Microbiota-mediated adaptation of non-mycorrhizal plants to phosphorus-limited soils

Most plants rely on the arbuscular mycorrhizal symbiosis to meet their P requirements. Interestingly, while several plant lineages have abandoned this symbiosis during their evolution, this loss is often associated to a symbiont switch, with the development of more recent associations, such as ectomycorrhizae or orchid mycorrhizae. Surprisingly, no particular adaptation has been described for non-mycorrhizal Brassicaceae, Cyperaceae, and Caryophyllaceae plants, raising the question of how they support their P nutrition. We hypothesize that diverse fungi may play analogous roles to arbuscular mycorrhizal fungi, contributing significantly to P nutrition of NM plants, particularly in P-deficient soils. we characterized the fungal root-associated microbiota of these three families of non-mycorrhizal plants. To that end, we conducted a large-scale ITS2 metabarcoding analysis on wild-growing non-mycorrhizal species across 7 sites of contrasting levels of plant-available P. Our results show that non-mycorrhizal plants select slightly different fungal communities compared with their mycorrhizal neighbours, albeit with little similarities between non-mycorrhizal families. With the aim to identify taxa linked to shoot P accumulation, we used a machine-learning approach and discovered 85 fungal taxa associated with higher P accumulation in non-mycorrhizal plants, primarily from the Helotiales (24 OTUs) and Pleosporales (19 OTUs) orders, including known plant-beneficial lineages. With the hypothesis that these Helotiales fungi are of prime importance for nutrition of non-mycorrhizal plants, we isolated representative strains of two of these taxa and examined their effects on growth and P content of three non-mycorrhizal plant species. Our results showed that fungi from these lineages enhance the growth and P acquisition of several native non-mycorrhizal plant species under P-limiting conditions via mycorrhizal-like P transfer mechanisms. These findings establish the association with diverse Helotiales mycorrhizal-like fungi as new nutritional adaptations, balancing the loss of the arbuscular mycorrhizal symbiosis in non-mycorrhizal plants.