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

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    Evaluation Summary:

    This study addresses the effect of brassinosteroid hormones on acidification of the apoplast. The authors characterize a novel ionic channel involved in this process as well as a gradient of H+-ATPase activity, providing evidence for a fast brassinosteroid response that has so far received little attention. A combination of computational modeling and quantitative cell physiology is used to explain the regulation of proton pumping into Arabidopsis root cell walls. The authors show that regulation of AHA proton pump activity by the activated brassinosteroid receptor complex could potentially explain the experimentally determined zonation of root cell wall pH and growth. The work will be of interest to plant biologists as well as cell biologists in general.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)

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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.

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  1. Author Response

    Reviewer #3 (Public review):

    1. The central component of the model is the fast activation of AHA by BRI1, a rapid, non-transcriptional response. More experimental support is needed to establish that, in the root, AHAs are activated rapidly and not by the transcriptional pathway. Minami et al., 2019 showed that AHA activation in the hypocotyls requires tens of minutes and is likely mediated by the accumulation of SAUR proteins. In other words, the activation is not a rapid BRI1mediated phosphorylation. The model, however, uses the findings from Minami et al 2019 as the support for the immediate activation of AHAs by phosphorylation (at the line 143).

    The kinetics of AHA activation possibly through the accumulation of SAUR proteins is now discussed in detail in the Discussion section. In fact, this process is much slower …

  2. Evaluation Summary:

    This study addresses the effect of brassinosteroid hormones on acidification of the apoplast. The authors characterize a novel ionic channel involved in this process as well as a gradient of H+-ATPase activity, providing evidence for a fast brassinosteroid response that has so far received little attention. A combination of computational modeling and quantitative cell physiology is used to explain the regulation of proton pumping into Arabidopsis root cell walls. The authors show that regulation of AHA proton pump activity by the activated brassinosteroid receptor complex could potentially explain the experimentally determined zonation of root cell wall pH and growth. The work will be of interest to plant biologists as well as cell biologists in general.

    (This preprint has been reviewed by eLife. We include the …

  3. Reviewer #1 (Public Review):

    This work addresses a so far much overlooked aspect in plant signaling systems being the physiological reality of how components primarily identified by genetic means work together to achieve a functional physiological system. The genetically well-defined system of brassinosteroid signaling in Arabidopsis roots is employed as a convenient model system.
    For this accurate determination of the number of proteins involved, the kinetics of activation and ODE-based modelling are used by the authors.

    The results focus on one aspect of root brassinosteroid signaling, expansion of root cells as they enter into the extension zone of the root. Several parameters such as wall acidification and cell wall swelling are used as early output determinants of the BR signaling system.

    The authors show convincingly that BR …

  4. Reviewer #2 (Public Review):

    The manuscript entitled "Computational modeling and quantitative cell physiology reveal central parameters for the brassinosteroid-regulated cell growth of the Arabidopsis root" by Ruth Grobeholz et al. presents a hybrid computational and experimental study on the fast response to brassinosteroids of epidermal cells in the elongation and in the meristematic zones of Arabidopsis primary root. The study focuses on the regulation of ionic transport through the plasma membrane that is elicited upon BL induction. This is supported by experimental data on ion fluxes and pH dependence with BRI1 receptor in Arabidopsis roots, analyzing WT and bri1-301 mutant. The combination of modeling and experimental data reveal a new component of the fast BR response. This new component is a cation channel, CNGC10, which the …

  5. Reviewer #3 (Public Review):

    The authors create a computational model that aims to understand how the regulation of proton pumps by brassinosteroid receptor complexes translates into membrane potential changes and cell wall pH. They build the model using known facts from the brassinosteroid literature as well as published cell compartment volumes and membrane densities of some signaling components. To obtain further parameters for their model, the authors quantify the densities of BIR3 and AHA2 and found that the density of the proton pump increases along the differentiation gradient in the root, and that the ratio of AHA to BRI1 dramatically increases in the elongation zone.

    Their model focuses on the rapid responses to the external application of brassinosteroid BL, and as such it could predict the dose response of apoplastic pH to …