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

Abstract

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.

Keywords: Arbuscular mycorrhizal fungi; broad bean (Vicia faba); insect host location; pea aphid (Acyrthosiphon pisum); phosphorus; plant volatiles..

Fig. 1.

Effect of AM fungi, P addition, and aphids on total leaf P concentration (mg g^–1 of DW; A); total leaf N concentration (mg g^–1 of DW; B); leaf N: P ratio (C); plant above-ground biomass (g DW; D), and concentration of soil PO₄ (mg g^–1 of DW; E).

Fig. 2.

Effect of treatment on emission of plant volatiles (ng g^–1 of DW 24h^–1). (A) Overall main effect of AM fungi on emission of naphthalene (there was no significant interaction between AMF and P treatments). (B–D) Effect of interaction between AM fungi and P addition on emission of (S)-linalool (B), (E)-caryophyllene (C), and (R)-germacrene D (D). Bars sharing a letter are not significantly different from each other (P>0.05). An asterisk indicates bars that are significantly different (P<0.05).

Fig. 3.

(A) Effect of AM fungi and P additions on attractiveness of plants to aphids. The attractiveness was calculated as time spent by aphids in olfactometer chambers treated with plant headspace samples subtracted by the mean time spent in areas treated with solvent blanks. Asterisks indicate that headspace samples were significantly attractive relative to the solvent blanks. (B) Effect of P additions and aphids on percentage of root length colonized by AM fungi. Bars sharing a letter are not significantly different from each other (P>0.05).

Fig. 4.

(A) Association between percentage root length colonized by AM fungi and attractiveness of plants to aphids (R ²=0.19; F _1,23=5.37, P=0.030). (B) Association between total leaf P concentration and attractiveness of plants to aphids (R ²=0.04; F _1,23=0.99, P=0.330). (C) Association between percentage root length colonized by AM fungi and total leaf P concentration (R ²=0.20, F _1,46=11.48, P=0.001).