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      The Potassium Transporter OsHAK5 Alters Rice Architecture via ATP-Dependent Transmembrane Auxin Fluxes

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          Abstract

          Plant HAK/KUP/KT family members function as plasma membrane (PM) H +/K + symporters and may modulate chemiosmotically-driven polar auxin transport (PAT). Here, we show that inactivation of OsHAK5, a rice K + transporter gene, decreased rootward and shootward PAT, tiller number, and the length of both lateral roots and root hairs, while OsHAK5 overexpression increased PAT, tiller number, and root hair length, irrespective of the K + supply. Inhibitors of ATP-binding-cassette type-B transporters, NPA and BUM, abolished the OsHAK5-overexpression effect on PAT. The mechanistic basis of these changes included the OsHAK5-mediated decrease of transmembrane potential (depolarization), increase of extracellular pH, and increase of PM-ATPase activity. These findings highlight the dual roles of OsHAK5 in altering cellular chemiosmotic gradients (generated continuously by PM H +-ATPase) and regulating ATP-dependent auxin transport. Both functions may underlie the prominent effect of OsHAK5 on rice architecture, which may be exploited in the future to increase crop yield via genetic manipulations.

          Abstract

          The potassium transporter OsHAK5 in rice acts as a convergence point between the developmental pathways of tillering, lateral root and root-hair growth, and the auxin transport pathway. This study reveals dual roles of OsHAK5 in altering cellular chemiosmotic gradients (generated continuously by plasma membrane H +-ATPase) and regulating ATP-dependent auxin transport.

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          Most cited references62

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          Plasticity of the Arabidopsis root system under nutrient deficiencies.

          Plant roots show a particularly high variation in their morphological response to different nutrient deficiencies. Although such changes often determine the nutrient efficiency or stress tolerance of plants, it is surprising that a comprehensive and comparative analysis of root morphological responses to different nutrient deficiencies has not yet been conducted. Since one reason for this is an inherent difficulty in obtaining nutrient-deficient conditions in agar culture, we first identified conditions appropriate for producing nutrient-deficient plants on agar plates. Based on a careful selection of agar specifically for each nutrient being considered, we grew Arabidopsis (Arabidopsis thaliana) plants at four levels of deficiency for 12 nutrients and quantified seven root traits. In combination with measurements of biomass and elemental concentrations, we observed that the nutritional status and type of nutrient determined the extent and type of changes in root system architecture (RSA). The independent regulation of individual root traits further pointed to a differential sensitivity of root tissues to nutrient limitations. To capture the variation in RSA under different nutrient supplies, we used principal component analysis and developed a root plasticity chart representing the overall modulations in RSA under a given treatment. This systematic comparison of RSA responses to nutrient deficiencies provides a comprehensive view of the overall changes in root plasticity induced by the deficiency of single nutrients and provides a solid basis for the identification of nutrient-sensitive steps in the root developmental program.
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            Osmotic stress responses and plant growth controlled by potassium transporters in Arabidopsis.

            Osmotic adjustment plays a fundamental role in water stress responses and growth in plants; however, the molecular mechanisms governing this process are not fully understood. Here, we demonstrated that the KUP potassium transporter family plays important roles in this process, under the control of abscisic acid (ABA) and auxin. We generated Arabidopsis thaliana multiple mutants for K(+) uptake transporter 6 (KUP6), KUP8, KUP2/SHORT HYPOCOTYL3, and an ABA-responsive potassium efflux channel, guard cell outward rectifying K(+) channel (GORK). The triple mutants, kup268 and kup68 gork, exhibited enhanced cell expansion, suggesting that these KUPs negatively regulate turgor-dependent growth. Potassium uptake experiments using (86)radioactive rubidium ion ((86)Rb(+)) in the mutants indicated that these KUPs might be involved in potassium efflux in Arabidopsis roots. The mutants showed increased auxin responses and decreased sensitivity to an auxin inhibitor (1-N-naphthylphthalamic acid) and ABA in lateral root growth. During water deficit stress, kup68 gork impaired ABA-mediated stomatal closing, and kup268 and kup68 gork decreased survival of drought stress. The protein kinase SNF1-related protein kinases 2E (SRK2E), a key component of ABA signaling, interacted with and phosphorylated KUP6, suggesting that KUP functions are regulated directly via an ABA signaling complex. We propose that the KUP6 subfamily transporters act as key factors in osmotic adjustment by balancing potassium homeostasis in cell growth and drought stress responses.
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              Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development.

              Arabidopsis possesses several genes related to the multidrug resistance (MDR) genes of animals, one of which, AtMDR1, was shown to be induced by the hormone auxin. Plants having mutations in AtMDR1 or its closest relative, AtPGP1, were isolated by a reverse genetic strategy. Auxin transport activity was greatly impaired in atmdr1 and atmdr1 atpgp1 double mutant plants. Epinastic cotyledons and reduced apical dominance were mutant phenotypes consistent with the disrupted basipetal flow of auxin. The auxin transport inhibitor 1-naphthylphthalamic acid was shown to bind tightly and specifically to AtMDR1 and AtPGP1 proteins. The results indicate that these two MDR-like genes of Arabidopsis encode 1-naphthylphthalamic acid binding proteins that are required for normal auxin distribution and auxin-mediated development.
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                Author and article information

                Contributors
                Journal
                Plant Commun
                Plant Commun
                Plant Communications
                Elsevier
                2590-3462
                29 April 2020
                14 September 2020
                29 April 2020
                : 1
                : 5
                : 100052
                Affiliations
                [1 ]State Key Laboratory of Crop Genetics and Germplasm Enhancement, MOA Key Laboratory of Plant Nutrition and Fertilization in Lower-Middle Reaches of the Yangtze River, Nanjing Agricultural University, Nanjing 210095, China
                [2 ]State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, Anhui 230036, China
                [3 ]The R.H. Smith Faculty of Agriculture, Food, and Environment, The Hebrew University of Jerusalem, Rehovot 76100, Israel
                [4 ]Department of Plant Science and Landscape Architecture, University of Maryland, College Park, MD, USA
                Author notes
                []Corresponding author lyu@ 123456njau.edu.cn
                [∗∗ ]Corresponding author ghxu@ 123456njau.edu.cn
                Article
                S2590-3462(20)30035-3 100052
                10.1016/j.xplc.2020.100052
                7747981
                33367257
                20c80f58-0bbb-4211-a249-597742b481f5
                © 2020 The Author(s)

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 10 April 2019
                : 29 May 2019
                : 27 April 2020
                Categories
                Research Article

                rice,potassium transporter,architecture,root,shoot,auxin
                rice, potassium transporter, architecture, root, shoot, auxin

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