Clade-specific positive selection on a developmental gene: BRANCHLESS TRICHOME and the evolution of stellate trichomes in Physaria (Brassicaceae)

• Highly-branched stellate trichomes are a synapomorphy of Physaria.
• BRANCHLESS TRICHOME (BLT) shows an elevated dN/dS ratio in Physaria.
• As many as 13% of the codons in BLT experienced positive selection in Physaria.
• Most positively selected codons cluster in the coiled-coil domain of the protein.
• We offer 3 hypotheses for why the selective shift affected the entire stellate clade.

Positive selection is known to drive the evolution of genes involved in evolutionary arms races, but what role does it play in the evolution of genes involved in developmental processes? We used the single-celled epidermal trichomes of Brassicaceae as a model to uncover the molecular evolutionary processes that contributed to the transition from dendritic trichomes, as seen in most species of Brassicaceae, to the distinctive stellate trichomes of the genus Physaria. We explored the role of positive selection on the evolution of BRANCHLESS TRICHOME (BLT), a candidate gene for changes in trichome branching pattern. Maximum likelihood models of codon evolution point to a shift in selective pressure affecting the evolution of BLT across the entire Physaria clade, and we found strong evidence that positive selection has acted on a subset of Physaria BLT codons. Almost all of the 10 codon sites with the highest probability of having evolved under positive selection are clustered in a predicted coiled-coil domain, pointing to changes in protein–protein interactions. Thus, our findings suggest that selection acted on BLT to modify its interactions with other proteins. The fact that positive selection occurred throughout the radiation of Physaria could reflect selection to stabilize development in response to an abrupt switch from the dendritic form to the stellate form, divergent selection for diversification of the stellate form, or both. These results point to the need for evolutionary developmental studies of BLT and its interacting proteins in Physaria.

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