Chromosome size matters: genome evolution in the cyperid clade

Abstract

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.

Fig. 1.

Comparisons between holoploid (1C; A and B) genome sizes, mean chromosome sizes (2C/2n; D and E) and chromosome numbers (2n; G and H) among cyperids (grey), Poales (excluding cyperids: yellow), non-Poales seed plants (violet) and Lentibulariaceae (green). The results from raw data are shown in (A), (D) and (G), whereas (B), (E) and (H) are based on log₁₀-transformed data. Unique letters above the boxplots indicate significant differences among groups, and numbers at the bottom of the boxplots show the sample size (species number) of each group. The distribution of genome sizes, mean chromosome sizes and chromosome numbers within cyperids are shown in (C), (F) and (I), respectively. The boxes cover 50% of the data values ranging between the 25th and 75th percentiles, whereas the whiskers above and below each box represent the interquartile range multiplied by 1.5. The line within each box represents the median, and outlying values are indicated by small circles. The alpha value was set at 0.05.

Fig. 2.

Holoploid genome (A) and chromosome (B) sizes mapped onto the phylogeny of cyperids. The length of the bars adjacent to the tips of the phylogeny represent the genome (1C: Mbp) and chromosome size (2C/2n: Mbp) of each species, respectively, according to the scale bar on the right side of each phylogeny. Species without chromosome number data do not have bars adjacent to them in (B). Family (Juncaceae and Thurniaceae) and tribal associations (Cyperaceae) are indicated by the colours given in the key. Genome and chromosome sizes were mapped onto the phylogeny with the R package GGTREEEXTRA v.1.0.4 (Xu et al., 2021).

Fig. 3.

The association between diploid chromosome numbers and holoploid genome size (1C; A), as well as mean chromosome size (2C/2n; B) across the cyperids. Values corresponding to the Juncaceae and 16 tribes of Cyperaceae are indicated by the colours shown to the right-hand side of (B). All data were log transformed. Statistical significance (P <0.05) between variables, as determined by phylogenetic generalized least squares (PGLS) performed using the R package CAPER v.1.0.1 (Orme, 2013), is indicated by a solid regression line.

Fig. 4.

The association between mean chromosome size (2C/2n) and extent of occurrence (A), niche size (B) and annual precipitation (C) in cyperids as determined by phylogenetic generalized least squares (PGLS) performed using the R package CAPER v.1.0.1 (Orme, 2013). These three predictor variables received relatively high AICw and log-likelihood scores, and corrections for multiple comparisons were implemented using the method of Benjamini and Hochberg (1995). Significant relationships are indicated by solid regression lines, whereas marginally significant relationships between variables are indicated by broken lines. All variables were log transformed, except for Niche size, which was square-root transformed.