Direct nitrogen, phosphorus and carbon exchanges between Mucoromycotina ‘fine root endophyte’ fungi and a flowering plant in novel monoxenic cultures

Abstract

Summary Most plants form mycorrhizal associations with mutualistic soil fungi. Through these partnerships, resources are exchanged including photosynthetically fixed carbon for fungal‐acquired nutrients. Recently, it was shown that the diversity of associated fungi is greater than previously assumed, extending to Mucoromycotina fungi. These Mucoromycotina ‘fine root endophytes’ (MFRE) are widespread and generally co‐colonise plant roots together with Glomeromycotina ‘coarse’ arbuscular mycorrhizal fungi (AMF). Until now, this co‐occurrence has hindered the determination of the direct function of MFRE symbiosis. To overcome this major barrier, we developed new techniques for fungal isolation and culture and established the first monoxenic in vitro cultures of MFRE colonising a flowering plant, clover. Using radio‐ and stable‐isotope tracers in these in vitro systems, we measured the transfer of 33P, 15N and 14C between MFRE hyphae and the host plant. Our results provide the first unequivocal evidence that MFRE fungi are nutritional mutualists with a flowering plant by showing that clover gained both 15N and 33P tracers directly from fungus in exchange for plant‐fixed C in the absence of other micro‐organisms. Our findings and methods pave the way for a new era in mycorrhizal research, firmly establishing MFRE as both mycorrhizal and functionally important in terrestrial ecosystems.

GlobalAMFungi: a global database of arbuscular mycorrhizal fungal occurrences from high‐throughput sequencing metabarcoding studies

“…Similar to the above‐listed databases, GlobalAMFungi so far includes only the Glomeromycotinian AM fungal taxa, while the putative AM fungi from the Mucoromycotina subphylum (Orchard et al ., 2017; Albornoz et al ., 2022) might be included in future updates of the database when the real nature of the symbiosis is described in more detail (e.g. Hoysted et al ., 2023). Compared with the above‐listed databases, GlobalAMFungi provides orders of magnitude more data on the distribution of AM fungal taxa together with detailed metadata about samples, obtained from original publications or global databases.…”

The good, the bad, and the phosphate: regulation of beneficial and detrimental plant–microbe interactions by the plant phosphate status

“…Besides AM symbiosis, also the symbiosis with Mucoromycotina fine root endophytes (Hoysted et al ., 2023) and in woody plants with ectomycorrhizal fungi (Bücking & Heyser, 2003; Cairney, 2011) contributes to the P i nutrition. Yet, only little is known about the molecular programs that enable these associations (Garcia et al ., 2015) and no evidence for the involvement of the plant PSR system in the regulation of associations with fine root endophytes or ectomycorrhizal fungi has been described yet.…”

Fungal symbiont diversity drives growth of Holcus lanatus depending on soil nutrient availability

“…We were not able to discern whether MFRE or AM fungi were responsible for supplying plants with 15 N in the MFRE+AM fungi pots; however, given the similar %TRL colonisation by each fungal symbiont, and recent research confirming direct N transfer from MFRE to a vascular plant in vitro (Hoysted et al, 2023), it is likely that both fungal symbionts contributed to the N nutrition of H. lanatus in our experiment. We observed striking differences in plant morphological and physiological characteristics between the two fungal inoculation treatments.…”

“…Other Mucoromycotina fungi closely related to symbiotic Endogonales are saprotrophic, indicating that MFRE may well share at least some of the molecular machinery required for a facultative saprotrophic lifestyle (Spatafora et al, 2016). The putative saprotrophic capabilities of MFRE and their assumed ability to access and transfer N from organic sources to plants-albeit only tested so far with non-vascular plants (e.g., liverworts; Field et al, 2019)-support the hypothesis that MFRE have a complementary role in plant nutrition alongside AM fungi, with potentially important ecological implications for plant community structure and nutrient cycling, especially with regard to N (Field et al, 2019;Howard et al, 2022;Hoysted et al, 2019Hoysted et al, , 2023.…”

“…MFRE are an understudied group of Endogonales soil fungi that are common across a wide variety of habitats (Albornoz et al., 2021; Kowal et al., 2022; Orchard, Standish, Dickie, et al., 2017). Although MFRE are molecularly and morphologically distinct from Glomeromycotina AM fungi (Orchard, Hilton, Bending, et al., 2017), they share some functional characteristics with the latter, such as obtaining C from plants in exchange for N and P (Field et al., 2016, 2019; Field, Rimington, et al., 2015; Hoysted et al., 2019, 2023). However, unlike strictly biotrophic AM fungi, MFRE can be isolated and grown in vitro in the absence of a plant host (Field, Rimington, et al., 2015; Hoysted et al., 2023).…”