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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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      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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        Auxin transport promotes Arabidopsis lateral root initiation.

        Lateral root development in Arabidopsis provides a model for the study of hormonal signals that regulate postembryonic organogenesis in higher plants. Lateral roots originate from pairs of pericycle cells, in several cell files positioned opposite the xylem pole, that initiate a series of asymmetric, transverse divisions. The auxin transport inhibitor N-1-naphthylphthalamic acid (NPA) arrests lateral root development by blocking the first transverse division(s). We investigated the basis of NPA action by using a cell-specific reporter to demonstrate that xylem pole pericycle cells retain their identity in the presence of the auxin transport inhibitor. However, NPA causes indoleacetic acid (IAA) to accumulate in the root apex while reducing levels in basal tissues critical for lateral root initiation. This pattern of IAA redistribution is consistent with NPA blocking basipetal IAA movement from the root tip. Characterization of lateral root development in the shoot meristemless1 mutant demonstrates that root basipetal and leaf acropetal auxin transport activities are required during the initiation and emergence phases, respectively, of lateral root development.
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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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            Author and article information

            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.

            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
            2577305
            08-PONE-RA-05704R2
            10.1371/journal.pone.0003673
            18989371
            (Editor)
            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.
            Counts
            Pages: 13
            Categories
            Research Article
            Computational Biology/Systems Biology
            Plant Biology/Plant Biochemistry and Physiology
            Plant Biology/Plant Growth and Development

            Uncategorized

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