title: Phylloquinone (vitamin K(1) ) biosynthesis in plants: two peroxisomal thioesterases of Lactobacillales origin hydrolyze 1,4-dihydroxy-2-naphthoyl-CoA.
abstract: It is not known how plants cleave the thioester bond of 1,4-dihydroxy-2-naphthoyl-CoA (DHNA-CoA), a necessary step to form the naphthoquinone ring of phylloquinone (vitamin K(1) ). In fact, only recently has the hydrolysis of DHNA-CoA been demonstrated to be enzyme driven in vivo, and the cognate thioesterase characterized in the cyanobacterium Synechocystis. With a few exceptions in certain prokaryotic (Sorangium and Opitutus) and eukaryotic (Cyanidium, Cyanidioschyzon and Paulinella) organisms, orthologs of DHNA-CoA thioesterase are missing outside of the cyanobacterial lineage. In this study, genomic approaches and functional complementation experiments identified two Arabidopsis genes encoding functional DHNA-CoA thioesterases. The deduced plant proteins display low percentages of identity with cyanobacterial DHNA-CoA thioesterases, and do not even share the same catalytic motif. GFP-fusion experiments demonstrated that the Arabidopsis proteins are targeted to peroxisomes, and subcellular fractionations of Arabidopsis leaves confirmed that DHNA-CoA thioesterase activity occurs in this organelle. In vitro assays with various aromatic and aliphatic acyl-CoA thioester substrates showed that the recombinant Arabidopsis enzymes preferentially hydrolyze DHNA-CoA. Cognate T-DNA knock-down lines display reduced DHNA-CoA thioesterase activity and phylloquinone content, establishing in vivo evidence that the Arabidopsis enzymes are involved in phylloquinone biosynthesis. Extraordinarily, structure-based phylogenies coupled to comparative genomics demonstrate that plant DHNA-CoA thioesterases originate from a horizontal gene transfer with a bacterial species of the Lactobacillales order.
authors.affiliation: Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE 68588, USA.
authors.forename: Joshua R
authors.initials: JR
authors.lastname: Widhalm
authors.forename: Anne-Lise
authors.initials: AL
authors.lastname: Ducluzeau
authors.forename: Nicole E
authors.initials: NE
authors.lastname: Buller
authors.forename: Christian G
authors.initials: CG
authors.lastname: Elowsky
authors.forename: Laura J
authors.initials: LJ
authors.lastname: Olsen
authors.forename: Gilles J C
authors.initials: GJ
authors.lastname: Basset
mesh_terms: D000214:Acyl Coenzyme A / Q000378:metabolism*; D017360:Arabidopsis / Q000166:cytology / Q000201:enzymology* / Q000235:genetics; D029681:Arabidopsis Proteins / Q000235:genetics / Q000302:isolation & purification / Q000378:metabolism; D001426:Bacterial Proteins / Q000235:genetics; D055786:Gene Knockout Techniques; D022761:Gene Transfer, Horizontal; D005816:Genetic Complementation Test; D023281:Genomics; D005838:Genotype; D006868:Hydrolysis; D056546:Lactobacillales / Q000201:enzymology* / Q000235:genetics; D016254:Mutagenesis, Insertional; D020675:Peroxisomes / Q000201:enzymology* / Q000378:metabolism; D010802:Phylogeny; D018515:Plant Leaves / Q000201:enzymology / Q000378:metabolism; D011993:Recombinant Fusion Proteins; D013379:Substrate Specificity; D046939:Synechocystis / Q000201:enzymology / Q000235:genetics; D013869:Thiolester Hydrolases / Q000235:genetics* / Q000302:isolation & purification / Q000378:metabolism; D010837:Vitamin K 1 / Q000031:analogs & derivatives* / Q000737:chemistry / Q000378:metabolism*; D014815:Vitamins / Q000737:chemistry / Q000378:metabolism*
chemical_list: D000214:Acyl Coenzyme A; D029681:Arabidopsis Proteins; D001426:Bacterial Proteins; D011993:Recombinant Fusion Proteins; D014815:Vitamins; D010837:Vitamin K 1; D013869:Thiolester Hydrolases