Phylloquinone (PhQ) is found predominantly in thylakoid membranes of photosynthetic tissues where it functions in photosystem I electron transport. PhQ has also been detected in plasma membranes, but neither the molecular basis nor the significance of this noncanonical pathway has been elucidated. Here we provide evidence of plasma membrane PhQ biosynthesis in a non-photosynthetic holoparasite Phelipanche aegyptiaca. A nonphotosynthetic role is supported by transcription of the entire suite of PhQ biosynthetic genes, plasma membrane-localization of the terminal enzymes, and detection of PhQ in Phelipanche seeds. Analysis of PhQ-coexpressed genes in the holoparasite revealed increased cellular commitment to oxidation-reduction and defense relative to photosynthetic parasites. Coexpression network inference identified oxidoreductases involved in plasma membrane electron transport, implicating PhQ in a transmembrane redox relay associated with parasitism. Plasma membrane PhQ biosynthesis is also predicted to occur in photoautotrophic taxa via alternative splicing, suggesting nonplastidial PhQ is evolutionarily conserved.
Phylloquinone is a lipophilic naphthoquinone found predominantly in chloroplasts and best known for its function in photosystem I electron transport and disulfide bridge formation of photosystem II subunits. Phylloquinone has also been detected in plasma membrane preparations of heterotrophic tissues with potential transmembrane redox function, but the molecular basis for this noncanonical pathway is unknown. Here we provide evidence of plasma membrane phylloquinone biosynthesis in a nonphotosynthetic holoparasite Phelipanche aegyptiaca. A nonphotosynthetic and nonplastidial role for phylloquinone is supported by transcription of phylloquinone biosynthetic genes during seed germination and haustorium development, by plasma membrane-localization of alternative terminal enzymes, and by detection of phylloquinone in germinated seeds. Comparative gene network analysis with photosynthetically competent parasites revealed a bias of P. aegyptiaca phylloquinone genes toward coexpression with oxidoreductases involved in plasma membrane electron transport. Genes encoding the plasma membrane phylloquinone pathway are also present in several photoautotrophic taxa of Asterids, suggesting an ancient origin of multifunctionality. Our findings suggest that nonphotosynthetic holoparasites exploit alternative targeting of phylloquinone for transmembrane redox signaling associated with parasitism.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.