A ZIP1 separation-of-function allele reveals that centromere pairing drives meiotic segregation of achiasmate chromosomes in budding yeast

Kurdzo, Emily L; Chuong, Hoa; Evatt, Jared M; Dawson, Dean

doi:10.1371/journal.pgen.1007513

Cited by 9 publications

(3 citation statements)

References 39 publications

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“…Accordingly, the SC is required to ensure proper segregation at the first meiotic division, and alterations or removal of this structure can lead to meiotic failures and aneuploidy ( Hassold et al . 2007 ; Geisinger and Benavente 2016 ; Gao and Colaiácovo 2018 ; Hughes et al 2018 ; Kurdzo et al 2018 ). The SC is a unique structure in that the overall order or pattern is highly conserved between organisms, forming an ∼100 nm evolutionarily conserved tripartite structure that can be seen at high resolution ( Moses 1968 ; Zickler and Kleckner 1999 ; Cahoon et al 2017 ).…”

Section: Resultsmentioning

confidence: 99%

A molecular cell biology toolkit for the study of meiosis in the silkworm Bombyx mori

Xiang

Tsuchiya

Guo

et al. 2023

G3: Genes, Genomes, Genetics

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Meiosis is usually described as four essential and sequential processes: (1) homolog pairing; (2) synapsis, mediated by the synaptonemal complex (SC); (3) crossing over; and (4) segregation. In this canonical model, the maturation of crossovers into chiasmata plays a vital role in holding homologs together and ensuring their segregation at the first meiotic division. However, Lepidoptera (moths and butterflies) undergo three distinct meiotic processes, only one of which is canonical. Lepidoptera males utilize two meiotic processes: canonical meiosis that produces nucleated fertile sperm, and a noncanonical meiosis that produces anucleated nonfertile sperm which are nonetheless essential for reproduction. Lepidoptera females, which carry heteromorphic sex chromosomes, undergo a completely achiasmate (lacking crossovers) meiosis, thereby requiring an alternative mechanism to ensure proper homolog segregation. Here we report the development of a molecular cell biology toolkit designed to properly analyze features of meiosis, including the SC structure and function, in the silkworm Bombyx mori. In addition to standard homology searches to identify Bombyx orthologs of known SC encoding genes, we developed an ortholog discovery app (Shinyapp) to identify Bombyx orthologs of proteins involved in several meiotic processes. We used this information to clone genes expressed in the testes and then created antibodies against their protein products. We used the antibodies to confirm the localization of these proteins in normal male spermatocytes, as well as using in vitro assays to confirm orthologous interactions. The development of this toolkit will facilitate further study of the unique meiotic processes that characterize meiosis in Lepidoptera.

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Section: Resultsmentioning

confidence: 99%

A molecular cell biology toolkit for the study of meiosis in the silkworm Bombyx mori

Xiang

Tsuchiya

Guo

et al. 2023

G3: Genes, Genomes, Genetics

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“…In budding yeast, it has been possible to demonstrate directly that centromere pairing in prophase is necessary for subsequent disjunction of nonexchange partner chromosomes in anaphase I (60). Since shugoshin is acting at the centromeres in this interval, we tested whether it is important for the meiotic segregation of nonexchange chromosomes.…”

Section: Resultsmentioning

confidence: 99%

Shugoshin protects centromere pairing and promotes segregation of nonexchange partner chromosomes in meiosis

Almeida

Evatt

Chuong

et al. 2019

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

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Faithful chromosome segregation during meiosis I depends upon the formation of connections between homologous chromosomes. Crossovers between homologs connect the partners, allowing them to attach to the meiotic spindle as a unit, such that they migrate away from one another at anaphase I. Homologous partners also become connected by pairing of their centromeres in meiotic prophase. This centromere pairing can promote proper segregation at anaphase I of partners that have failed to become joined by a crossover. Centromere pairing is mediated by synaptonemal complex (SC) proteins that persist at the centromere when the SC disassembles. Here, using mouse spermatocyte and yeast model systems, we tested the role of shugoshin in promoting meiotic centromere pairing by protecting centromeric synaptonemal components from disassembly. The results show that shugoshin protects the centromeric SC in meiotic prophase and, in anaphase, promotes the proper segregation of partner chromosomes that are not linked by a crossover.

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“…To test this, we used live cell imaging to monitor the pro-metaphase behavior of centromeres that were paired in prophase. For these experiments we used well characterized mini-chromosomes (circular centromere plasmids) that act as partners in meiosis I 19 . These mini-chromosomes carry natural yeast centromeres, origins of DNA replication, and do not become connected by crossovers.…”

Section: Prophase Centromere Pairing Dissolves In Pro-metaphasementioning

confidence: 99%

Centromere Pairing in Prophase Allows Partner Chromosomes to Orient on the Meiosis I Spindle

Evatt

Chuong²,

Meyer³

et al. 2022

Preprint

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Proper chromosome segregation in meiosis I relies on the formation of connections between homologous chromosomes. Crossovers between homologs provide a connection that allows them to attach correctly to the meiosis I spindle. Tension is transmitted across the crossover when the partners attach to microtubules from opposing poles of the spindle. Tension stabilizes microtubule attachments that will pull the partners towards opposite poles at anaphase. Paradoxically, in many organisms, non-crossover partners segregate correctly. The mechanism by which non-crossover partners become bi-oriented on the meiotic spindle is unknown. Both crossover and non-crossover partners pair their centromeres in early in meiosis (prophase). In budding yeast, centromere pairing, is correlated with subsequent correct segregation of the partners. The mechanism by which centromere pairing, in prophase, promotes later correct attachment of the partners to the metaphase spindle is unknown. We used live cell imaging to track the bi-orientation process of non-crossover chromosomes. We find that centromere pairing allows the establishment of connections between the partners that allows their later interdependent attachment to the meiotic spindle using tension-sensing bi-orientation machinery. Because all chromosome pairs experience centromere pairing, our findings suggest that crossover chromosomes also utilize this mechanism to achieve maximal segregation fidelity.

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A ZIP1 separation-of-function allele reveals that centromere pairing drives meiotic segregation of achiasmate chromosomes in budding yeast

Cited by 9 publications

References 39 publications

A molecular cell biology toolkit for the study of meiosis in the silkworm Bombyx mori

A molecular cell biology toolkit for the study of meiosis in the silkworm Bombyx mori

Shugoshin protects centromere pairing and promotes segregation of nonexchange partner chromosomes in meiosis

Centromere Pairing in Prophase Allows Partner Chromosomes to Orient on the Meiosis I Spindle

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