RGF1 controls root meristem size through ROS signalling

Abstract

Stem cell niche and root meristem size are maintained by intercellular interactions and signaling networks of a peptide hormone, Root Meristem Growth Factor 1 (RGF1). How RGF1 regulates root meristem development is an essential question to understand stem cell function. Although five receptors of RGF1 have been identified, the downstream signaling mechanism remains unknown. Here, we report a series of signaling events following RGF1 action. The RGF1-receptor pathway controls the distribution of reactive oxygen species (ROS) along the developmental zones of the Arabidopsis root. We identify a novel transcription factor, RGF1 INDUCIBLE TRANSCRIPTION FACTOR 1 ( RITF1) that plays a central role in mediating RGF1 signaling. Manipulating RITF1 expression leads to redistribution of ROS along the root developmental zones. Changes in ROS distribution, in turn, enhance the stability of the PLETHORA2 (PLT2) protein, a master regulator of root stem cells. Our study, thus, clearly depicts a signaling cascade initiated by RGF1, linking the RGF1 peptide to ROS regulatory mechanisms.Roots encounter various environmental conditions and respond by altering their growth. Root growth arises through controlled cell division in the meristematic zone, equivalent to the transit amplifying zone in animals. After division, most cells increase their size in the elongation zone and mature in the differentiation zone. The size of these developmental zones is determined by intrinsic and extrinsic signals. Reactive oxygen species (ROS) are an intrinsic signal for establishing the size of the meristematic zone. Superoxide (O 2 − ) primarily accumulates in the meristematic zone, while hydrogen peroxide (H 2 O 2 ) mainly accumulates in the differentiation zone 1,2 . The balance between O 2 − and H 2 O 2 modulates the transition from proliferation to differentiation 2 .

Receptor-like protein kinase-mediated signaling in controlling root meristem homeostasis

“…RGF1 treatment resulted in enhanced O 2accumulation in the meristematic zone, thus enhancing the stability of PLT2 protein to increase the proximal root meristem size. Consistent with this, the ritf1 mutants displayed reduced proximal root meristem size and RGF1-induced O 2accumulation, suggesting that RITF1 has a crucial role in mediating RGF1 signaling (Yamada et al 2020) (Fig. 3B).…”

The Roles of Peptide Hormones and Their Receptors during Plant Root Development

“…Furthermore, a recent discovery has uncovered the regulation mechanisms of root meristem development under the RGF1-receptor pathway. The RGF1-RGFR signaling pathway modulates ROS distribution along the developmental zones of the Arabidopsis root and enhances the PLT2 protein stability [ 45 ]. Genetic evidence also showed that the RGF1-receptor pathway is required to maintain proper gradients of PLT proteins in the proximal meristem [ 41 ].…”

“…Despite the ligand-receptor pairs having been identified, the downstream signaling of RGF1 remained elusive and the molecular mechanisms involved in root meristem development and the PLT1/2 stability were still unknown. Since RGF1 is received in the meristematic zone by the receptors, the meristematic zone-specific transcriptome analysis after RGF1 treatment was conducted to understand the downstream gene in the meristematic zone [ 45 ]. The transcriptome analysis detects significant alteration of expression of the genes related to ROS suggesting that RGF1 might signal through a ROS intermediate to control the size of the meristematic zone.…”

“…The transcriptome analysis detects significant alteration of expression of the genes related to ROS suggesting that RGF1 might signal through a ROS intermediate to control the size of the meristematic zone. Levels of O 2 •– are elevated in the meristematic zone after RGF1 treatment [ 45 ]. On the other hand, H 2 O 2 concentrations are decreased in the elongation and differentiation zone according to RGF1 treatment [ 45 ].…”

“…Levels of O 2 •– are elevated in the meristematic zone after RGF1 treatment [ 45 ]. On the other hand, H 2 O 2 concentrations are decreased in the elongation and differentiation zone according to RGF1 treatment [ 45 ]. Furthermore, pharmaceutical treatments with RGF1 confirm that the alterations of these ROS distributions modulate the meristematic zone size [ 45 ].…”