Auxin requirements for a meristematic state in roots depend on a dual brassinosteroid function

Summary The organization of the root meristem is maintained by a complex interplay between plant hormones signaling pathways that both interpret and determine their accumulation and distribution. Brassinosteroids (BR) and auxin signaling pathways control the number of meristematic cells in the Arabidopsis root, via an interaction that appears to involve contradicting molecular outcomes, with BR promoting auxin signaling input but also repressing its output. However, whether this seemingly incoherent effect is significant for meristem function is unclear. Here, we established that a dual effect of BR on auxin, with BR simultaneously promoting auxin biosynthesis and repressing auxin transcriptional output, is essential for meristem maintenance. Blocking BR-induced auxin synthesis resulted in rapid BR-mediated meristem loss. Conversely, plants with reduced BR levels were resistant to loss of auxin biosynthesis and these meristems maintained their normal morphology despite a 10-fold decrease in auxin levels. In agreement, injured root meristems which rely solely on local auxin synthesis, regenerated when both auxin and BR synthesis were inhibited. Use of BIN2 as a tool to selectively inhibit BR signaling, revealed meristems with distinct phenotypes depending on the perturbed tissue; meristem reminiscent of BR-deficient mutants or of high BR exposure. This enabled mapping BR-auxin interactions to the outer epidermis and lateral root cap tissues, and demonstrated the essentiality of BR signaling in these tissues for meristem maintenance. BR activity in internal tissues however, proved necessary to control BR homeostasis. Together, we demonstrate a basis for inter-tissue coordination and how a critical ratio between these hormones determines the meristematic state.