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J. Biol. Chem., Vol. 281, Issue 25, 17189-17196, June 23, 2006

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A Plant Locus Essential for Phylloquinone (Vitamin K₁) Biosynthesis Originated from a Fusion of Four Eubacterial Genes^*

Jeferson Gross¹, Won Kyong Cho, Lina Lezhneva, Jon Falk, Karin Krupinska, Kazuo Shinozaki^¶, Motoaki Seki^¶, Reinhold G. Herrmann, and Jörg Meurer²

From the Department Biology I, Botany, Ludwig-Maximilians-University Munich, Menzinger Strasse 67, D-80638 Munich, Germany, the Institute of Botany, University of Kiel, Olshausenstrasse 40, D-24098 Kiel, Germany, and the ^¶Plant Mutation Exploration Team, Plant Functional Genomics Research Group, RIKEN Genomic Sciences Center, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama City, Kanagawa, 230-0045, Japan

Phylloquinone is a compound present in all photosynthetic plants serving as cofactor for Photosystem I-mediated electron transport. Newly identified seedling-lethal Arabidopsis thaliana mutants impaired in the biosynthesis of phylloquinone possess reduced Photosystem I activity. The affected gene, called PHYLLO, consists of a fusion of four previously individual eubacterial genes, menF, menD, menC, and menH, required for the biosynthesis of phylloquinone in photosynthetic cyanobacteria and the respiratory menaquinone in eubacteria. The fact that homologous men genes reside as polycistronic units in eubacterial chromosomes and in plastomes of red algae strongly suggests that PHYLLO derived from a plastid operon during endosymbiosis. The principle architecture of the fused PHYLLO locus is conserved in the nuclear genomes of plants, green algae, and the diatom alga Thalassiosira pseudonana. The latter arose from secondary endosymbiosis of a red algae and a eukaryotic host indicating selective driving forces for maintenance and/or independent generation of the composite gene cluster within the nuclear genomes. Besides, individual menF genes, encoding active isochorismate synthases (ICS), have been established followed by splitting of the essential 3' region of the menF module of PHYLLO only in genomes of higher plants. This resulted in inactivation of the ICS activity encoded by PHYLLO and enabled a metabolic branch from the phylloquinone biosynthetic route to independently regulate the synthesis of salicylic acid required for plant defense. Therefore, gene fusion, duplication, and fission events adapted a eubacterial multienzymatic system to the metabolic requirements of plants.

Received for publication, February 23, 2006 , and in revised form, April 13, 2006.

^* 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.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) DQ084385 [GenBank] (cDNA RAFL 09-32-CO5 and DQ084386 [GenBank] (phyllo from Arabidopsis).

¹ Received a Ph.D. scholarship from the CAPES Foundation, subordinated to the Brazilian Ministry of Education.

² Supported by Grants ME 1794/1 and SFB TR1 from the German Science Foundation. To whom correspondence should be addressed. Tel.: 49-89-17861288; Fax: 49-89-1782274; E-mail: joerg.meurer{at}lrz.uni-muenchen.de.

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