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      Arabidopsis uses two gluconeogenic gateways for organic acids to fuel seedling establishment

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          Abstract

          Gluconeogenesis is a fundamental metabolic process that allows organisms to make sugars from non-carbohydrate stores such as lipids and protein. In eukaryotes only one gluconeogenic route has been described from organic acid intermediates and this relies on the enzyme phospho enolpyruvate carboxykinase (PCK). Here we show that two routes exist in Arabidopsis, and that the second uses pyruvate, orthophosphate dikinase (PPDK). Gluconeogenesis is critical to fuel the transition from seed to seedling. Arabidopsis pck1 and ppdk mutants are compromised in seed-storage reserve mobilization and seedling establishment. Radiolabelling studies show that PCK predominantly allows sugars to be made from dicarboxylic acids, which are products of lipid breakdown. However, PPDK also allows sugars to be made from pyruvate, which is a major product of protein breakdown. We propose that both routes have been evolutionarily conserved in plants because, while PCK expends less energy, PPDK is twice as efficient at recovering carbon from pyruvate.

          Abstract

          During seed germination plants use gluconeogenesis to mobilize noncarbohydrate energy reserves. Here Eastmond et al. show that plants, unlike other eukaryotes, do not solely rely on a gluconeogenic pathway via the enzyme PCK but also use a second pathway relying on PPDK.

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          Most cited references38

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          Genome-wide insertional mutagenesis of Arabidopsis thaliana.

          J M Alonso (2003)
          Over 225,000 independent Agrobacterium transferred DNA (T-DNA) insertion events in the genome of the reference plant Arabidopsis thaliana have been created that represent near saturation of the gene space. The precise locations were determined for more than 88,000 T-DNA insertions, which resulted in the identification of mutations in more than 21,700 of the approximately 29,454 predicted Arabidopsis genes. Genome-wide analysis of the distribution of integration events revealed the existence of a large integration site bias at both the chromosome and gene levels. Insertion mutations were identified in genes that are regulated in response to the plant hormone ethylene.
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            Genome-wide atlas of transcription during maize development.

            Maize is an important model species and a major constituent of human and animal diets. It has also emerged as a potential feedstock and model system for bioenergy research due to recent worldwide interest in developing plant biomass-based, carbon-neutral liquid fuels. To understand how the underlying genome sequence results in specific plant phenotypes, information on the temporal and spatial transcription patterns of genes is crucial. Here we present a comprehensive atlas of global transcription profiles across developmental stages and plant organs. We used a NimbleGen microarray containing 80,301 probe sets to profile transcription patterns in 60 distinct tissues representing 11 major organ systems of inbred line B73. Of the 30,892 probe sets representing the filtered B73 gene models, 91.4% were expressed in at least one tissue. Interestingly, 44.5% of the probe sets were expressed in all tissues, indicating a substantial overlap of gene expression among plant organs. Clustering of maize tissues based on global gene expression profiles resulted in formation of groups of biologically related tissues. We utilized this dataset to examine the expression of genes that encode enzymes in the lignin biosynthetic pathway, and found that expansion of distinct gene families was accompanied by divergent, tissue-specific transcription patterns of the paralogs. This comprehensive expression atlas represents a valuable resource for gene discovery and functional characterization in maize. © 2011 The Authors. The Plant Journal © 2011 Blackwell Publishing Ltd.
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              Seed storage oil mobilization.

              Storage oil mobilization starts with the onset of seed germination. Oil bodies packed with triacylglycerol (TAG) exist in close proximity with glyoxysomes, the single membrane-bound organelles that house most of the biochemical machinery required to convert fatty acids derived from TAG to 4-carbon compounds. The 4-carbon compounds in turn are converted to soluble sugars that are used to fuel seedling growth. Biochemical analysis over the last 50 years has identified the main pathways involved in this process, including beta-oxidation, the glyoxylate cycle, and gluconeogenesis. In the last few years molecular genetic dissection of the overall process in the model oilseed species Arabidopsis has provided new insight into its complexity, particularly with respect to the specific role played by individual enzymatic steps and the subcellular compartmentalization of the glyoxylate cycle. Both abscisic acid (ABA) and sugars inhibit storage oil mobilization and a substantial degree of the control appears to operate at the transcriptional level.

                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                10 April 2015
                : 6
                : 6659
                Affiliations
                [1 ]Department of Plant Biology and Crop Science, Rothamsted Research, West Common , Harpenden, Hertfordshire AL5 2JQ, UK
                [2 ]Department of Plant Sciences, University of Cambridge , Downing Street, Cambridge CB2 3EA, UK
                [3 ]College of Natural and Agricultural Sciences, Center for Plant Cell Biology, University of California , Riverside, California 92521, USA
                [4 ]Max-Planck-Insitüt für Molekulare Pflanzenphysiologie , Am Mühlenberg 1, Potsdam-Golm D-14476, Germany
                [5 ]Departmento de Biologia Vegetal, Universidade Federal de Vicosa , Vicosa, Minas Gerais 36570-000, Brazil
                Author notes
                Article
                ncomms7659
                10.1038/ncomms7659
                4403315
                25858700
                0f81a33f-276e-4875-9ac5-b8766791c518
                Copyright © 2015, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 06 August 2014
                : 17 February 2015
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