Abstract
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.
Author Summary The role of regulatory changes for adaptive evolution has long been debated. cis-regulatory changes have been proposed to be especially likely to contribute to phenotypic adaptation, because they are expected to have fewer negative side effects than protein-coding changes. Here we assess the regulatory divergence between two closely related plant species that differ in their mating system and floral traits. We directly assess cis-regulatory divergence by quantifying the expression levels of both alleles in F1 hybrids of these species, and we find that genes showing cis-regulatory divergence are enriched in genomic regions that are responsible for floral and reproductive differences between the species. In combination with information on gene function for genes with cis-regulatory divergence in flower buds, this suggests that cis-regulatory changes might have been important for morphological differentiation between these species. Additionally we discover that transposable elements, which accumulate differently depending on mating system, might be involved in rapid regulatory divergence. These findings are an important step towards a better understanding of the role and the mechanisms of rapid regulatory divergence between plant species.
