A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes.
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.
Gross
Jeferson
J
Department Biology I, Botany, Ludwig-Maximilians-University Munich, Menzinger Strasse 67, D-80638 Munich, Germany.
Cho
Won Kyong
WK
Department Biology I, Botany, Ludwig-Maximilians-University Munich, Menzinger Strasse 67, D-80638 Munich, Germany.
Lezhneva
Lina
L
Department Biology I, Botany, Ludwig-Maximilians-University Munich, Menzinger Strasse 67, D-80638 Munich, Germany.
Falk
Jon
J
Institute of Botany, University of Kiel, Olshausenstrasse 40, D-24098 Kiel, Germany.
Krupinska
Karin
K
Institute of Botany, University of Kiel, Olshausenstrasse 40, D-24098 Kiel, Germany.
Shinozaki
Kazuo
K
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.
Seki
Motoaki
M
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.
Herrmann
Reinhold G
RG
Department Biology I, Botany, Ludwig-Maximilians-University Munich, Menzinger Strasse 67, D-80638 Munich, Germany.
Meurer
Jörg
J
Department Biology I, Botany, Ludwig-Maximilians-University Munich, Menzinger Strasse 67, D-80638 Munich, Germany. Electronic address: joerg.meurer@lrz.uni-muenchen.de.
D020418:Algal Proteins / Q000235:genetics / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics; D001483:Base Sequence; D002467:Cell Nucleus / Q000378:metabolism; D000460:Chlorophyta / Q000378:metabolism; D019143:Evolution, Molecular; D008956:Models, Chemical; D008957:Models, Genetic; D008969:Molecular Sequence Data; D010940:Plant Proteins / Q000737:chemistry*; D012689:Sequence Homology, Nucleic Acid; D013559:Symbiosis; D010837:Vitamin K 1 / Q000737:chemistry / Q000378:metabolism* / Q000494:pharmacology*
D020418:Algal Proteins; D010940:Plant Proteins; D010837:Vitamin K 1