Arbuscular mycorrhizal (AM) fungi form symbioses with the roots of most plants across nearly every ecosystem on Earth. AM-plant interactions usually involve transfer of AM-acquired nutrients from the soil, such as phosphate and nitrate, to the plant host in exchange for carbohydrates (i.e. sugars) and lipids generated through photosynthesis. This intimate association often imparts multiple benefits to host plants, such as enriched nutrient status and priming of plant defences, both of which can increase growth and disease resistance. AM fungi are therefore ecologically important and of great interest for potential exploitation in agriculture to help reduce the need for application of chemical inputs.
Carbon-for-nutrient exchange between AM fungi and their hosts is relatively well-studied in single AM-plant interactions, however in natural systems plants interact concurrently with a myriad of additional organisms that may span the entire symbiotic continuum from parasitic to mutualistic interactions. Our previous research demonstrated that when AM-colonised potato roots are parasitised by plant-parasitic nematodes (economically important pathogens of crops), the host plant dramatically reduces the transfer of carbon resources to the fungus. However, the mechanisms underpinning this dynamic and competitive allocation of host resources was unknown.
To address this, we investigated the mechanisms underpinning the responses of mycorrhizal plants to simultaneous parasitic interactions, using potatoes, AM fungi and plant parasitic nematodes as a model system. We wanted to understand whether the types and stoichiometry of carbon compounds transferred to mutualistic AM fungi remain the same when parasitic nematodes are present or not. Is there was a universal regulatory mechanism for all AM-destined host resources or if there is discrete regulation for each type of resource? Finally, we wanted to find out whether the responses and mechanisms of plant-AM symbioses to parasitism were conserved across plant species and types of pests.
We grew potato plants in split-root systems and introduced AM fungal inoculum into one of the root compartments. We were then able to assess the spatial impact of parasitic nematode infection of plant-AM interactions by inoculating the nematodes into either the same or opposing root compartments relative to the fungus. We used a combination of radioisotope (14C) tracing, metabolomics, and transcriptomics to track the movement, the type, and the mechanisms by which host plant photosynthates were transferred to the AM fungi.
We found that host plants allocated the majority of their labelled carbon resources towards tissues interacting with mutualistic AM fungi versus those interacting with the parasitic nematodes (Fig 1).
Driven by this data we found that parasitised hosts supplied a reduced amount of hexoses to their AM fungal partners, however the supply of fatty acids was maintained. Metabolite flux corresponded with the expression of hexose and fatty acid transporter genes in co-colonised plants. We repeated this experiment using Medicago truncatula and the pea aphid Myzus persicae and found consistent results, suggesting this is a general mechanism of plant-driven resource allocation in scenarios involving multiple symbionts (Fig 2).
Significance & Conclusions: Our findings suggest that whilst parasitism causes the host plant to direct carbon-based resources preferentially towards AM fungal-colonised roots and away from the parasite, it restricts the export of hexoses but maintains the transfer of fatty acids to the AM fungi, maintaining AM-derived benefits. Our research suggests this could be a universal plant mechanism to ensure the viability and functionality of mutualistic AM fungi are maintained long-term, throughout on-going parasitism
Link to paper : rdcu.be/dw3NU