Plasma membrane phylloquinone biosynthesis in nonphotosynthetic parasitic plants

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dc.contributor.authorGu, Xien
dc.contributor.authorChen, Ing-Ginen
dc.contributor.authorHarding, Scott A.en
dc.contributor.authorNyamdari, Batbayaren
dc.contributor.authorOrtega, Maria A.en
dc.contributor.authorClermont, Kristenen
dc.contributor.authorWestwood, James H.en
dc.contributor.authorTsai, Chung-Juien
dc.contributor.departmentSchool of Plant and Environmental Sciencesen
dc.date.accessioned2021-07-30T13:06:00Zen
dc.date.available2021-07-30T13:06:00Zen
dc.date.issued2021-04en
dc.description.abstractNonphotosynthetic holoparasites exploit flexible targeting of phylloquinone biosynthesis to facilitate plasma membrane redox signaling. 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 (PM) preparations of heterotrophic tissues with potential transmembrane redox function, but the molecular basis for this noncanonical pathway is unknown. Here, we provide evidence of PM 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 PM-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 PM electron transport. Genes encoding the PM 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.en
dc.description.notesWe thank L.-J. Xue for the GCC Python script, M. Curley, M. Tsai, N. Rodman, and K.B. Aulakh for laboratory assistance, M.K. Kandasamy for confocal microscopy assistance, and D. Lynn (Emory University) for insightful discussion. This research was supported by Georgia Research Alliance-Hank Haynes Forest Biotechnology Endowment (C.-J.T.), National Science Foundation grants IOS-1444567, IOS-1546867 (C.J.T.), and IOS-1238057 (J.H.W.), National Institute of Food and Agriculture grant VA-135997 (J.H.W.), and University of Georgia Graduate School's Innovative and Interdisciplinary Research Grant (X.G.).en
dc.description.sponsorshipGeorgia Research Alliance-Hank Haynes Forest Biotechnology Endowment; National Science FoundationNational Science Foundation (NSF) [IOS-1444567, IOS-1546867, IOS-1238057]; National Institute of Food and AgricultureUnited States Department of Agriculture (USDA)National Institute of Food and Agriculture [VA-135997]; University of Georgia Graduate School's Innovative and Interdisciplinary Research Granten
dc.description.versionPublished versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.doihttps://doi.org/10.1093/plphys/kiab031en
dc.identifier.eissn1532-2548en
dc.identifier.issn0032-0889en
dc.identifier.issue4en
dc.identifier.pmid33793953en
dc.identifier.urihttp://hdl.handle.net/10919/104455en
dc.identifier.volume185en
dc.language.isoenen
dc.rightsCreative Commons Attribution 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titlePlasma membrane phylloquinone biosynthesis in nonphotosynthetic parasitic plantsen
dc.title.serialPlant Physiologyen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten
dc.type.dcmitypeStillImageen

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