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      Phosphorylation of RhoGDI1, a Rho GDP dissociation inhibitor, regulates root hair development in Arabidopsis under salt stress

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          Plants must actively regulate their growth to acclimate to stressful environments and optimize growth. Here, we describe a mechanism by which a root hair–specific response is important for salt tolerance in seedlings. We determined that SALT OVERLY SENSITIVE 2 (SOS2), a kinase that acts as a key master regulator in salt resistance, participates in root hair development under salt stress via a mechanism involving phosphorylation of (GUANOSINE NUCLEOTIDE DIPHOSPHATE DISSOCIATION INHIBITOR 1) RhoGDI1. We further demonstrated that the SOS2–RhoGDI1–ROP2 (SOS2–RhoGDI1–Rho GTPASE OF PLANTS 2) module regulates root hair initiation and growth to provide plant salt tolerance.

          Abstract

          To ensure optimal growth, plants actively regulate their growth and development based on environmental changes. Among these, salt stress significantly influences growth and yield. In this study, we demonstrate that the growth of root hairs of salt-stressed Arabidopsis thaliana seedlings is regulated by the SALT OVERLY SENSITIVE 2 (SOS2)–GUANOSINE NUCLEOTIDE DIPHOSPHATE DISSOCIATION INHIBITOR 1 (RhoGDI1)–Rho GTPASE OF PLANTS 2 (ROP2) module. We show here that the kinase SOS2 is activated by salt stress and subsequently phosphorylates RhoGDI1, a root hair regulator, thereby decreasing its stability. This change in RhoGDI1 abundance resulted in a fine-tuning of polar localization of ROP2 and root hair initiation followed by polar growth, demonstrating how SOS2-regulated root hair development is critical for plant growth under salt stress. Our results reveal how a tissue-specific response to salt stress balances the relationship of salt resistance and basic growth.

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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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            The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter.

            In Arabidopsis thaliana, the SOS1 (Salt Overly Sensitive 1) locus is essential for Na(+) and K(+) homeostasis, and sos1 mutations render plants more sensitive to growth inhibition by high Na(+) and low K(+) environments. SOS1 is cloned and predicted to encode a 127-kDa protein with 12 transmembrane domains in the N-terminal part and a long hydrophilic cytoplasmic tail in the C-terminal part. The transmembrane region of SOS1 has significant sequence similarities to plasma membrane Na(+)/H(+) antiporters from bacteria and fungi. Sequence analysis of various sos1 mutant alleles reveals several residues and regions in the transmembrane as well as the tail parts that are critical for SOS1 function in plant salt tolerance. SOS1 gene expression in plants is up-regulated in response to NaCl stress. This up-regulation is abated in sos3 or sos2 mutant plants, suggesting that it is controlled by the SOS3/SOS2 regulatory pathway.
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              Elucidating the molecular mechanisms mediating plant salt-stress responses.

              Contents Summary 523 I. Introduction 523 II. Sensing salt stress 524 III. Ion homeostasis regulation 524 IV. Metabolite and cell activity responses to salt stress 527 V. Conclusions and perspectives 532 Acknowledgements 533 References 533 SUMMARY: Excess soluble salts in soil (saline soils) are harmful to most plants. Salt imposes osmotic, ionic, and secondary stresses on plants. Over the past two decades, many determinants of salt tolerance and their regulatory mechanisms have been identified and characterized using molecular genetics and genomics approaches. This review describes recent progress in deciphering the mechanisms controlling ion homeostasis, cell activity responses, and epigenetic regulation in plants under salt stress. Finally, we highlight research areas that require further research to reveal new determinants of salt tolerance in plants.
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                Author and article information

                Contributors
                Journal
                Proc Natl Acad Sci U S A
                Proc Natl Acad Sci U S A
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                17 August 2023
                22 August 2023
                17 February 2024
                : 120
                : 34
                : e2217957120
                Affiliations
                [1] aState Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, China Agricultural University , Beijing 100193, China
                Author notes
                1To whom correspondence may be addressed. Email: guoyan@ 123456cau.edu.cn .

                Edited by José R. Dinneny, Stanford University, Stanford, CA; received October 25, 2022; accepted July 7, 2023 by Editorial Board Member Philip N. Benfey

                Author information
                https://orcid.org/0000-0002-9436-212X
                https://orcid.org/0000-0002-6955-8008
                Article
                202217957
                10.1073/pnas.2217957120
                10450838
                37590409
                5abc0a43-5672-4c27-9fff-cd7872360aa2
                Copyright © 2023 the Author(s). Published by PNAS.

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

                History
                : 25 October 2022
                : 07 July 2023
                Page count
                Pages: 11, Words: 7012
                Funding
                Funded by: MOST | National Natural Science Foundation of China (NSFC), FundRef 501100001809;
                Award ID: 32130007
                Award Recipient : Yan Guo
                Categories
                research-article, Research Article
                plant-bio, Plant Biology
                428
                Biological Sciences
                Plant Biology

                salt stress,root hair,sos
                salt stress, root hair, sos

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