The fungal root endophyte Serendipita indica modifies extracellular nucleotides to subvert plant immunity

Abstract

One sentence abstractImmune modulation by metabolites in plant fungus interaction\n\nAbstractExtracellular adenosine 5'-triphosphate (eATP) is an essential signaling molecule that mediates different cellular processes through its interaction with membrane-associated receptor proteins in animals and plants. eATP regulates plant growth, development and responses to biotic and abiotic stresses. Its accumulation in the apoplast induces ROS production and cytoplasmic calcium increase mediating a defense response to invading microbes. We demonstrate that perception of eATP is important in plant-fungus interaction and that during colonization by the beneficial root endophyte Serendipita indica accumulation of eATP in the apoplast occurs at early symbiotic stages. We show by liquid chromatography-tandem mass spectrometry, cytological and functional analysis that S. indica subvert eATP host response by secreting SiE5NT, an enzymatically active ecto-5'nucleotidase capable of hydrolyzing eATP to adenosine. A. thaliana lines producing extracellular SiE5NT are signi?cantly better colonized and have reduced eATP levels and defense signaling, indicating that SiE5NT functions as a compatibility factor. Our data show that extracellular bioactive nucleotides play an important role in fungus-root interactions and that fungi can modify plant derived metabolites in the apoplast to modulate host immunity.