Molecular and Evolutionary Strategies of Meiotic Cheating by Selfish Centromeres

Akera, Takashi; Trimm, Emily; Lampson, Michael A.

doi:10.2139/ssrn.3244531

Cited by 2 publications

(8 citation statements)

References 48 publications

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“…Maize, for example, contains different numbers and sizes of heterochromatic regions (knobs) that have preferential segregation during female meiosis (49–51). Similarly, drive of more than one centromere has been observed in species of Mus (52, 53).…”

Section: Discussionsupporting

confidence: 53%

Dramatically diverseS. pombe wtfmeiotic drivers all display high gamete-killing efficiency

Núñez

Sabbarini

Eickbush

et al. 2019

Preprint

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Meiotic drivers are selfish genetic loci that force their transmission into more than 50% of the viable gametes made by heterozygotes. Meiotic drivers are known to cause infertility in a diverse range of eukaryotes and are predicted to affect the evolution of genome structure and meiosis. The wtf gene family of Schizosaccharomyces pombe includes both meiotic drivers and drive suppressors and thus offers a tractable model organism to study drive systems. Currently, only a handful of wtf genes have been functionally characterized and those genes only partially reflect the diversity of the wtf gene family. In this work, we functionally test 22 additional wtf genes. We identify eight new drivers that share between 30-90% amino acid identity with previously characterized drivers. Despite the vast divergence between these genes, they generally drive into >85% gametes when heterozygous. We also find three new wtf genes that suppress drive, including two that also act as autonomous drivers. Additionally, we find that wtf genes do not underlie a weak (64%) transmission bias caused by a locus or loci on chromosome 1. Finally, we find that some Wtf proteins have expression or localization patterns that are distinct from the poison and antidote proteins encoded by drivers and suppressors, suggesting some wtf genes may have non-meiotic drive functions. Overall, this work expands our understanding of the wtf gene family and the burden selfish driver genes impose on S. pombe.Article SummaryDuring gametogenesis, the two gene copies at a given locus, known as alleles, are each transmitted to 50% of the gametes (e.g. sperm). However, some alleles cheat so that they are found in more than the expected 50% of gametes, often at the expense of fertility. This selfish behavior is known as meiotic drive. Some members of the wtf gene family in the fission yeast, Schizosaccharomyces pombe, kill the gametes (spores) that do not inherit them, resulting in meiotic drive favoring the wtf allele. Other wtf genes act as suppressors of drive. However, the wtf gene family is diverse and only a small subset of the genes has been characterized. Here we analyze the functions of other members of this gene family and found eight new drivers as well as three new suppressors of drive. Surprisingly, we find that drive is relatively insensitive to changes in wtf gene sequence as highly diverged wtf genes execute gamete killing with similar efficiency. Finally, we also find that the expression and localization of some Wtf proteins are distinct from those of known drivers and suppressors, suggesting that these proteins may have non-meiotic drive functions.

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Section: Discussionsupporting

confidence: 53%

Dramatically diverseS. pombe wtfmeiotic drivers all display high gamete-killing efficiency

Núñez

Sabbarini

Eickbush

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…One hypothesis is that there is a constraint on kinetochore size, and that exceeding the upper size limit results in fitness costs (e.g. errors in mitosis and meiosis), creating a selective force that eliminates fusions except those that decrease kinetochore size, in species with bigger kinetochores [36,38].…”

Section: Drive Involving Bivalents and Trivalentsmentioning

confidence: 99%

“…How do stronger centromeres interact with the spindle with tyrosinated α-tubulin asymmetry in order to produce this biased flipping behaviour and affect orientation towards the egg? Taking an important first step towards addressing this question, a 2019 study was able to show that major microtubule destabilizing factors, mitotic centromere-associated kinesin (MCAK) and the chromosome passenger complex (CPC), were recruited more to the stronger centromeres in intraspecific hybrid mice (figure 3 a ) [38,46–48]. Microtubule destabilizers are recruited to pericentromeres and are critical for error correction during cell division [49,50].…”

Section: Drive Involving Bivalents and Trivalentsmentioning

confidence: 99%

“…It was previously shown that kinetochore-localized BUB1 catalyses histone H2A phosphorylation (H2A pT121) to recruit Shugoshin, which is the scaffold for MCAK and CPC at the pericentromeres [53,54]. The authors of the 2019 study found that the entire BUB1 pathway is amplified on stronger centromeres [38]. Experimental recruitment of BUB1 to pericentromeric major satellite cancelled the asymmetry by increasing MCAK and CPC levels across the bivalent, and biased orientation was lost under this condition.…”

Section: Drive Involving Bivalents and Trivalentsmentioning

confidence: 99%

“…Taken together, this suggests that expanded centromeric minor satellite repeats build larger kinetochores, with more BUB1, which in turn recruit more destabilizing factors such as MCAK to the pericentromere, making stronger centromeres more prone to microtubule detachment and flipping. When the spindle migrates towards the cortex, an increase in tyrosinated α-tubulin on the cortical side of the spindle makes detachment more likely to happen on the cortical side, resulting in biased flipping towards the egg side (figure 3 b ) [38]. From differences in centromere DNA sequence to spindle asymmetry, the studies discussed above provide a strong start to a comprehensive molecular model for the mechanism of centromere drive.…”

Section: Drive Involving Bivalents and Trivalentsmentioning

confidence: 99%

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Unravelling the mystery of female meiotic drive: where we are

Clark

Akera

2021

Open Biol.

Self Cite

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Female meiotic drive is the phenomenon where a selfish genetic element alters chromosome segregation during female meiosis to segregate to the egg and transmit to the next generation more frequently than Mendelian expectation. While several examples of female meiotic drive have been known for many decades, a molecular understanding of the underlying mechanisms has been elusive. Recent advances in this area in several model species prompts a comparative re-examination of these drive systems. In this review, we compare female meiotic drive of several animal and plant species, highlighting pertinent similarities.

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Molecular and Evolutionary Strategies of Meiotic Cheating by Selfish Centromeres

Cited by 2 publications

References 48 publications

Dramatically diverseS. pombe wtfmeiotic drivers all display high gamete-killing efficiency

Dramatically diverseS. pombe wtfmeiotic drivers all display high gamete-killing efficiency

Unravelling the mystery of female meiotic drive: where we are

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