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

Abstract

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.

Keywords: arbuscular mycorrhizal fungi; broad bean (Vicia faba); common mycelial network; induced plant defense; insect host location; inter-plant communication; pea aphid (Acyrthosiphon pisum); rhizosphere signaling; volatile organic compounds.

Figure 1. Attractiveness to pea aphids (Acyrthosiphon pisum) of headspace samples of broad beans that were either connected or unconnected to an aphid-infested donor plant via a common mycelial network. Samples were collected during 0–24, 48–72, and 72–96 h after aphid placement on donor plants (donor not analyzed 48–72 h). Attractiveness was calculated as the mean time spent (minutes) in olfactometer areas treated with headspace samples minus that with solvent only. Differences in attractiveness among treatments are indicated by letters. Bars sharing a letter are not significantly different (p > 0.05) and each time period is interpreted independently. Within treatments, asterisks indicate that samples were significantly attractive or repellent compared with solvent controls (* = p < 0.05; ** = p < 0.01; *** = p < 0.001).