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.

• Keywords
• Angiosperms, CENH3, asymmetric and symmetric meiosis, bryophytes, centromere drive, chromosome size, ferns, genome size, gymnosperms, lycophytes, post-polyploid diploidization,
• MeSH
• Biological Evolution MeSH
• Centromere * genetics   MeSH
• Chromosomes, Plant * genetics   MeSH
• Cycadopsida genetics   MeSH
• Genome Size * MeSH
• Phylogeny MeSH
• Genome, Plant * genetics   MeSH
• Histones genetics   metabolism   MeSH
• Ferns genetics   physiology   MeSH
• Magnoliopsida genetics   MeSH
• Meiosis * genetics   MeSH
• Evolution, Molecular * MeSH
• Polyploidy MeSH
• Plants genetics   MeSH
• Selection, Genetic MeSH
• Publication type
• Journal Article MeSH
• Names of Substances
• Histones MeSH

BACKGROUND AND AIMS: While variation in genome size and chromosome numbers and their consequences are often investigated in plants, the biological relevance of variation in chromosome size remains poorly known. Here, we examine genome and mean chromosome size in the cyperid clade (families Cyperaceae, Juncaceae and Thurniaceae), which is the largest vascular plant lineage with predominantly holocentric chromosomes. METHODS: We measured genome size in 436 species of cyperids using flow cytometry, and augment these data with previously published datasets. We then separately compared genome and mean chromosome sizes (2C/2n) amongst the major lineages of cyperids and analysed how these two genomic traits are associated with various environmental factors using phylogenetically informed methods. KEY RESULTS: We show that cyperids have the smallest mean chromosome sizes recorded in seed plants, with a large divergence between the smallest and largest values. We found that cyperid species with smaller chromosomes have larger geographical distributions and that there is a strong inverse association between mean chromosome size and number across this lineage. CONCLUSIONS: The distinct patterns in genome size and mean chromosome size across the cyperids might be explained by holokinetic drive. The numerous small chromosomes might function to increase genetic diversity in this lineage where crossovers are limited during meiosis.

• Keywords
• Chromosome number, Cyperaceae, Juncaceae, Thurniaceae, chromosome size, distribution range size, genome size, holocentric chromosomes, holokinetic drive,
• MeSH
• Chromosomes, Plant * genetics   MeSH
• Genome Size MeSH
• Phylogeny MeSH
• Genome, Plant genetics   MeSH
• Evolution, Molecular * MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH

Previous studies on grass species suggested that the total centromere size (sum of all centromere sizes in a cell) may be determined by the genome size, possibly because stable scaling is important for proper cell division. However, it is unclear whether this relationship is universal. Here we analyze the total centromere size using the CenH3-immunofluorescence area as a proxy in 130 taxa including plants, animals, fungi, and protists. We verified the reliability of our methodological approach by comparing our measurements with available ChIP-seq-based measurements of the size of CenH3-binding domains. Data based on these two independent methods showed the same positive relationship between the total centromere size and genome size. Our results demonstrate that the genome size is a strong predictor (R-squared = 0.964) of the total centromere size universally across Eukaryotes. We also show that this relationship is independent of phylogenetic relatedness and centromere type (monocentric, metapolycentric, and holocentric), implying a common mechanism maintaining stable total centromere size in Eukaryotes.

• MeSH
• Centromere physiology   MeSH
• Genome Size MeSH
• Fungi genetics   MeSH
• Evolution, Molecular MeSH
• Plants genetics   MeSH
• Animals MeSH
• Check Tag
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH