Toward a 3D model of phyllotaxis based on a biochemically plausible auxin-transport mechanism.
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ABSTRACT:
SUBMITTER: Hartmann FP
PROVIDER: S-EPMC6490938 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Recent studies show that plant organ positioning may be mediated by localized concentrations of the plant hormone auxin. Auxin patterning in the shoot apical meristem is in turn brought about by the subcellular polar distribution of the putative auxin efflux mediator, PIN1. However, the question of what signals determine PIN1 polarization and how this gives rise to regular patterns of auxin concentration remains unknown. Here we address these questions by using mathematical modeling combined with confocal imaging. We propose a model that is based on the assumption that auxin influences the polarization of its own efflux within the meristem epidermis. We show that such a model is sufficient to create regular spatial patterns of auxin concentration on systems with static and dynamic cellular connectivities, the latter governed by a mechanical model. We also optimize parameter values for the PIN1 dynamics by using a detailed auxin transport model, for which parameter values are taken from experimental estimates, together with a template consisting of cell and wall compartments as well as PIN1 concentrations quantitatively extracted from confocal data. The model shows how polarized transport can drive the formation of regular patterns.
| S-EPMC1326488 | biostudies-literature
Project description:A striking phenomenon unique to the kingdom of plants is the regular arrangement of lateral organs around a central axis, known as phyllotaxis. Recent molecular-genetic experiments indicate that active transport of the plant hormone auxin is the key process regulating phyllotaxis. A conceptual model based on these experiments, introduced by Reinhardt et al. [Reinhardt, D., Pesce, E. R., Stieger, P., Mandel, T., Baltensperger, K., et al. (2003) Nature 426, 255-260], provides an intuitively plausible interpretation of the data, but raises questions of whether the proposed mechanism is, in fact, capable of producing the observed temporal and spatial patterns, is robust, can start de novo, and can account for phyllotactic transitions, such as the frequently observed transition from decussate to spiral phyllotaxis. To answer these questions, we created a computer simulation model based on data described previously or in this paper and reasonable hypotheses. The model reproduces, within the standard error, the divergence angles measured in Arabidopsis seedlings and the effects of selected experimental manipulations. It also reproduces distichous, decussate, and tricussate patterns. The model thus offers a plausible link between molecular mechanisms of morphogenesis and the geometry of phyllotaxis.
| S-EPMC1345713 | biostudies-literature
Project description:Plants continuously generate new organs through the activity of populations of stem cells called meristems. The shoot apical meristem initiates leaves, flowers, and lateral meristems in highly ordered, spiralled, or whorled patterns via a process called phyllotaxis. It is commonly accepted that the active transport of the plant hormone auxin plays a major role in this process. Current hypotheses propose that cellular hormone transporters of the PIN family would create local auxin maxima at precise positions, which in turn would lead to organ initiation. To explain how auxin transporters could create hormone fluxes to distinct regions within the plant, different concepts have been proposed. A major hypothesis, canalization, proposes that the auxin transporters act by amplifying and stabilizing existing fluxes, which could be initiated, for example, by local diffusion. This convincingly explains the organised auxin fluxes during vein formation, but for the shoot apical meristem a second hypothesis was proposed, where the hormone would be systematically transported towards the areas with the highest concentrations. This implies the coexistence of two radically different mechanisms for PIN allocation in the membrane, one based on flux sensing and the other on local concentration sensing. Because these patterning processes require the interaction of hundreds of cells, it is impossible to estimate on a purely intuitive basis if a particular scenario is plausible or not. Therefore, computational modelling provides a powerful means to test this type of complex hypothesis. Here, using a dedicated computer simulation tool, we show that a flux-based polarization hypothesis is able to explain auxin transport at the shoot meristem as well, thus providing a unifying concept for the control of auxin distribution in the plant. Further experiments are now required to distinguish between flux-based polarization and other hypotheses.
| S-EPMC2565506 | biostudies-literature
Project description:BackgroundIn 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 Arabidopsis, 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.ResultsWe propose a reflected flow 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 Division Factor 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.ConclusionWe 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 reverse fountain has not yet been formed or has been disrupted. In addition, the proximal maxima are formed under the reflected flow 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 reflected flow 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.
| S-EPMC2921385 | biostudies-literature
Project description:Null models for the effect of combination therapies are widely used to evaluate synergy and antagonism of drugs. Due to the relevance of null models, their suitability is continuously discussed. Here, we contribute to the discussion by investigating the properties of five null models. Our study includes the model proposed by David J. Hand, which we refer to as Hand model. The Hand model has been introduced almost 20 years ago but hardly was used and studied. We show that the Hand model generalizes the principle of dose equivalence compared to the Loewe model and resolves the ambiguity of the Tallarida model. This provides a solution to the persisting conflict about the compatibility of two essential model properties: the sham combination principle and the principle of dose equivalence. By embedding several null models into a common framework, we shed light in their biochemical validity and provide indications that the Hand model is biochemically most plausible. We illustrate the practical implications and differences between null models by examining differences of null models on published data.
| S-EPMC6395630 | biostudies-literature
Project description:Root architecture is a crucial part of plant adaptation to soil heterogeneity and is mainly controlled by root branching. The process of root system development can be divided into two successive steps: lateral root initiation and lateral root development/emergence which are controlled by different fluxes of the plant hormone auxin. While shoot architecture appears to be highly regular, following rules such as the phyllotactical spiral, root architecture appears more chaotic. We used stochastic modeling to extract hidden rules regulating root branching in Arabidopsis thaliana. These rules were used to build an integrative mechanistic model of root ramification based on auxin. This model was experimentally tested using plants with modified rhythm of lateral root initiation or mutants perturbed in auxin transport. Our analysis revealed that lateral root initiation and lateral root development/emergence are interacting with each other to create a global balance between the respective ratio of initiation and emergence. A mechanistic model based on auxin fluxes successfully predicted this property and the phenotype alteration of auxin transport mutants or plants with modified rhythms of lateral root initiation. This suggests that root branching is controlled by mechanisms of lateral inhibition due to a competition between initiation and development/emergence for auxin.
| S-EPMC2577305 | biostudies-literature
Project description:Here we discuss the formation of phyllotactic patterns in the shoot apical meristem (SAM) of plants, where the spatial distribution of the phytohormone auxin determines phyllotaxis in a domain that is growing and changing in time. We assume that the concentration of auxin modifies the mechanical properties of the domain and that the mechanical stress field in the SAM orients the flux of auxin. To study this problem we propose a mechanism for pattern formation in growing domains with variable curvature. The dynamics of chemicals is modeled by a reaction-diffusion system that produces a three dimensional pattern of chemical concentrations that changes the stress field in the domain while growing. The growth process is modeled by a phase-field order parameter which determines the location of the boundaries of the domain. This field is coupled to the chemical concentration through a curvature term that affects the local mechanical stress in the domain. The local stress changes in turn modify the chemical patterns. Our model constitutes a useful and novel approach in theoretical biology, as many developmental processes in organisms seem to be affected by the changes of curvature, size, mechanical stress and other physical aspects. Several patterns seen in many plants are reproduced under certain conditions by our model.
| S-EPMC6095518 | biostudies-literature
Project description:Language-related event-related potential (ERP) components such as the N400 have traditionally been associated with linguistic or cognitive functional interpretations. By contrast, it has been considerably more difficult to relate these components to neurobiologically grounded accounts of language. Here, we propose a theoretical framework based on a predictive coding architecture, within which negative language-related ERP components such as the N400 can be accounted for in a neurobiologically plausible manner. Specifically, we posit that the amplitude of negative language-related ERP components reflects precision-weighted prediction error signals, i.e., prediction errors weighted by the relevance of the information source leading to the error. From this perspective, precision has a direct link to cue validity in a particular language and, thereby, to relevance of individual linguistic features for internal model updating. We view components such as the N400 and LAN as members of a family with similar functional characteristics and suggest that latency and topography differences between these components reflect the locus of prediction errors and model updating within a hierarchically organized cortical predictive coding architecture. This account has the potential to unify findings from the full range of the N400 literature, including word-level, sentence-, and discourse-level results as well as cross-linguistic differences.
| S-EPMC6393377 | biostudies-literature
Project description:Lateral organ distribution at the shoot apical meristem defines specific and robust phyllotaxis patterns that have intrigued biologists and mathematicians for centuries. In silico studies have revealed that this self-organizing process can be recapitulated by modeling the polar transport of the phytohormone auxin. Phyllotactic patterns change between species and developmental stages, but the processes behind these variations have remained unknown. Here we use regional complementation experiments to reveal that phyllotactic switches in Arabidopsis shoots can be mediated by PLETHORA-dependent control of local auxin biosynthesis.
| S-EPMC3549086 | biostudies-other
Project description:The periodic formation of plant organs such as leaves and flowers gives rise to intricate patterns that have fascinated biologists and mathematicians alike for hundreds of years [1]. The plant hormone auxin plays a central role in establishing these patterns by promoting organ formation at sites where it accumulates due to its polar, cell-to-cell transport [2-6]. Although experimental evidence as well as modeling suggest that feedback from auxin to its transport direction may help specify phyllotactic patterns [7-12], the nature of this feedback remains unclear [13]. Here we reveal that polarization of the auxin efflux carrier PIN-FORMED 1 (PIN1) is regulated by the auxin response transcription factor MONOPTEROS (MP) [14]. We find that in the shoot, cell polarity patterns follow MP expression, which in turn follows auxin distribution patterns. By perturbing MP activity both globally and locally, we show that localized MP activity is necessary for the generation of polarity convergence patterns and that localized MP expression is sufficient to instruct PIN1 polarity directions non-cell autonomously, toward MP-expressing cells. By expressing MP in the epidermis of mp mutants, we further show that although MP activity in a single-cell layer is sufficient to promote polarity convergence patterns, MP in sub-epidermal tissues helps anchor these polarity patterns to the underlying cells. Overall, our findings reveal a patterning module in plants that determines organ position by orienting transport of the hormone auxin toward cells with high levels of MP-mediated auxin signaling. We propose that this feedback process acts broadly to generate periodic plant architectures.
| S-EPMC5154752 | biostudies-literature