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      Nitrate transporter 1.1 alleviates lead toxicity in Arabidopsis by preventing rhizosphere acidification

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          Abstract

          Exposure to Pb 2+ increases NRT1.1-mediated uptake of nitrate in Arabidopsis and is associated with decreased uptake of Pb into the plant, which is a consequence of decreased acidification in the rhizosphere.

          Abstract

          Identification of the mechanisms that control lead (Pb) concentration in plants is a prerequisite for minimizing dietary uptake of Pb from contaminated crops. This study examines how nitrate uptake by roots affects Pb uptake and reveals a new resistance strategy for plants to cope with Pb contamination. We investigated the interaction between nitrate transporter (NRT)-mediated NO 3 uptake and exposure to Pb in Arabidopsis using NRT-related mutants. Exposure to Pb specifically stimulated NRT1.1-mediated nitrate uptake. Loss of function of NRT1.1 in nrt1.1-knockout mutants resulted in greater Pb toxicity and higher Pb accumulation in nitrate-sufficient growth medium, whereas no difference was seen between wild-type plants and null-mutants for NRT1.2, NRT2.1, NRT2.2, NRT2.4, and NRT2.5. These results indicate that only NRT1.1-mediated NO 3 uptake alleviated Pb toxicity in the plants. Further examination indicated that rhizosphere acidification, which favors Pb entry to roots by increasing its availability, is prevented when NRT1.1 is functional and both NO 3 and NH 4 + are present in the medium.

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          Most cited references51

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          CHL1 functions as a nitrate sensor in plants.

          Ions serve as essential nutrients in higher plants and can also act as signaling molecules. Little is known about how plants sense changes in soil nutrient concentrations. Previous studies showed that T101-phosphorylated CHL1 is a high-affinity nitrate transporter, whereas T101-dephosphorylated CHL1 is a low-affinity transporter. In this study, analysis of an uptake- and sensing-decoupled mutant showed that the nitrate transporter CHL1 functions as a nitrate sensor. Primary nitrate responses in CHL1T101D and CHLT101A transgenic plants showed that phosphorylated and dephosphorylated CHL1 lead to a low- and high-level response, respectively. In vitro and in vivo studies showed that, in response to low nitrate concentrations, protein kinase CIPK23 can phosphorylate T101 of CHL1 to maintain a low-level primary response. Thus, CHL1 uses dual-affinity binding and a phosphorylation switch to sense a wide range of nitrate concentrations in the soil, thereby functioning as an ion sensor in higher plants. For a video summary of this article, see the PaperFlick file with the Supplemental Data available online.
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            Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants.

            S Clemens (2006)
            Over the past 200 years emissions of toxic heavy metals have risen tremendously and significantly exceed those from natural sources for practically all metals. Uptake and accumulation by crop plants represents the main entry pathway for potentially health-threatening toxic metals into human and animal food. Of major concern are the metalloids arsenic (As) and selenium (Se), and the metals cadmium (Cd), mercury (Hg), and lead (Pb). This review discusses the molecular mechanisms of toxic metal accumulation in plants and algae, the responses to metal exposure, as well as our understanding of metal tolerance and its evolution. The main emphasis will be on cadmium, which is by far the most widely studied of the non-essential toxic metals/metalloids. Entry via Zn2+, Fe2+, and Ca2+ transporters is the molecular basis of Cd2+ uptake into plant cells. Much less is known about the partitioning of non-essential metals and about the genes underlying the enormous diversity among plants with respect to Cd accumulation in different tissues. Numerous studies have described symptoms and responses of plants upon toxic metal exposure. Mysterious are primary targets of toxicity, the degree of specificity of responses, the sensing and the signaling events that lead to transcriptional activation. All plants apparently possess a basal tolerance of toxic non-essential metals. For Cd and As, this is largely dependent on the phytochelatin pathway. Not understood is the molecular biology of Cd hypertolerance in certain plant species such as the metallophytes Arabidopsis halleri or Thlaspi caerulescens.
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              A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants.

              Members of the plant NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER (NRT1/PTR) family display protein sequence homology with the SLC15/PepT/PTR/POT family of peptide transporters in animals. In comparison to their animal and bacterial counterparts, these plant proteins transport a wide variety of substrates: nitrate, peptides, amino acids, dicarboxylates, glucosinolates, IAA, and ABA. The phylogenetic relationship of the members of the NRT1/PTR family in 31 fully sequenced plant genomes allowed the identification of unambiguous clades, defining eight subfamilies. The phylogenetic tree was used to determine a unified nomenclature of this family named NPF, for NRT1/PTR FAMILY. We propose that the members should be named accordingly: NPFX.Y, where X denotes the subfamily and Y the individual member within the species. Copyright © 2013 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                J Exp Bot
                J. Exp. Bot
                exbotj
                Journal of Experimental Botany
                Oxford University Press (UK )
                0022-0957
                1460-2431
                01 November 2019
                15 August 2019
                15 August 2019
                : 70
                : 21
                : 6363-6374
                Affiliations
                [1 ] State Key Laboratory of Plant Physiology and Biochemistry, College of Natural Resources and Environmental Science, Zhejiang University , Hangzhou, China
                [2 ] Michigan State University , USA
                Author notes

                These authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0003-0896-8596
                Article
                erz374
                10.1093/jxb/erz374
                6859734
                31414122
                cf7ebb0f-ff73-465c-9d83-a8855a5b0f17
                © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Experimental Biology.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 16 April 2019
                : 05 August 2019
                : 04 August 2019
                : 26 September 2019
                Page count
                Pages: 12
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Award ID: 31622051
                Award ID: 31670258
                Funded by: Fundamental Research Funds for the Central Universities 10.13039/501100012226
                Award ID: 2017XZZX002-06
                Categories
                Research Papers
                Plant—Environment Interactions

                Plant science & Botany
                lead,nitrate,nitrate transporters,pb resistance,ph,phytoremediation
                Plant science & Botany
                lead, nitrate, nitrate transporters, pb resistance, ph, phytoremediation

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