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      Aluminium is essential for root growth and development of tea plants ( Camellia sinensis)

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          Abstract

          On acid soils, the trivalent aluminium ion (Al 3+) predominates and is very rhizotoxic to most plant species. For some native plant species adapted to acid soils including tea ( Camellia sinensis), Al 3+ has been regarded as a beneficial mineral element. In this study, we discovered that Al 3+ is actually essential for tea root growth and development in all the tested varieties. Aluminum ion promoted new root growth in five representative tea varieties with dose‐dependent responses to Al 3+ availability. In the absence of Al 3+, the tea plants failed to generate new roots, and the root tips were damaged within 1 d of Al deprivation. Structural analysis of root tips demonstrated that Al was required for root meristem development and activity. In situ morin staining of Al 3+ in roots revealed that Al mainly localized to nuclei in root meristem cells, but then gradually moved to the cytosol when Al 3+ was subsequently withdrawn. This movement of Al 3+ from nuclei to cytosols was accompanied by exacerbated DNA damage, which suggests that the nuclear‐targeted Al primarily acts to maintain DNA integrity. Taken together, these results provide novel evidence that Al 3+ is essential for root growth in tea plants through maintenance of DNA integrity in meristematic cells.

          Abstract

          Ionic aluminium (Al 3+) has been known to be rhizotoxic to most plant species. However, we demonstrate that Al 3+ is essential for tea root growth and development through maintenance of DNA integrity in meristematic cells.

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          Most cited references40

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          Physiological functions of beneficial elements.

          Aluminum (Al), cobalt (Co), sodium (Na), selenium (Se), and silicon (Si) are considered beneficial elements for plants: they are not required by all plants but can promote plant growth and may be essential for particular taxa. These beneficial elements have been reported to enhance resistance to biotic stresses such as pathogens and herbivory, and to abiotic stresses such as drought, salinity, and nutrient toxicity or deficiency. The beneficial effects of low doses of Al, Co, Na and Se have received little attention compared to toxic effects that typically occur at higher concentrations. Better understanding of the effects of beneficial elements is important to improve crop productivity and enhance plant nutritional value for a growing world population.
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            Plasma membrane-localized transporter for aluminum in rice.

            Aluminum (Al) is the most abundant metal in the Earth's crust, but its trivalent ionic form is highly toxic to all organisms at low concentrations. How Al enters cells has not been elucidated in any organisms. Herein, we report a transporter, Nrat1 (Nramp aluminum transporter 1), specific for trivalent Al ion in rice. Nrat1 belongs to the Nramp (natural resistance-associated macrophage protein) family, but shares a low similarity with other Nramp members. When expressed in yeast, Nrat1 transports trivalent Al ion, but not other divalent ions, such as manganese, iron, and cadmium, or the Al-citrate complex. Nrat1 is localized at the plasma membranes of all cells of root tips except epidermal cells. Knockout of Nrat1 resulted in decreased Al uptake, increased Al binding to cell wall, and enhanced Al sensitivity, but did not affect the tolerance to other metals. Expression of Nrat1 is up-regulated by Al in the roots and regulated by a C2H2 zinc finger transcription factor (ART1). We therefore concluded that Nrat1 is a plasma membrane-localized transporter for trivalent Al, which is required for a prior step of final Al detoxification through sequestration of Al into vacuoles.
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              Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex.

              Rice (Oryza sativa) is the most aluminum (Al)-resistant crop species among the small-grain cereals, but the mechanisms responsible for this trait are still unclear. Using two rice cultivars differing in Al resistance, rice sp. japonica 'Nipponbare' (an Al-resistant cultivar) and rice sp. indica 'Zhefu802' (an Al-sensitive cultivar), it was found that Al content in the root apex (0-10 mm) was significantly lower in Al-resistant 'Nipponbare' than in sensitive 'Zhefu802', with more of the Al localized to cell walls in 'Zhefu802', indicating that an Al exclusion mechanism is operating in 'Nipponbare'. However, neither organic acid efflux nor changes in rhizosphere pH appear to be responsible for the Al exclusion. Interestingly, cell wall polysaccharides (pectin, hemicellulose 1, and hemicellulose 2) in the root apex were found to be significantly higher in 'Zhefu802' than in 'Nipponbare' in the absence of Al, and Al exposure increased root apex hemicellulose content more significantly in 'Zhefu802'. Root tip cell wall pectin methylesterase (PME) activity was constitutively higher in 'Zhefu802' than in 'Nipponbare', although Al treatment resulted in increased PME activity in both cultivars. Immunolocalization of pectins showed a higher proportion of demethylated pectins in 'Zhefu802', indicating a higher proportion of free pectic acid residues in the cell walls of 'Zhefu802' root tips. Al adsorption and desorption kinetics of root tip cell walls also indicated that more Al was adsorbed and bound Al was retained more tightly in 'Zhefu802', which was consistent with Al content, PME activity, and pectin demethylesterification results. These responses were specific to Al compared with other metals (CdCl(2), LaCl(3), and CuCl(2)), and the ability of the cell wall to adsorb these metals was also not related to levels of cell wall pectins. All of these results suggest that cell wall polysaccharides may play an important role in excluding Al specifically from the rice root apex.
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                Author and article information

                Contributors
                hliao@fafu.edu.cn
                Journal
                J Integr Plant Biol
                J Integr Plant Biol
                10.1111/(ISSN)1744-7909
                JIPB
                Journal of Integrative Plant Biology
                John Wiley and Sons Inc. (Hoboken )
                1672-9072
                1744-7909
                15 May 2020
                July 2020
                : 62
                : 7 ( doiID: 10.1111/jipb.v62.7 )
                : 984-997
                Affiliations
                [ 1 ] Root Biology Center, College of Resources and Environment Fujian Agriculture and Forestry University Fuzhou 350002 China
                [ 2 ] Vector‐Borne Virus Research Center Fujian Agriculture and Forestry University Fuzhou 350002 China
                [ 3 ] Global Institute for Food Security University of Saskatchewan Saskatoon S7N 4J8 Canada
                Author notes
                [*] [* ]Correspondence: Hong Liao ( hliao@ 123456fafu.edu.cn )

                These authors contributed equally to this work.

                Article
                JIPB12942
                10.1111/jipb.12942
                7383589
                32320136
                d6b90214-7676-430d-b774-5f584cc3084d
                © 2020 The Authors. Journal of Integrative Plant Biology Published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 02 February 2020
                : 14 April 2020
                Page count
                Figures: 8, Tables: 0, Pages: 14, Words: 6748
                Funding
                Funded by: National Natural Science Foundation of China , open-funder-registry 10.13039/501100001809;
                Funded by: Natural Science Foundation of Fujian Province in China
                Categories
                Molecular Physiology
                Molecular Physiology
                Custom metadata
                2.0
                July 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.5 mode:remove_FC converted:27.07.2020

                aluminium,essential,meristem,root,tea
                aluminium, essential, meristem, root, tea

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