Developmental Systems Drift and the Evolution of Redundancy in Plants

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Development in eukaryotes is controlled to a large extent by a conserved set of regulatory genes that fulfil very similar functions in related species. However, a number of examples have been described in yeast and animals where a phenotypically conserved trait is controlled by divergent molecular pathways. This so-called developmental systems drift becomes apparent, when mutations in orthologous genes in related species cause different phenotypes. One possible reason for this is differential redundancy between two genes in one, but not the other species. We have recently identified a pertinent example in the Red Shepherd’s Purse Capsella rubella, where a loss-of-function mutation in the BLADE ON PETIOLE2 (BOP2) gene leads to a fully penetrant formation of ectopic bracts, which is not seen in bop2 mutants in the closely related model plant Arabidopsis thaliana; in the latter, bract formation is only seen in bop1 bop2 double mutants, together with a host of additional mutant phenotypes. We hypothesize that this difference reflects differential redundancy between BOP1 and BOP2 between the two species, with the two genes still fully redundant in A. thaliana for all of their functions, but not in C. rubella, where redundancy is seen for most processes, but not for the suppression of bract formation. This partial resolution of redundancy reflects a first step towards subfunctionalization of the two genes, an important process in the evolution of redundancy. While both developmental systems drift and subfunctionalization have been studied intensively from a theoretical perspective, little is known about the molecular basis, population genetics and developmental consequences of early-stage subfunctionalizing mutations in plants. Therefore, the proposed project will exploit the example of BOP1/2 to empirically address these issues from an evolutionary and functional perspective. In particular, we will pursue the following main objectives. (1) We will define in detail the molecular difference between A. thaliana and C. rubella BOP1 that is responsible for the presumed loss of BOP1 function in bract suppression. This will identify one of the first early subfunctionalizing mutations between two redundant genes in plants. (2) We will analyze the population genetics of this subfunctionalizing mutation in Capsella to test the hypothesis that it became fixed in C. rubella due to drift. In addition, we will experimentally test the status of BOP1/2 redundancy in other Brassicaceae to determine whether resolution of redundancy between this gene pair is also ongoing in other taxa. (3) We will test the hypothesis that redundancy serves to render developmental processes more robust by comparing the frequency of developmental errors regarding bract suppression between Capsella and Arabidopsis. Together, these studies will provide unprecedented insight into the early stages of subfunctionalization and into developmental systems drift in plants.