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J. Biol. Chem., Vol. 282, Issue 7, 4613-4625, February 16, 2007

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Channeling of Eukaryotic Diacylglycerol into the Biosynthesis of Plastidial Phosphatidylglycerol^*

Markus Fritz, Heiko Lokstein^¶, Dieter Hackenberg^||, Ruth Welti^**, Mary Roth^**, Ulrich Zähringer, Martin Fulda¹, Wiebke Hellmeyer, Claudia Ott, Frank P. Wolter^¶¶, and Ernst Heinz

From the Biozentrum Klein Flottbek, Universität Hamburg, Ohnhorststrasse 18, D-22609 Hamburg, Germany, the Max-Planck-Gesellschaft, Generalverwaltung, Hofgartenstrasse 8, D-80539 München, Germany, the ^¶Institut für Biochemie und Biologie, Universität Potsdam, Pflanzenphysiologie, Karl-Liebknecht-Strasse 24–25, D-14476 Golm, Germany, the ^||Institut für Biologie/Pflanzenphysiologie, Humboldt-Universität zu Berlin, Unter den Linden 6, D-10099 Berlin, the ^**Division of Biology, Kansas State University, Kansas Lipidomics Research Center, Manhattan, Kansas 66506-4901, the Leibniz-Zentrum für Medizin und Biowissenschaften, Forschungszentrum Borstel, Parkallee 4, D-23845 Borstel, Germany, the Albrecht-von-Haller-Institut für Pflanzenwissenschaften, Georg-August Universität Göttingen, Biochemie der Pflanze, Justus-von-Liebig-Weg 11, D-37077 Göttingen, Germany, and the ^¶¶Bundesverband Deutscher Pflanzenzüchter, GVSmbH, Kaufmannstrasse 71–73, D-53115 Bonn, Germany

Plastidial glycolipids contain diacylglycerol (DAG) moieties, which are either synthesized in the plastids (prokaryotic lipids) or originate in the extraplastidial compartment (eukaryotic lipids) necessitating their transfer into plastids. In contrast, the only phospholipid in plastids, phosphatidylglycerol (PG), contains exclusively prokaryotic DAG backbones. PG contributes in several ways to the functions of chloroplasts, but it is not known to what extent its prokaryotic nature is required to fulfill these tasks. As a first step toward answering this question, we produced transgenic tobacco plants that contain eukaryotic PG in thylakoids. This was achieved by targeting a bacterial DAG kinase into chloroplasts in which the heterologous enzyme was also incorporated into the envelope fraction. From lipid analysis we conclude that the DAG kinase phosphorylated eukaryotic DAG forming phosphatidic acid, which was converted into PG. This resulted in PG with 2–3 times more eukaryotic than prokaryotic DAG backbones. In the newly formed PG the unique 3-trans-double bond, normally confined to 3-trans-hexadecenoic acid, was also found in sn-2-bound cis-unsaturated C18 fatty acids. In addition, a lipidomics technique allowed the characterization of phosphatidic acid, which is assumed to be derived from eukaryotic DAG precursors in the chloroplasts of the transgenic plants. The differences in lipid composition had only minor effects on measured functions of the photosynthetic apparatus, whereas the most obvious phenotype was a significant reduction in growth.

Received for publication, June 30, 2006 , and in revised form, December 8, 2006.

This paper is dedicated to Prof. Dr. A. Benson on the occasion of his 90th birthday.

^* This work was supported by the Gesellschaft für Technische Zusammenarbeit (Grant 91.7860.9-01-114) and the Bundesministerium für Bildung und Forschung (Napus 2000, FK 0312252F). Mass spectrometry performed at the Kansas Lipidomics Research Center (KLRC) Analytical Laboratory was supported by National Science Foundation (NSF) Grants MCB 0455318 and DBI 0521587 and by NSF EPSCoR Grant EPS-0236913, and by National Institutes of Health Grant P20 RR16475 from the National Center for Research Resources. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Table S1, Fig. 1S, and additional references.

¹ To whom correspondence should be addressed: Tel.: 49-551-39-5750; Fax: 49-551-39-5749; E-mail: mfulda{at}gwdg.de.

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