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      An Auxin Transport-Based Model of Root Branching in Arabidopsis thaliana

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          Abstract

          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 phyllotactic 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 rythms 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.

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          Most cited references27

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          Local, efflux-dependent auxin gradients as a common module for plant organ formation.

          Plants, compared to animals, exhibit an amazing adaptability and plasticity in their development. This is largely dependent on the ability of plants to form new organs, such as lateral roots, leaves, and flowers during postembryonic development. Organ primordia develop from founder cell populations into organs by coordinated cell division and differentiation. Here, we show that organ formation in Arabidopsis involves dynamic gradients of the signaling molecule auxin with maxima at the primordia tips. These gradients are mediated by cellular efflux requiring asymmetrically localized PIN proteins, which represent a functionally redundant network for auxin distribution in both aerial and underground organs. PIN1 polar localization undergoes a dynamic rearrangement, which correlates with establishment of auxin gradients and primordium development. Our results suggest that PIN-dependent, local auxin gradients represent a common module for formation of all plant organs, regardless of their mature morphology or developmental origin.
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            The auxin influx carrier LAX3 promotes lateral root emergence.

            Lateral roots originate deep within the parental root from a small number of founder cells at the periphery of vascular tissues and must emerge through intervening layers of tissues. We describe how the hormone auxin, which originates from the developing lateral root, acts as a local inductive signal which re-programmes adjacent cells. Auxin induces the expression of a previously uncharacterized auxin influx carrier LAX3 in cortical and epidermal cells directly overlaying new primordia. Increased LAX3 activity reinforces the auxin-dependent induction of a selection of cell-wall-remodelling enzymes, which are likely to promote cell separation in advance of developing lateral root primordia.
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              Organization and cell differentiation in lateral roots of Arabidopsis thaliana.

              Lateral root formation in plants involves the stimulation of mature pericycle cells to proliferate and redifferentiate to create a new organ. The simple organization of the root of Arabidopsis thaliana allows the development of lateral root primordia to be characterized histologically. We have divided the process of lateral root development into 8 stages defined by specific anatomical characteristics and cell divisions. To identify the cell types in the developing primordium we have generated a collection of marker lines that express beta-glucuronidase in a tissue- or cell type-specific manner in the root. Using these tools we have constructed a model describing the lineage of each cell type in the lateral root. These studies show that organization and cell differentiation in the lateral root primordia precede the appearance of a lateral root meristem, with differential gene expression apparent after the first set of divisions of the pericycle.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2008
                19 November 2008
                : 3
                : 11
                : e3673
                Affiliations
                [1 ]IRD, UMR DIAPC (INRA/IRD/Montpellier SupAgro/UM2), Equipe Rhizogenèse, Montpellier, France
                [2 ]INRIA, UMR DAP (CIRAD/INRIA/INRA/Montpellier SupAgro/UM2), Virtual Plants, Montpellier, France
                [3 ]Université Montpellier II, UMR DIAPC (INRA/IRD/Montpellier SupAgro/UM2), Equipe Rhizogenèse, Montpellier, France
                University of Nottingham, United Kingdom
                Author notes

                Conceived and designed the experiments: ML YG CJA CG LL. Performed the experiments: ML YG CJA CG LL. Analyzed the data: ML YG CJA CG LL. Wrote the paper: ML YG CG LL.

                Article
                08-PONE-RA-05704R2
                10.1371/journal.pone.0003673
                2577305
                18989371
                b090243b-7f05-4b89-b6fe-46e8071144cf
                Lucas et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 29 July 2008
                : 21 October 2008
                Page count
                Pages: 13
                Categories
                Research Article
                Computational Biology/Systems Biology
                Plant Biology/Plant Biochemistry and Physiology
                Plant Biology/Plant Growth and Development

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