Cell Dynamics in WOX5-Overexpressing Root Tips: The Impact of Local Auxin Biosynthesis

Abstract

Root stem cell niche functioning requires the formation and maintenance of the specific "auxin-rich domain" governed by directional auxin transport and local auxin production. Auxin maximum co-localizes with the WOX5 expression domain in the quiescent center that separates mitotically active proximal and distal root meristems. Here we unravel the interconnected processes happening under WOX5 overexpression by combining in vivo experiments and mathematical modeling. We showed that WOX5-induced TAA1mediated auxin biosynthesis is the cause, whereas auxin accumulation, PIN transporters relocation, and auxin redistribution between proximal and distal root meristems are its subsequent effects that influence the formation of the well-described phenotype with an enlarged root cap. These findings helped us to clarify the role of WOX5, which serves as a local QC-specific regulator that activates biosynthesis of non-cell-autonomous signal auxin to regulate the distal meristem functioning. The mathematical model with WOX5-mediated auxin biosynthesis and auxin-regulated cell growth, division, and detachment reproduces the columella cells dynamics in both wild type and under WOX5 dysregulation.

Root stem cell niche networks: it’s complexed! Insights from Arabidopsis

“…Treating WOX5–GR-induced overexpression plants with differentiation-inducing CLE40 peptide indicated that only the first mature columella layer may undergo de-differentiation ( Berckmans et al , 2020 ). However, reproduction of the WOX5–GR-inducible overexpression experiments with a focus on cell division dynamics suggested that the observed multiple stem cell phenotype is exclusively caused by proliferation of columella stem cells ( Savina et al , 2020 ), which are subsequently maintained in their undifferentiated state.…”

“…Upon induction of ectopic WOX5-GR expression, prior to any morphological change, the TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS1 ( TAA1 ) gene that is involved in auxin biosynthesis is up-regulated and has its expression domain expanded into the columella ( Savina et al , 2020 ). A similar pattern was observed for the auxin polar transporters PIN1 and PIN4, suggesting that WOX5 ectopic expression impacts both auxin biosynthesis and transport.…”

“…Mathematical modelling supported the hypothesis that WOX5-induced TAA1-mediated auxin biosynthesis is sufficient to explain the phenotypes observed in the columella. Absence of QC quiescence and the presence of one or two stem cells were predicted for a 50% reduction in TAA1-dependent synthesis in a WT background ( Savina et al , 2020 ). Accordingly, wox5-1 might be an in vivo representation of this predicted phenotype, since it displays QC divisions, and indeed it was shown to have reduced TAA1 marker expression.…”

Hormonal Regulation of Stem Cell Proliferation at the Arabidopsis thaliana Root Stem Cell Niche

“…In Arabidopsis , root growth is not compromised by genetic perturbations that result in alterations in the division patterns of the QC cells, suggesting that low division rate of the QC cells is not strictly necessary for the function and the organization of the root meristem under optimal growth conditions ( Vanstraelen et al, 2009 ; González-García et al, 2011 ; Cruz-Ramírez et al, 2013 ; Savina et al, 2020 ; Wang et al, 2020 ). The division of the QC cells has been shown to increase in frequency in older Arabidopsis seedlings ( Timilsina et al, 2019 ), and it can also be actively modulated to cope with the current needs of the root.…”

“…In the root SCN, WOX5 promotes auxin accumulation in the QC by inducing the expression of the auxin biosynthetic enzymes YUCCA1 ( Tian et al, 2014 ), tryptophan aminotransferase of arabidopsis1 (TAA1; Savina et al, 2020 ), and by repressing the expression of auxin conjugation genes ( Gonzali et al, 2005 ). As WOX5 expression is induced by auxin in the QC ( Sarkar et al, 2007 ), this establishes an auxin—WOX5-positive feedback loop in these cells.…”