaryotes. A combinational theory discussing evolution, maintenance and loss of sex may resolve the problem. The main function of sex is the restoration of DNA and consequently a higher quality of offspring. Recombination at meiosis evolved, perhaps, as a repair mechanism of DNA strand damages. This mechanism is most efficient for DNA restoration in multicellular eukaryotes, because the initial cell starts with a re-optimized genome, which is passed to all the daughter cells. Meiosis acts also as creator of variation in haploid stages, in which selection can purge most efficiently deleterious mutations. A prolonged diploid phase buffers the effects of deleterious recessive alleles as well as epigenetic defects and is thus optimal for prolonged growth periods. For complex multicellular organisms, the main advantage of sexuality is thus the alternation of diploid and haploid stages, combining advantages of both. A loss of sex is constrained by several, partly group-specific, developmental features. Hybridization may trigger shifts from sexual to asexual reproduction, but crossing barriers of the parental sexual species limit this process. For the concerted break-up of meiosis-outcrossing cycles plus silencing of secondary features, various group-specific changes in the regulatory system may be required. An establishment of asexuals requires special functional modifications and environmental opportunities. Costs for maintenance of meiotic sex are consequently lower than a shift to asexual reproduction.

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Sex as a response to oxidative DNA damage

Cited by 6 publications

References 0 publications

Meiosis and the Paradox of Sex in Nature

Meiosis and the Paradox of Sex in Nature

The oxidative damage initiation hypothesis for meiosis

A combinational theory for maintenance of sex

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