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

• Published in: Current biology Vol. 31; no. 20; pp. 4462 - 4472.e6
• Main Authors: Ackerman-Lavert, M., Fridman, Y., Matosevich, R., Khandal, H., Friedlander-Shani, L., Vragović, K., Ben El, R., Horev, G., Tarkowská, D., Efroni, I., Savaldi-Goldstein, S.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 25.10.2021
• Subjects: Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; auxin; brassinosteroid; Brassinosteroids - metabolism; differentiation; Gene Expression Regulation, Plant; hormone biosynthesis; Hormones - metabolism; Indoleacetic Acids - metabolism; inter-tissue communication; Meristem - metabolism; meristem maintenance; Plant Roots - metabolism; regeneration; root; differentiation; auxin; inter-tissue communication; regeneration; hormone biosynthesis; root; brassinosteroid; meristem maintenance
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.07.075

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. •BR signaling dictates auxin requirements for meristem maintenance and regeneration•Root meristems are maintained despite low auxin levels, if BR signaling is absent•Cell-specific expression of BIN2 reveals spatial control of meristem maintenance•This links BR production in the stele to outer tissue-BR control of the meristem Plant hormones like brassinosteroid (BR) and auxin interact to control root growth. Ackerman-Lavert et al. show that BR incoherent effect on auxin, promoting signaling input and repressing output, dictates the root meristematic state. In the absence of BR signaling, the meristem can be maintained even with deleteriously low auxin levels.