Plant-microbe interactions through a lens: tales from the mycorrhizosphere.

BACKGROUND: The soil microbiome plays a pivotal role in maintaining ecological balance, supporting food production, preserving water quality and safeguarding human health. Understanding the intricate dynamics within the soil microbiome necessitates unravelling complex bacterial-fungal interactions (BFIs). BFIs occur in diverse habitats, such as the phyllosphere, rhizosphere and bulk soil, where they exert substantial influence on plant-microbe associations, nutrient cycling and overall ecosystem functions. In various symbiotic associations, fungi form mycorrhizal connections with plant roots, enhancing nutrient uptake through the root and mycorrhizal pathways. Concurrently, specific soil bacteria, including mycorrhiza helper bacteria, play a pivotal role in nutrient acquisition and promoting plant growth. Chemical communication and biofilm formation further shape plant-microbial interactions, affecting plant growth, disease resistance and nutrient acquisition processes. SCOPE: Promoting synergistic interactions between mycorrhizal fungi and soil microbes holds immense potential for advancing ecological knowledge and conservation. However, despite the significant progress, gaps remain in our understanding of the evolutionary significance, perception, functional traits and ecological relevance of BFIs. Here we review recent findings obtained with respect to complex microbial communities - particularly in the mycorrhizosphere - and include the latest advances in the field, outlining their profound impacts on our understanding of ecosystem dynamics and plant physiology and function. CONCLUSIONS: Deepening our understanding of plant BFIs can help assess their capabilities with regard to ecological and agricultural safe-guarding, in particular buffering soil stresses, and ensuring sustainable land management practices. Preserving and enhancing soil biodiversity emerge as critical imperatives in sustaining life on Earth amidst pressures of anthropogenic climate change. A holistic approach integrates scientific knowledge on bacteria and fungi, which includes their potential to foster resilient soil ecosystems for present and future generations.

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

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 33 P, 15 N and 14 C 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 15 N and 33 P 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.

Functional complementarity of ancient plant-fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts.

Liverworts, which are amongst the earliest divergent plant lineages and important ecosystem pioneers, often form nutritional mutualisms with arbuscular mycorrhiza-forming Glomeromycotina and fine-root endophytic Mucoromycotina fungi, both of which coevolved with early land plants. Some liverworts, in common with many later divergent plants, harbour both fungal groups, suggesting these fungi may complementarily improve plant access to different soil nutrients. We tested this hypothesis by growing liverworts in single and dual fungal partnerships under a modern atmosphere and under 1500 ppm [CO2 ], as experienced by early land plants. Access to soil nutrients via fungal partners was investigated with 15 N-labelled algal necromass and 33 P orthophosphate. Photosynthate allocation to fungi was traced using 14 CO2 . Only Mucoromycotina fungal partners provided liverworts with substantial access to algal 15 N, irrespective of atmospheric CO2 concentration. Both symbionts increased 33 P uptake, but Glomeromycotina were often more effective. Dual partnerships showed complementarity of nutrient pool use and greatest photosynthate allocation to symbiotic fungi. We show there are important functional differences between the plant-fungal symbioses tested, providing new insights into the functional biology of Glomeromycotina and Mucoromycotina fungal groups that form symbioses with plants. This may explain the persistence of the two fungal lineages in symbioses across the evolution of land plants.