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

• Published in: bioRxiv
• Main Authors: Grosseholz, Ruth, Wanke, Friederike, Rohr, Leander, Gloeckner, Nina, Rausch, Luiselotte, Scholl, Stefan, Scacchi, Emanuele, Amelie-Jette Spazierer, Shabala, Lana, Shabala, Sergey, Schumacher, Karin, Kummer, Ursula, Harter, Klaus Jw
• Format: Paper
• Language: English
• Published: Cold Spring Harbor Cold Spring Harbor Laboratory Press 16.05.2022
• Subjects: Acidification; Apoplast; Arabidopsis; Brassinosteroids; Cell walls; Computer applications; Elongation; Hyperpolarization; Ordinary differential equations; Physiology; Potassium transporter
• DOI: 10.1101/2021.04.13.439595

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 could 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 demonstrated 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 predicted 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. Competing Interest Statement The authors have declared no competing interest. Footnotes * 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 cell elongation in the epidermis of the Arabidopsis root tip. 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 demonstrated 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 predicted 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 capable of triggering and guiding cellular elongation through the fast response to BR, a central process in plant development.