Transmission ratio distortion is frequent in Arabidopsis thaliana controlled crosses

Abstract

The equal probability of transmission of alleles from either parent during sexual reproduction is a central tenet of genetics and evolutionary biology. Yet, there are many cases where this rule is violated. The preferential transmission of alleles or genotypes is termed transmission ratio distortion (TRD). Examples of TRD have been identified in many species, implying that they are universal, but the resolution of species-wide studies of TRD are limited. We have performed a species-wide screen for TRD in over 500 segregating F₂ populations of Arabidopsis thaliana using pooled reduced-representation genome sequencing. TRD was evident in up to a quarter of surveyed populations. Most populations exhibited distortion at only one genomic region, with some regions being repeatedly affected in multiple populations. Our results begin to elucidate the species-level architecture of biased transmission of genetic material in A. thaliana, and serve as a springboard for future studies into the biological basis of TRD in this species.

Fig. 1

Z-score estimated segregation distortion is evident in a wide range of crosses. Genotypic combinations surveyed in this F₂ screen are shown in blue, and populations with significant segregation distortion based on Z-score metrics in green. Grandparental accessions are ordered by the geographic location of their collection (Cao et al. 2011). Female grandparents are located on the y-axis and male grandparents on the x-axis. Intercrosses between grandparents that were not attempted are in black

Fig. 2

A representative F₂ population, POP035 (ICE63 × Vash-1), with significant segregation distortion. Distortion in this population was detected with both thresholds (FDR and Z-score outlier). a The beta-binomial modeled allele frequency (blue) across each chromosome is plotted in the upper panel. 95% confidence intervals are indicated by the shaded grey area and the expected frequency of 0.5 is marked by the dashed black line. b The –log₁₀ of the p-value derived from the non-parametric statistical test. The dashed black line in this panel represents the FDR corrected (n = 240) significance threshold (p < 0.05)

Fig. 3

Genomic properties of distorted loci. a The fraction of surveyed F₂ populations that exhibited segregation distortion at either one or two genomic loci. b The number of populations containing distorted loci that reside on each of the five A. thaliana chromosomes

Fig. 4

Many grandparental accessions contributed biased alleles. Each grandparent contributed its genetic material to a median of 14 distinct F₂ populations. Plotted is the fraction of F₂ populations with one shared grandparent that are significantly distorted as measured either by (a) 2.5× Z-score deviation, or (b) FDR corrected deviation from beta-binomial modeled allele frequencies

Fig. 5

Mapping intervals refined using k-mer coverage and bulked segregant analysis. a The coverage of unique 21 nt k-mers is plotted for POP035 (ICE63 × Vash-1) after whole-genome resequencing. The first peak in coverage represents 21-mers found in only one of the two grandparents (red arrow), while the second, larger peak represents those sequences found in both (black arrow). b The upper panel displays the beta-binomial modeled allele frequency estimates (blue) and their 95% confidence intervals (grey) for POP035 as described in the legend for Fig. 2. In the lower panel, the coverage of 21-mers unique to only one of the two grandparents (coverage < 25×) is plotted in 1 Mb sliding windows (50 kb steps). Coverage decreases in the candidate regions. Intervals (grey box) are defined by merging windows with values within 1× coverage of the minimal window in each population. c Bulked segregant analysis was performed for Star-8, an accession that repeatedly contributed distorted loci. Sequencing reads were combined for populations exhibiting distortion when crossed with Star-8, and for populations not exhibiting distortion when crossed to Star-8 (normal pool). A candidate interval (grey box) was obtained by merging all segregating positions within 5% of the maximal allele frequency