Translatome analyses capture of opposing tissue-specific brassinosteroid signals orchestrating root meristem differentiation

The mechanisms ensuring balanced growth remain a critical question in developmental biology. In plants, this balance relies on spatiotemporal integration of hormonal signaling pathways, but the understanding of the precise contribution of each hormone is just beginning to take form. Brassinosteroid (BR) hormone is shown here to have opposing effects on root meristem size, depending on its site of action. BR is demonstrated to both delay and promote onset of stem cell daughter differentiation, when acting in the outer tissue of the root meristem, the epidermis, and the innermost tissue, the stele, respectively. To understand the molecular basis of this phenomenon, a comprehensive spatiotemporal translatome mapping of Arabidopsis roots was performed. Analyses of wild type and mutants featuring different distributions of BR revealed autonomous, tissue-specific gene responses to BR, implying its contrasting tissue-dependent impact on growth. BR-induced genes were primarily detected in epidermal cells of the basal meristem zone and were enriched by auxin-related genes. In contrast, repressed BR genes prevailed in the stele of the apical meristem zone. Furthermore, auxin was found to mediate the growth-promoting impact of BR signaling originating in the epidermis, whereas BR signaling in the stele buffered this effect. We propose that context-specific BR activity and responses are oppositely interpreted at the organ level, ensuring coherent growth. Significance Brassinosteroid (BR) differentially regulates the number of stem cell daughters in the root meristem. How its activity coordinates and maintains the meristem size remains unknown. We show that BR signal coordinates root growth by evoking distinct and often opposing responses in specific tissues. Whereas epidermal BR signal promotes stem cell daughter proliferation, the stele-derived BR signal induces their differentiation. Using a comprehensive tissue-specific translatome survey, we uncovered a context-specific effect of BR signaling on gene expression. Auxin genes, activated by epidermal BR perception, are necessary for induction of cell division. Conversely, the stele BR perception, accompanied by gene repression, restrains the epidermal effect. Therefore, a site-specific BR signal is essential for balanced organ growth.