Female meiotic drive in plants: mechanisms and dynamics

Finseth, Findley

doi:10.1016/j.gde.2023.102101

Cited by 7 publications

(2 citation statements)

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“…As noted, centromeres are characterized by rapid DNA sequence and kinetochore protein evolution within and between species ( Malik and Henikoff 2009 ; Rhind et al 2011 ; Melters et al 2013 ; Logsdon et al 2023 ; Wlodzimierz et al 2023b ), which presents a paradox given their conserved cellular function ( Henikoff et al 2001 ). An influential model to explain rapid centromere evolution is the drive hypothesis ( Malik 2009 ; Akera et al 2019 ; Finseth 2023 ). This model considers female meiosis, as it occurs in animals and plants, in which only one of the four meiotic products survives to differentiate into an egg or gametophyte ( Fig.…”

Section: What Drives Rapid Centromere Evolution?mentioning

confidence: 99%

The structure, function, and evolution of plant centromeres

Naish,

Henderson

2024

Genome Res.

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Centromeres are essential regions of eukaryotic chromosomes responsible for the formation of kinetochore complexes, which connect to spindle microtubules during cell division. Notably, although centromeres maintain a conserved function in chromosome segregation, the underlying DNA sequences are diverse both within and between species and are predominantly repetitive in nature. The repeat content of centromeres includes high-copy tandem repeats (satellites), and/or specific families of transposons. The functional region of the centromere is defined by loading of a specific histone 3 variant (CENH3), which nucleates the kinetochore and shows dynamic regulation. In many plants, the centromeres are composed of satellite repeat arrays that are densely DNA methylated and invaded by centrophilic retrotransposons. In some cases, the retrotransposons become the sites of CENH3 loading. We review the structure of plant centromeres, including monocentric, holocentric, and metapolycentric architectures, which vary in the number and distribution of kinetochore attachment sites along chromosomes. We discuss how variation in CENH3 loading can drive genome elimination during early cell divisions of plant embryogenesis. We review how epigenetic state may influence centromere identity and discuss evolutionary models that seek to explain the paradoxically rapid change of centromere sequences observed across species, including the potential roles of recombination. We outline putative modes of selection that could act within the centromeres, as well as the role of repeats in driving cycles of centromere evolution. Although our primary focus is on plant genomes, we draw comparisons with animal and fungal centromeres to derive a eukaryote-wide perspective of centromere structure and function.

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Section: What Drives Rapid Centromere Evolution?mentioning

confidence: 99%

The structure, function, and evolution of plant centromeres

Naish,

Henderson

2024

Genome Res.

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“…8 Female meiotic drive is thought to be accomplished through preferential segregation to the egg, exploiting the inherent asymmetry in female meiosis: only the chromosomes that segregate to the egg will transmit. 3,[9][10][11] In contrast, male meiosis undergoes symmetric divisions, and cheating mostly happens post-meiosis. 5,7,8 Male (and spore killer) meiotic drivers typically act through the sabotage or death of competitor sperm/spores that do not carry them.…”

Section: Introductionmentioning

confidence: 99%

An egg sabotaging mechanism drives non-Mendelian transmission in mice

Clark,

Greenberg,

Silva

et al. 2024

Preprint

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SummaryDuring meiosis, homologous chromosomes segregate so that alleles are transmitted equally to haploid gametes, following Mendel’s Law of Segregation. However, some selfish genetic elements drive in meiosis to distort the transmission ratio and increase their representation in gametes. The established paradigms for drive are fundamentally different for female vs male meiosis. In male meiosis, selfish elements typically kill gametes that do not contain them. In female meiosis, killing is predetermined, and selfish elements bias their segregation to the single surviving gamete (i.e., the egg in animal meiosis). Here we show that a selfish element on mouse chromosome 2,R2d2, drives using a hybrid mechanism in female meiosis, incorporating elements of both male and female drivers. IfR2d2is destined for the polar body, it manipulates segregation to sabotage the egg by causing aneuploidy that is subsequently lethal in the embryo, so that surviving progeny preferentially containR2d2. In heterozygous females,R2d2orients randomly on the metaphase spindle but lags during anaphase and preferentially remains in the egg, regardless of its initial orientation. Thus, the egg genotype is either euploid withR2d2or aneuploid with both homologs of chromosome 2, with only the former generating viable embryos. Consistent with this model,R2d2heterozygous females produce eggs with increased aneuploidy for chromosome 2, increased embryonic lethality, and increased transmission ofR2d2. In contrast to a male meiotic driver, which kills its sister gametes produced as daughter cells in the same meiosis,R2d2eliminates “cousins” produced from meioses in which it should have been excluded from the egg.

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