Feremycorrhizal symbiosis confers growth and nutritional benefits to mycorrhizal and non-mycorrhizal crops

Abstract

Feremycorrhiza (FM) is a newly discovered plant-fungus symbiosis that improves plant growth and nutrition without development of interface structures (i.e. no root colonization). The host plant range in the FM symbiosis is currently unknown. We report the results of controlled environment investigations characterizing the capability of crops to establish FM symbiosis with Austroboletus occidentalis, along with comprehensive in vitro studies to unravel the functional mechanisms underlying the phosphorus (P) nutritional benefits conferred to host plants. After 16 weeks of growth in a natural low-nutrient field soil (containing indigenous microbes), two mycorrhizal crops [wheat (Triticum aestivum) and barley (Hordeum vulgare)], and the non-mycorrhizal crop canola (Brassica napus) inoculated with A. occidentalis had significantly higher shoot biomass compared to the control (non-inoculated) plants. The FM symbiosis also led to significant grain yield increases in wheat (by 54%) and barley (by 37%) compared to the control plants, while canola was harvested before setting seeds due to slow growth under nutrient deficiency. In all crops, the FM symbiosis significantly improved the shoot nutrient content, including that of P, potassium and magnesium. Total nitrogen accumulation (shoot + grain content) was also significantly higher in all inoculated vs control crops. Inoculated treatments had reduced soil pH compared to the control, which was attributed to fungal activities in soil, leading to greater nutrient (P, in particular) availability to host plants. Presence of A. occidentalis in soil did not affect root colonization by indigenous arbuscular mycorrhizal fungi in wheat and barley, and no root colonization was detected in canola. Our in vitro studies demonstrated the solubilization, by A. occidentalis, of the water-insoluble P forms, including calcium phosphate (CaP, as hydroxyapatite), iron phosphate (FePO4), and aluminium phosphate (AlPO4) via exudation of organic acid anions (mainly oxalate, along with citrate and fumarate). The 31P nuclear magnetic resonance (NMR) spectroscopy revealed the presence of similar P species (dominated by orthophosphate and long-chain inorganic polyphosphates) in the agar-based media supplemented with different P forms (KH2PO4, CaP, FePO4 or AlPO4), indicating that all three water-insoluble P compounds were solubilized and transformed by the FM fungus. Furthermore, our in vitro studies revealed that the FM fungus converted a large proportion of the solubilized P (free orthophosphate) into long-chain inorganic polyphosphates (making up to 51% of total P in the media). The results demonstrated that the three important grain crops, regardless of their capacity to support arbuscular mycorrhizae, could get the growth and nutritional benefits from the FM symbiosis, emphasizing the potential of A. occidentalis as a novel fungal biofertilizer for agricultural crops.