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      EXPANSIN A1-mediated radial swelling of pericycle cells positions anticlinal cell divisions during lateral root initiation

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          Organ formation is an essential process in plants and animals, driven by cell division and cell identity establishment. Root branching where lateral roots form along the primary root axis increases the root system and aids the capture of water and nutrients. We have discovered that tight control of the cell width is necessary to coordinate asymmetric cell divisions in cells that give rise to a new lateral root organ. Although biomechanical processes have been shown to play a role in plant organogenesis, including lateral root formation, our data give mechanistic insights into cell size control during lateral root initiation.

          Abstract

          In plants, postembryonic formation of new organs helps shape the adult organism. This requires the tight regulation of when and where a new organ is formed and a coordination of the underlying cell divisions. To build a root system, new lateral roots are continuously developing, and this process requires the tight coordination of asymmetric cell division in adjacent pericycle cells. We identified EXPANSIN A1 (EXPA1) as a cell wall modifying enzyme controlling the divisions marking lateral root initiation. Loss of EXPA1 leads to defects in the first asymmetric pericycle cell divisions and the radial swelling of the pericycle during auxin-driven lateral root formation. We conclude that a localized radial expansion of adjacent pericycle cells is required to position the asymmetric cell divisions and generate a core of small daughter cells, which is a prerequisite for lateral root organogenesis.

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          Lateral root development in Arabidopsis: fifty shades of auxin.

          The developmental plasticity of the root system represents a key adaptive trait enabling plants to cope with abiotic stresses such as drought and is therefore important in the current context of global changes. Root branching through lateral root formation is an important component of the adaptability of the root system to its environment. Our understanding of the mechanisms controlling lateral root development has progressed tremendously in recent years through research in the model plant Arabidopsis thaliana (Arabidopsis). These studies have revealed that the phytohormone auxin acts as a common integrator to many endogenous and environmental signals regulating lateral root formation. Here, we review what has been learnt about the myriad roles of auxin during lateral root formation in Arabidopsis. Copyright © 2013 Elsevier Ltd. All rights reserved.
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            Auxin control of root development.

            A plant's roots system determines both the capacity of a sessile organism to acquire nutrients and water, as well as providing a means to monitor the soil for a range of environmental conditions. Since auxins were first described, there has been a tight connection between this class of hormones and root development. Here we review some of the latest genetic, molecular, and cellular experiments that demonstrate the importance of generating and maintaining auxin gradients during root development. Refinements in the ability to monitor and measure auxin levels in root cells coupled with advances in our understanding of the sources of auxin that contribute to these pools represent important contributions to our understanding of how this class of hormones participates in the control of root development. In addition, we review the role of identified molecular components that convert auxin gradients into local differentiation events, which ultimately defines the root architecture.
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              Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis.

              Tissue mechanics have been shown to play a key role in the regulation of morphogenesis in animals [1-4] and may have an equally important role in plants [5-9]. The aerial organs of plants are formed at the shoot apical meristem following a specific phyllotactic pattern [10]. The initiation of an organ from the meristem requires a highly localized irreversible surface deformation, which depends on the demethylesterification of cell wall pectins [11]. Here, we used atomic force microscopy (AFM) to investigate whether these chemical changes lead to changes in tissue mechanics. By mapping the viscoelasticity and elasticity in living meristems, we observed increases in tissue elasticity, correlated with pectin demethylesterification, in primordia and at the site of incipient organs. Measurements of tissue elasticity at various depths showed that, at the site of incipient primordia, the first increases occurred in subepidermal tissues. The results support the following causal sequence of events: (1) demethylesterification of pectin is triggered in subepidermal tissue layers, (2) this contributes to an increase in elasticity of these layers-the first observable mechanical event in organ initiation, and (3) the process propagates to the epidermis during the outgrowth of the organ. Copyright © 2011 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                23 April 2019
                3 April 2019
                3 April 2019
                : 116
                : 17
                : 8597-8602
                Affiliations
                [1] aSchool of Biosciences, University of Nottingham , Sutton Bonington LE12 5RD, United Kingdom;
                [2] bCentre for Plant Integrative Biology, University of Nottingham , Sutton Bonington LE12 5RD, United Kingdom;
                [3] cCenter for Organismal Studies, Heidelberg University , 69120 Heidelberg, Germany;
                [4] dNanoscale and Microscale Research Centre, University of Nottingham , Nottingham NG7 2RD, United Kingdom;
                [5] eDepartment of Plant Biotechnology and Bioinformatics, Ghent University , B-9052 Ghent, Belgium;
                [6] fCenter for Plant Systems Biology, VIB , B-9052 Ghent, Belgium;
                [7] gVIB-UGent Center for Medical Biotechnology , B-9000 Ghent, Belgium;
                [8] hDepartment of Biomolecular Medicine, Ghent University , B-9000 Ghent, Belgium;
                [9] iDepartment of Plant and Environmental Sciences, University of Copenhagen , 1871 Frederiksberg C, Denmark
                Author notes
                4To whom correspondence may be addressed. Email: alexis.maizel@ 123456cos.uni-heidelberg.de or ivsme@ 123456psb.vib-ugent.be .

                Edited by Philip N. Benfey, Duke University, Durham, NC, and approved March 6, 2019 (received for review December 22, 2018)

                Author contributions: P.R., A.M., and I.D.S. designed research; P.R., P.R.D., G.A.R., M.S., V.V., L.D.V., E.M., A.V.B., K.S., K.M., B.J., B.v.d.C., T.G., and I.D.S. performed research; Z.L. contributed new reagents/analytic tools; P.R., U.V., T.B., M.J.B., K.G., A.M., and I.D.S. analyzed data; and P.R., A.M., and I.D.S. wrote the paper.

                1Present address: Department of Botany and Plant Biology, University of Geneva, 1211 Geneva, Switzerland.

                2Present address: Division of Biological Science, Graduate School of Science and Technology, Nara Institute of Science and Technology, 630-0192 Nara, Japan.

                3A.M. and I.D.S. contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-7371-6806
                http://orcid.org/0000-0001-8656-2060
                http://orcid.org/0000-0003-0475-390X
                http://orcid.org/0000-0001-6843-1059
                http://orcid.org/0000-0003-4607-8893
                Article
                201820882
                10.1073/pnas.1820882116
                6486723
                30944225
                bd666d20-0b2b-42d2-809c-618dc4080b08
                Copyright © 2019 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 6
                Funding
                Funded by: RCUK | Biotechnology and Biological Sciences Research Council (BBSRC) 501100000268
                Award ID: BB_BB/H022457/1
                Award Recipient : Ive De Smet
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: FOR2581
                Award Recipient : Alexis Maizel
                Funded by: Marie Curie European Reintegration Grant
                Award ID: PERG06-GA-2009-256354
                Award Recipient : Ive De Smet
                Categories
                Biological Sciences
                Plant Biology

                lateral root development,cell wall remodeling,expansin a1,radial cell expansion,arabidopsis thaliana

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