Cis-Regulatory Changes Associated with a Recent Mating System Shift and Floral Adaptation in Capsella

Area of Science:

• Evolutionary genetics
• Plant reproductive biology
• Molecular evolution

Background:

• The selfing syndrome describes convergent floral and reproductive trait evolution in response to self-fertilization.
• Understanding the molecular genetic basis of the selfing syndrome is crucial but remains limited.
• Recent divergence between selfing Capsella rubella and outcrossing Capsella grandiflora offers a model for studying rapid evolutionary changes.

Purpose of the Study:

• To investigate the role of cis-regulatory changes in the recent evolution of the selfing syndrome in Capsella rubella.
• To assess allele-specific expression (ASE) and identify genes with regulatory divergence.
• To explore the potential contribution of transposable elements (TEs) to regulatory evolution.

Main Methods:

• Assessed allele-specific expression (ASE) in leaves and flower buds of interspecific F1 hybrids (C. grandiflora x C. rubella) for 18,452 genes.
• Employed a hierarchical Bayesian approach to analyze genomic read data and account for technical variation.
• Analyzed the association of transposable element (TE) insertions and small RNA profiles with gene expression biases.

Main Results:

• Found extensive evidence of cis-regulatory changes, with 44% of assayed genes showing ASE.
• Identified a significant enrichment of cis-regulatory changes in flower buds, specifically in regions linked to floral trait divergence.
• Detected an excess of heterozygous TE insertions near genes with ASE, and TE insertions targeted by small RNAs were linked to reduced gene expression.

Conclusions:

• Cis-regulatory changes play a significant role in the recent adaptive floral evolution associated with the shift to selfing in Capsella.
• Differences in transposable element (TE) dynamics between selfing and outcrossing species may facilitate rapid regulatory divergence.
• This study highlights the importance of regulatory evolution in shaping mating system shifts.