Auxin coordinates cell states during Arabidopsis root development

ABSTRACT Cell-to-cell variation in gene expression can be highly detrimental and, in some contexts, is actively buffered out; however, in other contexts, it is crucial and actively amplified. For example, variation must be minimized to build organs with consistent size and shape, yet the initiation of organogenesis requires a subset of cells to take on a new fate, a process that often relies on small differences between cells. In plants, much of development is controlled by the hormone auxin, which has been hypothesized to coordinate cell responses by inducing degradation of transcriptional repressors. To quantify the level of cell-to-cell variation and directly test its connection to auxin signaling, we assessed variation in expression of a lateral root founder cell marker GATA23 when auxin levels or responsiveness was modulated. We found that auxin acted as both an amplifier and a constrainer of transcriptional variation during the initiation of a new root. We then extended this work to analysis of root regeneration, where auxin was also found to play a critical role in coordinating cells during fate transitions. ARTICLE SUMMARY During organogenesis, cell-to-cell variation is induced, enabling some cells to adopt a new identity and differentiate. Despite this dependence on variation, organogenesis is robust in developmental stages and outcomes. In plants, organogenesis is usually controlled by the hormone auxin, and we hypothesized that auxin ensures coordination among differentiating cells to enable robust development. Using Arabidopsis lateral root development as a model, our results showed that cells receiving the highest auxin dosage both amplify their own auxin response and repress the auxin response in neighboring cells receiving lower auxin dosage, establishing separation between differentiating and non-differentiating cells and ensuring coordinated organogenesis.