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Plant development is a complex task, and many processes involve changes in the asymmetric subcellular distribution of cell components that strongly depend on cell polarity. Cell polarity regulates anisotropic growth and polar localization of membrane proteins and helps to identify the cell's position relative to its neighbors within an organ. Cell polarity is critical in a variety of plant developmental processes, including embryogenesis, cell division, and response to external stimuli. The most conspicuous downstream effect of cell polarity is the polar transport of the phytohormone auxin, which is the only known hormone transported in a polar fashion in and out of cells by specialized exporters and importers. The biological processes behind the establishment of cell polarity are still unknown, and researchers have proposed several models that have been tested using computer simulations. The evolution of computer models has progressed in tandem with scientific discoveries, which have highlighted the importance of genetic, chemical, and mechanical input in determining cell polarity and regulating polarity-dependent processes such as anisotropic growth, protein subcellular localization, and the development of organ shapes. The purpose of this review is to provide a comprehensive overview of the current understanding of computer models of cell polarity establishment in plants, focusing on the molecular and cellular mechanisms, the proteins involved, and the current state of the field. [ABSTRACT FROM AUTHOR]

Differential cell growth enables flexible organ bending in the presence of environmental signals such as light or gravity. A prominent example of the developmental processes based on differential cell growth is the formation of the apical hook that protects the fragile shoot apical meristem when it breaks through the soil during germination. Here, we combined in silico and in vivo approaches to identify a minimal mechanism producing auxin gradient-guided differential growth during the establishment of the apical hook in the model plant Arabidopsis thaliana. Computer simulation models based on experimental data demonstrate that asymmetric expression of the PIN-FORMED auxin efflux carrier at the concave (inner) versus convex (outer) side of the hook suffices to establish an auxin maximum in the epidermis at the concave side of the apical hook. Furthermore, we propose a mechanism that translates this maximum into differential growth, and thus curvature, of the apical hook. Through a combination of experimental and in silico computational approaches, we have identified the individual contributions of differential cell elongation and proliferation to defining the apical hook and reveal the role of auxin-ethylene crosstalk in balancing these two processes. [ABSTRACT FROM AUTHOR]

The stem cell niche in the root meristem plays a critical role during the development of plant root systems. The polar cell-to-cell transport generates the distribution maximum of the phytohormone auxin that plays a critical role during growth and patterning of roots. Recently, the transcription factor WOX5 (WUSCHEL-RELATED HOMEOBOX 5) was identified as a master regulator of root stem cell niche patterning. Here, we demonstrate that WOX5 coordinates local auxin production and thus controls spatial restriction and maintenance of the auxin maximum in the quiescent center (QC) of the root. In turn, this root-associated auxin maximum feeds back on WOX5 expression via IAA17-dependent regulation of auxin responses. Both our experimental studies and in silico computer modeling simulations suggest that the feedback circuit between WOX5 activity and auxin signaling maximum is at the heart of auxin-mediated root patterning.In plants, the patterning of stem cell-enriched meristems requires a graded auxin response maximum that emerges from the concerted action of polar auxin transport, auxin biosynthesis, auxin metabolism, and cellular auxin response machinery. However, mechanisms underlying this auxin response maximum-mediated root stem cell maintenance are not fully understood. Here, we present unexpected evidence that WUSCHEL-RELATED HOMEOBOX 5 (WOX5) transcription factor modulates expression of auxin biosynthetic genes in the quiescent center (QC) of the root and thus provides a robust mechanism for the maintenance of auxin response maximum in the root tip. This WOX5 action is balanced through the activity of indole-3-acetic acid 17 (IAA17) auxin response repressor. Our combined genetic, cell biology, and computational modeling studies revealed a previously uncharacterized feedback loop linking WOX5-mediated auxin production to IAA17-dependent repression of auxin responses. This WOX5–IAA17 feedback circuit further assures the maintenance of auxin response maximum in the root tip and thereby contributes to the maintenance of distal stem cell (DSC) populations. Our experimental studies and in silico computer simulations both demonstrate that the WOX5–IAA17 feedback circuit is essential for the maintenance of auxin gradient in the root tip and the auxin-mediated root DSC differentiation. [ABSTRACT FROM PUBLISHER]

Summary: The apical-basal axis of the early plant embryo determines the body plan of the adult organism. To establish a polarized embryonic axis, plants evolved a unique mechanism that involves directional, cell-to-cell transport of the growth regulator auxin. Auxin transport relies on PIN auxin transporters [1], whose polar subcellular localization determines the flow directionality. PIN-mediated auxin transport mediates the spatial and temporal activity of the auxin response machinery [2–7] that contributes to embryo patterning processes, including establishment of the apical (shoot) and basal (root) embryo poles [8]. However, little is known of upstream mechanisms guiding the (re)polarization of auxin fluxes during embryogenesis [9]. Here, we developed a model of plant embryogenesis that correctly generates emergent cell polarities and auxin-mediated sequential initiation of apical-basal axis of plant embryo. The model relies on two precisely localized auxin sources and a feedback between auxin and the polar, subcellular PIN transporter localization. Simulations reproduced PIN polarity and auxin distribution, as well as previously unknown polarization events during early embryogenesis. The spectrum of validated model predictions suggests that our model corresponds to a minimal mechanistic framework for initiation and orientation of the apical-basal axis to guide both embryonic and postembryonic plant development. [ABSTRACT FROM AUTHOR]

Carrier-dependent, intercellular auxin transport is central to the developmental patterning of higher plants (tracheophytes). The evolution of this polar auxin transport might be linked to the translocation of some PIN auxin efflux carriers from their presumably ancestral localization at the endoplasmic reticulum (ER) to the polar domains at the plasma membrane. Here we propose an eventually ancient mechanism of intercellular auxin distribution by ER-localized auxin transporters involving intracellular auxin retention and switch-like release from the ER. The proposed model integrates feedback circuits utilizing the conserved nuclear auxin signaling for the regulation of PIN transcription and a hypothetical ER-based signaling for the regulation of PIN-dependent transport activity at the ER. Computer simulations of the model revealed its plausibility for generating auxin channels and localized auxin maxima highlighting the possibility of this alternative mechanism for polar auxin transport. [Copyright &y& Elsevier]

Cell polarity reflected by asymmetric distribution of proteins at the plasma membrane is a fundamental feature of unicellular and multicellular organisms. It remains conceptually unclear how cell polarity is kept in cell wall-encapsulated plant cells. We have used super-resolution and semi-quantitative live-cell imaging in combination with pharmacological, genetic, and computational approaches to reveal insights into the mechanism of cell polarity maintenance in Arabidopsis thaliana.We show that polar-competent PIN transporters for the phytohormone auxin are delivered to the center of polar domains by super-polar recycling. Within the plasma membrane, PINs are recruited into non-mobile membrane clusters and their lateral diffusion is dramatically reduced, which ensures longer polar retention. At the circumventing edges of the polar domain, spatially defined internalization of escaped cargos occurs by clathrin-dependent endocytosis. Computer simulations confirm that the combination of these processes provides a robust mechanism for polarity maintenance in plant cells. Moreover, our study suggests that the regulation of lateral diffusion and spatially defined endocytosis, but not super-polar exocytosis have primary importance for PIN polarity maintenance. [ABSTRACT FROM AUTHOR]

Phytohormone auxin plays a key role in regulating plant organogenesis. However, understanding the complex feedback signaling network that involves at least 29 proteins in Arabidopsis in the dynamic context remains a significant challenge. To address this, we transplanted an auxin-responsive feedback circuit responsible for plant organogenesis into yeast. By generating dynamic microfluidic conditions controlling gene expression, protein degradation, and binding affinity of auxin response factors to DNA, we illuminate feedback signal processing principles in hormone-driven gene expression. In particular, we recorded the regulatory mode shift between stimuli counting and rapid signal integration that is context-dependent. Overall, our study offers mechanistic insights into dynamic auxin response interplay trackable by synthetic gene circuits, thereby offering instructions for engineering plant architecture. [ABSTRACT FROM AUTHOR]

Cells convert electrical signals into chemical outputs to facilitate the active transport of information across larger distances. This electrical-to-chemical conversion requires a tightly regulated expression of ion channels. Alterations of ion channel expression provide landmarks of numerous pathological diseases, such as cardiac arrhythmia, epilepsy, or cancer. Although the activity of ion channels can be locally regulated by external light or chemical stimulus, it remains challenging to coordinate the expression of ion channels on extended spatial-temporal scales. Here, we engineered yeast Saccharomyces cerevisiae to read and convert chemical concentrations into a dynamic potassium channel expression. A synthetic dual-feedback circuit controls the expression of engineered potassium channels through phytohormones auxin and salicylate to produce a macroscopically coordinated pulses of the plasma membrane potential. Our study provides a compact experimental model to control electrical activity through gene expression in eukaryotic cell populations setting grounds for various cellular engineering, synthetic biology, and potential therapeutic applications. [ABSTRACT FROM AUTHOR]

Plant development is exceptionally flexible as manifested by its potential for organogenesis and regeneration, which are processes involving rearrangements of tissue polarities. Fundamental questions concern how individual cells can polarize in a coordinated manner to integrate into the multicellular context. In canalization models, the signaling molecule auxin acts as a polarizing cue, and feedback on the intercellular auxin flow is key for synchronized polarity rearrangements. We provide a novel mechanistic framework for canalization, based on up-to-date experimental data and minimal, biologically plausible assumptions. Our model combines the intracellular auxin signaling for expression of PINFORMED (PIN) auxin transporters and the theoretical postulation of extracellular auxin signaling for modulation of PIN subcellular dynamics. Computer simulations faithfully and robustly recapitulated the experimentally observed patterns of tissue polarity and asymmetric auxin distribution during formation and regeneration of vascular systems and during the competitive regulation of shoot branching by apical dominance. Additionally, our model generated new predictions that could be experimentally validated, highlighting a mechanistically conceivable explanation for the PIN polarization and canalization of the auxin flow in plants. [ABSTRACT FROM AUTHOR]

Plants develop new organs to adjust their bodies to dynamic changes in the environment. How independent organs achieve anisotropic shapes and polarities is poorly understood. To address this question, we constructed a mechano-biochemical model for Arabidopsis root meristem growth that integrates biologically plausible principles. Computer model simulations demonstrate how differential growth of neighboring tissues results in the initial symmetry-breaking leading to anisotropic root growth. Furthermore, the root growth feeds back on a polar transport network of the growth regulator auxin. Model, predictions are in close agreement with in vivo patterns of anisotropic growth, auxin distribution, and cell polarity, as well as several root phenotypes caused by chemical, mechanical, or genetic perturbations. Our study demonstrates that the combination of tissue mechanics and polar auxin transport organizes anisotropic root growth and cell polarities during organ outgrowth. Therefore, a mobile auxin signal transported through immobile cells drives polarity and growth mechanics to coordinate complex organ development. [ABSTRACT FROM AUTHOR]

Availability of the essential macronutrient nitrogen in soil plays a critical role in plant growth, development, and impacts agricultural productivity. Plants have evolved different strategies for sensing and responding to heterogeneous nitrogen distribution. Modulation of root system architecture, including primary root growth and branching, is among the most essential plant adaptions to ensure adequate nitrogen acquisition. However, the immediate molecular pathways coordinating the adjustment of root growth in response to distinct nitrogen sources, such as nitrate or ammonium, are poorly understood. Here, we show that growth as manifested by cell division and elongation is synchronized by coordinated auxin flux between two adjacent outer tissue layers of the root. This coordination is achieved by nitrate‐dependent dephosphorylation of the PIN2 auxin efflux carrier at a previously uncharacterized phosphorylation site, leading to subsequent PIN2 lateralization and thereby regulating auxin flow between adjacent tissues. A dynamic computer model based on our experimental data successfully recapitulates experimental observations. Our study provides mechanistic insights broadening our understanding of root growth mechanisms in dynamic environments. SYNOPSIS: Effective soil exploitation by plants depends on rapid adjustment of root systems to available nutrients. Here, root growth adaptation to distinct nitrogen sources is shown to involve modulation of auxin distribution via phosphorylation of the PIN2 auxin carrier. Nitrogen source type (nitrate vs. ammonium) differentially regulates cell elongation and division patterns in Arabidopsis root tip tissues.Nitrogen source type regulates directionality of auxin transport in the root tip.Root growth adjustment to nitrogen source is mediated by PIN2 phosphorylation at S439.PIN2 phosphorylation affects auxin flux via modulation of PIN2 polarized localization at the plasma membrane. [ABSTRACT FROM AUTHOR]

Summary: Cell and tissue polarization is fundamental for plant growth and morphogenesis. The polar, cellular localization of Arabidopsis PIN‐FORMED (PIN) proteins is crucial for their function in directional auxin transport. The clustering of PIN polar cargoes within the plasma membrane has been proposed to be important for the maintenance of their polar distribution. However, the more detailed features of PIN clusters and the cellular requirements of cargo clustering remain unclear.Here, we characterized PIN clusters in detail by means of multiple advanced microscopy and quantification methods, such as 3D quantitative imaging or freeze‐fracture replica labeling. The size and aggregation types of PIN clusters were determined by electron microscopy at the nanometer level at different polar domains and at different developmental stages, revealing a strong preference for clustering at the polar domains.Pharmacological and genetic studies revealed that PIN clusters depend on phosphoinositol pathways, cytoskeletal structures and specific cell‐wall components as well as connections between the cell wall and the plasma membrane.This study identifies the role of different cellular processes and structures in polar cargo clustering and provides initial mechanistic insight into the maintenance of polarity in plants and other systems. [ABSTRACT FROM AUTHOR]

The article presents research report on auxin-regulable oscillatory circuit drives the root clock in Arabidopsis. Topics include how gene expression oscillations coordinate with cell division and growth to create the periodic pattern of organ spacing; and time course analyses of in-phase gene oscillations in the mutant showed a persistent signal in the oscillation zone (OZ).

How gene activities and biomechanics together direct organ shapes is poorly understood. Plant leaf and floral organs develop from highly similar initial structures and share similar gene expression patterns, yet they gain drastically different shapes later—flat and bilateral leaf primordia and radially symmetric floral primordia, respectively. We analyzed cellular growth patterns and gene expression in young leaves and flowers of Arabidopsis thaliana and found significant differences in cell growth rates, which correlate with convergence sites of phytohormone auxin that require polar auxin transport. In leaf primordia, the PRESSED - FLOWER -expressing middle domain grows faster than adjacent adaxial domain and coincides with auxin convergence. In contrast, in floral primordia, the LEAFY -expressing domain shows accelerated growth rates and pronounced auxin convergence. This distinct cell growth dynamics between leaf and flower requires changes in levels of cell-wall pectin de-methyl-esterification and mechanical properties of the cell wall. Data-driven computer model simulations at organ and cellular levels demonstrate that growth differences are central to obtaining distinct organ shape, corroborating in planta observations. Together, our study provides a mechanistic basis for the establishment of early aerial organ symmetries through local modulation of differential growth patterns with auxin and biomechanics. [Display omitted] • Leaf and floral primordia share similar gene expression and initial domain partition • Local growth-rate differences across domains explain primordia shape differences • Two primordia have different patterns of cell-wall rigidity and auxin convergence • When incorporating growth dynamics, models explain different organ shapes Peng et al. show that different growth dynamics determine the shape of plant aerial organs, leaf and floral primordia, which share similar initial geometry. Experiments and simulations are combined to link growth dynamics with biomechanics and polar auxin transport. [ABSTRACT FROM AUTHOR]

Auxin and brassinosteroids (BR) are crucial growth regulators and display overlapping functions during plant development. Here, we reveal an alternative phytohormone crosstalk mechanism, revealing that BR signaling controls PIN-LIKES (PILS)-dependent nuclear abundance of auxin. We performed a forward genetic screen for imperial pils (imp) mutants that enhance the overexpression phenotypes of PILS5 putative intracellular auxin transport facilitator. Here, we report that the imp1 mutant is defective in the BR-receptor BRASSINOSTEROID INSENSITIVE 1 (BRI1). Our set of data reveals that BR signaling transcriptionally and post-translationally represses the accumulation of PILS proteins at the endoplasmic reticulum, thereby increasing nuclear abundance and signaling of auxin. We demonstrate that this alternative phytohormonal crosstalk mechanism integrates BR signaling into auxin-dependent organ growth rates and likely has widespread importance for plant development. • Impaired BR perception enhances PILS5 overexpression phenotypes • BR signaling increases PILS protein turnover • BR signaling defines PILS-dependent nuclear abundance and signaling of auxin • PILS-dependent BR-auxin crosstalk affects organ growth Sun et al. reveal that BR signaling limits the accumulation of PILS proteins at the endoplasmic reticulum, thereby increasing nuclear abundance and signaling of auxin. This alternative phytohormonal crosstalk mechanism integrates BR signaling into auxin-dependent organ growth rates and likely has widespread importance for plant development. [ABSTRACT FROM AUTHOR]