Kristina Vragović, Ayala Sela, Lilach Friedlander-Shani, Yulia Fridman, Yael Hacham, Neta Holland, Elizabeth Bartom, Todd C. Mockler, and Sigal Savaldi-Goldstein

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.

Abstract

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.

See: http://www.pnas.org/content/112/3/923.abstract.html?etoc

PNAS January 20, 2015 vol. 112 no. 3 923-928

Fig. 1.  Stem cell daughter differentiation is inversely controlled by BR activity in the epidermis and the stele. (A) Longitudinal and cross-sections of the Arabidopsis root. Each color depicts a tissue, also corresponding to the expression pattern of the tagged ribosomal protein (see Fig. 2A). C, cortex; En, endodermis; Ep, epidermis; LR/C, lateral root cap and columella; and St, stele. Yellow line marks the stem cell niche. Asterisks indicate QC cells. (B) Confocal microscopy image of the root meristem of the triple mutant bri1, brl1, brl3, Col-0 (wild type), and both single and triple mutants expressing pGL2-BRI1. The arrow marks the onset of cell elongation/differentiation. PI staining to show cell borders appears in white. (Scale bar, 50 μm.) (C) Cortical cell numbers of the wild type and mutants depicted in B. (D) Root-meristem wild type and bri1, brl1, brl3; pGL2-BRI1 cell numbers, counted over time. DAG, days after germination. Note the similar curve, reflecting balanced rate of cell proliferation and cell differentiation. (E) Edu staining, applied to detect cells in S phase, is shown as pink nuclei. Nuclei with DAPI staining appear purple. Meristems correspond to the same genotypes shown in B. (F) Cortical cell number of wild type and bri1, brl1, brl3; pGL2-BRI1 in the absence and presence of endodermal BRI1 (pSCR-BRI1). (G and H) Cortical cell number of wild type, bri1, brl1, brl3; pGL2-BRI1 in the absence and presence of stele BRI1 (pSHR-BRI1), and bri1, brl1, brl3 expressing pSHR-BRI1 (G), and in the absence and presence of BR (H). Mean ± SE; *P < 0.05 and **P < 0.01 with two-tailed t test.