Extracellular 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 show here that perception of extracellular nucleotides, such as eATP, is important in plant–fungus interactions and that during colonization by the beneficial root endophyte Serendipita indica eATP accumulates in the apoplast at early symbiotic stages. Using liquid chromatography–tandem mass spectrometry, and cytological and functional analysis, we show that S. indica secrets SiE5′NT, an enzymatically active ecto‐5′‐nucleotidase capable of hydrolyzing nucleotides in the apoplast. Arabidopsis thaliana lines producing extracellular SiE5′NT are significantly better colonized, have reduced eATP levels, and altered responses to biotic stresses, indicating that SiE5′NT functions as a compatibility factor. Our data suggest that extracellular bioactive nucleotides and their perception play an important role in fungus–root interactions and that fungal‐derived enzymes can modify apoplastic metabolites to promote fungal accommodation.

SummaryPlants survey their environment for the presence of potentially harmful or beneficial microbes. During colonization, cell surface receptors perceive microbe‐derived or modified‐self ligands and initiate appropriate responses. The recognition of fungal chitin oligomers and the subsequent activation of plant immunity are well described. In contrast, the mechanisms underlying β‐glucan recognition and signaling activation remain largely unexplored. Here, we systematically tested immune responses towards different β‐glucan structures and show that responses vary between plant species. While leaves of the monocots Hordeum vulgare and Brachypodium distachyon can recognize longer (laminarin) and shorter (laminarihexaose) β‐1,3‐glucans with responses of varying intensity, duration and timing, leaves of the dicot Nicotiana benthamiana activate immunity in response to long β‐1,3‐glucans, whereas Arabidopsis thaliana and Capsella rubella perceive short β‐1,3‐glucans. Hydrolysis of the β‐1,6 side‐branches of laminarin demonstrated that not the glycosidic decoration but rather the degree of polymerization plays a pivotal role in the recognition of long‐chain β‐glucans. Moreover, in contrast to the recognition of short β‐1,3‐glucans in A. thaliana, perception of long β‐1,3‐glucans in N. benthamiana and rice is independent of CERK1, indicating that β‐glucan recognition may be mediated by multiple β‐glucan receptor systems.

Ligand recognition by cell-surface receptors underlies development and immunity in both animals and plants. Modulating receptor signalling is critical for appropriate cellular responses but the mechanisms ensuring this are poorly understood. Here, we show that signalling by plant receptors for pathogen-associated molecular patterns (PAMPs) in immunity and CLAVATA3/EMBRYO SURROUNDING REGION-RELATED peptides (CLEp) in development uses a similar regulatory module. In the absence of ligand, signalling is dampened through association with specific type-2C protein phosphatases. Upon activation, PAMP and CLEp receptors phosphorylate divergent cytosolic kinases, which, in turn, phosphorylate the phosphatases, thereby promoting receptor signalling. Our work reveals a regulatory circuit shared between immune and developmental receptor signalling, which may have broader important implications for plant receptor kinase-mediated signalling in general.

15Extracellular adenosine 5′-triphosphate (eATP) is an essential signaling molecule