A link between LEAFY and B-gene homologues in Welwitschia mirabilis sheds light on ancestral mechanisms prefiguring floral development

Abstract

- Flowering plants evolved from an unidentified gymnosperm ancestor. Comparison of the mechanisms controlling development in angiosperm flowers and gymnosperm cones may help to elucidate the mysterious origin of the flower. - We combined gene expression studies with protein behaviour characterization in Welwitschia mirabilis to test whether the known regulatory links between LEAFY and its MADS-box gene targets, central to flower development, might also contribute to gymnosperm reproductive development. - We found that WelLFY, one of two LEAFY-like genes in Welwitschia, could be an upstream regulator of the MADS-box genes APETALA3/PISTILLATA-like (B-genes). We demonstrated that, even though their DNA-binding domains are extremely similar, WelLFY and its paralogue WelNDLY exhibit distinct DNA-binding specificities, and that, unlike WelNDLY, WelLFY shares with its angiosperm orthologue the capacity to bind promoters of Welwitschia B-genes. Finally, we identified several cis-elements mediating these interactions in Welwitschia and obtained evidence that the link between LFY homologues and B-genes is also conserved in two other gymnosperms, Pinus and Picea. - Although functional approaches to investigate cone development in gymnosperms are limited, our state-of-the-art biophysical techniques, coupled with expression studies, provide evidence that crucial links, central to the control of floral development, may already have existed before the appearance of flowers.This work was supported by funding from the Centre National de la Recherche Scientifique (ATIP+ to F.P.), the ANAgence Nationale de la Recherche (ANR) (Plant-TFcode to F.P. and C.P.S.), PhD fellowships from the University J. Fourier, Grenoble (to E.M. and M.M.), Grenoble Alliance for Cell and Structural Biology (ANR-10-LABX-49-01), the SYNTHESYS Project (to E.M.), the Floral Genome Project (National Science Foundation (NSF) Plant Genome Research Program project DBI-0115684 to M.W.F.) and NSF DEB-9974374 (to M.W.F.)