Plasma membrane phylloquinone biosynthesis in nonphotosynthetic parasitic plants.

Xi Gu,Ing-Gin Chen,Chung-Jui Tsai,Kristen Clermont,Batbayar Nyamdari,Scott A Harding,James H Westwood,Maria A Ortega

doi:10.1093/plphys/kiab031

Abstract

Nonphotosynthetic 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.

Highlights

Phylloquinone is a membrane-bound naphthoquinone derivative known to function as an essential electron acceptor in photosystem I (PSI; Brettel et al, 1986)
We propose that parasitic plants exploit alternative phylloquinone targeting for plasma membrane (PM) redox regulation associated with parasitism
Phelipanche aegyptiaca contains the full complement of phylloquinone biosynthetic genes Phylloquinone pathway protein sequences of Mimulus guttatus, a photoautotroph from Phrymaceae sister to Orobanchaceae, were searched against transcript assemblies available from the Parasitic Plant Genome Project (Yang et al, 2015)

Summary

Introduction

Phylloquinone (vitamin K1) is a membrane-bound naphthoquinone derivative known to function as an essential electron acceptor in photosystem I (PSI; Brettel et al, 1986). Phylloquinone serves as an electron carrier for protein disulfide bond formation crucial for PSII assembly (Furt et al, 2010; Karamoko et al, 2011; Lu et al, 2013).

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