The influence of competing root symbionts on below-ground plant resource allocation

1. Plants typically interact with multiple above- and below-ground organisms simultaneously, with their symbiotic relationships spanning a continuum ranging from mutualism, such as with arbuscular mycorrhizal fungi (AMF), to parasitism, including symbioses with plant-parasitic nematodes (PPN). 2. Although research is revealing the patterns of plant resource allocation to mutualistic AMF partners under different host and environmental constraints, the root ecosystem, with multiple competing symbionts, is often ignored. Such competition is likely to heavily influence resource allocation to symbionts. 3. Here, we outline and discuss the competition between AMF and PPN for the finite supply of host plant resources, highlighting the need for a more holistic understanding of the influence of below-ground interactions on plant resource allocation. Based on recent developments in our understanding of other symbiotic systems such as legume–rhizobia and AMF-aphid-plant, we propose hypotheses for the distribution of plant resources between contrasting below-ground symbionts and how such competition may affect the host. 4. We identify relevant knowledge gaps at the physiological and molecular scales which, if resolved, will improve our understanding of the true ecological significance and potential future exploitation of AMF-PPN-plant interactions in order to optimize plant growth. To resolve these outstanding knowledge gaps, we propose the application of well-established methods in isotope tracing and nutrient budgeting to monitor the movement of nutrients between symbionts. By combining these approaches with novel time of arrival experiments and experimental systems involving multiple plant hosts interlinked by common mycelial networks, it may be possible to reveal the impact of multiple, simultaneous colonizations by competing symbionts on carbon and nutrient flows across ecologically important scales

Sequence of introduction determines the success of contrasting root symbionts and their host

Many crop species play host to a diverse range of soil-borne symbionts ranging from parasitic, such as potato cyst nematodes (PCN), to mutualistic, including arbuscular mycorrhizal fungi (AMF). Each of these organisms may establish symbiosis with the host prior to the arrival of another which may impact the fitness of all parties involved. We simulated a range of arrival time scenarios for both AMF and PCN and determined their consequences on potato host plants and subsequent symbionts to reflect the likely complexity of symbioses that occur in the field. Simulations were focussed on the first few weeks of plant growth to identify the importance of symbiont interactions during early plant development. Our data indicate that the order in which symbionts are introduced to crop roots is not only important for their own success, but also for that of the host and its additional symbionts. The presence of AMF increased the PCN population on the host, with earlier introduction of AMF increasing the magnitude of the effect. However, presence of AMF also increased the potato's tolerance to PCN, ameliorating the negative effects of the increased PCN burden. This tolerance was stronger the earlier the AMF were introduced and was sustained even when AMF were introduced after PCN. Overall, we show that the initial few weeks of crop emergence and growth may reflect a window of opportunity where the prosperity of the crop and its tolerance of parasites can potentially be influenced by coordinating application of AMF propagules. Additionally, these timings impact the success of below-ground plant parasites that can persist and impact crops for several years

Phytophagy impacts the quality and quantity of plant carbon resources acquired by mutualistic arbuscular mycorrhizal fungi

Arbuscular mycorrhizal (AM) fungi associate with the roots of many plant species, enhancing their host access to soil nutrients while obtaining their carbon supply directly as photosynthates. AM fungi often face competition for plant carbon from other organisms. The mechanisms by which plants prioritise carbon allocation to mutualistic AM fungi over parasitic symbionts remain poorly understood. Here, we show that host potato plants (Solanum tuberosum cv. Désirée) selectively allocate carbon resources to tissues interacting with AM fungi rather than those interacting with phytophagous parasites (the nematode Globodera pallida). We found that plants reduce the supply of hexoses but maintain the flow of plant21 derived fatty acids to AM fungi when concurrently interacting with parasites. Transcriptomic analysis suggest that plants prioritise carbon transfer to AM fungi by maintaining expression of fatty acid biosynthesis and transportation pathways, whilst decreasing the expression of mycorrhizal-induced hexose transporters. We also report similar findings from a different plant host species (Medicago truncatula) and phytophagous pest (the aphid Myzus persicae). These findings suggest a general mechanism of plant-driven resource allocation in scenarios involving multiple symbionts

Arbuscular mycorrhizal fungal‐induced tolerance is determined by fungal identity and pathogen density

Societal Impact Statement Plant-parasitic nematodes are a major concern for global food security, and many existing control options are being phased out due to adverse impacts on the environment. Here, we show that although application of arbuscular mycorrhizal fungi (AMF) increases host tolerance to these parasites, these benefits decrease as the parasite burden increases, limiting long-term benefits. This effect was consistent between experiments in the glasshouse and in the field environment, demonstrating the relevance of research into usable technologies. Our findings have potential to aid decision making regarding application of AMF inocula for optimum results in agricultural systems. Summary Plant-parasitic nematodes are a leading global threat to crop production and food security aims. Control strategies based on nematicides and fertilisers are increasingly undesirable due to economic and environmental impacts. Arbuscular mycorrhizal fungi (AMF) may induce host tolerance against pests such as the potato cyst nematode (PCN). Here, we determined the impact of PCN density on the tolerance induced by AMF-host interactions. Additionally, we evaluated the effects of five AMF inocula on PCN fitness though glasshouse and field trials. Greater PCN densities reduce the increased tolerance that AMF may confer on their hosts. This may be due to reduced mycorrhizal colonisation of hosts under higher PCN infection and potentially a threshold at which the presence of PCN severely impacts fungal growth. When tested in the field, the outcomes of AMF inoculation on crop yields were still positive. Inoculation of soil in the field also increased PCN multiplication, suggesting that AMF-induced tolerance may become reduced in the near future when the threshold PCN density is reached. Addition of AMF to agricultural soils may provide a short-term benefit yet lead to a long-term detriment by increasing PCN populations. The effects observed were driven by only one out of the five introduced AMF species, indicating that the remaining species were redundant for this application. This raises important considerations for future application of AMF inocula in agricultural systems and aids our understanding of how widely used ‘beneficial’ soil amendments impact the agricultural ecosystem

Disruption of carbon for nutrient exchange between potato and arbuscular mycorrhizal fungi enhanced cyst nematode fitness and host pest tolerance

Plants simultaneously interact with a range of biotrophic symbionts, ranging from mutualists such as arbuscular mycorrhizal fungi (AMF), to parasites such as the potato cyst nematode (PCN). The exchange of mycorrhizal-acquired nutrients for plant-fixed carbon (C) is well studied; however, the impact of competing symbionts remains underexplored. In this study, we examined mycorrhizal nutrient and host resource allocation in potato with and without AMF and PCN using radioisotope tracing, whilst determining the consequences of such allocation. The presence of PCN disrupted C for nutrient exchange between plants and AMF, with plant C overwhelmingly obtained by the nematodes. Despite this, AMF maintained transfer of nutrients on PCN-infected potato, ultimately losing out in their C for nutrient exchange with the host. Whilst PCN exploited the greater nutrient reserves to drive population growth on AMF–potato, the fungus imparted tolerance to allow the host to bear the parasitic burden. Our findings provide important insights into the belowground dynamics of plant–AMF symbioses, where simultaneous nutritional and nonnutritional benefits conferred by AMF to hosts and their parasites are seldom considered in plant community dynamics. Our findings suggest this may be a critical oversight, particularly in the consideration of C and nutrient flows in plant and soil communities

Photosynthate transfer from an autotrophic orchid to conspecific heterotrophic protocorms through a common mycorrhizal network

The minute 'dust seeds' of some terrestrial orchids preferentially germinate and develop as mycoheterotrophic protocorms near conspecific adult plants. Here we test the hypothesis that mycorrhizal mycelial connections provide a direct pathway for transfer of recent photosynthate from conspecific green orchids to achlorophyllous protocorms. Mycelial networks of Ceratobasidium cornigerum connecting green Dactylorhiza fuchsii plants with developing achlorophyllous protocorms of the same species were established on oatmeal or water agar before the shoots of green plants were exposed to 14CO2. After incubation for 48 hours, the pattern of distribution of fixed carbon was visualised in intact entire autotrophic/protocorm systems using digital autoradiography and quantified in protocorms by liquid scintillation counting. Both methods of analysis revealed accumulation of 14C above background levels in protocorms, confirming that autotrophic plants supply carbon to juveniles via common mycorrhizal networks. A greater amount of transfer occurred to protocorms growing on water as distinct from oatmeal agar indicating that the polarity of transfer may be influenced by sink strength. We suggest this transfer pathway may contribute significantly to the pattern and processes determining localised orchid establishment in nature, and that 'parental nurture’ via common mycelial networks may be involved in these processes