Dynamic control of auxin distribution imposes a bilateral-to-radial symmetry switch during gynoecium development

Symmetry formation is a remarkable feature of biological life forms associated with evolutionary advantages and often with great beauty. Several examples exist in which organisms undergo a transition in symmetry during development. Such transitions are almost exclusively in the direction from radial to bilateral symmetry. Here, we describe the dynamics of symmetry establishment during development of the Arabidopsis gynoecium. We show that the apical style region undergoes an unusual transition from a bilaterally symmetric stage ingrained in the gynoecium due to its evolutionary origin to a radially symmetric structure. We also identify two transcription factors, INDEHISCENT and SPATULA, that are both necessary and sufficient for the radialization process. Our work furthermore shows that these two transcription factors control style symmetry by directly regulating auxin distribution. Establishment of specific auxin-signaling foci and the subsequent development of a radially symmetric auxin ring at the style are required for the transition to radial symmetry, because genetic manipulations of auxin transport can either cause loss of radialization in a wild-type background or rescue mutants with radialization defects. Whereas many examples have described how auxin provides polarity and specific identity to cells in a range of developmental contexts, our data presented here demonstrate that auxin can also be recruited to impose uniform identity to a group of cells that are otherwise differentially programmed.