Plasma membrane phylloquinone biosynthesis in nonphotosynthetic parasitic plants

Abstract

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.

Hypoxia-Induced Aquaporins and Regulation of Redox Homeostasis by a Trans-Plasma Membrane Electron Transport System in Maize Roots

“…Additionally, vitamin K 1 has been identified in maize and soybean PM [44,47] that acts as a mobile electron and proton carrier and as an effective antioxidant inside the membrane [100,101]. The upregulation of menG (Supplementary Table S1) and the higher abundance of the NAD(P)H:quinone reductase (Table 2) indicated a de novo synthesis of vitamin K 1 in root PM [102]. Further, the upregulation of the ubiquinone biosynthetic pathway (Supplementary Table S1) and downregulation of complex III further supported the function of vitamin K 1 in membrane protection.…”