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Segregation of recombined chromosomes during the two meiotic divisions. Black and white lines represent homologous chromosomes. Gray circles represent cohesin; open circles represent kinetechores. Arrows represent the meiotic spindle. See text for explanation.
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In most organisms homologous recombination is vital for the proper segregation of chromosomes during meiosis, the formation of haploid sex cells from diploid precursors. This review compares meiotic recombination and chromosome segregation in the fission yeast Schizosaccharomyces pombe and the distantly related budding yeast Saccharomyces cerevisia...
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Context 1
... meiosis two successive nuclear divisions follow a single round of DNA replication (Fig. 1). Homologous chromosomes segre- gate to opposite poles at MI, then sister chromatids segregate at MII. At MI, unlike mitosis or MII, one functional kinetochore, the proteinaceous bridge linking the chromosomes to the spindle microtubules, is associated with each homolog rather than with each chromatid. At MII, like mitosis, each sister ...
Context 2
... between homologs required to ensure proper positioning of the chromosomes on the MI spindle. SCC then must be released on the chromosome arms, distal to all reciprocal recombination events, to allow homologs to segregate. But SCC must be maintained proximal to the centromere until MII to properly orient the chromosomes on the MII spindle (Fig. 1). Centromere-proximal cohesion is then released, allowing sister chromatids to ...
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A physical connection between each pair of homologous chromosomes is crucial for reductional chromosome segregation during the first meiotic division and therefore for successful meiosis. Connection is provided by recombination (crossing over) initiated by programmed DNA double-strand breaks (DSBs). Although the topoisomerase-like protein Spo11 mak...
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Meiotic recombination, crucial for proper chromosome segregation and genome evolution, is initiated by programmed DNA double-strand breaks (DSBs) in yeasts and likely all sexually reproducing species. In fission yeast, DSBs occur up to hundreds of times more frequently at special sites, called hot spots, than in other regions of the genome. What di...
Citations
... Meiotic recombination is a key cellular process with major consequences for evolution. In the vast majority of sexually reproducing species, the formation of a crossing over is required for the proper segregation of homologs during meiosis (Baker et al. 1976; Davis and Smith 2001;Pardo-Manuel de Villena and Sapienza 2001;Gerton and Hawley 2005). Failure of this process often leads to meiotic arrest or the formation of aneuploid gametes with missing or extra chromosomes (Hassold et al. 2007;Handel and Schimenti 2010;Székvölgyi and Nicolas 2010;Brick et al. 2012;Mihola et al. 2019). ...
It is commonly thought that the long-term advantage of meiotic recombination is to dissipate genetic linkage, allowing natural selection to act independently on different loci. It is thus theoretically expected that genes with higher recombination rates evolve under more effective selection. On the other hand, recombination is often associated with GC-biased gene conversion (gBGC), which theoretically interferes with selection by promoting the fixation of deleterious GC alleles. To test these predictions, several studies assessed whether selection was more effective in highly recombining genes (due to dissipation of genetic link age) or less effective (due to gBGC), assuming a fixed distribution of fitness effects (DFE) for all genes. In this study, I directly derive the DFE from a gene's evolutionary history (shaped by mutation, selection, drift and gBGC) under empirical fitness landscapes. I show that genes that have experienced high levels of gBGC are less fit and thus have more opportunities for beneficial mutations. Only a small decrease in the genome-wide intensity of gBGC leads to the fixation of these beneficial mutations, particularly in highly recombining genes. This results in increased positive selection in highly recombining genes that is not caused by more effective selection. Additionally, I show that the death of a recombination hotspot can lead to a higher dN/dS than its birth, but with substitution patterns biased towards AT, and only at selected positions. This shows that controlling for a substitution bias towards GC is therefore not sufficient to rule out the contribution of gBGC to signatures of accelerated evolution. Finally, although gBGC does not affect the fixation probability of GC-conservative mutations, I show that by altering the DFE, gBGC can also significantly affect non-synonymous GC-conservative substitution patterns.
... Mutational alteration of genotype enables a sampling of the 'sequence space' of the organism and increases the chances of natural selection acting on better adapted alleles (Sundin & Weigand 2007). Individuals that are starved or deprived of other vital resources undergo sex in a wide variety of microorganisms, including yeast (Kassir et al. 1988;Mochizuki & Yamamoto 1992;Mai & Breeden 2000;Abdullah & Borts 2001;Davis & Smith 2001;van Werven & Amon 2011), and Chlamydomonas reinhardtii (Harris EH 1989;Quarmby 1994;Goodenough et al. 2007). ...
... The initial landmark event following karyogamy is the formation of a telomere-led chromosome bouquet, which migrates rapidly back and forth in the length of the cell in a dynein-led movement called horse-tailing (HT) [9,10]. Meiotic S (meiS) phase and recombination occur during horse-tailing, which is followed by the MI and meiosis II (MII) divisions (reviewed in [11][12][13]). Genetic tools have been deployed to identify and characterize proteins that function throughout these different phases. ...
Meiosis is a carefully choreographed dynamic process that re-purposes proteins from somatic/vegetative cell division, as well as meiosis-specific factors, to carry out the differentiation and recombination pathway common to sexually reproducing eukaryotes. Studies of individual proteins from a variety of different experimental protocols can make it difficult to compare details between them. Using a consistent protocol in otherwise wild-type fission yeast cells, this report provides an atlas of dynamic protein behaviour of representative proteins at different stages during normal zygotic meiosis in fission yeast. This establishes common landmarks to facilitate comparison of different proteins and shows that initiation of S phase likely occurs prior to nuclear fusion/karyogamy.
... Based on our survey of the literature, the fungi in Classes 4-6 are capable of sexual reproduction (Wickerham et al., 1970;Sutton, 1982;Goto et al., 1987;Briza et al., 1990;Raju and Perkins, 1994;Gordon and Martyn, 1997;Keller et al., 1997;Britz et al., 1998;Harrington and Wingfield, 1998;Davis and Smith, 2001;Galagan et al., 2003;Dean et al., 2005;Rau et al., 2005;Rouxel and Balesdent, 2005;Paoletti et al., 2007;Rossi and Languasco, 2007;Tavanti et al., 2007;TeBeest et al., 2007;Bentley et al., 2008;Alby et al., 2009;Seidl et al., 2009;Mestre et al., 2010;Pereira et al., 2011;Rubini et al., 2011;Kurtzman and Robnett, 2012;Wada et al., 2012;Böhm et al., 2013;Studt et al., 2013;Short et al., 2014;Terhem and van Kan, 2014;Marin-Felix et al., 2015;Meng et al., 2015;Belfiori et al., 2016;Cowger et al., 2016;Doughan and Rollins, 2016;Gazis et al., 2016;Lee et al., 2016;Pelin et al., 2016;Son et al., 2016;Evans and Kirk, 2017;Manan, 2017;Randlane et al., 2017;Vaghefi et al., 2017;Vanheule et al., 2017;Yin et al., 2017;Yu et al., 2017;Carreté et al., 2018;Chi et al., 2019;Suffert et al., 2019;Wang et al., 2019a,b;Wu et al., 2020). Apart from a few instances where sexual stages have not been reported (indicated with "U" in Figure 1), the only exception was the nematophagous fungus Dr. coniospora that apparently lack a sexual cycle completely (Zhang et al., 2016). ...
The Repeat-Induced Point (RIP) mutation pathway is a fungus-specific genome defense mechanism that mitigates the deleterious consequences of repeated genomic regions and transposable elements (TEs). RIP mutates targeted sequences by introducing cytosine to thymine transitions. We investigated the genome-wide occurrence and extent of RIP with a sliding-window approach. Using genome-wide RIP data and two sets of control groups, the association between RIP, TEs, and GC content were contrasted in organisms capable and incapable of RIP. Based on these data, we then set out to determine the extent and occurrence of RIP in 58 representatives of the Ascomycota. The findings were summarized by placing each of the fungi investigated in one of six categories based on the extent of genome-wide RIP. In silico RIP analyses, using a sliding-window approach with stringent RIP parameters, implemented simultaneously within the same genetic context, on high quality genome assemblies, yielded superior results in determining the genome-wide RIP among the Ascomycota. Most Ascomycota had RIP and these mutations were particularly widespread among classes of the Pezizomycotina, including the early diverging Orbiliomycetes and the Pezizomycetes. The most extreme cases of RIP were limited to representatives of the Dothideomycetes and Sordariomycetes. By contrast, the genomes of the Taphrinomycotina and Saccharomycotina contained no detectable evidence of RIP. Also, recent losses in RIP combined with controlled TE proliferation in the Pezizomycotina subphyla may promote substantial genome enlargement as well as the formation of sub-genomic compartments. These findings have broadened our understanding of the taxonomic range and extent of RIP in Ascomycota and how this pathway affects the genomes of fungi harboring it.
... At a broad scale, recombination rates across the threespine stickleback genome were conserved between the two populations. This broad-scale conservation of recombination rates is a feature observed in many taxa (Kong et al. 2002;Serre et al. 2005;Fledel-Alon et al. 2009;Stevison et al. 2016) and may reflect the necessity of crossing over for the proper segregation of chromosomes during meiosis (Mather 1936;Kaback et al. 1992;Davis and Smith 2001). Additionally, we observed differential rates of recombination associated with broad genomic regions that have been observed in other systems. ...
Meiotic recombination is a highly conserved process that has profound effects on genome evolution. At a fine-scale, recombination rates can vary drastically across genomes, often localized into small recombination “hotspots” with highly elevated rates, surrounded by regions with little recombination. In most species studied, the location of hotspots within genomes is highly conserved across broad evolutionary timescales. The main exception to this pattern is in mammals, where hotspot location can evolve rapidly among closely related species and even among populations within a species. Hotspot position in mammals is controlled by the gene, Prdm9, whereas in species with conserved hotspots, a functional Prdm9 is typically absent. Due to a limited number of species where recombination rates have been estimated at a fine-scale, it remains unclear whether hotspot conservation is always associated with the absence of a functional Prdm9. Threespine stickleback fish (Gasterosteus aculeatus) are an excellent model to examine the evolution of recombination over short evolutionary timescales. Using an LD-based approach, we found recombination rates indeed varied at a fine-scale across the genome, with many regions organized into narrow hotspots. Hotspots had highly divergent landscapes between stickleback populations, where only ∼15% of these hotspots were shared. Our results indicate fine-scale recombination rates may be diverging between closely related populations of threespine stickleback fish. Interestingly, we found only a weak association of a PRDM9 binding motif within hotspots, which suggests threespine stickleback fish may possess a novel mechanism for targeting recombination hotspots at a fine-scale.
... Other authors have proposed that planozygotes in species such as Polykrikos kofoidii divide by meiosis and mitosis 58 . A biphasic cycle has also been described in the yeast Schizosaccharomyces pombe, the zygotes of which undergo meiosis or mitosis depending on nutritional factors 59 . Although in this study we did not further investigate planozygote division, new insights could be obtained in future studies by monitoring the AG-chromosome in crosses of different K. mikimotoi strains under conditions aimed at increasing planozygote formation. ...
Dinoflagellates are a group of protists whose genome is unique among eukaryotes in terms of base composition, chromosomal structure and gene expression. Even after decades of research, the structure and behavior of their amazing chromosomes—which without nucleosomes exist in a liquid crystalline state—are still poorly understood. We used flow cytometry and fluorescence in situ hybridization (FISH) to analyze the genome size of three species of the toxic dinoflagellate genus Karenia as well the organization and behavior of the chromosomes in different cell-cycle stages. FISH was also used to study the distribution patterns of ribosomal DNA (45S rDNA), telomeric and microsatellites repeats in order to develop chromosomal markers. The results revealed several novel and important features regarding dinoflagellate chromosomes during mitosis, including their telocentric behavior and radial arrangement along the nuclear envelope. Additionally, using the (AG)10 probe we identified an unusual chromosome in K. selliformis and especially in K. mikimotoi that is characterized by AG repeats along its entire length. This feature was employed to easily differentiate morphologically indistinguishable life-cycle stages. The evolutionary relationship between Karenia species is discussed with respect to differences in both DNA content and the chromosomal distribution patterns of the DNA sequences analyzed.
... Les DSB déclenchent ensuite la recombinaison entre les chromosomes paternel et maternel afin de promouvoir l'échange d'informations génétiques. La recombinaison méiotique est 16 essentielle à la génération de la diversité génétique et à l'évolution moléculaire, elle contribue également à assurer un alignement correct des paires de chromosomes homologues sur le fuseau (Baudat et al., 2013;Davis et Smith, 2001). ...
... DSBs then trigger the recombination between the paternal and maternal chromosomes to promote the exchange of genetic information. Meiotic recombination is key to the generation of genetic diversity and molecular evolution, it also contributes to ensuring proper alignment of homologous chromosome pairs on the spindle (Baudat et al., 2013;Davis and Smith, 2001 Adapted from online source (https://en.wikipedia.org/wiki/Hfr_cell). ...
DNA is constantly exposed to both endogenous and exogenous genotoxic insults. Multiple DNA repair mechanisms are exploited to guard the genome and epigenome stability. Homologous recombination (HR) plays a major role in repairing DNA double strand breaks (DSBs) and restarting stalled replication forks under replicative stress. These two processes are both coupled to chromatin assembly. Chromatin assembly factor 1 (CAF-1) is a highly conserved histone chaperone known to function in a network of nucleosome assembly coupled to DNA repair and replication, by depositing newly synthesized histone (H3-H4)2 tetramers onto the DNA. The fission yeast CAF-1 complex consists of three subunits Pcf1, Pcf2 and Pcf3. CAF-1 has been previously reported to act at the DNA synthesis step during the process of recombination-dependent replication (RDR) and protects the D-loop from disassembly by the RecQ helicase family member, Rqh1. In this study, we addressed the role of CAF-1 during homologous-recombination-mediated DNA repair in fission yeast.Using in vivo and in vitro approaches, we validated interactions within a complex containing Rqh1, CAF-1, PCNA, and Histone H3. We showed that Rqh1 interacts with both Pcf1 and Pcf2 independently of each other, and the Pcf1-Rqh1 interaction is stimulated by DNA damage. We developed an in vivo chromatin binding assay to monitor the association of CAF-1 to the chromatin upon DNA damage. We observed that replication stress but not double strand break favors CAF-1 association to the chromatin. We identified that several HR factors are required for CAF-1 association to the chromatin upon replication stress. In support of this, we have identified physical interactions between Pcf1 and HR factors, including RPA and Rad51. Our data suggest that CAF-1 would associate with the site of recombination-dependent DNA synthesis through physical interactions with HR factors. Put together, this work contributes to strengthening the role of CAF-1 coupled to DNA repair, and reveals the crosstalk between HR factors and chromatin assembly.
... Class II COs do not exhibit interference (1). Mammals, budding yeast (Saccharomyces cerevisiae), and plants all have both types of COs (2), but some organisms have only one or the other (3,4). According to the double-strand break (DSB) repair model in S. cerevisiae (5), the formation of class I COs is dependent on a set of meiosisspecific proteins, collectively referred to as ZMM proteins (ZIP1, ZIP2, ZIP3, ZIP4, MER3, MSH4, and MSH5). ...
Significance
Crossovers (COs) ensure the accurate segregation of homologous chromosomes during meiosis. Failure to create the right number of crossovers may lead to unequal distribution of genetic materials to daughter cells and sterility. CO proteins, which specially localize to crossover sites during meiosis, play critical roles in CO formation. Here, we identify a CO protein in rice, named HEI10 Interaction Protein 1 (HEIP1), which is conserved in higher plants. Our results reveal its possible molecular mechanism for CO control in meiosis.
... Meiotic recombination is a highly-conserved process across a broad range of taxa (de 64 Massy 2013;Petes 2001). Recombination creates new allelic combinations by breaking apart haplotypes (Coop and Przeworski 2007;Otto and Lenormand 2002), promotes the proper 66 segregation of chromosomes during meiosis in many species (Davis and Smith 2001;Fledel-67 Alon et al. 2009;Kaback et al. 1992;Mather 1936), and has a pronounced impact on the 68 evolution of genomes (Mugal et al. 2015;Webster and Hurst 2012). In many species, meiotic 69 recombination occurs in small 1-2 kb regions called recombination "hotspots" which are 70 surrounded by large genomic regions with little to no recombination (Barton et al. 2008;Baudat 71 et al. 2010;Hellsten et al. 2013;Jeffreys et al. 1998;McVean et al. 2004;Myers et al. 2005;72 Steiner et al. 2002). ...
... http://dx.doi.org/10.1101/430249 doi: bioRxiv preprint first posted online Sep. 29, 2018; a feature observed in many taxa (Fledel-Alon et al. 2009;Kong et al. 2002;Serre et al. 2005;590 Stevison et al. 2015) and may reflect the necessity of crossing over for the proper segregation of 591 chromosomes during meiosis (Davis and Smith 2001;Fledel-Alon et al. 2009;Kaback et al. 592 1992;Mather 1936). Additionally, we observed differential rates of recombination associated 593 with broad genomic regions that have been observed in other systems. ...
Meiotic recombination is a highly conserved process that has profound effects on genome evolution. Recombination rates can vary drastically at a fine-scale across genomes and often localize to small recombination 'hotspots' with highly elevated rates surrounded by regions with little recombination. Hotspot targeting to specific genomic locations is variable across species. In some mammals, hotspots have divergent landscapes between closely related species which is directed by the binding of the rapidly evolving protein, PRDM9. In many species outside of mammals, hotspots are generally conserved and tend to localize to regions with open chromatin such as transcription start sites. It remains unclear if the location of recombination hotspots diverge in taxa outside of mammals. Threespine stickleback fish (Gasterosteus aculeatus) are an excellent model to examine the evolution of recombination over short evolutionary timescales. Using an LD-based approach, we found recombination rates varied at a fine-scale across the genome, with many regions organized into narrow hotspots. Hotspots had divergent landscapes between stickleback populations, where only ~15% were shared, though part of this divergence could be due to demographic history. Additionally, we did not detect a strong association of PRDM9 with recombination hotspots in threespine stickleback fish. Our results suggest fine-scale recombination rates may be diverging between closely related populations of threespine stickleback fish and argue for additional molecular characterization to verify the extent of the divergence.
... In ( ), both meiotic recombination and DNA breakage are regulated by rec6, rec7, rec12, rec14, and rec15 proteins; thus, breakage and recombination are biologically linked [8,9]. The fission yeast rec12 protein catalyzes double-strand DNA (dsDNA) breaks that initiate recombination [10,11]. ...
Homologous recombination plays an important role in maintaining the genome stability of prokaryotic and eukaryotic organisms. In this study, gene expression and alterations in homologous recombination frequency were investigated under H2O2 and CuSO4 induced oxidative stress in the unicellular, eukaryotic model organism. In order to increase the recombination frequency, mutant strains that possess distant located genes on the same chromosome were chosen and crossbred. The zygotes were treated with oxidative stress-inducing CuSO4 and H2O2. After the stress treatments, alterations in homologous recombination were investigated by using random spore analysis. Moreover, gene expression was analyzed with real-time PCR. We observed that the H2O2 and CuSO4 stress treatments decrease both gene expression and homologous recombination frequency in the fission yeast. Fission yeast, homologous recombination, H2O2 stress, CuSO4 stress, oxidative stress, chemical stress Gene expression regulation is one of the crucial mechanisms by which organisms respond to alterations in pH, osmolarity, temperature, and harmful toxins in their environment. This regulation leads to an increase in the stress protein levels and a decrease in non-essential cellular activities. The reduction in the non-essential cellular activity permits cellular resources to be conserved for adapting to the stress conditions, as well as repairing the damaged macro-molecules [1]. Transition metals are important in facilitating many biological processes due to their ability to donate and accept electrons, iron, copper, and manganese. For example, transitions metals that are pros-thetic groups of proteins can catalyze redox reactions. Nevertheless, excessive amounts of these metal ions can be toxic to cells [2]. A transitive metal, copper (Cu 2+), which serves as a cofactor to several enzymes, has been reported to cause extensive damage in microorganisms in high concentrations. Copper (Cu 2+) can react with superoxide anion (O2 −) and hydrogen peroxide (H2O2); this reaction results in hydroxyl free radical (OH-) release. Hydroxyl free radical (OH-) is one of the reactive oxygen species (ROS), and can cause damage to various cellular macromolecules either directly-by oxidizing carbohydrates, amino acids, phospholipids, and nucleic acids-or indirectly [3, 4]. Reactive oxygen species (O2 −, OH-, H2O2) are produced during the aerobic growth mostly as a consequence of electron transfer in the mitochondrial membrane. A set of cellular defense mechanisms scavenge O2 − and H2O2, so that a balance between production and detoxification is accomplished, and a non-toxic, steady-state is reached [5]. Homologous recombination is necessary for the recovery of the cells from oxidative stress [6]. Homologous recombination refers to the interaction of DNA sequences with homology and plays an essential role in the maintenance of genome stability in prokaryotic and eukaryotic organisms by (1) repairing double-strand breaks (DSBs), (2) repairing single-strand gaps that are caused by replication fork collapse or DNA-damaging agents. Homologous recombination is also vital in meiosis for establishing a physical connection between homologous chromosomes [7]. In (), both meiotic recombination and DNA breakage are regulated by rec6, rec7, rec12, rec14, and rec15 proteins; thus, breakage and recombination are biologically linked [8, 9]. The fission yeast rec12 protein catalyzes double-strand DNA (dsDNA) breaks that initiate recombination [10, 11]. Rec12 protein and its active site tyrosine are important for crossover recombination. In meiosis, catalytically-active rec12 is required for normal chiasmatic segregation, while catalytically-inactive rec12 protein facilitates chiasmatic segregation. Moreover, rec12 and its active
