Centromere drive may propel the evolution of chromosome and genome size in plants

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Authors

PLAČKOVÁ Klára BUREŠ Petr LYSÁK Martin ZEDEK František

Year of publication 2024
Type Article in Periodical
Magazine / Source Annals of Botany
MU Faculty or unit

Faculty of Science

Citation
Web https://academic.oup.com/aob/advance-article/doi/10.1093/aob/mcae149/7743260?login=true
Doi http://dx.doi.org/10.1093/aob/mcae149
Keywords Angiosperms; asymmetric and symmetric meiosis; bryophytes; CENH3; centromere drive; chromosome size; ferns; genome size; gymnosperms; lycophytes; post-polyploid diploidization
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Description Background Genome size is influenced by natural selection and genetic drift acting on variations from polyploidy and repetitive DNA sequences. We hypothesized that centromere drive, where centromeres compete for inclusion in the functional gamete during meiosis, may also affect genome and chromosome size. This competition occurs in asymmetric meiosis, where only one of the four meiotic products becomes a gamete. If centromere drive influences chromosome size evolution, it may also impact post-polyploid diploidization, where a polyploid genome is restructured to function more like a diploid through chromosomal rearrangements, including fusions. We tested if plant lineages with asymmetric meiosis exhibit faster chromosome size evolution compared to those with only symmetric meiosis, which lack centromere drive as all four meiotic products become gametes. We also examined if positive selection on centromeric histone H3 (CENH3), a protein that can suppress centromere drive, is more frequent in these asymmetric lineages.Methods We analysed plant groups with different meiotic modes: asymmetric in gymnosperms and angiosperms, and symmetric in bryophytes, lycophytes and ferns. We selected species based on available CENH3 gene sequences and chromosome size data. Using Ornstein-Uhlenbeck evolutionary models and phylogenetic regressions, we assessed the rates of chromosome size evolution and the frequency of positive selection on CENH3 in these clades.Results Our analyses showed that clades with asymmetric meiosis have a higher frequency of positive selection on CENH3 and increased rates of chromosome size evolution compared to symmetric clades.Conclusions Our findings support the hypothesis that centromere drive accelerates chromosome and genome size evolution, potentially also influencing the process of post-polyploid diploidization. We propose a model which in a single framework helps explain the stability of chromosome size in symmetric lineages (bryophytes, lycophytes and ferns) and its variability in asymmetric lineages (gymnosperms and angiosperms), providing a foundation for future research in plant genome evolution.
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