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      A salt stress‐activated GSO1‐SOS2‐SOS1 module protects the Arabidopsis root stem cell niche by enhancing sodium ion extrusion

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          Abstract

          Soil salinity impairs plant growth reducing crop productivity. Toxic accumulation of sodium ions is counteracted by the Salt Overly Sensitive (SOS) pathway for Na + extrusion, comprising the Na + transporter SOS1, the kinase SOS2, and SOS3 as one of several Calcineurin‐B‐like (CBL) Ca 2 + sensors. Here, we report that the receptor‐like kinase GSO1/SGN3 activates SOS2, independently of SOS3 binding, by physical interaction and phosphorylation at Thr16. Loss of GSO1 function renders plants salt sensitive and GSO1 is both sufficient and required for activating the SOS2‐SOS1 module in yeast and in planta. Salt stress causes the accumulation of GSO1 in two specific and spatially defined areas of the root tip: in the endodermis section undergoing Casparian strip (CS) formation, where it reinforces the CIF‐GSO1‐SGN1 axis for CS barrier formation; and in the meristem, where it creates the GSO1‐SOS2‐SOS1 axis for Na + detoxification. Thus, GSO1 simultaneously prevents Na + both from diffusing into the vasculature, and from poisoning unprotected stem cells in the meristem. By protecting the meristem, receptor‐like kinase‐conferred activation of the SOS2‐SOS1 module allows root growth to be maintained in adverse environments.

          Abstract

          This report identifies a receptor‐kinase which activates a sodium ion extrusion pathway in roots growing in high salt concentrations.

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          Most cited references81

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          Na+ tolerance and Na+ transport in higher plants.

          M. Tester (2003)
          Tolerance to high soil [Na(+)] involves processes in many different parts of the plant, and is manifested in a wide range of specializations at disparate levels of organization, such as gross morphology, membrane transport, biochemistry and gene transcription. Multiple adaptations to high [Na(+)] operate concurrently within a particular plant, and mechanisms of tolerance show large taxonomic variation. These mechanisms can occur in all cells within the plant, or can occur in specific cell types, reflecting adaptations at two major levels of organization: those that confer tolerance to individual cells, and those that contribute to tolerance not of cells per se, but of the whole plant. Salt-tolerant cells can contribute to salt tolerance of plants; but we suggest that equally important in a wide range of conditions are processes involving the management of Na(+) movements within the plant. These require specific cell types in specific locations within the plant catalysing transport in a coordinated manner. For further understanding of whole plant tolerance, we require more knowledge of cell-specific transport processes and the consequences of manipulation of transporters and signalling elements in specific cell types.
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            GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.

            We have used the Escherichia coli beta-glucuronidase gene (GUS) as a gene fusion marker for analysis of gene expression in transformed plants. Higher plants tested lack intrinsic beta-glucuronidase activity, thus enhancing the sensitivity with which measurements can be made. We have constructed gene fusions using the cauliflower mosaic virus (CaMV) 35S promoter or the promoter from a gene encoding the small subunit of ribulose bisphosphate carboxylase (rbcS) to direct the expression of beta-glucuronidase in transformed plants. Expression of GUS can be measured accurately using fluorometric assays of very small amounts of transformed plant tissue. Plants expressing GUS are normal, healthy and fertile. GUS is very stable, and tissue extracts continue to show high levels of GUS activity after prolonged storage. Histochemical analysis has been used to demonstrate the localization of gene activity in cells and tissues of transformed plants.
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              Salt Tolerance Mechanisms of Plants

              Crop loss due to soil salinization is an increasing threat to agriculture worldwide. This review provides an overview of cellular and physiological mechanisms in plant responses to salt. We place cellular responses in a time- and tissue-dependent context in order to link them to observed phases in growth rate that occur in response to stress. Recent advances in phenotyping can now functionally or genetically link cellular signaling responses, ion transport, water management, and gene expression to growth, development, and survival. Halophytes, which are naturally salt-tolerant plants, are highlighted as success stories to learn from. We emphasize that (a) filling the major knowledge gaps in salt-induced signaling pathways, (b) increasing the spatial and temporal resolution of our knowledge of salt stress responses, (c) discovering and considering crop-specific responses, and (d) including halophytes in our comparative studies are all essential in order to take our approaches to increasing crop yields in saline soils to the next level.
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                Author and article information

                Contributors
                jkudla@uni-muenster.de
                guoyan@cau.edu.cn
                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
                22 May 2023
                July 2023
                22 May 2023
                : 42
                : 13 ( doiID: 10.1002/embj.v42.13 )
                : e113004
                Affiliations
                [ 1 ] State Key Laboratory of Plant Physiology and Biochemistry College of Biological Sciences, China Agricultural University Beijing China
                [ 2 ] Beijing Key Laboratory of Development and Quality Control of Ornamental Crops, College of Horticulture China Agricultural University Beijing China
                [ 3 ] Institut für Biologie und Biotechnologie der Pflanzen (IBBP) Westfälische Wilhelms‐Universität Münster Münster Germany
                [ 4 ] Instituto de Bioquímica Vegetal y Fotosíntesis, cicCartuja CSIC‐Universidad de Sevilla Sevilla Spain
                [ 5 ] Ministry of Education Key Laboratory of Cell Activities and Stress Adaptations, School of Life Sciences Lanzhou University Lanzhou China
                Author notes
                [*] [* ] Corresponding author. Tel: +49 251 83‐24813; E‐mail: jkudla@ 123456uni-muenster.de

                Corresponding author. Tel: +86‐10‐6273‐2882; E‐mail: guoyan@ 123456cau.edu.cn

                Author information
                https://orcid.org/0000-0003-2833-3264
                https://orcid.org/0000-0002-2445-677X
                https://orcid.org/0000-0002-1797-9468
                https://orcid.org/0000-0002-9153-6331
                https://orcid.org/0000-0002-3148-6897
                https://orcid.org/0000-0003-4510-8624
                https://orcid.org/0000-0002-8238-767X
                https://orcid.org/0000-0002-6955-8008
                Article
                EMBJ2022113004
                10.15252/embj.2022113004
                10308370
                37211994
                9050287e-4352-42a2-a458-039016db3e74
                © 2023 The Authors. Published under the terms of the CC BY NC ND 4.0 license.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 31 March 2023
                : 07 November 2022
                : 19 April 2023
                Page count
                Figures: 14, Tables: 0, Pages: 25, Words: 17925
                Funding
                Funded by: China Scholarship Council (CSC)
                Award ID: 201806350012
                Funded by: Deutsche Forschungsgemeinschaft (DFG)
                Award ID: 410758888
                Funded by: MEC | Agencia Estatal de Investigación (AEI)
                Award ID: RTI2018‐094027‐B‐100
                Funded by: MOST | National Key Research and Development Program of China (NKPs)
                Award ID: 2022YFA1303400
                Funded by: MOST | National Natural Science Foundation of China (NSFC) , doi 10.13039/501100001809;
                Award ID: 31921001
                Categories
                Article
                Articles
                Custom metadata
                2.0
                03 July 2023
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.0 mode:remove_FC converted:29.06.2023

                Molecular biology
                arabidopsis,meristem,receptor‐like kinase,salt stress,sos pathway,plant biology
                Molecular biology
                arabidopsis, meristem, receptor‐like kinase, salt stress, sos pathway, plant biology

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