The menD and menE homologs code for 2-succinyl-6-hydroxyl-2,4-cyclohexadiene-1-carboxylate synthase and O-succinylbenzoic acid–CoA synthase in the phylloquinone biosynthetic pathway of Synechocystis sp. PCC 6803

131

162

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.

Section: Psimentioning

confidence: 99%

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

Gross

Cho

Lezhneva

et al. 2006

131

162

“…The phylloquinone molecule is composed of a naphthoquinone ring, which can exist in the oxidized quinone or in the reduced hydroquinone form, and a prenyl side chain derived from phytyl-diphosphate. The biosynthesis of menaquinone, a bacterial vitamin K analog carrying an unsaturated side chain, and of phylloquinone has been studied in Escherichia coli and in cyanobacteria, respectively (7)(8)(9). The naphthoquinone ring is derived from chorismate, which is converted into 1,4-dihydroxy-2-naphthoate (DHNA) by six consecutive reactions (Fig.…”

mentioning

confidence: 99%

“…The role of phylloquinone in photosynthesis has been studied by employing loss-of-function mutants of cyanobacteria (menA, menB, menD, menE, menG) (7,9,10). A block in biosynthesis resulting in total loss of phylloquinone has only a minor impact on photosynthesis or growth of Synechocystis under low light conditions, presumably, because other hydroquinones, such as plastoquinone, can largely substitute for phylloquinone deficiency in PSI (7).…”

mentioning

confidence: 99%

Deficiency in Phylloquinone (Vitamin K1) Methylation Affects Prenyl Quinone Distribution, Photosystem I Abundance, and Anthocyanin Accumulation in the Arabidopsis AtmenG Mutant

Lohmann

Schöttler

Bréhélin

et al. 2006

106

Phylloquinone (vitamin K 1 ) is synthesized in cyanobacteria and in chloroplasts of plants, where it serves as electron carrier of photosystem I. The last step of phylloquinone synthesis in cyanobacteria is the methylation of 2-phytyl-1,4-naphthoquinone by the menG gene product. Here, we report that the uncharacterized Arabidopsis gene At1g23360, which shows sequence similarity to menG, functionally complements the Synechocystis menG mutant. An Arabidopsis mutant, AtmenG, carrying a T-DNA insertion in the gene At1g23360 is devoid of phylloquinone, but contains an increased amount of 2-phytyl-1,4-naphthoquinone. Phylloquinone and 2-phytyl-1,4-naphthoquinone in thylakoid membranes of wild type and AtmenG, respectively, predominantly localize to photosystem I, whereas excess amounts of prenyl quinones are stored in plastoglobules. Photosystem I reaction centers are decreased in AtmenG plants under high light, as revealed by immunoblot and spectroscopic measurements. Anthocyanin accumulation and chalcone synthase (CHS1) transcription are affected during high light exposure, indicating that alterations in photosynthesis in AtmenG affect gene expression in the nucleus. Photosystem II quantum yield is decreased under high light. Therefore, the loss of phylloquinone methylation affects photosystem I stability or turnover, and the limitation in functional photosystem I complexes results in overreduction of photosystem II under high light.

“…Loss of phylloquinone synthesis has different effects in cyanobacteria and land plants. In cyanobacteria, insertional inactivation of the menA, -B, -D, and -E genes leads to the complete absence of phylloquinone, which is replaced by plastoquinone-9 in PSI (2,3,16,36). However, inactivation of menG, the last enzyme involved in the phylloquinone synthesis pathway, leads to the accumulation of demethylphylloquinone, which replaces phylloquinone in PSI (5).…”

mentioning

confidence: 99%

“…PCC 6803 menDdeficient mutant, the missing phylloquinone is replaced by plastoquinone-9, which acts as a substitute for phylloquinone and mediates electron transfer from A 0 to F X (36). Consequently, the PSI complex is functional.…”

mentioning

confidence: 99%

Loss of Phylloquinone in Chlamydomonas Affects Plastoquinone Pool Size and Photosystem II Synthesis

Lefebvre-Legendre

Rappaport

Finazzi

et al. 2007

Phylloquinone functions as the electron transfer cofactor at the A 1 site of photosystem I. We have isolated and characterized a mutant of Chlamydomonas reinhardtii, menD1, that is deficient in MenD, which encodes 2-succinyl-6-hydroxy-2,4-cyclohexadiene-1-carboxylate synthase, an enzyme that catalyzes the first specific step of the phylloquinone biosynthetic pathway. The mutant is photosynthetically active but light-sensitive. Analysis of total pigments by mass spectrometry reveals that phylloquinone is absent in menD1, but plastoquinone levels are not affected. This is further confirmed by the rescue of menD1 by addition of phylloquinone to the growth medium. Analysis of electron transfer by absorption spectroscopy indicates that plastoquinone replaces phylloquinone in photosystem I and that electron transfer from A 1 to the iron-sulfur centers is slowed down at least 40-fold. Consistent with a replacement of phylloquinone by plastoquinone, the size of the free plastoquinone pool of menD1 is reduced by 20 -30%. In contrast to cyanobacterial MenD-deficient mutants, photosystem I accumulates normally in menD1, whereas the level of photosystem II declines. This decrease is because of reduced synthesis of the photosystem II core subunits. The relationship between plastoquinone occupancy of the A 1 site in photosystem I and the reduced accumulation of photosystem II is discussed.