Mechanics of meiosis

Rasmussen, Søren W.; Holm, Preben Bach

doi:10.1111/j.1601-5223.1980.tb01360.x

Cited by 144 publications

(19 citation statements)

References 73 publications

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“…In addition to other functions, the SC then facilitates the maturation of a fraction of recombination intermediates into mature crossovers, called chiasmata, that eventually ensure segregation of chromosomes in meiosis I (2). Budding yeast and mammalian meiosis also are characterized by the presence of telomeric bouquets during meiotic prophase, a phenomenon observed in many, if not most, other organisms (3,4). The telomere bouquet is a structure formed when telomeres cluster at a small area of the nuclear periphery (5).…”

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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 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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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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“…Interlocks could be resolved by coordinated breakage and rejoining of chromosomes (Holm et al 1982;Rasmussen 1986;Moens 1990) or by chromosome movement and SC disassembly during zygotene and pachytene (Conrad et al 2008;Koszul et al 2008). For chromosomes to escape an interlock by this latter mechanism, one or more telomeres of the interlocking chromosomes either have to separate from each other on the nuclear envelope or be released from the nuclear envelope so that one interlocking chromosome can be pulled away from the other (Rasmussen and Holm 1980). Meiotic chromosomes are large, complex structures that can be tens of microns in length, yet the size of many structural elements of interest such as recombination nodules (50-200 nm diameter) and the LEs of the SC (spaced 100-200 nm apart) is just beyond the resolution of conventional wide-field microscopy (von Wettstein et al 1984).…”

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Interlock Formation and Coiling of Meiotic Chromosome Axes During Synapsis

et al. 2009

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The meiotic prophase chromosome has a unique architecture. At the onset of leptotene, the replicated sister chromatids are organized along an axial element. During zygotene, as homologous chromosomes pair and synapse, a synaptonemal complex forms via the assembly of a transverse element between the two axial elements. However, due to the limitations of light and electron microscopy, little is known about chromatin organization with respect to the chromosome axes and about the spatial progression of synapsis in three dimensions. Three-dimensional structured illumination microscopy (3D-SIM) is a new method of superresolution optical microscopy that overcomes the 200-nm diffraction limit of conventional light microscopy and reaches a lateral resolution of at least 100 nm. Using 3D-SIM and antibodies against a cohesin protein (AFD1/REC8), we resolved clearly the two axes that form the lateral elements of the synaptonemal complex. The axes are coiled around each other as a left-handed helix, and AFD1 showed a bilaterally symmetrical pattern on the paired axes. Using the immunostaining of the axial element component (ASY1/HOP1) to find unsynapsed regions, entangled chromosomes can be easily detected. At the late zygotene/early pachytene transition, about one-third of the nuclei retained unsynapsed regions and 78% of these unsynapsed axes were associated with interlocks. By late pachytene, no interlocks remain, suggesting that interlock resolution may be an important and rate-limiting step to complete synapsis. Since interlocks are potentially deleterious if left unresolved, possible mechanisms for their resolution are discussed in this article.

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“…By late diplotene/early diakinesis, the SCs are fully degraded and the homologues (in this case, A chromosomes) held together by chiasmata alone [Rasmussen and Holm, 1980] are correctly oriented and subsequently segregated. Theoretically, Q chromosomes which did not form chiasmata to hold them together might, therefore, disperse and be lost.…”

Section: Discussionmentioning

confidence: 99%

“…1 f, g) most likely related to the coupling of regions with common repetitive DNA sequences, as seen in plants [Zickler and Kleckner, 1999;Page and Hawley, 2004]. A 2-phase-synapsis formation has been widely described both in allopolyploid plants and animals, including several species with different chromosome abnormalities [McClintock, 1933;Rasmussen and Holm, 1980;Gillies, 1989;Cuñado et al, 2002]. The second phase seems to require the highest formation of synapses possible; in order to overcome the pachytene checkpoint [Roeder and Bailis, 2000], a surveillance control ensuring the correct events take place in the meiotic cell, arresting or delaying the cycle in response to defects in cellular processes [Hartwell and Weinert, 1989].…”

Section: Discussionmentioning

confidence: 99%

Synaptonemal Complexes in the Hybridogenetic <b><i>Squalius alburnoides</i></b> Fish Complex: New Insights on the Gametogenesis of Allopolyploids

Nabais

Pereira²,

Cuñado³

et al. 2012

Cytogenet Genome Res

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In the Squalius alburnoides fish complex, allotriploid females (3n = 75) reproduce mostly by meiotic hybridogenesis, producing haploid gametes by means of the elimination of the heterospecific chromosome set and recombination between the 2 homospecific genomes. A synaptonemal complexes (SCs) analysis was performed in specimens from a confined southern population (Quarteira, Portugal) to understand chromosome dynamics during gametogenesis. The comparative study between hybrid females with QAA genome composition and the parental bisexual species Squalius aradensis (2n = 50, QQ genome) evidenced: (i) that allotriploid meiocytes comprise the complete chromosome set (75 chromosomes) in prophase I, proving the heterospecific genome (Q) is only excluded after pachytene stage, and (ii) a 2-phase synaptic process where initially, exclusively homologous SCs form and the unmatched univalents remain in a bouquet conformation, followed by the establishment of extensive non-homologous SCs with multivalent associations among the later. These findings disagree with most literature concerning the meiotic process in allotriploid vertebrates, since the most accountable mechanisms (premeiotic exclusion of the unmatched chromosome set and whole genome endoduplication) were not observed.

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Mechanics of meiosis

Cited by 144 publications

References 73 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

Interlock Formation and Coiling of Meiotic Chromosome Axes During Synapsis

Synaptonemal Complexes in the Hybridogenetic <b><i>Squalius alburnoides</i></b> Fish Complex: New Insights on the Gametogenesis of Allopolyploids

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