Brassinosteroid signaling and BRI1 dynamics went underground

Abstract

Brassinosteroids (BRs) are a group of steroid molecules perceived at the cell surface and that act as plant hormones. Since their discovery as crucial growth substances, BRs were mainly studied for their action in above ground organs and the BR signaling pathway was largely uncovered in the context of hypocotyl elongation. However, for the past two years, most of the exciting findings on BR signaling have been made using roots as a model. The Arabidopsis root is a system of choice for cell biology and allowed detailed characterization of BR perception at the cell membrane. In addition, a series of elegant articles dissected how BRs act in tissue specific manners to control root growth and development.

Figure 1. BRI1 trafficking to and from the cell surface.

ER, endoplasmic reticulum; TGN/EE, trans-Golgi network/early endosomes; MVB, multivesicular body; ERQC, ER quality control protein response; ERAD, ER-associated degradation; BRI1, BRASSINOSTEROID-INSENSITIVE-1; BAK1, BRI1-ASSOCIATED-KINASE-1; LRR, Leucine-Rich Repeat; ESCRT, ENDOSOMAL-SORTING-COMPLEX-REQUIRED-FOR-TRANSPORT; TPC, TPLATE-COMPLEX; AP-2, ADAPTOR-COMPLEX-2; Ub, K63-linked polyubiquitination. Question marks, ubiquitination may drive clathrin-dependent and/or -independent BRI1 endocytosis. Black arrows represent trafficking pathways, green and purple arrows indicate the recruitment of BRI1 into CME and CIE internalization pathways, respectively. Note that although CIE opens an interesting new window to dissect BRI1 trafficking, to date CME remains the main demonstrated internalization route of BRI1.

Figure 2. Regulation of BR receptor complex activation by the antagonistic action of BRs and BKI1.

Left, inhibited BRI1 receptor in the absence of ligand. Note that BAK1 may interact with BRI1 in this context, but has not been drawn for sake of clarity. Right, ligand-activated receptor complex. PM, Plasma Membrane; BRI1, BRASISNOSTEROID-INSENSITIVE-1; BAK1, BRI1-ASSOCIATED-KINASE-1; BKI1, BRI1-KINASE-INHIBITOR-1; PI4P, phosphatidylinositol 4-phosphate; [KR], Lysine and/or Arginine doublet. Kinase domains are represented by kidney-shape figures, the juxtamembrane segments are in orange, activation loops in red and C-terminal tails in brown. The area highlighted in red at the bottom of BRI1 kinase domain corresponds to the BKI1-binding surface and putative BAK1 interaction area. Phosphorylated residues are represented by orange circle labeled with the letter P, and lipid phosphorylation by yellow circles.

Figure 3. Tissue-specific features of BR-regulated root meristem size.

Left, schematic representation of an Arabidopsis root tip longitudinal section. Arrows indicate activation, blunt-ended lines indicate inhibition and bullet-ended lines indicate the different zone of the root. BZR1 expression pattern and subcellular localization is represented in yellow as indicated in the box at the bottom left corner. BES1, BR-INSENSITIVE-EMS-SUPPRESSOR-1; BZR1, BRASSINAZOLE-RESISTANT-1; BRAVO, BRASSINOSTEROIDS-AT-VASCULAR-AND-ORGANIZING-CENTER; ERF115, ETHYLENE-RESPONSE-FACTOR-115; QC, Quiescent Center.

Figure 4. Role of BR signaling in root tissue patterning.

Top left, schematic representation of an Arabidopsis root tip transversal section. Top right, regulation of BIN2 activity by OPS in phloem, TDR in cambium and BR signaling in xylem. Note that the role of BRs in the regulation of xylem differentiation has only been demonstrated in aerial parts. Bottom, regulation of TTG1 and EGL3 by BIN2 to control root epidermal patterning. Note that BR signaling is not specific of trichoblast cells and occurs in both cell types. As such, modulation of BR signaling and/or biosynthesis might control the atrichoblast/trichoblast ratio. This regulation might therefore be relevant during environmental interactions since root hair production is highly constrained by the root environment. Arrows and blunt-ended lines indicate inhibition and activation, respectively. Red crosses represent the release of BES1/BZR1 inhibition by BIN2 inactivation. BRs, Brassinosteroids; BRI1, BR-INSENSITIVE-1; BRLs, BRI1-LIKEs; BES1, BR-INSENSITIVE-EMS-SUPPRESSOR-1; BZR1, BRASSINAZOLE-RESISTANT-1; BIN2, BR-INSENSITIVE-2; OPS, OCTOPUS; TDIF, TRACHEARY-ELEMENT-DIFFERENTIATION-INHIBITORY-FACTOR; TDR, TDIF-RECEPTOR; pBES1/pBZR1, phosphorylated form of BES1/BZR1; TTG1, TRANSPARENT-TESTA-GLABRA1; EGL3, ENHANCER-OF-GLABRA3.