Analysis of allele-specific expression reveals cis-regulatory changes associated with a recent mating system shift and floral adaptation in Capsella
Kim A Steige , Johan Reimegård , Daniel Koenig , Douglas G Scofield , Tanja Slotte
Cis-regulatory changes have long been suggested to contribute to organismal adaptation. While cis-regulatory changes can now be identified on a transcriptome-wide scale, in most cases the adaptive significance and mechanistic basis of rapid cis-regulatory divergence remains unclear. Here, we have characterized cis-regulatory changes associated with recent adaptive floral evolution in the selfing plant Capsella rubella, which diverged from the outcrosser Capsella grandiflora less than 200 kya. We assessed allele-specific expression (ASE) in leaves and flower buds at a total of 18,452 genes in three interspecific F1 C. grandiflora x C. rubella hybrids. After accounting for technical variation and read-mapping biases using genomic reads, we estimate that an average of 44% of these genes show evidence of ASE, however only 6% show strong allelic expression biases. Flower buds, but not leaves, show an enrichment of genes with ASE in genomic regions responsible for phenotypic divergence between C. rubella and C. grandiflora. We further detected an excess of heterozygous transposable element (TE) insertions in the vicinity of genes with ASE, and TE insertions targeted by uniquely mapping 24-nt small RNAs were associated with reduced allelic expression of nearby genes. Our results suggest that cis-regulatory changes have been important for recent adaptive floral evolution in Capsella and that differences in TE dynamics between selfing and outcrossing species could be an important mechanism underlying rapid regulatory divergence.