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

Elife. 2022 Sep 7:11:e73031. doi: 10.7554/eLife.73031.

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.

Keywords: A. thaliana; br/bri1 perception; bri1 signaling; computational biology; computational modeling; plant biology; plant cell physiology; receptor complexes; systems biology; theoretical biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / metabolism
  • Brassinosteroids / metabolism
  • Computer Simulation
  • Gene Expression Regulation, Plant
  • Plant Roots
  • Potassium Channels / metabolism
  • Proton-Translocating ATPases / metabolism
  • Signal Transduction

Substances

  • Arabidopsis Proteins
  • Brassinosteroids
  • Potassium Channels
  • Proton-Translocating ATPases

Associated data

  • GEO/GSE123818

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.