Defining the pre-symbiotic transcriptional landscape of rice roots

Plants interact with a plethora of organisms in the rhizosphere, with outcomes that range from detrimental to beneficial. Arbuscular mycorrhizal (AM) symbiosis is the most ubiquitous beneficial plant interaction in terrestrial ecosystems and involves soil borne fungi of the Glomeromycotina. It is believed that plants detect diagnostic signals for the discrimination between beneficial arbuscular mycorrhizal (AM) fungi and parasitic fungi during the pre-symbiotic molecular crosstalk. Here, we investigated the transcriptome of rice roots upon exposure to the complete cocktail of fungal exudates from either beneficial Rhizophagus irregularis or pathogenic Magnaporthe oryzae. We report that regardless of the exudate donor species, the transcriptional response lacked diagnostic differences. Instead, the profiles were marked by the common suppression of symbiosis signalling components, accompanied by the induction of a generic stress response (GSR) and defense-related signature, which was retained in a suite of symbiosis signalling mutants impaired at different stages of symbiosis development. However, upon permitting physical engagement with AM fungi, a striking reversion in the transcriptional responses occurred marked by the simultaneous relaxation of symbiosis signalling suppression and down-regulation of defense-related and GSR markers, overall comparable between wild-type and mutants. Our data therefore reveal that rather than specific recognition in the rhizosphere, a sequence of signals orchestrates stress, immunity and symbiosis, pivoting towards symbiosis potentially at the stage of plant-fungal contact formation. Significance StatementMost plant roots engage in symbiosis with beneficial mycorrhizal fungi. Before physical contact, early signal exchanges involve diffusible molecules. The bouquet of chemicals released by beneficial versus detrimental fungi has been proposed to convey specificity for signal transduction, transcriptional output and responses. Here we characterised the transcriptomes of rice roots to exudates from beneficial and pathogenic fungi, and found that they lack specific signatures but elicit a generic stress and immune response and suppression of symbiosis signalling. This profile was reversed, along with activation of symbiotic transcriptional responses, only when AM fungi were allowed to establish physical contact. This reveals the need for additional, unknown, layers of signal exchanges for plants to commit to symbiosis.