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      FAX1, a Novel Membrane Protein Mediating Plastid Fatty Acid Export

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          Abstract

          Fatty acid synthesis in plants occurs in plastids, and thus, export for subsequent acyl editing and lipid assembly in the cytosol and endoplasmatic reticulum is required. Yet, the transport mechanism for plastid fatty acids still remains enigmatic. We isolated FAX1 ( fatty acid export 1), a novel protein, which inserts into the chloroplast inner envelope by α-helical membrane-spanning domains. Detailed phenotypic and ultrastructural analyses of FAX1 mutants in Arabidopsis thaliana showed that FAX1 function is crucial for biomass production, male fertility and synthesis of fatty acid-derived compounds such as lipids, ketone waxes, or pollen cell wall material. Determination of lipid, fatty acid, and wax contents by mass spectrometry revealed that endoplasmatic reticulum (ER)-derived lipids decreased when FAX1 was missing, but levels of several plastid-produced species increased. FAX1 over-expressing lines showed the opposite behavior, including a pronounced increase of triacyglycerol oils in flowers and leaves. Furthermore, the cuticular layer of stems from fax1 knockout lines was specifically reduced in C29 ketone wax compounds. Differential gene expression in FAX1 mutants as determined by DNA microarray analysis confirmed phenotypes and metabolic imbalances. Since in yeast FAX1 could complement for fatty acid transport, we concluded that FAX1 mediates fatty acid export from plastids. In vertebrates, FAX1 relatives are structurally related, mitochondrial membrane proteins of so-far unknown function. Therefore, this protein family might represent a powerful tool not only to increase lipid/biofuel production in plants but also to explore novel transport systems involved in vertebrate fatty acid and lipid metabolism.

          Abstract

          The novel protein FAX1 mediates the export of free fatty acids across the inner membrane of chloroplasts so that they can be processed in other plant cell organelles to generate oils, waxes, and other lipids.

          Author Summary

          Fatty acid synthesis in plants occurs in chloroplasts—the organelle more commonly known for conducting photosynthesis. For subsequent lipid assembly to be possible in the endoplasmatic reticulum (ER), export of these fatty acids across the chloroplast envelope membranes is required. The mechanism of this transport until now has not been known. We isolated FAX1 ( fatty acid export 1), a novel membrane protein in chloroplast inner envelopes. FAX1 function is crucial for biomass production, male fertility, and the synthesis of fatty acid-derived compounds like lipids, waxes, or cell wall material of pollen grains. Whereas ER-derived lipids decreased when FAX1 was missing, levels of plastid-produced lipids increased. FAX1 over-expressing mutants showed the opposite behavior, including an increase of triacyglycerol oils. Because FAX1 could complement for fatty acid transport in yeast, we concluded that FAX1 mediates the export of free fatty acids from chloroplasts. In vertebrates, FAX1 relatives are structurally related proteins of so-far unknown function in mitochondria. This protein family may thus represent a powerful tool not only to increase lipid oil and biofuel production in plants but also to explore novel transport systems in animals.

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          Most cited references 51

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          GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox.

          High-throughput gene expression analysis has become a frequent and powerful research tool in biology. At present, however, few software applications have been developed for biologists to query large microarray gene expression databases using a Web-browser interface. We present GENEVESTIGATOR, a database and Web-browser data mining interface for Affymetrix GeneChip data. Users can query the database to retrieve the expression patterns of individual genes throughout chosen environmental conditions, growth stages, or organs. Reversely, mining tools allow users to identify genes specifically expressed during selected stresses, growth stages, or in particular organs. Using GENEVESTIGATOR, the gene expression profiles of more than 22,000 Arabidopsis genes can be obtained, including those of 10,600 currently uncharacterized genes. The objective of this software application is to direct gene functional discovery and design of new experiments by providing plant biologists with contextual information on the expression of genes. The database and analysis toolbox is available as a community resource at https://www.genevestigator.ethz.ch.
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            A low-viscosity epoxy resin embedding medium for electron microscopy.

             A R Spurr (1968)
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              Acyl-lipid metabolism.

              Acyl lipids in Arabidopsis and all other plants have a myriad of diverse functions. These include providing the core diffusion barrier of the membranes that separates cells and subcellular organelles. This function alone involves more than 10 membrane lipid classes, including the phospholipids, galactolipids, and sphingolipids, and within each class the variations in acyl chain composition expand the number of structures to several hundred possible molecular species. Acyl lipids in the form of triacylglycerol account for 35% of the weight of Arabidopsis seeds and represent their major form of carbon and energy storage. A layer of cutin and cuticular waxes that restricts the loss of water and provides protection from invasions by pathogens and other stresses covers the entire aerial surface of Arabidopsis. Similar functions are provided by suberin and its associated waxes that are localized in roots, seed coats, and abscission zones and are produced in response to wounding. This chapter focuses on the metabolic pathways that are associated with the biosynthesis and degradation of the acyl lipids mentioned above. These pathways, enzymes, and genes are also presented in detail in an associated website (ARALIP: http://aralip.plantbiology.msu.edu/). Protocols and methods used for analysis of Arabidopsis lipids are provided. Finally, a detailed summary of the composition of Arabidopsis lipids is provided in three figures and 15 tables.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                3 February 2015
                February 2015
                27 February 2015
                : 13
                : 2
                Affiliations
                [1 ]Biochemie und Physiologie der Pflanzen, Department Biologie I - Botanik, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Germany
                [2 ]Research Center of Bioenergy and Bioremediation RCBB, College of Resources and Environment, Southwest University, Beibei Dist., Chongqing, P.R. China
                [3 ]Munich Centre for Integrated Protein Science CIPSM, Ludwig-Maximilians-Universität München, München, Germany
                [4 ]Max Planck Institut für Molekulare Pflanzenphysiologie MPIMP, Potsdam-Golm, Germany
                [5 ]Institute of Cellular and Molecular Botany, Department of Ecophysiology, University of Bonn, Bonn, Germany
                University of Massachusetts at Amherst, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NL JS KP. Performed the experiments: NL ILG PG VZ LS. Analyzed the data: NL PG LS KP. Wrote the paper: NL PG LS KP. Performed structural modeling: KP.

                Article
                PBIOLOGY-D-14-01492
                10.1371/journal.pbio.1002053
                4344464
                25646734

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                Page count
                Figures: 8, Tables: 3, Pages: 37
                Product
                Funding
                NL’s doctoral studies at the LMU Munich were supported by the China Scholarship Council (CSC). Further support was received from grants of the Deutsche Forschungsgemeinschaft (DFG) to JS and LS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                DNA microarray data are available in the ArrayExpress database ( www.ebi.ac.uk/arrayexpress) under accession number E-MTAB-3090. The sequence of PsFAX1 is deposited at GenBank, accession KF981436.

                Life sciences

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