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      Auxin‐dependent regulation of cell division rates governs root thermomorphogenesis

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          Abstract

          Roots are highly plastic organs enabling plants to adapt to a changing below‐ground environment. In addition to abiotic factors like nutrients or mechanical resistance, plant roots also respond to temperature variation. Below the heat stress threshold, Arabidopsis thaliana seedlings react to elevated temperature by promoting primary root growth, possibly to reach deeper soil regions with potentially better water saturation. While above‐ground thermomorphogenesis is enabled by thermo‐sensitive cell elongation, it was unknown how temperature modulates root growth. We here show that roots are able to sense and respond to elevated temperature independently of shoot‐derived signals. This response is mediated by a yet unknown root thermosensor that employs auxin as a messenger to relay temperature signals to the cell cycle. Growth promotion is achieved primarily by increasing cell division rates in the root apical meristem, depending on de novo local auxin biosynthesis and temperature‐sensitive organization of the polar auxin transport system. Hence, the primary cellular target of elevated ambient temperature differs fundamentally between root and shoot tissues, while the messenger auxin remains the same.

          Abstract

          A direct temperature‐sensing mechanism in the root acts on cell proliferation in the root apical meristem to control root growth.

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          Most cited references83

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          Genome-wide insertional mutagenesis of Arabidopsis thaliana.

          J Alonso (2003)
          Over 225,000 independent Agrobacterium transferred DNA (T-DNA) insertion events in the genome of the reference plant Arabidopsis thaliana have been created that represent near saturation of the gene space. The precise locations were determined for more than 88,000 T-DNA insertions, which resulted in the identification of mutations in more than 21,700 of the approximately 29,454 predicted Arabidopsis genes. Genome-wide analysis of the distribution of integration events revealed the existence of a large integration site bias at both the chromosome and gene levels. Insertion mutations were identified in genes that are regulated in response to the plant hormone ethylene.
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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 PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots.

              Local accumulation of the plant growth regulator auxin mediates pattern formation in Arabidopsis roots and influences outgrowth and development of lateral root- and shoot-derived primordia. However, it has remained unclear how auxin can simultaneously regulate patterning and organ outgrowth and how its distribution is stabilized in a primordium-specific manner. Here we show that five PIN genes collectively control auxin distribution to regulate cell division and cell expansion in the primary root. Furthermore, the joint action of these genes has an important role in pattern formation by focusing the auxin maximum and restricting the expression domain of PLETHORA (PLT) genes, major determinants for root stem cell specification. In turn, PLT genes are required for PIN gene transcription to stabilize the auxin maximum at the distal root tip. Our data reveal an interaction network of auxin transport facilitators and root fate determinants that control patterning and growth of the root primordium.
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                Author and article information

                Contributors
                marcel.quint@landw.uni-halle.de
                Journal
                EMBO J
                EMBO J
                10.1002/(ISSN)1460-2075
                EMBJ
                embojnl
                The EMBO Journal
                John Wiley and Sons Inc. (Hoboken )
                0261-4189
                1460-2075
                18 April 2023
                June 2023
                18 April 2023
                : 42
                : 11 ( doiID: 10.1002/embj.v42.11 )
                : e111926
                Affiliations
                [ 1 ] Institute of Agricultural and Nutritional Sciences Martin Luther University Halle‐Wittenberg Halle (Saale) Germany
                [ 2 ] Department of Biology, Institute of Molecular Plant Biology ETH Zürich Zürich Switzerland
                [ 3 ] Department of Cell and Metabolic Biology Leibniz Institute of Plant Biochemistry Halle (Saale) Germany
                [ 4 ] Max Planck Institute for Plant Breeding Research Cologne Germany
                Author notes
                [*] [* ]Corresponding author. Tel: +49 0345 5522739; E‐mail: marcel.quint@ 123456landw.uni-halle.de
                Author information
                https://orcid.org/0000-0002-5507-2621
                https://orcid.org/0000-0003-2708-5545
                https://orcid.org/0000-0001-8907-6922
                https://orcid.org/0000-0002-9406-4245
                https://orcid.org/0000-0001-9697-4990
                https://orcid.org/0000-0002-8905-0850
                https://orcid.org/0000-0002-0419-8275
                https://orcid.org/0000-0003-2935-4083
                Article
                EMBJ2022111926
                10.15252/embj.2022111926
                10233379
                37071525
                c73b02af-a41f-4e84-ac9d-12c03d824ad7
                © 2023 The Authors. Published under the terms of the CC BY 4.0 license.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 16 March 2023
                : 21 June 2022
                : 21 March 2023
                Page count
                Figures: 13, Tables: 0, Pages: 23, Words: 17705
                Funding
                Funded by: Alexander von Humboldt‐Stiftung (AvH) , doi 10.13039/100005156;
                Funded by: China Scholarship Council (CSC)
                Funded by: Deutsche Forschungsgemeinschaft , doi 10.13039/501100001659;
                Award ID: Qu 141/3‐2
                Award ID: Qu 141/12‐1
                Funded by: Leibniz‐Institut für Pflanzenbiochemie (IPB)
                Funded by: Rosa Luxemburg Stiftung (RLS) , doi 10.13039/501100007451;
                Funded by: Max Planck Society , doi 10.13039/501100004189;
                Categories
                Article
                Articles
                Custom metadata
                2.0
                01 June 2023
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.2.8 mode:remove_FC converted:01.06.2023

                Molecular biology
                arabidopsis thaliana,auxin,cell division,root,thermomorphogenesis,plant biology
                Molecular biology
                arabidopsis thaliana, auxin, cell division, root, thermomorphogenesis, plant biology

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