Feeding (or not feeding) a fungus: plants may not be so good to their fungal partners after all

Around 80% of land plants famously form symbiotic associations with soil fungi known as arbuscular mycorrhizal (AM) fungi. From this interaction, the plant gains several advantages including enhanced uptake of phosphorus provided by the fungus. The fungus, in turn, receives fixed carbon from the plant generated by photosynthesis. However, it is known that plants are smart about this and can ‘sanction’ symbionts that are not returning sufficient amounts of phosphorus in exchange for carbon. By contrast, if external CO₂ is high, plants can increase the amount of fixed carbon they allocate to AM fungal partners.

So whilst it seems the symbiotic interaction can be dynamically adjusted, we still understand little about how this works and what the effects other biotic and abiotic factors have on the balance of this globally-important symbiosis. In their recent paper published Open Access in Current Biology, Michael Charters, Steven Sait and Katie Field from the University of Leeds examine how insect herbivory and environmental CO₂ impact the balance achieved between wheat plants and AM fungi during their interactions.

Charters and colleagues vary the levels of available CO₂ to vary the available carbon ‘source’, and add aphids to the wheat plants to increase external carbon ‘sink’. The first surprising finding that the authors make is that increasing available CO_2, while increasing both root and shoot carbon levels in the wheat plants, did not result in increased allocation of fixed carbon to the AM fungus. This contradicts previous studies that find increased carbon allocation to AM fungi when CO₂ levels are high.

However, Charters and colleagues point out that wheat has been selected for high-yielding above-ground traits, and that this may have selected against below-ground traits such involving AM fungi. Previous studies indicating increased carbon allocation in higher CO₂ conditions were done using wild plants. Application of aphids to the wheat plants as a carbon ‘sink’ dramatically reduced the allocation of fixed carbon to the AM fungi. By contrast, allocation of phosphorus from the fungus to the plant was not affected, despite the AM fungi getting a low carbon reward from the plant.

The authors attempt to restore carbon allocation to AM fungi, the authors increase externally available CO₂ levels combined with aphid predation. However, this failed to restore carbon allocation to AM fungi and, interestingly, actually resulted in increased transfer of phosphorus from the fungus to the plant. So it seems that, while wheat plants can reduce carbon allocation to AM fungi in response to low external CO₂ or a powerful carbon ‘sink’ such as aphid herbivory, the AM fungi interacting with them do not reciprocate by reducing phosphorus allocation.

The reason why the AM fungus cannot limit phosphorus allocation to wheat plants reciprocally is unclear, but Charters and colleagues suggest that it may be simply because the fungus has no other choice in their experimental system. AM fungi are obligate symbionts, meaning that they need to enter into symbioses with plants in order to survive. There were no other plants in the setup used by Charters and colleagues, and so the fungi may fail to reduce phosphorus allocation to the wheat plants because there is no alternative option.

Whilst plants do benefit from associations with AM fungi, they do not absolutely require them to survive and so can afford to decrease carbon allocation when CO₂ is low or fixed carbon is being drained by insect herbivory. Moreover, the authors also showed that the AM fungi actually increase phosphorus allocation to wheat plants under conditions of high CO₂ and high aphid herbivory. One possible reason for this is that the AM fungi respond to the need for greater plant nutrient uptake in response to the expanding aphid population.

Charters and colleagues highlight that future studies need to address the findings of their experiments: ‘Future studies must now seek to investigate the effect of external biotic C sinks on resource exchange between AM fungi and multiple host plants (i.e., multiple C sources) in more complex, and ecologically relevant, networks.’ The results of this study highlight the need to attempt to replicate the more complex realities of plant ecosystems in experimental set-ups, and shows that multiple biotic and abiotic factors may be able to influence the balance of plant-AM fungi symbioses. Insect herbivores may therefore not only be bad news for plants but also the interactors that depend on them!