Evolvability and Functional Divergence in the Auxin-Signaling F-Box Family

Auxin is a small molecule hormone that shapes plant development and homeostasis. The evolution of more complex body plans in land plant lineages has been paralleled by gene duplication and divergence within nuclear auxin-signaling networks. Mapping how the structure/function relationship of these signaling proteins affects plant phenotype would allow rational engineering of plant growth, development and reproduction. Here, we determined this mapping for a subset of permissive mutations found in the auxin receptor F-box family of wild accessions of the reference plant Arabidopsis thaliana. To do this, we quantified the functional variation between the natural F-box variants and the phenotypic variation in accessions expressing these variants. In several cases quantitative changes in auxin sensitivity at the whole plant level were predicted by synthetic functional assays in yeast. Our findings revealed a strong connection between sequence variation in paralogs, altered molecular performance and phenotypic diversity at the organism-level. This approach provides a new method for harnessing the wealth of sequence information to guide future engineering efforts of diverse signaling pathways which rely on ubiquitin-mediated protein turnover.