Computational modeling and quantitative physiology reveal central parameters for brassinosteroid-regulated early cell physiological processes linked to elongation growth of the Arabidopsis root

Abstract

Brassinosteroids (BR) are key hormonal regulators of plant development. However, whereas the individual components of BR perception and signaling are well characterized experimentally, the question of how they can act and whether they are sufficient to carry out the critical function of cellular elongation remains open. Here, we combined computational modeling with quantitative cell physiology to understand the dynamics of the plasma membrane (PM)-localized BR response pathway during the initiation of cellular responses in the epidermis of the Arabidopsis root tip that are be linked to cell elongation. The model, consisting of ordinary differential equations, comprises the BR induced hyperpolarization of the PM, the acidification of the apoplast and subsequent cell wall swelling. We demonstrate that the competence of the root epidermal cells for the BR response predominantly depends on the amount and activity of H+-ATPases in the PM. The model further predicts that an influx of cations is required to compensate for the shift of positive charges caused by the apoplastic acidification. A potassium channel was subsequently identified and experimentally characterized, fulfilling this function. Thus, we established the landscape of components and parameters for physiological processes potentially linked to cell elongation, a central process in plant development.

The AUX1-AFB1-CNGC14 module establishes longitudinal root surface pH profile

“…Similar pattern of H + fluxes was determined in Arabidopsis thaliana, where the fluxes also correlated with root surface pH: an alkaline domain was observed at the border between meristematic and transition zones (Staal et al 2011). Other works have attempted to determine the pH of the epidermal cell walls, and show a general decrease of pH towards the maturation zone of the root (Barbez et al 2017;Moreau et al 2022;Großeholz et al 2022). It is important to keep in mind that changes in proton fluxes and membrane potential are not always correlated with change in pH.…”

“…We first hypothesized that the observed spatial surface pH gradients might originate from gradients of AHA ATPase abundance or activity (Großeholz et al . 2022).…”

“…We first hypothesized that the observed spatial surface pH gradients might originate from gradients of AHA ATPase abundance or activity (Großeholz et al 2022). The immunolocalization of endogenous AHAs, however, didn't reveal any obvious reduction in AHA abundance in the transition zone (Fig.…”

“…Increased cytokinin signaling led to shortening of the meristem, similarly to an inducible relocalization of AHA2 fused to the glucocorticoid receptor. Finally, Großeholz et al . (2022) quantified the AHA2-GFP signal and demonstrated an increasing AHA2-GFP membrane abundance towards the maturation zone of Arabidopsis thaliana root, which correlated with increased acidification of the root surface.…”

“…Increased cytokinin signaling led to shortening of the meristem, similarly to an inducible relocalization of AHA2 fused to the glucocorticoid receptor. Finally, Großeholz et al (2022) quantified the AHA2-GFP signal and demonstrated an increasing AHA2-GFP membrane abundance towards the maturation zone of Arabidopsis thaliana root, which correlated with increased acidification of the root surface. Still, the observed patterns of proton fluxes along the root zones (Weisenseel and Meyer 1997), and in particular the existence of the alkaline domain around the transition zone of the root, cannot be simply explained by the expression or abundance of AHA proton pumps.…”