Root meristem organization is maintained by an interplay between hormone signaling pathways that both interpret and determine their accumulation and distribution. The interacting hormones Brassinosteroids (BR) and auxin control the number of meristematic cells in the Arabidopsis root. BR was reported both to promote auxin signaling input and to repress auxin signaling output. Whether these contradicting molecular outcomes co-occur and what their significance in meristem function is remain unclear. Here, we established a dual effect of BR on auxin, with BR simultaneously promoting auxin biosynthesis and repressing auxin transcriptional output, which 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 a critical loss of auxin biosynthesis, maintaining their meristem morphology. 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 yielded meristems with distinct phenotypes depending on the perturbed tissue: meristem reminiscent either of BR-deficient mutants or of high BR exposure. This enabled mapping of the BR-auxin interaction that maintains the meristem to the outer epidermis and lateral root cap tissues and demonstrated the essentiality of BR signaling in these tissues for meristem response to BR. BR activity in internal tissues however, proved necessary to control BR levels. Together, we demonstrate a basis for inter-tissue coordination and how a critical ratio between these hormones determines the meristematic state.

Faculty of Biology Technion Israel Institute of Technology Haifa 3200003 Israel

Institute of Plant Sciences and Genetics in Agriculture Faculty of Agriculture The Hebrew University of Jerusalem Rehovot Israel

Laboratory of Growth Regulators Institute of Experimental Botany Czech Academy of Sciences and Palacky University Olomouc Czech Republic

Lorey 1 Lokey Interdisciplinary Center for Life Sciences and Engineering Technion Israel Institute of Technology Haifa 3200003 Israel

Curr Biol. 2021 Oct 25;31(20):R1392-R1395. doi: 10.1016/j.cub.2021.09.007. PubMed

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