Spo11-Accessory Proteins Link Double-Strand Break Sites to the Chromosome Axis in Early Meiotic Recombination

Panizza, Silvia; Mendoza, Marco Antonio; Berlinger, Marc; Huang, Lingzhi; Nicolas, Alain; Shirahige, Katsuhiko; Klein, Franz

doi:10.1016/j.cell.2011.07.003

Cited by 353 publications

(658 citation statements)

References 70 publications

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“…The marked MutLg-dependence and -independence of VDE-initiated COs in inserts at HIS4 and at URA3, respectively, are paralleled by the levels of occupancy of the meiotic axis proteins Hop1 and Red1 (Panizza et al, 2011; Figure 4A, Figure 4-figure supplement 1A). To test further the suggestion that differential Hop1 occupancy is correlated with differences in CO formation at these loci, we examined the resolvase-dependence of VDE-initiated COs in pch2D mutants.…”

Section: Altered Hop1 Occupancy In Pch2 Mutants Is Associated With Almentioning

confidence: 83%

“…Restriction site polymorphisms at flanking HindIII sites, combined with the heterozygous VRS site, allow differentiation of parental and recombinant DNA molecules. This recombination reporter was inserted at two loci: HIS4 and URA3, which are 'hot' and 'cold', respectively, for Spo11-initiated recombination and Red1/Hop1 occupancy (Borde et al, 1999;Buhler et al, 2007;Panizza et al, 2011;Wu and Lichten, 1995; also see Figure 4A and Figure 4-figure supplement 1, below). Consistent with previous reports, Spo11-DSBs and the resulting crossovers, are about five times more frequent in inserts at HIS4 than at URA3 (Figure 1-figure supplement 1A).…”

Section: Resultsmentioning

confidence: 99%

“…Malkova and coworkers used the HO endonuclease to initiate recombination in meiotic cells at LEU2, also a 'hot' locus (Panizza et al, 2011;Wu and Lichten, 1995). The resulting COs were dependent on Msh4, a ZMM protein, to the same degree as are Spo11-induced COs, suggesting that these nuclease-induced COs at the axis enriched LEU2 locus were the products of ZMM/MutLg-dependent JM resolution (Malkova et al, 2000).…”

Section: Discussion Local Chromosome Context Influences Meiotic Co Fomentioning

confidence: 99%

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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: Altered Hop1 Occupancy In Pch2 Mutants Is Associated With Almentioning

confidence: 83%

Section: Resultsmentioning

confidence: 99%

Section: Discussion Local Chromosome Context Influences Meiotic Co Fomentioning

confidence: 99%

See 1 more Smart Citation

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

Medhi¹,

Goldman

Lichten³

2016

Preprint

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“…1A) (8,11). Throughout the process, recombination complexes are associated with chromosome structural axes and/or the SC, as in a variety of organisms (2,14,15).…”

Section: Resultsmentioning

confidence: 99%

Interference-mediated synaptonemal complex formation with embedded crossover designation

Zhang

Espagne

Muyt

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Biological systems exhibit complex patterns at length scales ranging from the molecular to the organismic. Along chromosomes, events often occur stochastically at different positions in different nuclei but nonetheless tend to be relatively evenly spaced. Examples include replication origin firings, formation of chromatin loops along chromosome axes and, during meiosis, localization of crossover recombination sites ("crossover interference"). We present evidence in the fungus Sordaria macrospora that crossover interference is part of a broader pattern that includes synaptonemal complex (SC) nucleation. This pattern comprises relatively evenly spaced SC nucleation sites, among which a subset are crossover sites that show a classical interference distribution. This pattern ensures that SC forms regularly along the entire length of the chromosome as required for the maintenance of homolog pairing while concomitantly having crossover interactions locally embedded within the SC structure as required for both DNA recombination and structural events of chiasma formation. This pattern can be explained by a threshold-based designation and spreading interference process. This model can be generalized to give diverse types of related and/or partially overlapping patterns, in two or more dimensions, for any type of object.spatial patterning | synapsis initiation site | recombination/synapsis | crossover designation M eiosis is the specialized cellular cycle that yields haploid gametes for sexual reproduction. A central feature of the meiotic program is recombination (1, 2). DNA/DNA recombination interactions, initiated by programmed double-strand breaks (DSBs), mediate the recognition and juxtaposition (pairing) of homologous chromosomes. A minority subset of these interactions matures into reciprocal crossover recombination products (COs); the remaining majority matures primarily into interhomolog non-crossover products (NCOs). COs promote genetic diversity but also are required for the segregation of homologous chromosomes (homologs) via their role in creating chiasmata (3).A nearly universal feature of meiosis is that COs occur along a particular chromosome at different positions in different meiotic nuclei. Nonetheless, along any given chromosome, COs tend to be evenly spaced. This pattern results from the reduced possibility that a second cross-over will occur if a crossover has occurred nearby. The existence of such a pattern was identified more than a century ago as the genetic phenomenon of CO interference (4, 5). In this phenomenon, occurrence of a CO in one genetic interval is accompanied by a reduced probability that another CO will occur along the same chromosome in a nearby interval. This effect implies the existence of communication along chromosomes, with an event at one position triggering occurrence of an "interference signal" that spreads outward, inhibiting occurrence of subsequent events nearby.A second central feature of the meiotic program is the synaptonemal complex (SC). This prominent structure link...

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“…At the time of initiation, Spo11-mediated DSBs occur in intimate association with this complex (Panizza et al, 2011). At stages of CO/NCO differentiation, CO recombination interactions exhibit preferential association with domains in which Mek1 is hyperabundant (Joshi et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Shu1 Promotes Homolog Bias of Meiotic Recombination in Saccharomyces cerevisiae

Hong

Kim

2013

Molecules and Cells

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Homologous recombination occurs closely between homologous chromatids with highly ordered recombinosomes through RecA homologs and mediators. The present study demonstrates this relationship during the period of "partner choice" in yeast meiotic recombination. We have examined the formation of recombination intermediates in the absence or presence of Shu1, a member of the PCSS complex, which also includes Psy3, Csm2, and Shu2. DNA physical analysis indicates that Shu1 is essential for promoting the establishment of homolog bias during meiotic homologous recombination, and the partner choice is switched by Mek1 kinase activity. Furthermore, Shu1 promotes both crossover (CO) and non-crossover (NCO) pathways of meiotic recombination. The inactivation of Mek1 kinase allows for meiotic recombination to progress efficiently, but is lost in homolog bias where most doublestrand breaks (DSBs) are repaired via stable intersister joint molecules. Moreover, the Srs2 helicase deletion cells in the budding yeast show slightly reduced COs and NCOs, and Shu1 promotes homolog bias independent of Srs2. Our findings reveal that Shu1 and Mek1 kinase activity have biochemically distinct roles in partner choice, which in turn enhances the understanding of the mechanism associated with the precondition for homolog bias.

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Spo11-Accessory Proteins Link Double-Strand Break Sites to the Chromosome Axis in Early Meiotic Recombination

Cited by 353 publications

References 70 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

Interference-mediated synaptonemal complex formation with embedded crossover designation

Shu1 Promotes Homolog Bias of Meiotic Recombination in Saccharomyces cerevisiae

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