A Signaling Module Controlling the Stem Cell Niche in Arabidopsis Root Meristems

Abstract

The niches of the Arabidopsis shoot and root meristems, the organizing center (OC) and the quiescent center (QC), orchestrate the fine balance of stem cell maintenance and the provision of differentiating descendants. They express the functionally related homeobox genes WUSCHEL (WUS) and WOX5, respectively, that promote stem cell fate in adjacent cells. Shoot stem cells signal back to the OC by secreting the CLAVATA3 (CLV3) dodecapeptide, which represses WUS expression. However, the signals controlling homeostasis of the root stem cell system are not identified to date. Here we show that the differentiating descendants of distal root stem cells express CLE40, a peptide closely related to CLV3. Reducing CLE40 levels delays differentiation and allows stem cell proliferation. Conversely, increased CLE40 levels drastically alter the expression domain of WOX5 and promote stem cell differentiation. We report that the receptor kinase ACR4, previously shown to control cell proliferation, is an essential component, and also a target, of CLE40 signaling. Our results reveal how, in contrast to the shoot system, signals originating from differentiated cells, but not the stem cells, determine the size and position of the root niche.

RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana

“…There are several parallel signaling pathways involved in root stem cell niche maintenance, such as SHR-SCR [46][47][48][49][50], CLE40-ACR4/CLV1-WOX5 [19,20], and RGF1-PLT pathways [25,30,51,52]. To examine which pathway was mainly affected in the quintuple mutant, The expression levels and patterns of both SHR and SCR are not significantly altered in the quintuple mutant compared with the wild-type plant (Supplementary information, Figure S3A and S3B), which is consistent with root cross section results, showing that there are no obvious cell differentiation defects in the quintuple mutant (Supplementary information, Figure S1C).…”

“…CLV3 is perceived by three different receptors or putative receptors, CLAVA-TA1 (CLV1), CLAVATA 2 (CLV2)-CORYNE (CRN), and RPK2/TOAD2, to limit stem cell size by restricting the expression of a homeodomain transcription factor, WUSCHEL (WUS), via a negative feedback loop [13][14][15][16][17][18]. On the other hand, CLE40 is perceived by its putative receptor complex containing two different RLKs, ARA-BIDOPSIS CRIKLY4 (ACR4) and CLV1, to inhibit the expression of a root version of homeodomain transcription factor, WOX5 [19,20]. TRACHEARY ELEMENT DIFFERENTIATION INHIBITORY FACTOR (TDIF)/ CLE41/CLE44 peptide regulates vascular development in Arabidopsis.…”

Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF–TDR signalling

“…CLV3-WUS signalling makes a negative feedback loop to maintain the homoeostasis of stem cell population in the shoot apical meristem [11][12][13] . A similar CLE peptide-receptortranscription factor system is involved in the maintenance of columella stem cells in the root apical meristem 14 . Previous studies have revealed the importance of individual peptide signals in meristem maintenance, however, the manner of intracellular signal transduction mechanisms regulating cell fates is still a mystery.…”

A Tale of Two Systems: Peptide Ligand-Receptor Pairs in Plant Development

“…CLE40 was shown to be expressed in the columella stem cells, and the cle40 mutant shows multiple layers of columella stem cells, which is similar to the phenotype of the acr4 (Stahl et al 2009). Consistent with this, acr4 mutants are nearly insensitive to CLE40 peptide application, supporting the view that CLE40 and ACR4 form a ligand-receptor pair in root meristem maintenance (De Smet et al 2008;Hirakawa et al 2008).…”

“…Another interesting CLE peptide named CLE40 requires the ACR4 receptor kinase, in which receptor ectodomain is unrelated to the LRR domain found in other known CLE receptors (Stahl et al 2009). CLE40 was shown to be expressed in the columella stem cells, and the cle40 mutant shows multiple layers of columella stem cells, which is similar to the phenotype of the acr4 (Stahl et al 2009).…”