CLE40 Signaling Regulates Root Stem Cell Fate

Abstract

The quiescent center (QC) of the Arabidopsis (Arabidopsis thaliana) root meristem acts as an organiser that promotes stem cell fate in adjacent cells and patterns the surrounding stem cell niche. The stem cells distal from the QC, the columella stem cells (CSCs), are maintained in an undifferentiated state by the QC-expressed transcription factor WUSCHEL RELATED HOMEOBOX 5 (WOX5) and give rise to the columella cells (CCs). Differentiated CCs provide a feedback signal via secretion of the peptide CLAVATA3/ESR-RELATED 40 (CLE40), which acts through the receptor kinases ARABIDOPSIS CRINKLY4 (ACR4) and CLAVATA1 (CLV1) to control WOX5 expression. Previously, WOX5 protein movement from the QC into CSCs was proposed to be required for CSC maintenance, and the CLE40/CLV1/ACR4 signalling module was suggested to restrict WOX5 mobility or function. Here, these assumptions were tested by exploring the function of CLE40/CLV1/ACR4 in CSC maintenance. However, no role for CLE40/CLV1/ACR4 in constricting the mobility of WOX5 or other fluorescent test proteins was identified. Furthermore, in contrast to previous observations, WOX5 mobility was not required to inhibit CSC differentiation. We propose that WOX5 acts mainly in the QC, where other short-range signals are generated that not only inhibit differentiation but also promote stem cell division in adjacent cells. Therefore, the main function of columella-derived CLE40 signal is to position the QC at a defined distance from the root tip by repressing QC-specific gene expression via the ACR4/CLV1 receptors in the distal domain and by promoting WOX5 expression via the CLV2 receptor in the proximal meristem.

Protein complex stoichiometry and expression dynamics of transcription factors modulate stem cell division

“…Thus, we do not conclude here that SEU and WOX5 are the only upstream regulators of SHR, and we propose that it is likely that other proteins act in concert with or upstream of SEU and WOX5 to regulate SHR expression in the vasculature. For example, it has been shown that treatment with CLAVATA3/ESR-RELATED 40 peptide (CLE40p) rapidly increases WOX5 protein expression in the vascular initials, and that this CLE40p-dependent upregulation of WOX5 protein expression is also dependent on CLAVATA2 (CLV2) (30). This suggests that there is a gene regulatory network upstream of WOX5 that controls its protein localization, and therefore regulation of SHR, in the vasculature.…”

“…While WOX5 transcript is largely absent in the stele (28-30), a WOX5:WOX5-GFP translational fusion shows WOX5 protein expression in the vasculature initials (31) ( Figure 2B). As WOX5 has been shown to be a mobile protein (30), we postulated that WOX5 protein localization in the vascular initials could be due to WOX5 movement from the QC ( Figure 2C). To this end, we performed Pair Correlation Function (pCF) analysis on the WOX5:WOX5-GFP translational fusion and compared its movement to a protein that is able to move (35S:GFP) and a protein that is not able to move (TMO5:3xGFP) from the QC to the vascular initials (19) (see Methods).…”

“…The 35S:GFP; UBQ10:mCherry; SHR:SHR-GFP; SCR:SCR-GFP; SHR:SHR-GFP, SCR:SCR:mCherry; and TMO5:3xGFP lines are described in (19). The WOX5:WOX5-GFP line is described in (30), the pCYCD6:GUS-GFP line is described in (7), and the SEU:SEU-GFP line is described in (45). The WOX5 TPT line (TPT_3.11260.1E) was obtained from the Arabidopsis Biological Resource Center (ABRC: https://abrc.osu.edu).…”

Shedding the Last Layer: Mechanisms of Root Cap Cell Release

“…Differentiated COL cells produce the small signaling peptide CLE40 [39]. CLE40 is perceived by the receptor kinases ARABIDOPSIS CRINKLY4 (ACR4) and CLAVATA1 (CLV1) which promotes COL cell differentiation [40] and the position of the QC [41]. The CLE40 module may regulate the movement of factors from the QC that promote 'stemness' [40,42].…”

The Role of Plasmodesmata-Associated Receptor in Plant Development and Environmental Response

“…In addition, plants use a range of PD-PM receptors to sense endogenous and exogenous signals for plant growth stimulation and development. These PD-PM receptors include the leucine-rich repeat (LRR) receptor kinase CLAVATA1 (CLV1) and the non-LRR receptor kinase ARABIDOPSIS CRINKLY4 (ACR4), which are required for shoot and root stemness maintenance in arabidopsis, respectively [40,70,[72][73][74][98][99][100]. Moreover, tissue morphogenesis is another key factor in the biological process during plant growth and development, which usually involves an alteration in cell number, size, shape, and position.…”