Increasing phosphorus supply is not the mechanism by which arbuscular mycorrhiza increase attractiveness of bean (Vicia faba) to aphids.

Arbuscular mycorrhizal (AM) fungi, important plant mutualists, provide plants with nutrients such as phosphorus (P) in return for carbon. AM fungi also enhance the attractiveness of plants to aphids via effects on emissions of plant volatiles used in aphid host location. We tested whether increased P uptake by plants is the mechanism through which AM fungi alter the volatile profile of plants and aphid behavioural responses by manipulating the availability of P and AM fungi to broad beans (Vicia faba L.) in a multi-factorial design. If AM fungi affect plant volatiles only via increased P acquisition, we predicted that the emission of volatiles and the attractiveness of mycorrhizal beans to aphids would be similar to those of non-mycorrhizal beans supplied with additional P. AM fungi and P addition increased leaf P concentrations by 40 and 24%, respectively. The production of naphthalene was less in mycorrhizal plants, regardless of P addition. By contrast, production of (S)-linalool, (E)-caryophyllene and (R)-germacrene D was less in plants colonized by AM fungi but only in the absence of P additions. The attractiveness of plants to pea aphids (Acyrthosiphon pisum Harris) was positively affected by AM fungi and correlated with the extent of root colonization; however, attractiveness was neither affected by P treatment nor correlated with leaf P concentration. These findings suggest that increased P uptake is not the main mechanism by which mycorrhiza increase the attractiveness of plants to aphids. Instead, the mechanism is likely to operate via AM fungi-induced plant systemic signalling.

Underground allies: how and why do mycelial networks help plants defend themselves?: What are the fitness, regulatory, and practical implications of defence-related signaling between plants via common mycelial networks?

Most land plants associate with mycorrhizal fungi that can connect roots of neighboring plants in common mycelial networks (CMNs). Recent evidence shows that CMNs transfer warning signals of pathogen and aphid attack between plants. However, we do not know how defence-related signaling via CMNs operates or how ubiquitous it is. Nor do we know what the ecological relevance and fitness consequences are, particularly from the perspective of the mycorrhizal fungus. Here, we focus on the potential fitness benefits for mycorrhizal fungi and outline hypothetical scenarios in which signal transfer via CMNs is modulated in order to acquire the most benefit for the fungus (i.e. acquisition of carbon) for minimal cost. We speculate that the signal may be quantitative and may elicit plant defence responses on different levels depending on the distance the signal is transferred. Finally, we discuss the possibility of practical applications of this phenomenon for crop protection.

Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack.

The roots of most land plants are colonised by mycorrhizal fungi that provide mineral nutrients in exchange for carbon. Here, we show that mycorrhizal mycelia can also act as a conduit for signalling between plants, acting as an early warning system for herbivore attack. Insect herbivory causes systemic changes in the production of plant volatiles, particularly methyl salicylate, making bean plants, Vicia faba, repellent to aphids but attractive to aphid enemies such as parasitoids. We demonstrate that these effects can also occur in aphid-free plants but only when they are connected to aphid-infested plants via a common mycorrhizal mycelial network. This underground messaging system allows neighbouring plants to invoke herbivore defences before attack. Our findings demonstrate that common mycorrhizal mycelial networks can determine the outcome of multitrophic interactions by communicating information on herbivore attack between plants, thereby influencing the behaviour of both herbivores and their natural enemies.

How rapid is aphid-induced signal transfer between plants via common mycelial networks?

Arbuscular mycorrhizal (AM) fungi are important plant mutualists that can connect roots of neighboring plants to form common mycelial networks. A recent study demonstrated that these networks can act as conduits for aphid-induced signals between plants, activating chemical defenses in uninfested neighboring plants so that they become unattractive to aphids but attractive to their enemies (parasitoids). The benefit to the neighboring plants will increase if the signal speed is rapid, enabling them to respond before aphids attack. Here, we determine the speed of aphid-induced signal transfer between plants infested with aphids ("donor") and neighboring aphid-free plants that were either connected or unconnected to the donor via a common mycelial network. Induced changes in plant volatiles from neighbors connected to donors started within 24 h of aphid infestation of donors. This demonstrates a rapid signal, implying potential benefit to plants receiving the signal, and raises intriguing ecological and evolutionary questions.