A Pathway for Synapsis Initiation during Zygotene in Drosophila Oocytes

Tanneti, Nikhila S.; Landy, Kathryn; Joyce, Eric F.; McKim, Kim S.

doi:10.1016/j.cub.2011.10.005

Cited by 92 publications

(156 citation statements)

References 25 publications

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“…However, as zygotene proceeds, numerous medial sites of SC initiation are observed also. This process may have parallels to the initiation of SC formation in Drosophila melanogaster females, in which SC formation is observed first at clustered centromeres (9) and appears to spread out from that cluster supplemented by a number of sites of interstitial SC formation (10). Another example of a role of subtelomeric sequences is in homolog pairing, as described by del Carmen Calderon et al (64).…”

Section: Discussionmentioning

confidence: 90%

“…Although the formation of the SC at clustered centromeres and at a small number of interstitial sites is concurrent with the establishment of chromosome pairing (9,10), the absence of the SC prevents meiotic pairing both at the centromeres and along the arms of homologous chromosomes (11)(12)(13). Moreover, SC formation is required for normal levels of DSB formation (14,15) as well as for the maturation of recombination intermediates into crossovers.…”

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confidence: 99%

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Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea

Xiang

Miller

Ross

et al. 2014

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

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In the 1920s, József Gelei proposed that chromosome pairing in flatworms resulted from the formation of a telomere bouquet followed by the extension of synapsis from telomeres at the base of the bouquet, thus facilitating homolog pairing in a processive manner. A modern interpretation of Gelei's model postulates that the synaptonemal complex (SC) is nucleated close to the telomeres and then extends progressively along the full length of chromosome arms. We used the easily visible meiotic chromosomes, a well-characterized genome, and RNAi in the sexual biotype of the planarian Schmidtea mediterranea to test that hypothesis. By identifying and characterizing S. mediterranea homologs of genes encoding synaptonemal complex protein 1 (SYCP1), the topoisomerase-like protein SPO11, and RAD51, a key player in homologous recombination, we confirmed that SC formation begins near the telomeres and progresses along chromosome arms during zygotene. Although distal regions pair at the time of bouquet formation, pairing of a unique interstitial locus is not observed until the formation of full-length SC at pachytene. Moreover, neither full extension of the SC nor homologous pairing is dependent on the formation of double-strand breaks. These findings validate Gelei's speculation that full-length pairing of homologous chromosomes is mediated by the extension of the SC formed near the telomeres. S. mediterranea thus becomes the first organism described (to our knowledge) that forms a canonical telomere bouquet but does not require double-strand breaks for synapsis between homologous chromosomes. However, the initiation of SC formation at the base of the telomere bouquet, which then is followed by full-length homologous pairing in planarian spermatocytes, is not observed in other species and may not be conserved.

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Section: Discussionmentioning

confidence: 90%

mentioning

confidence: 99%

Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea

Xiang

Miller

Ross

et al. 2014

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

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“…In these organisms, SC formation is independent of recombination and CO designation; moreover, both recombination initiation and interference is or can be implemented after SC formation (40)(41)(42)(43). In these cases, the interference process seems limited to patterning of COs, and not SC nucleation, suggesting that an important functional rationale for interference may relate to CO/chiasma formation (27).…”

Section: Complex Spatial Patterns Can Arise In a Single Interference-mentioning

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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“…SMC1 localizes to centromeres during meiosis in both sexes and persists on centromeres until anaphase II in male meiosis (Khetani and Bickel 2007;Yan et al 2010). Both SMC1 and SMC3 localize to LEs in female prophase I and loss of either protein completely ablates formation of LEs and SCs (Khetani and Bickel 2007;Tanneti et al 2011;Yan and McKee 2013). However, as yet there is only indirect evidence for roles of SMC1 and SMC3 in arm or centromere cohesion.…”

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confidence: 99%

Sisters Unbound Is Required for Meiotic Centromeric Cohesion in Drosophila melanogaster

et al. 2014

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Regular meiotic chromosome segregation requires sister centromeres to mono-orient (orient to the same pole) during the first meiotic division (meiosis I) when homologous chromosomes segregate, and to bi-orient (orient to opposite poles) during the second meiotic division (meiosis II) when sister chromatids segregate. Both orientation patterns require cohesion between sister centromeres, which is established during meiotic DNA replication and persists until anaphase of meiosis II. Meiotic cohesion is mediated by a conserved four-protein complex called cohesin that includes two structural maintenance of chromosomes (SMC) subunits (SMC1 and SMC3) and two non-SMC subunits. In Drosophila melanogaster, however, the meiotic cohesion apparatus has not been fully characterized and the non-SMC subunits have not been identified. We have identified a novel Drosophila gene called sisters unbound (sunn), which is required for stable sister chromatid cohesion throughout meiosis. sunn mutations disrupt centromere cohesion during prophase I and cause high frequencies of non-disjunction (NDJ) at both meiotic divisions in both sexes. SUNN co-localizes at centromeres with the cohesion proteins SMC1 and SOLO in both sexes and is necessary for the recruitment of both proteins to centromeres. Although SUNN lacks sequence homology to cohesins, bioinformatic analysis indicates that SUNN may be a structural homolog of the non-SMC cohesin subunit stromalin (SA), suggesting that SUNN may serve as a meiosis-specific cohesin subunit. In conclusion, our data show that SUNN is an essential meiosis-specific Drosophila cohesion protein. MEIOSIS is a specialized cell division that generates haploid gametes from diploid precursor cells and is essential for sexual reproduction. Segregation of chromosomes during meiosis occurs in two stages called meiosis I and meiosis II that follow a single round of DNA replication. During meiosis I, homologs pair and orient toward opposite poles of the spindle (bi-orient) with sister centromeres oriented toward the same pole (mono-oriented). As a result, homologous chromosomes segregate to opposite poles at the onset of anaphase I in a reductional segregation pattern. In meiosis II, as in mitosis, the sister centromeres are bi-oriented and sister chromatids segregate to opposite poles at the onset of anaphase II, a pattern referred to as equational segregation (Page and Hawley 2003;Petronczki et al. 2003).In most eukaryotes, pairing of homologs during meiosis I is facilitated and reinforced by synapsis and recombination. Synapsis involves formation of elaborate zipper-like structures, called synaptonemal complexes (SCs), which hold homologs tightly together during prophase I. SCs are composed of the tightly paired sister chromatid axes of the two homologs, known as axial elements (AEs) before synapsis or as lateral elements (LEs) after synapsis, crosslinked by multiple transverse filament (TF) proteins. Synapsis initiates at a limited number of discrete sites of homolog alignment during zygotene and subs...

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A Pathway for Synapsis Initiation during Zygotene in Drosophila Oocytes

Cited by 92 publications

References 25 publications

Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea

Synaptonemal complex extension from clustered telomeres mediates full-length chromosome pairing in Schmidtea mediterranea

Interference-mediated synaptonemal complex formation with embedded crossover designation

Sisters Unbound Is Required for Meiotic Centromeric Cohesion in Drosophila melanogaster

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