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      Metabolomics of laminae and midvein during leaf senescence and source–sink metabolite management in Brassica napus L. leaves

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          Abstract

          Metabolomics of leaf laminae and veins during ageing reveal tissue specificities and different senescence programmes.

          Abstract

          Leaf senescence is a long developmental process important for nutrient management and for source to sink remobilization. Constituents of the mesophyll cells are progressively degraded to provide nutrients to the rest of the plant. Up to now, studies on leaf senescence have not paid much attention to the role of the different leaf tissues. In the present study, we dissected leaf laminae from the midvein to perform metabolite profiling. The laminae mesophyll cells are the source of nutrients, and in C 3 plants they contain Rubisco as the most important nitrogen storage pool. Veins, rich in vasculature, are the place where all the nutrients are translocated, and sometimes interconverted, before being exported through the phloem or the xylem. The different metabolic changes we observed in laminae and midvein with ageing support the idea that the senescence programme in these two tissues is different. Important accumulations of metabolites in the midvein suggest that nutrient translocations from source leaves to sinks are mainly controlled at this level. Carbon and nitrogen long-distance molecules such as fructose, glucose, aspartate, and asparagine were more abundant in the midvein than in laminae. In contrast, sucrose, glutamate, and aspartate were more abundant in laminae. The concentrations of tricarboxylic acid (TCA) compounds were also lower in the midvein than in laminae. Since nitrogen remobilization increased under low nitrate supply, plants were grown under two nitrate concentrations. The results revealed that the senescence-related differences were mostly similar under low and high nitrate conditions except for some pathways such as the TCA cycle.

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          Most cited references43

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          Transcriptome of Arabidopsis leaf senescence

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            Protein degradation - an alternative respiratory substrate for stressed plants.

            In cellular circumstances under which carbohydrates are scarce, plants can metabolize proteins and lipids as alternative respiratory substrates. Respiration of protein is less efficient than that of carbohydrate as assessed by the respiratory quotient; however, under certain adverse conditions, it represents an important alternative energy source for the cell. Significant effort has been invested in understanding the regulation of protein degradation in plants. This has included an investigation of how proteins are targeted to the proteosome, and the processes of senescence and autophagy. Here we review these events with particular reference to amino acid catabolism and its role in supporting the tricarboxylic acid cycle and direct electron supply to the ubiquinone pool of the mitochondrial electron transport chain in plants. Copyright © 2011 Elsevier Ltd. All rights reserved.
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              Comprehensive dissection of spatiotemporal metabolic shifts in primary, secondary, and lipid metabolism during developmental senescence in Arabidopsis.

              Developmental senescence is a coordinated physiological process in plants and is critical for nutrient redistribution from senescing leaves to newly formed sink organs, including young leaves and developing seeds. Progress has been made concerning the genes involved and the regulatory networks controlling senescence. The resulting complex metabolome changes during senescence have not been investigated in detail yet. Therefore, we conducted a comprehensive profiling of metabolites, including pigments, lipids, sugars, amino acids, organic acids, nutrient ions, and secondary metabolites, and determined approximately 260 metabolites at distinct stages in leaves and siliques during senescence in Arabidopsis (Arabidopsis thaliana). This provided an extensive catalog of metabolites and their spatiotemporal cobehavior with progressing senescence. Comparison with silique data provides clues to source-sink relations. Furthermore, we analyzed the metabolite distribution within single leaves along the basipetal sink-source transition trajectory during senescence. Ceramides, lysolipids, aromatic amino acids, branched chain amino acids, and stress-induced amino acids accumulated, and an imbalance of asparagine/aspartate, glutamate/glutamine, and nutrient ions in the tip region of leaves was detected. Furthermore, the spatiotemporal distribution of tricarboxylic acid cycle intermediates was already changed in the presenescent leaves, and glucosinolates, raffinose, and galactinol accumulated in the base region of leaves with preceding senescence. These results are discussed in the context of current models of the metabolic shifts occurring during developmental and environmentally induced senescence. As senescence processes are correlated to crop yield, the metabolome data and the approach provided here can serve as a blueprint for the analysis of traits and conditions linking crop yield and senescence.
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                Author and article information

                Journal
                J Exp Bot
                J. Exp. Bot
                exbotj
                Journal of Experimental Botany
                Oxford University Press (UK )
                0022-0957
                1460-2431
                06 February 2018
                06 September 2017
                06 September 2017
                : 69
                : 4 , Special Issue: Plant Senescence
                : 891-903
                Affiliations
                INRA-AgroParisTech, Institut Jean-Pierre Bourgin, Saclay Plant Sciences, Versailles, France
                Author notes

                These authors contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-6720-8135
                http://orcid.org/0000-0001-5846-4121
                http://orcid.org/0000-0003-0719-9350
                Article
                erx253
                10.1093/jxb/erx253
                5853214
                28992054
                78c0ac5f-4b78-44b7-a44c-4c3bc66f54c1
                © The Author(s) 2017. 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 License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 30 March 2017
                : 03 July 2017
                Page count
                Pages: 13
                Categories
                Research Papers

                Plant science & Botany
                leaf senescence,metabolomics,phloem,source–sink relationship
                Plant science & Botany
                leaf senescence, metabolomics, phloem, source–sink relationship

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