The kinetochore prevents centromere-proximal crossover recombination during meiosis

Vincenten, Nadine; Kuhl, Lisa Marie; Lam, Isabel; Oke, Ashwini; Kerr, Alastair; Hochwagen, Andreas; Fung, Jennifer C.; Keeney, Scott; Vader, Gerben; Marston, Adèle L.

doi:10.7554/elife.10850

Cited by 114 publications

(171 citation statements)

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“…Serrentino et al (2013) showed that enrichment for the budding yeast ZMM protein, Zip3, at DSB sites is correlated with interhomolog CO levels. Specialized chromosome elements also impact meiotic recombination in budding yeast: COs are differentially reduced relative to NCOs near telomeres (Chen et al, 2008); and interhomolog recombination is inhibited near centromeres (Chen et al, 2008;Roeder, 1988, 1986;Vincenten et al, 2015). Locus-specific differences in CO/NCO ratios also have been observed in mouse meiosis (de Boer et al, 2015), locus-specific differences in partner choice have been reported in S. pombe (Hyppa and Smith, 2010), and crossover suppression by centromeres is observed in many species (Talbert and Henikoff, 2010).…”

Section: Discussion Local Chromosome Context Influences Meiotic Co Fomentioning

confidence: 99%

Local chromosome context is a major determinant of crossover pathway biochemistry during budding yeast meiosis

Medhi¹,

Goldman

Lichten³

2016

Preprint

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The budding yeast genome contains regions where meiotic recombination initiates more frequently than in others. This pattern parallels enrichment for the meiotic chromosome axis proteins Hop1 and Red1. These proteins are important for Spo11-catalyzed double strand break formation; their contribution to crossover recombination remains undefined. Using the sequencespecific VMA1-derived endonuclease (VDE) to initiate recombination in meiosis, we show that chromosome structure influences the choice of proteins that resolve recombination intermediates to form crossovers. At a Hop1-enriched locus, most VDE-initiated crossovers, like most Spo11-initiated crossovers, required the meiosis-specific MutLg resolvase. In contrast, at a locus with lower Hop1 occupancy, most VDE-initiated crossovers were MutLg-independent. In pch2 mutants, the two loci displayed similar Hop1 occupancy levels, and VDE-induced crossovers were similarly MutLg-dependent. We suggest that meiotic and mitotic recombination pathways coexist within meiotic cells, and that features of meiotic chromosome structure determine whether one or the other predominates in different regions.

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Section: Discussion Local Chromosome Context Influences Meiotic Co Fomentioning

confidence: 99%

Local chromosome context is a major determinant of crossover pathway biochemistry during budding yeast meiosis

Medhi¹,

Goldman

Lichten³

2016

Preprint

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“…The inappropriate occurrence of crossovers in the proximity of the primary constriction of monocentric chromosomes affects negatively the meiotic chromosome segregation by influencing the centromeric cohesion (Talbert and Henikoff 2010;Vincenten et al 2015). Accordingly, the occurrence of very few crossovers is reported for holocentric organisms, generally one or two per rod and ring bivalent, respectively, mostly located at the noncentromeric terminal regions (Cuacos et al 2015).…”

Section: Discussionmentioning

confidence: 99%

“…The Cf19 complex of yeast [also known as the constitutive centromere-associated network (CCAN) in other organisms] prevents meiotic double-strand breaks (DSBs) proximal to the centromeres, which are essential to initiate recombination (Vincenten et al 2015). Nevertheless, although meiotic DSBs are suppressed at core centromeric regions in yeast, they frequently occur only a few kilobases away from the centromeres (Buhler et al 2007;Pan et al 2011).…”

Section: Discussionmentioning

confidence: 99%

Restructuring of Holocentric Centromeres During Meiosis in the Plant Rhynchospora pubera

et al. 2016

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Centromeres are responsible for the correct segregation of chromosomes during mitosis and meiosis. Holocentric chromosomes, characterized by multiple centromere units along each chromatid, have particular adaptations to ensure regular disjunction during meiosis. Here we show by detecting CENH3, CENP-C, tubulin, and centromeric repeats that holocentromeres may be organized differently in mitosis and meiosis of Rhynchospora pubera. Contrasting to the mitotic linear holocentromere organization, meiotic centromeres show several clusters of centromere units (cluster-holocentromeres) during meiosis I. They accumulate along the poleward surface of bivalents where spindle fibers perpendicularly attach. During meiosis II, the cluster-holocentromeres are mostly present in the midregion of each chromatid. A linear holocentromere organization is restored after meiosis during pollen mitosis. Thus, a not yet described case of a cluster-holocentromere organization, showing a clear centromere restructuration between mitosis and meiosis, was identified in a holocentric organism.KEYWORDS holocentric chromosomes; CENH3; CENP-C; centromere structure/organization; inverted meiosis T HE centromere is the chromosome site responsible for spindle fiber attachment and faithful chromosome segregation during mitosis and meiosis. In general, every eukaryotic chromosome has a centromere on which the kinetochore complex assembles (Cleveland et al. 2003;Burrack and Berman 2012). In most eukaryotes, centromeric nucleosomes contain CENH3 (also known as CENP-A, a histone H3 variant that replaces canonical H3 at the centromere), and usually spans several hundred kilobase pairs often in association with centromere-specific repeats (Steiner and Henikoff 2015).Centromere organization and dynamics vary between mitosis and meiosis (Duro and Marston 2015;Ohkura 2015). During mitosis, sister chromatids are held together by centromere cohesion until metaphase. Simultaneous with the disruption of cohesion, sister chromatids are pulled to opposite poles during anaphase. In contrast, during meiosis, sister centromere cohesion is ensured until metaphase II (Ishiguro and Watanabe 2007). The stepwise regulation of cohesion release during meiosis I (MI) and II (MII) is well studied in organisms with one primary constriction per chromosome (monocentric), ensuring the segregation of homologs at MI followed by the segregation of sister chromatids at MII (Duro and Marston 2015).Contrary to monocentrics, the centromeres of holocentric chromosomes are distributed almost over the entire chromosome length and cohesion occurs along the entire associated sister chromatids (Maddox et al. 2004). Although this does not imply much difference during mitotic divisions, the presence of a holokinetic centromere (holocentromere) imposes obstacles to the dynamics of chromosome segregation in meiosis. Due to their alternative chromosome organization, species with holocentric chromosomes cannot perform the two-step cohesion loss during meiosis typical for monocentric species...

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“…Also, assuming that crossing over usually takes place in or near genes, differences in DNA sequence may contribute, including a high concentration of tandem repeats and/or a lack of genes in heterochromatin. Recently, Vincenten et al (2015) provided strong support for two of these hypotheses by showing that, in Saccharomyces cerevisiae, a kinetochore (centromere) protein complex called Ctf19 both inhibits nearby double-strand breaks needed for crossing over and promotes cohesion enrichment that also interferes with meiotic crossing over.…”

mentioning

confidence: 99%

“…First, crossover suppression need not be mediated by heterochromatin. For example, centromeres without heterochromatin can suppress nearby crossing over (the "centromere effect"), as can NORs (Beadle 1932;Mather 1939;Petes and Botstein 1977;Yamamoto and Miklos 1978;Lambie and Roeder 1986;Resnick 1987;Kota et al 1993;Choo 1998;Blitzblau et al 2007;Lichten 2008;Vincenten et al 2015). Furthermore, most of the maize genome is comprised of retrotransposons where little if any crossing over occurs, even though many of the retrotransposons are present in distal euchromatin (Fu et al 2002;Yao et al 2002).…”

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confidence: 99%

Meiotic Crossing Over in Maize Knob Heterochromatin

et al. 2017

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There is ample evidence that crossing over is suppressed in heterochromatin associated with centromeres and nucleolus organizers (NORs). This characteristic has been attributed to all heterochromatin, but the generalization may not be justified. To investigate the relationship of crossing over to heterochromatin that is not associated with centromeres or NORs, we used a combination of fluorescence in situ hybridization of the maize 180-bp knob repeat to show the locations of knob heterochromatin and fluorescent immunolocalization of MLH1 protein and AFD1 protein to show the locations of MLH1 foci on maize synaptonemal complexes (SCs, pachytene chromosomes). MLH1 foci correspond to the location of recombination nodules (RNs) that mark sites of crossing over. We found that MLH1 foci occur at similar frequencies per unit length of SC in interstitial knobs and in the 1 mm segments of SC in euchromatin immediately to either side of interstitial knobs. These results indicate not only that crossing over occurs within knob heterochromatin, but also that crossing over is not suppressed in the context of SC length in maize knobs. However, because there is more DNA per unit length of SC in knobs compared to euchromatin, crossing over is suppressed (but not eliminated) in knobs in the context of DNA length compared to adjacent euchromatin.

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The kinetochore prevents centromere-proximal crossover recombination during meiosis

Cited by 114 publications

References 77 publications

Local chromosome context is a major determinant of crossover pathway biochemistry during budding yeast meiosis

Local chromosome context is a major determinant of crossover pathway biochemistry during budding yeast meiosis

Restructuring of Holocentric Centromeres During Meiosis in the Plant Rhynchospora pubera

Meiotic Crossing Over in Maize Knob Heterochromatin

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