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.

Herbivore-driven disruption of arbuscular mycorrhizal carbon-for-nutrient exchange is ameliorated by neighboring plants.

Arbuscular mycorrhizal fungi colonize the roots of most plants, forming a near-ubiquitous symbiosis1 that is typically characterized by the bi-directional exchange of fungal-acquired nutrients for plant-fixed carbon.2 Mycorrhizal fungi can form below-ground networks3,4,5,6 with potential to facilitate the movement of carbon, nutrients, and defense signals across plant communities.7,8,9 The importance of neighbors in mediating carbon-for-nutrient exchange between mycorrhizal fungi and their plant hosts remains equivocal, particularly when other competing pressures for plant resources are present. We manipulated carbon source and sink strengths of neighboring pairs of host plants through exposure to aphids and tracked the movement of carbon and nutrients through mycorrhizal fungal networks with isotope tracers. When carbon sink strengths of both neighboring plants were increased by aphid herbivory, plant carbon supply to extraradical mycorrhizal fungal hyphae was reduced, but mycorrhizal phosphorus supply to both plants was maintained, albeit variably, across treatments. However, when the sink strength of only one plant in a pair was increased, carbon supply to mycorrhizal fungi was restored. Our results show that loss of carbon inputs into mycorrhizal fungal hyphae from one plant may be ameliorated through inputs of a neighbor, demonstrating the responsiveness and resilience of mycorrhizal plant communities to biological stressors. Furthermore, our results indicate that mycorrhizal nutrient exchange dynamics are better understood as community-wide interactions between multiple players rather than as strict exchanges between individual plants and their symbionts, suggesting that mycorrhizal C-for-nutrient exchange is likely based more on unequal terms of trade than the "fair trade" model for symbiosis.

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.

Carbon for nutrient exchange between Lycopodiella inundata and Mucoromycotina fine root endophytes is unresponsive to high atmospheric CO2.

Non-vascular plants associating with arbuscular mycorrhizal (AMF) and Mucoromycotina 'fine root endophyte' (MFRE) fungi derive greater benefits from their fungal associates under higher atmospheric [CO2] (a[CO2]) than ambient; however, nothing is known about how changes in a[CO2] affect MFRE function in vascular plants. We measured movement of phosphorus (P), nitrogen (N) and carbon (C) between the lycophyte Lycopodiella inundata and Mucoromycotina fine root endophyte fungi using 33P-orthophosphate, 15 N-ammonium chloride and 14CO2 isotope tracers under ambient and elevated a[CO2] concentrations of 440 and 800 ppm, respectively. Transfers of 33P and 15 N from MFRE to plants were unaffected by changes in a[CO2]. There was a slight increase in C transfer from plants to MFRE under elevated a[CO2]. Our results demonstrate that the exchange of C-for-nutrients between a vascular plant and Mucoromycotina FRE is largely unaffected by changes in a[CO2]. Unravelling the role of MFRE in host plant nutrition and potential C-for-N trade changes between symbionts under different abiotic conditions is imperative to further our understanding of the past, present and future roles of plant-fungal symbioses in ecosystems.

Mucoromycotina Fine Root Endophyte Fungi Form Nutritional Mutualisms with Vascular Plants.

Fungi and plants have engaged in intimate symbioses that are globally widespread and have driven terrestrial biogeochemical processes since plant terrestrialization >500 million years ago. Recently, hitherto unknown nutritional mutualisms involving ancient lineages of fungi and nonvascular plants have been discovered, although their extent and functional significance in vascular plants remain uncertain. Here, we provide evidence of carbon-for-nitrogen exchange between an early-diverging vascular plant (Lycopodiella inundata) and Mucoromycotina (Endogonales) fine root endophyte fungi. Furthermore, we demonstrate that the same fungal symbionts colonize neighboring nonvascular and flowering plants. These findings fundamentally change our understanding of the physiology, interrelationships, and ecology of underground plant-fungal symbioses in modern terrestrial ecosystems by revealing the nutritional role of Mucoromycotina fungal symbionts in vascular plants.

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.

Aphid Colonization Affects Potato Root Exudate Composition and the Hatching of a Soil Borne Pathogen.

Plants suffer multiple, simultaneous biotic threats from both above and below ground. These pests and/or pathogens are commonly studied on an individual basis and the effects of above-ground pests on below-ground pathogens are poorly defined. Root exudates from potato plants (Solanum tuberosum L.) were analyzed to characterize the top-down plant-mediated interactions between a phloem-sucking herbivore (Myzus persicae) and a sedentary, endoparasitic nematode (Globodera pallida). Increasing inocula of the aphid, M. persicae, reduced the root mass of potato plants. Exudates collected from these roots induced significantly lower hatching of second-stage juveniles from G. pallida eggs over a 28-day period, than those from uninfested control plants. Inhibition of hatch was significantly positively correlated with size of aphid inoculum. Diminished hatching was partially recovered after treatment with root exudate from uninfested potato plants indicating that the effect on hatching is reversible but cannot be fully recovered. Glucose and fructose content was reduced in root exudates from aphid-infested potato plants compared to controls and these sugars were found to induce hatching of G. pallida, but not to the same degree as potato root exudates (PRE). Supplementing aphid-infested PRE with sugars did not recover the hatching potential of the treatment, suggesting that additional compounds play an important role in egg hatch. The first gene upregulated in the closely related potato cyst nematode Globodera rostochiensis post-exposure to host root exudate, Neprilysin-1, was confirmed to be upregulated in G. pallida cysts after exposure to PRE and was also upregulated by the sugar treatments. Significantly reduced upregulation of Gpa-nep-1 was observed in cysts treated with root exudates from potato plants infested with greater numbers of aphids. Our data suggest that aphid infestation of potato plants affects the composition of root exudates, with consequential effects on the hatching and gene expression of G. pallida eggs. This work shows that an above-ground pest can indirectly impact the rhizosphere and reveals secondary effects for control of an economically important below-ground pathogen.

A mycorrhizal revolution.

It has long been postulated that symbiotic fungi facilitated plant migrations onto land through enhancing the scavenging of mineral nutrients and exchanging these for photosynthetically fixed organic carbon. Today, land plant-fungal symbioses are both widespread and diverse. Recent discoveries show that a variety of potential fungal associates were likely available to the earliest land plants, and that these early partnerships were probably affected by changing atmospheric CO2 concentrations. Here, we evaluate current hypotheses and knowledge gaps regarding early plant-fungal partnerships in the context of newly discovered fungal mutualists of early and more recently evolved land plants and the rapidly changing views on the roles of plant-fungal symbioses in the evolution and ecology of the terrestrial biosphere.

A Plant-Feeding Nematode Indirectly Increases the Fitness of an Aphid.

Plants suffer multiple, simultaneous assaults from above and below ground. In the laboratory, pests and/or pathogen attack are commonly studied on an individual basis. The molecular response of the plant to attack from multiple organisms and the interaction of different defense pathways is unclear. The inducible systemic responses of the potato (Solanum tuberosum L.) host plant were analyzed to characterize the plant-mediated indirect interactions between a sedentary, endoparasitic nematode (Globodera pallida), and a phloem-sucking herbivore (Myzus persicae). The reproductive success of M. persicae was greater on potato plants pre-infected with G. pallida compared to control plants. Salicylic acid (SA) increased systemically in the leaves of potato plants following nematode and aphid infection singly with a corresponding increase in expression of SA-mediated marker genes. An increase in jasmonic acid associated with aphid infection was suppressed when plants were co-infected with nematodes. Our data suggests a positive, asymmetric interaction between a sedentary endoparasitic nematode and a sap-sucking insect. The systemic response of the potato plant following infection with G. pallida indirectly influences the performance of M. persicae. This work reveals additional secondary benefits of controlling individual crop pests.