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

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.

[1]  Jia Li,et al.  SAUR15 interaction with BRI1 activates plasma membrane H+-ATPase to promote organ development of Arabidopsis , 2022, Plant physiology.

[2]  A. Reiner-Benaim,et al.  The root meristem is shaped by brassinosteroid control of cell geometry , 2021, Nature Plants.

[3]  N. Guex,et al.  A single-cell morpho-transcriptomic map of brassinosteroid action in the Arabidopsis root , 2021, Molecular plant.

[4]  K. T. ten Tusscher,et al.  Bootstrapping and Pinning down the Root Meristem; the Auxin–PLT–ARR Network Unites Robustness and Sensitivity in Meristem Growth Control , 2021, International journal of molecular sciences.

[5]  M. Strnad,et al.  Local brassinosteroid biosynthesis enables optimal root growth , 2020, Nature Plants.

[6]  Ursula Kummer,et al.  Impact of explicit area scaling on kinetic models involving multiple compartments , 2020, bioRxiv.

[7]  K. T. ten Tusscher,et al.  A Self-Organized PLT/Auxin/ARR-B Network Controls the Dynamics of Root Zonation Development in Arabidopsis thaliana. , 2020, Developmental cell.

[8]  Jia Li,et al.  Molecular Mechanisms of Brassinosteroid-Mediated Responses to Changing Environments in Arabidopsis , 2020, International journal of molecular sciences.

[9]  Sebastian Wolf Deviating from the Beaten Track: New Twists in Brassinosteroid Receptor Function , 2020, International journal of molecular sciences.

[10]  Xiaoli Ma,et al.  PscB: A Browser to Explore Plant Single Cell RNA-Sequencing Datasets , 2020 .

[11]  K. Harter,et al.  Specifying the role of BAK1-interacting receptor-like kinase 3 in brassinosteroid signaling. , 2020, Journal of integrative plant biology.

[12]  Ursula Kummer,et al.  Computational systems biology of cellular processes in Arabidopsis thaliana: an overview , 2019, Cellular and Molecular Life Sciences.

[13]  M. Duszyn,et al.  Cyclic nucleotide gated channels (CNGCs) in plant signalling-Current knowledge and perspectives. , 2019, Journal of plant physiology.

[14]  K. Harter,et al.  Three-Fluorophore FRET Enables the Analysis of Ternary Protein Association in Living Plant Cells , 2019, bioRxiv.

[15]  Vivek Krishnakumar,et al.  An ‘eFP‐Seq Browser’ for visualizing and exploring RNA sequencing data , 2019, The Plant journal : for cell and molecular biology.

[16]  Shin-Ichiro Inoue,et al.  Brassinosteroid Induces Phosphorylation of the Plasma Membrane H+-ATPase during Hypocotyl Elongation in Arabidopsis thaliana. , 2019, Plant & cell physiology.

[17]  K. T. ten Tusscher,et al.  In Silico Roots: Room for Growth. , 2019, Trends in plant science.

[18]  Jia Li,et al.  Thermal-Enhanced bri1-301 Instability Reveals a Plasma Membrane Protein Quality Control System in Plants , 2018, Front. Plant Sci..

[19]  K. Harter,et al.  BRI1 controls vascular cell fate in the Arabidopsis root through RLP44 and phytosulfokine signaling , 2018, Proceedings of the National Academy of Sciences.

[20]  Ying Gu,et al.  Impact of acidic pH on plant cell wall polysaccharide structure and dynamics: insights into the mechanism of acid growth in plants from solid-state NMR , 2018, Cellulose.

[21]  Linchuan Liu,et al.  A Temperature-Sensitive Misfolded bri1-301 Receptor Requires Its Kinase Activity to Promote Growth1[OPEN] , 2018, Plant Physiology.

[22]  Wei Yuan,et al.  BR-INSENSITIVE1 regulates hydrotropic response by interacting with plasma membrane H+-ATPases in Arabidopsis , 2018, Plant signaling & behavior.

[23]  Riccardo Di Mambro,et al.  Acidic cell elongation drives cell differentiation in the Arabidopsis root , 2018, The EMBO journal.

[24]  L. Hothorn,et al.  Mechanistic basis for the activation of plant membrane receptor kinases by SERK-family coreceptors , 2018, Proceedings of the National Academy of Sciences.

[25]  M. Ibañes,et al.  A Sizer model for cell differentiation in Arabidopsis thaliana root growth , 2018, Molecular systems biology.

[26]  Xiaofeng Wang,et al.  The Arabidopsis Leucine-Rich Repeat Receptor Kinase BIR3 Negatively Regulates BAK1 Receptor Complex Formation and Stabilizes BAK1 , 2017, Plant Cell.

[27]  P. Benfey,et al.  Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root , 2017, Proceedings of the National Academy of Sciences.

[28]  W. Busch,et al.  Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana , 2017, Proceedings of the National Academy of Sciences.

[29]  M. Ptashnyk,et al.  Mathematical modelling and analysis of the brassinosteroid and gibberellin signalling pathways and their interactions. , 2017, Journal of theoretical biology.

[30]  D. MacLean,et al.  Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains , 2017, eLife.

[31]  M. Lucas,et al.  A multi-scale model of the interplay between cell signalling and hormone transport in specifying the root meristem of Arabidopsis thaliana. , 2016, Journal of theoretical biology.

[32]  H. Juan,et al.  Integrating Phosphoproteomics and Bioinformatics to Study Brassinosteroid-Regulated Phosphorylation Dynamics in Arabidopsis , 2015, BMC Genomics.

[33]  K. Harter,et al.  Phytosulfokine Regulates Growth in Arabidopsis through a Response Module at the Plasma Membrane That Includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+-ATPase, and BAK1[OPEN] , 2015, Plant Cell.

[34]  Zhi-Yong Wang,et al.  Spatiotemporal Brassinosteroid Signaling and Antagonism with Auxin Pattern Stem Cell Dynamics in Arabidopsis Roots , 2015, Current Biology.

[35]  T. Cuin,et al.  Receptor kinase-mediated control of primary active proton pumping at the plasma membrane. , 2014, The Plant journal : for cell and molecular biology.

[36]  Zhi-Xin Wang,et al.  Structural insights into the negative regulation of BRI1 signaling by BRI1-interacting protein BKI1 , 2014, Cell Research.

[37]  K. Harter,et al.  A receptor-like protein mediates the response to pectin modification by activating brassinosteroid signaling , 2014, Proceedings of the National Academy of Sciences.

[38]  Michael P. Pound,et al.  Systems Analysis of Auxin Transport in the Arabidopsis Root Apex[W][OPEN] , 2014, Plant Cell.

[39]  Cyclic nucleotide gated channel 10 negatively regulates salt tolerance by mediating Na+ transport in Arabidopsis , 2014, Journal of Plant Research.

[40]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[41]  S. D. de Vries,et al.  A Mathematical Model for the Coreceptors SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 and SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE3 in BRASSINOSTEROID INSENSITIVE1-Mediated Signaling[C][W] , 2013, Plant Physiology.

[42]  K. Harter,et al.  Computational modelling of the BRI1 receptor system. , 2013, Plant, cell & environment.

[43]  J. Borst,et al.  Visualization of BRI 1 and BAK 1 ( SERK 3 ) membrane receptor hetero-oligomers during brassinosteroid signaling , 2013 .

[44]  K. Harter,et al.  The Arabidopsis B-type response regulator 18 homomerizes and positively regulates cytokinin responses. , 2012, The Plant journal : for cell and molecular biology.

[45]  J. Molenaar,et al.  A Mathematical Model for BRASSINOSTEROID INSENSITIVE1-Mediated Signaling in Root Growth and Hypocotyl Elongation1[W] , 2012, Plant Physiology.

[46]  P. Benfey,et al.  A Gene Regulatory Network for Root Epidermis Cell Differentiation in Arabidopsis , 2012, PLoS genetics.

[47]  K. Harter,et al.  Latest News on Arabidopsis Brassinosteroid Perception and Signaling , 2011, Front. Plant Sci..

[48]  Sven Sahle,et al.  Applications and trends in systems biology in biochemistry , 2011, The FEBS journal.

[49]  Christophe Godin,et al.  The auxin signalling network translates dynamic input into robust patterning at the shoot apex , 2011, Molecular systems biology.

[50]  Joachim Kilian,et al.  The activation of the Arabidopsis P-ATPase 1 by the brassinosteroid receptor BRI1 is independent of threonine 948 phosphorylation , 2011, Plant signaling & behavior.

[51]  J. Borst,et al.  Quantification of the Brassinosteroid Insensitive1 Receptor in Planta1[C][W] , 2011, Plant Physiology.

[52]  Ioannis Xenarios,et al.  A qualitative continuous model of cellular auxin and brassinosteroid signaling and their crosstalk , 2011, Bioinform..

[53]  K. Harter,et al.  A fast brassinolide-regulated response pathway in the plasma membrane of Arabidopsis thaliana. , 2011, The Plant journal : for cell and molecular biology.

[54]  S. Clouse Brassinosteroid Signal Transduction: From Receptor Kinase Activation to Transcriptional Networks Regulating Plant Development , 2011, Plant Cell.

[55]  Cristina N Butterfield,et al.  Development and Stem Cells Research Article , 2022 .

[56]  Filip Vandenbussche,et al.  Apoplastic Alkalinization Is Instrumental for the Inhibition of Cell Elongation in the Arabidopsis Root by the Ethylene Precursor 1-Aminocyclopropane-1-Carboxylic Acid1[W][OA] , 2011, Plant Physiology.

[57]  Rainer Breitling,et al.  What is Systems Biology? , 2010, Front. Physiology.

[58]  C. Seidel,et al.  Stem Cell Signaling in Arabidopsis Requires CRN to Localize CLV2 to the Plasma Membrane1[W][OA] , 2009, Plant Physiology.

[59]  Sarala M. Wimalaratne,et al.  The Systems Biology Graphical Notation , 2009, Nature Biotechnology.

[60]  Kirstin Elgass,et al.  Novel Application of Fluorescence Lifetime and Fluorescence Microscopy Enables Quantitative Access to Subcellular Dynamics in Plant Cells , 2009, PloS one.

[61]  T. Pfannschmidt Plant Signal Transduction , 2009, Methods in Molecular Biology.

[62]  Michael Darsow,et al.  ChEBI: a database and ontology for chemical entities of biological interest , 2007, Nucleic Acids Res..

[63]  Daniel L. Mace,et al.  A High-Resolution Root Spatiotemporal Map Reveals Dominant Expression Patterns , 2007, Science.

[64]  D. Christopher,et al.  The cyclic nucleotide gated cation channel AtCNGC10 traffics from the ER via Golgi vesicles to the plasma membrane of Arabidopsis root and leaf cells , 2007, BMC Plant Biology.

[65]  Nicholas J. Provart,et al.  An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets , 2007, PloS one.

[66]  S. Merlot,et al.  Constitutive activation of a plasma membrane H+‐ATPase prevents abscisic acid‐mediated stomatal closure , 2007, The EMBO journal.

[67]  D. Webb,et al.  The cyclic nucleotide-gated calmodulin-binding channel AtCNGC10 localizes to the plasma membrane and influences numerous growth responses and starch accumulation in Arabidopsis thaliana , 2007, Planta.

[68]  Mudita Singhal,et al.  COPASI - a COmplex PAthway SImulator , 2006, Bioinform..

[69]  Kris Vissenberg,et al.  The Root Apex of Arabidopsis thaliana Consists of Four Distinct Zones of Growth Activities , 2006, Plant signaling & behavior.

[70]  John M. Walker,et al.  Arabidopsis Protocols , 2006, Methods in Molecular Biology™.

[71]  Falk Schreiber,et al.  VANTED: A system for advanced data analysis and visualization in the context of biological networks , 2006, BMC Bioinformatics.

[72]  M. Palmgren,et al.  Regulation of Plant Plasma Membrane H+- and Ca2+-ATPases by Terminal Domains , 2005, Journal of bioenergetics and biomembranes.

[73]  J. Chory,et al.  Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1 , 2005, Nature.

[74]  Cathy H. Wu,et al.  The Universal Protein Resource (UniProt) , 2004, Nucleic Acids Res..

[75]  M. Palmgren,et al.  Energization of Transport Processes in Plants. Roles of the Plasma Membrane H+-ATPase1 , 2004, Plant Physiology.

[76]  B. André,et al.  K+ channel interactions detected by a genetic system optimized for systematic studies of membrane protein interactions. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[77]  A. Hager Role of the plasma membrane H+-ATPase in auxin-induced elongation growth: historical and new aspects , 2003, Journal of Plant Research.

[78]  F. Maathuis,et al.  Energization of potassium uptake in Arabidopsis thaliana , 1993, Planta.

[79]  S. Clouse Brassinosteroid signal transduction: clarifying the pathway from ligand perception to gene expression. , 2002, Molecular cell.

[80]  T. Altmann,et al.  Brassinosteroid-Regulated Gene Expression , 2002, Plant Physiology.

[81]  Dirk Inzé,et al.  GATEWAY vectors for Agrobacterium-mediated plant transformation. , 2002, Trends in plant science.

[82]  E. Blancaflor,et al.  Changes in Root Cap pH Are Required for the Gravity Response of the Arabidopsis Root , 2001, Plant Cell.

[83]  J. Chory,et al.  BRI1 is a critical component of a plasma-membrane receptor for plant steroids , 2001, Nature.

[84]  I. Newman,et al.  Ion transport in roots: measurement of fluxes using ion-selective microelectrodes to characterize transporter function. , 2001, Plant, cell & environment.

[85]  Daniel J. Cosgrove,et al.  Loosening of plant cell walls by expansins , 2000, Nature.

[86]  T. Hunter,et al.  Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. , 2000, Plant physiology.

[87]  Advanced patch-clamp techniques and single-channel analysis , 1999 .

[88]  B. Regenberg,et al.  C-terminal deletion analysis of plant plasma membrane H(+)-ATPase: yeast as a model system for solute transport across the plant plasma membrane. , 1995, The Plant cell.

[89]  R. Serrano,et al.  Identification of an autoinhibitory domain in the C-terminal region of the plant plasma membrane H(+)-ATPase. , 1991, The Journal of biological chemistry.

[90]  M. Palmgren Regulation of plant plasma membrane H+‐ATPase activity , 1991 .

[91]  Judith L. Flippen-Anderson,et al.  Plant Growth-Promoting Brassinosteroids , 1988 .

[92]  R. Cerana,et al.  Regulating effects of brassino steroids and of sterols on growth and H+ secretion in maize roots , 1984 .

[93]  R. Cerana,et al.  Effects of a brassinosteroid on growth and electrogenic proton extrusion in maize root segments , 1983 .

[94]  R. Cerana,et al.  Effects of a brassinosteroid on growth and electrogenic proton extrusion in Azuki bean epicotyls , 1983 .

[95]  日高 弘義,et al.  血小板のcyclic nucleotide (血小板) , 1976 .

[96]  N. Higinbotham Electropotentials of Plant Cells , 1973 .