Meiosis as an Evolutionary Adaptation for DNA Repair

Bernstein, Harris; Bernstein, Carol; Michod, Richard E.

doi:10.5772/25117

Cited by 33 publications

(21 citation statements)

References 118 publications

(76 reference statements)

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“…1. Homologous recombination: Homologous recombination evolved in the prokaryotes because it plays an important role in DNA repair (Bernstein et al 2011;Bernstein et al 1989). Prokaryotes do not alternate between haploid and diploid generations because protein aggregation is not a substantial enough problem for them to benefit from heterozygosity, even under stressful conditions (main text).…”

Section: Appendix A3 Recombination and Simple Organismsmentioning

confidence: 99%

“…Synapsis: A key step in the evolution of meiosis from mitosis is the synapsis of homologous chromosomes (Wilkins and Holliday 2009). DNA repair proteins seem to have been recruited to assist with the formation of chiasmata (Bernstein et al 2011). The formation of chiasmata may have initially improved the fidelity of recombination (by preventing ectopic recombination for example), but the chiasmata also help homologous chromosomes to properly align, so they can segregate correctly during meiosis and ensure that each daughter cell has a proper karyotype (Bernstein et al 2011;Gorelick and Heng 2010;Wilkins and Holliday 2009;Heng 2007).…”

Section: Appendix A3 Recombination and Simple Organismsmentioning

confidence: 99%

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The thermodynamics of protein aggregation reactions may underpin the enhanced metabolic efficiency associated with heterosis, some balancing selection, and the evolution of ploidy levels

Ginn

2017

Progress in Biophysics and Molecular Biology

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Identifying the physical basis of heterosis (or "hybrid vigor") has remained elusive despite over a hundred years of research on the subject. The three main theories of heterosis are dominance theory, overdominance theory, and epistasis theory. Kacser and Burns (1981) identified the molecular basis of dominance, which has greatly enhanced our understanding of its importance to heterosis. This paper aims to explain how overdominance, and some features of epistasis, can similarly emerge from the molecular dynamics of proteins. Possessing multiple alleles at a gene locus results in the synthesis of different allozymes at reduced concentrations. This in turn reduces the rate at which each allozyme forms soluble oligomers, which are toxic and must be degraded, because allozymes co-aggregate at low efficiencies. The model developed in this paper can explain how heterozygosity impacts the metabolic efficiency of an organism. It can also explain why the viabilities of some inbred lines seem to decline rapidly at high inbreeding coefficients (F > 0.5), which may provide a physical basis for truncation selection for heterozygosity. Finally, the model has implications for the ploidy level of organisms. It can explain why polyploids are frequently found in environments where severe physical stresses promote the formation of soluble oligomers. The model can also explain why complex organisms, which need to synthesize aggregation-prone proteins that contain intrinsically unstructured regions (IURs) and multiple domains because they facilitate complex protein interaction networks (PINs), tend to be diploid while haploidy tends to be restricted to relatively simple organisms.

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Section: Appendix A3 Recombination and Simple Organismsmentioning

confidence: 99%

Section: Appendix A3 Recombination and Simple Organismsmentioning

confidence: 99%

The thermodynamics of protein aggregation reactions may underpin the enhanced metabolic efficiency associated with heterosis, some balancing selection, and the evolution of ploidy levels

Ginn

2017

Progress in Biophysics and Molecular Biology

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“…The emergence of sex would have enhanced DNA repair yet came with significant costs including the twofold cost of sex (de Visser & Elena, ; Bernstein et al , ; Goddard, ; McDonald et al , ). Intriguingly, sex may have been especially advantageous in dealing with oxidative stress from the endosymbiont that formed the pre‐mitochondrion, as this aerobic bacterium would have generated high levels of ROS (Blackstone, ; Bernstein et al , ; Horandl & Speijer, ). Sex would have been particularly effective in repairing subsequent ROS‐induced DNA damage via homologous recombination.…”

Section: Discussionmentioning

confidence: 99%

Metabolism‐induced oxidative stress and DNA damage selectively trigger genome instability in polyploid fungal cells

et al. 2019

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Understanding how cellular activities impact genome stability is critical to multiple biological processes including tumorigenesis and reproductive biology. The fungal pathogen Candida albicans displays striking genome dynamics during its parasexual cycle as tetraploid cells, but not diploid cells, exhibit genome instability and reduce their ploidy when grown on a glucose‐rich “pre‐sporulation” medium. Here, we reveal that C. albicans tetraploid cells are metabolically hyperactive on this medium with higher rates of fermentation and oxidative respiration relative to diploid cells. This heightened metabolism results in elevated levels of reactive oxygen species (ROS), activation of the ROS‐responsive transcription factor Cap1, and the formation of DNA double‐strand breaks. Genetic or chemical suppression of ROS levels suppresses each of these phenotypes and also protects against genome instability. These studies reveal how endogenous metabolic processes can generate sufficient ROS to trigger genome instability in polyploid C. albicans cells. We also discuss potential parallels with metabolism‐induced instability in cancer cells and speculate that ROS‐induced DNA damage could have facilitated ploidy cycling prior to a conventional meiosis in eukaryotes.

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“…Such sequences might have been related to the spread of retrotransposons in early eukaryotes, of which many types are very ancient in eukaryotes but absent in bacteria and archaea [27]. Another hypothesis is that pairing and recombination initially arose as a way to repair mutational damage caused by increased oxidative stress due to rising atmospheric oxygen or endosymbiosis [7,[28][29][30]. This scenario presupposes that DNA maintenance is inefficient in the absence of meiosis; however, prokaryotes (including archaea) have efficient repair mechanisms that involve recombination but not meiosis [9].…”

Section: The Origin Of Synapsis and Meiotic Recombinationmentioning

confidence: 99%

Evolutionary mysteries in meiosis

Lenormand

Engelstädter

Johnston

et al. 2016

Preprint

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Meiosis is a key event of sexual life cycles in eukaryotes. Its mechanistic details have been uncovered in several model organisms and most of its essential features have received various and often contradictory evolutionarily interpretations. In this perspective, we present an overview of these often "weird" features. We discuss the origin of meiosis (origin of ploidy reduction and recombination, two-step meiosis), its secondary modifications (in polyploids or asexuals, inverted meiosis), its importance in punctuating life cycles (meiotic arrests, epigenetic resetting, meiotic asymmetry, meiotic fairness) and features associated with recombination (disjunction constraints, heterochiasmy, crossover interference and hotspots). We present the various evolutionary scenarios and selective pressures that have been proposed to account for these features and we highlight that their evolutionary significance often remains largely mysterious. Resolving these mysteries will likely provide decisive steps towards understanding why sex and recombination is found in the majority of eukaryotes.

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Meiosis as an Evolutionary Adaptation for DNA Repair

Cited by 33 publications

References 118 publications

The thermodynamics of protein aggregation reactions may underpin the enhanced metabolic efficiency associated with heterosis, some balancing selection, and the evolution of ploidy levels

The thermodynamics of protein aggregation reactions may underpin the enhanced metabolic efficiency associated with heterosis, some balancing selection, and the evolution of ploidy levels

Metabolism‐induced oxidative stress and DNA damage selectively trigger genome instability in polyploid fungal cells

Evolutionary mysteries in meiosis

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