A plausible mechanism for auxin patterning along the developing root

<p>Abstract</p> <p>Background</p> <p>In plant roots, auxin is critical for patterning and morphogenesis. It regulates cell elongation and division, the development and maintenance of root apical meristems, and other processes. In <it>Arabidopsis</it>, auxin distribution along the central root axis has several maxima: in the root tip, in the basal meristem and at the shoot/root junction. The distal maximum in the root tip maintains the stem cell niche. Proximal maxima may trigger lateral or adventitious root initiation.</p> <p>Results</p> <p>We propose a <it>reflected flow </it>mechanism for the formation of the auxin maximum in the root apical meristem. The mechanism is based on auxin's known activation and inhibition of expressed PIN family auxin carriers at low and high auxin levels, respectively. Simulations showed that these regulatory interactions are sufficient for self-organization of the auxin distribution pattern along the central root axis under varying conditions. The mathematical model was extended with rules for discontinuous cell dynamics so that cell divisions were also governed by auxin, and by another morphogen <it>Division Factor </it>which combines the actions of cytokinin and ethylene on cell division in the root. The positional information specified by the gradients of these two morphogens is able to explain root patterning along the central root axis.</p> <p>Conclusion</p> <p>We present here a plausible mechanism for auxin patterning along the developing root, that may provide for self-organization of the distal auxin maximum when the <it>reverse fountain </it>has not yet been formed or has been disrupted. In addition, the proximal maxima are formed under the <it>reflected flow </it>mechanism in response to periods of increasing auxin flow from the growing shoot. These events may predetermine lateral root initiation in a rhyzotactic pattern. Another outcome of the <it>reflected flow </it>mechanism - the predominance of lateral or adventitious roots in different plant species - may be based on the different efficiencies with which auxin inhibits its own transport in different species, thereby distinguishing two main types of plant root architecture: taproot vs. fibrous.</p

Combined in silico/in vivo analysis of mechanisms providing for root apical meristem self-organization and maintenance.

Background and aimsThe root apical meristem (RAM) is the plant stem cell niche which provides for the formation and continuous development of the root. Auxin is the main regulator of RAM functioning, and auxin maxima coincide with the sites of RAM initiation and maintenance. Auxin gradients are formed due to local auxin biosynthesis and polar auxin transport. The PIN family of auxin transporters plays a critical role in polar auxin transport, and two mechanisms of auxin maximum formation in the RAM based on PIN-mediated auxin transport have been proposed to date: the reverse fountain and the reflected flow mechanisms.MethodsThe two mechanisms are combined here in in silico studies of auxin distribution in intact roots and roots cut into two pieces in the proximal meristem region. In parallel, corresponding experiments were performed in vivo using DR5::GFP Arabidopsis plants.Key resultsThe reverse fountain and the reflected flow mechanism naturally cooperate for RAM patterning and maintenance in intact root. Regeneration of the RAM in decapitated roots is provided by the reflected flow mechanism. In the excised root tips local auxin biosynthesis either alone or in cooperation with the reverse fountain enables RAM maintenance.ConclusionsThe efficiency of a dual-mechanism model in guiding biological experiments on RAM regeneration and maintenance is demonstrated. The model also allows estimation of the concentrations of auxin and PINs in root cells during development and under various treatments. The dual-mechanism model proposed here can be a powerful tool for the study of several different aspects of auxin function in root

Callose homeostasis at plasmodesmata: molecular regulators and developmental relevance

Plasmodesmata are membrane-lined channels that are located in the plant cell wall and that physically interconnect the cytoplasm and the endoplasmic reticulum (ER) of adjacent cells. Operating as controllable gates, plasmodesmata regulate the symplastic trafficking of micro- and macromolecules, such as endogenous proteins [transcription factors (TFs)] and RNA-based signals (mRNA, siRNA, etc.), hence mediating direct cell-to-cell communication and long distance signaling. Besides this physiological role, plasmodesmata also form gateways through which viral genomes can pass, largely facilitating the pernicious spread of viral infections. Plasmodesmatal trafficking is either passive (e.g., diffusion) or active and responses both to developmental and environmental stimuli. In general, plasmodesmatal conductivity is regulated by the controlled build-up of callose at the plasmodesmatal neck, largely mediated by the antagonistic action of callose synthases (CalSs) and beta-1,3-glucanases. Here, in this theory and hypothesis paper, we outline the importance of callose metabolism in PD SEL control, and highlight the main molecular factors involved. In addition, we also review other proteins that regulate symplastic PD transport, both in a developmental and stress-responsive framework, and discuss on their putative role in the modulation of PD callose turn-over. Finally, we hypothesize on the role of structural sterols in the regulation of (PD) callose deposition and outline putative mechanisms by which this regulation may occur

Mathematical Modelling of Auxin Transport in Plant Tissues:Flux Meets Signalling and Growth

Plant hormone auxin has critical roles in plant growth, dependent on its heterogeneous distribution in plant tissues. Exactly how auxin transport and developmental processes such as growth coordinate to achieve the precise patterns of auxin observed experimentally is not well understood. Here we use mathematical modelling to examine the interplay between auxin dynamics and growth and their contribution to formation of patterns in auxin distribution in plant tissues. Mathematical models describing the auxin-related signalling pathway, PIN and AUX1 dynamics, auxin transport, and cell growth in plant tissues are derived. A key assumption of our models is the regulation of PIN proteins by the auxin-responsive ARF-Aux/IAA signalling pathway, with upregulation of PIN biosynthesis by ARFs. Models are analysed and solved numerically to examine the long-time behaviour and auxin distribution. Changes in auxin-related signalling processes are shown to be able to trigger transition between passage and spot type patterns in auxin distribution. The model was also shown to be able to generate isolated cells with oscillatory dynamics in levels of components of the auxin signalling pathway which could explain oscillations in levels of ARF targets that have been observed experimentally. Cell growth was shown to have influence on PIN polarisation and determination of auxin distribution patterns. Numerical simulation results indicate that auxin-related signalling processes can explain the different patterns in auxin distributions observed in plant tissues, whereas the interplay between auxin transport and growth can explain the `reverse-fountain' pattern in auxin distribution observed at plant root tips

Alignment between PIN1 Polarity and Microtubule Orientation in the Shoot Apical Meristem Reveals a Tight Coupling between Morphogenesis and Auxin Transport

Morphogenesis during multicellular development is regulated by intercellular signaling molecules as well as by the mechanical properties of individual cells. In particular, normal patterns of organogenesis in plants require coordination between growth direction and growth magnitude. How this is achieved remains unclear. Here we show that in Arabidopsis thaliana, auxin patterning and cellular growth are linked through a correlated pattern of auxin efflux carrier localization and cortical microtubule orientation. Our experiments reveal that both PIN1 localization and microtubule array orientation are likely to respond to a shared upstream regulator that appears to be biomechanical in nature. Lastly, through mathematical modeling we show that such a biophysical coupling could mediate the feedback loop between auxin and its transport that underlies plant phyllotaxis

Theoretical approaches to understanding root vascular patterning: a consensus between recent models

The root vascular tissues provide an excellent system for studying organ patterning, as the specification of these tissues signals a transition from radial symmetry to bisymmetric patterns. The patterning process is controlled by the combined action of hormonal signaling/transport pathways, transcription factors, and miRNA that operate through a series of non-linear pathways to drive pattern formation collectively. With the discovery of multiple components and feedback loops controlling patterning, it has become increasingly difficult to understand how these interactions act in unison to determine pattern formation in multicellular tissues. Three independent mathematical models of root vascular patterning have been formulated in the last few years, providing an excellent example of how theoretical approaches can complement experimental studies to provide new insights into complex systems. In many aspects these models support each other; however, each study also provides its own novel findings and unique viewpoints. Here we reconcile these models by identifying the commonalities and exploring the differences between them by testing how transferable findings are between models. New simulations herein support the hypothesis that an asymmetry in auxin input can direct the formation of vascular pattern. We show that the xylem axis can act as a sole source of cytokinin and specify the correct pattern, but also that broader patterns of cytokinin production are also able to pattern the root. By comparing the three modelling approaches, we gain further insight into vascular patterning and identify several key areas for experimental investigatio

Modeling auxin feedback signaling for polarized auxin transport in plant development

Plants are fascinating biological systems with a great potential for adaption of their developmental programs to environmental cues. In contrast to animals, plants cannot run away and thus they had to develop specialized mechanisms to react to rapid changes in the environment. These plant-specific mechanisms including light perception, tropism and developmental reprogramming (de novo organ formation, tissue re-shaping), represent highly dynamic regulatory processes that are linked and intertwined on the molecular, cellular and tissue levels. The ultimate communication between these different levels is the key to understand how plants realize their developmental decisions. Cell signaling, tissue polarization, directional transport of signaling molecules within tissues are among those biological processes that allow for such multilevel organization in plant development. Nevertheless our understanding of these processes remains largely elusive. This doctoral thesis demonstrates the results of multidisciplinary studies at the interface between several scientific disciplines, including mathematics, computer science (under supervision of Prof. Willy Govaerts) and cell and developmental biology (under guidance of Prof. Jiří Friml). Therefore, I will utilize state-of-the-art mathematical and computational techniques combined with the most recent biological data to address cell and tissue polarities as well as graded distribution patterns of the plant phytohormone auxin, in the context of plant developmental flexibility. The main goal of the research presented herein was to explore general principles of auxin feedback regulation and its outstanding roles in auxin-driven plant development. A special focus was given to the combination of local auxin signaling cues (inside and outside of the cell), subcellular dynamics (trafficking of auxin carriers) and cell-type specific factors (spatial patterns of gene activity) to account for the developmental patterns observed in planta such as canalization of auxin transport, leaf venation patterning, tissue regeneration and establishment and maintenance of cell and tissue polarities. The core of the thesis will start with a general introduction to the models for auxin-mediated plant development and will be followed by presentation of various scientific results and their potential implications for hopefully better understanding of patterning mechanisms in plants. Finally, the summarizing chapter of this thesis aims to translate the results of these various studies to the more general concept of the local auxin feedback regulation in plants

Systems Biology Approach Pinpoints Minimum Requirements for Auxin Distribution during Fruit Opening : Plant Systems Biology

The phytohormone auxin is implied in steering various developmental decisions during plant morphogenesis in a concentration-dependent manner. Auxin maxima have been shown to maintain meristematic activity, for example, of the root apical meristem, and position new sites of outgrowth, such as during lateral root initiation and phyllotaxis. More recently, it has been demonstrated that sites of auxin minima also provide positional information. In the developing Arabidopsis fruit, auxin minima are required for correct differentiation of the valve margin. It remains unclear, however, how this auxin minimum is generated and maintained. Here, we employ a systems biology approach to model auxin transport based on experimental observations. This allows us to determine the minimal requirements for its establishment. Our simulations reveal that two alternative processes—which we coin “flux-barrier” and “flux-passage”—are both able to generate an auxin minimum, but under different parameter settings. Both models are in principle able to yield similar auxin profiles but present qualitatively distinct patterns of auxin flux. The models were tested by tissue-specific inducible ablation, revealing that the auxin minimum in the fruit is most likely generated by a flux-passage process. Model predictions were further supported through 3D PIN localization imaging and implementing experimentally observed transporter localization. Through such an experimental–modeling cycle, we predict how the auxin minimum gradually matures during fruit development to ensure timely fruit opening and seed dispersal.Peer reviewe