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      Manganese in Plants: From Acquisition to Subcellular Allocation

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          Abstract

          Manganese (Mn) is an important micronutrient for plant growth and development and sustains metabolic roles within different plant cell compartments. The metal is an essential cofactor for the oxygen-evolving complex (OEC) of the photosynthetic machinery, catalyzing the water-splitting reaction in photosystem II (PSII). Despite the importance of Mn for photosynthesis and other processes, the physiological relevance of Mn uptake and compartmentation in plants has been underrated. The subcellular Mn homeostasis to maintain compartmented Mn-dependent metabolic processes like glycosylation, ROS scavenging, and photosynthesis is mediated by a multitude of transport proteins from diverse gene families. However, Mn homeostasis may be disturbed under suboptimal or excessive Mn availability. Mn deficiency is a serious, widespread plant nutritional disorder in dry, well-aerated and calcareous soils, as well as in soils containing high amounts of organic matter, where bio-availability of Mn can decrease far below the level that is required for normal plant growth. By contrast, Mn toxicity occurs on poorly drained and acidic soils in which high amounts of Mn are rendered available. Consequently, plants have evolved mechanisms to tightly regulate Mn uptake, trafficking, and storage. This review provides a comprehensive overview, with a focus on recent advances, on the multiple functions of transporters involved in Mn homeostasis, as well as their regulatory mechanisms in the plant’s response to different conditions of Mn availability.

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          Distribution of the Elements in Some Major Units of the Earth's Crust

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            IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth.

            Plants are the principal source of iron in most diets, yet iron availability often limits plant growth. In response to iron deficiency, Arabidopsis roots induce the expression of the divalent cation transporter IRT1. Here, we present genetic evidence that IRT1 is essential for the uptake of iron from the soil. An Arabidopsis knockout mutant in IRT1 is chlorotic and has a severe growth defect in soil, leading to death. This defect is rescued by the exogenous application of iron. The mutant plants do not take up iron and fail to accumulate other divalent cations in low-iron conditions. IRT1-green fluorescent protein fusion, transiently expressed in culture cells, localized to the plasma membrane. We also show, through promoter::beta-glucuronidase analysis and in situ hybridization, that IRT1 is expressed in the external cell layers of the root, specifically in response to iron starvation. These results clearly demonstrate that IRT1 is the major transporter responsible for high-affinity metal uptake under iron deficiency.
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              Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice.

              Paddy rice (Oryza sativa) is able to accumulate high concentrations of Mn without showing toxicity; however, the molecular mechanisms underlying Mn uptake are unknown. Here, we report that a member of the Nramp (for the Natural Resistance-Associated Macrophage Protein) family, Nramp5, is involved in Mn uptake and subsequently the accumulation of high concentrations of Mn in rice. Nramp5 was constitutively expressed in the roots and encodes a plasma membrane-localized protein. Nramp5 was polarly localized at the distal side of both exodermis and endodermis cells. Knockout of Nramp5 resulted in a significant reduction in growth and grain yield, especially when grown at low Mn concentrations. This growth reduction could be partially rescued by supplying high concentrations of Mn but not by the addition of Fe. Mineral analysis showed that the concentration of Mn and Cd in both the roots and shoots was lower in the knockout line than in wild-type rice. A short-term uptake experiment revealed that the knockout line lost the ability to take up Mn and Cd. Taken together, Nramp5 is a major transporter of Mn and Cd and is responsible for the transport of Mn and Cd from the external solution to root cells.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                26 March 2020
                2020
                : 11
                : 300
                Affiliations
                Plant Nutrition Laboratory, Institute of Agricultural and Nutritional Sciences, Martin Luther University Halle-Wittenberg , Halle (Salle), Germany
                Author notes

                Edited by: Manuel Nieves-Cordones, Center for Edaphology and Applied Biology of Segura, Spanish National Research Council, Spain

                Reviewed by: Sebastien Thomine, UMR 9198 Institut de Biologie Intégrative de la Cellule (I2BC), France; Mathieu Pottier, University of Liège, Belgium

                *Correspondence: Santiago Alejandro, santiago.alejandro-martinez@ 123456landw.uni-halle.de

                This article was submitted to Plant Nutrition, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.00300
                7113377
                32273877
                1126bb53-5303-49b1-8fb7-403311047e48
                Copyright © 2020 Alejandro, Höller, Meier and Peiter.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 05 December 2019
                : 02 March 2020
                Page count
                Figures: 3, Tables: 1, Equations: 0, References: 230, Pages: 23, Words: 0
                Funding
                Funded by: Deutsche Forschungsgemeinschaft 10.13039/501100001659
                Funded by: European Regional Development Fund 10.13039/501100008530
                Award ID: ZS/2016/06/79740
                Categories
                Plant Science
                Review

                Plant science & Botany
                manganese transport,manganese uptake,manganese deficiency,manganese toxicity,intracellular distribution,arabidopsis,rice,barley

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