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      Mechanical modelling quantifies the functional importance of outer tissue layers during root elongation and bending

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          Abstract

          • Root elongation and bending require the coordinated expansion of multiple cells of different types. These processes are regulated by the action of hormones that can target distinct cell layers. We use a mathematical model to characterise the influence of the biomechanical properties of individual cell walls on the properties of the whole tissue.

          • Taking a simple constitutive model at the cell scale which characterises cell walls via yield and extensibility parameters, we derive the analogous tissue-level model to describe elongation and bending. To accurately parameterise the model, we take detailed measurements of cell turgor, cell geometries and wall thicknesses.

          • The model demonstrates how cell properties and shapes contribute to tissue-level extensibility and yield. Exploiting the highly organised structure of the elongation zone (EZ) of the Arabidopsis root, we quantify the contributions of different cell layers, using the measured parameters. We show how distributions of material and geometric properties across the root cross-section contribute to the generation of curvature, and relate the angle of a gravitropic bend to the magnitude and duration of asymmetric wall softening.

          • We quantify the geometric factors which lead to the predominant contribution of the outer cell files in driving root elongation and bending.

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          Most cited references37

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          A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity.

          Lateral roots are formed at regular intervals along the main root by recurrent specification of founder cells. To date, the mechanism by which branching of the root system is controlled and founder cells become specified remains unknown. Our study reports the identification of the auxin regulatory components and their target gene, GATA23, which control lateral root founder cell specification. Initially, a meta-analysis of lateral root-related transcriptomic data identified the GATA23 transcription factor. GATA23 is expressed specifically in xylem pole pericycle cells before the first asymmetric division and is correlated with oscillating auxin signaling maxima in the basal meristem. Also, functional studies revealed that GATA23 controls lateral root founder cell identity. Finally, we show that an Aux/IAA28-dependent auxin signaling mechanism in the basal meristem controls GATA23 expression. We have identified the first molecular components that control lateral root founder cell identity in the Arabidopsis root. These include an IAA28-dependent auxin signaling module in the basal meristem region that regulates GATA23 expression and thereby lateral root founder cell specification and root branching patterns. Copyright © 2010 Elsevier Ltd. All rights reserved.
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            Anisotropic expansion of the plant cell wall.

            Plants shape their organs with a precision demanded by optimal function; organ shaping requires control over cell wall expansion anisotropy. Focusing on multicellular organs, I survey the occurrence of expansion anisotropy and discuss its causes and proposed controls. Expansion anisotropy of a unit area of cell wall is characterized by the direction and degree of anisotropy. The direction of maximal expansion rate is usually regulated by the direction of net alignment among cellulose microfibrils, which overcomes the prevailing stress anisotropy. In some stems, the directionality of expansion of epidermal cells is controlled by that of the inner tissue. The degree of anisotropy can vary widely as a function of position and of treatment. The degree of anisotropy is probably controlled by factors in addition to the direction of microfibril alignment. I hypothesize that rates of expansion in maximal and minimal directions are regulated by distinct molecular mechanisms that regulate interactions between matrix and microfibrils.
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              Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis.

              A genetic analysis of root development in Arabidopsis thaliana has identified mutants that have abnormal morphogenesis. Four of these root morphogenesis mutants show dramatic alterations in post-embryonic root development. The short-root mutation results in a change from indeterminate to determinate root growth and the loss of internal root cell layers. The cobra and lion's tail mutations cause abnormal root cell expansion which is conditional upon the rate of root growth. Expansion is greatest in the epidermal cells in cobra and in the stele cells in lion's tail. The sabre mutation causes abnormal cell expansion that is greatest in the root cortex cell layer and is independent of the root growth rate. The tissue-specific effects of these mutations were characterized with monoclonal antibodies and a transgenic marker line. Genetic combinations of the four mutants have provided insight into the regulation of growth and cell shape during Arabidopsis root development.
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                Author and article information

                Journal
                New Phytol
                New Phytol
                nph
                The New Phytologist
                BlackWell Publishing Ltd (Oxford, UK )
                0028-646X
                1469-8137
                June 2014
                18 March 2014
                : 202
                : 4
                : 1212-1222
                Affiliations
                [1 ]School of Mathematics, University of Birmingham Edgbaston, Birmingham, B15 2TT, UK
                [2 ]Centre for Ultrastructural Imaging, King's College London London, SE1 1UL, UK
                [3 ]Centre for Plant Integrative Biology, University of Nottingham Sutton Bonington, LE12 5RD, UK
                [4 ]School of Physics & Astronomy, University of Nottingham, University Park Nottingham, NG7 2RD, UK
                [5 ]School of Computer Science, University of Nottingham Jubilee Campus, Nottingham, NG8 1BB, UK
                [6 ]School of Biosciences, University of Nottingham Sutton Bonington, LE12 5RD, UK
                [7 ]School of Mathematics, University of Manchester Oxford Road, Manchester, M13 9PL, UK
                Author notes
                Author for correspondence: Rosemary J. Dyson Tel: +44 (0)121 4143415 Email: r.j.dyson@ 123456bham.ac.uk
                Article
                10.1111/nph.12764
                4286105
                24641449
                d0a5cce7-4428-41e1-9029-8928f30af4f1
                © 2014 The Authors. New Phytologist © 2014 New Phytologist Trust.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 18 October 2013
                : 02 February 2014
                Categories
                Research

                Plant science & Botany
                arabidopsis thaliana,elongation,extensibility,gravitropism,mechanical modelling,multiscale

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