Journal
MOLECULAR BIOLOGY AND EVOLUTION
Volume 32, Issue 10, Pages 2501-2514Publisher
OXFORD UNIV PRESS
DOI: 10.1093/molbev/msv169
Keywords
gene expression; adaptation; self-fertilization; allele-specific expression; mating system evolution; cis-regulatory evolution
Funding
- Swedish Research Council
- Knut and Alice Wallenberg Foundation
- SNIC through Uppsala Multidisciplinary Center for Advanced Computational Science (UPPMAX) [b2012122]
- Erik Philip-Sorensen foundation
- Nilsson-Ehle foundation
- Magnus Bergvall foundation
- Royal Swedish Academy of Sciences
- Human Frontier Science Program [LT000783]
- German Research Foundation [WE 2897]
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The selfing syndrome constitutes a suite of floral and reproductive trait changes that have evolved repeatedly across many evolutionary lineages in response to the shift to selfing. Convergent evolution of the selfing syndrome suggests that these changes are adaptive, yet our understanding of the detailed molecular genetic basis of the selfing syndrome remains limited. Here, we investigate the role of cis-regulatory changes during the recent evolution of the selfing syndrome in Capsella rubella, which split from the outcrosser Capsella grandiflora less than 200 ka. We assess 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. Using a hierarchical Bayesian approach that accounts for technical variation using genomic reads, we find evidence for extensive cis-regulatory changes. On average, 44% of the assayed genes show evidence of ASE; however, only 6% show strong allelic expression biases. Flower buds, but not leaves, show an enrichment of cis-regulatory changes in genomic regions responsible for floral and reproductive trait divergence between C. rubella and C. grandiflora. We further detected an excess of heterozygous transposable element (TE) insertions near genes with ASE, and TE insertions targeted by uniquely mapping 24-nt small RNAs were associated with reduced expression of nearby genes. Our results suggest that cis-regulatory changes have been important during the recent adaptive floral evolution in Capsella and that differences in TE dynamics between selfing and outcrossing species could be important for rapid regulatory divergence in association with mating system shifts.
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