Maternal Exposure to Ozone Modulates the Endophyte-Conferred Resistance to Aphids in Lolium multiflorum Plants

Abstract

Plants are challenged by biotic and abiotic stress factors and the incidence of one can increase or decrease resistance to another. These relations can also occur transgenerationally. For instance, progeny plants whose mothers experienced herbivory can be more resistant to herbivores. Certain fungal endophytes that are vertically transmitted endow plants with alkaloids and resistance to herbivores. However, endophyte-symbiotic plants exposed to the oxidative agent ozone became susceptible to aphids. Here, we explored whether this effect persists transgenerationally. We exposed Lolium multiflorum plants with and without fungal endophyte Epichloë occultans to ozone (120 or 0 ppb), and then, challenged the progeny with aphids (Rhopalosiphum padi). The endophyte was the main factor determining the resistance to aphids, but its importance diminished in plants with ozone history. This negative ozone effect on the endophyte-mediated resistance was apparent on aphid individual weights. Phenolic compounds in seeds were increased by the symbiosis and diminished by the ozone. The endophyte effect on phenolics vanished in progeny plants while the negative ozone effect persisted. Independently of ozone, the symbiosis increased the plant biomass (≈24%). Although ozone can diminish the importance of endophyte symbiosis for plant resistance to herbivores, it would be compensated by host growth stimulation.

Keywords: Lolium multiflorum; Rhopalosiphum padi; fungal endophyte; maternal effects; symbiosis; transgenerational effects.

Figure 1

Scheme of the experimental design. The upper part of the figure represents the open-top chambers in which ozone was manipulated [without ozone ≈ 0 ppb (O₃⁻) and with ozone ≈ 120 ppb (O₃⁺)] and Lolium multiflorum maternal plant symbiotic (E+) and non-symbiotic (E−) with the fungal endophyte Epichloë occultans. The lower part shows the progeny plants and herbivory treatment by the aphid Rhopalosiphum padi for 21 days. The arrows indicate the maternal ozone history (light blue is O₃⁻ and orange is O₃⁺).

Figure 2

Population size (number of aphids per plant) and population structure [proportion of individuals per instar: “nymphs” (no pattern design) and “apterous + winged adults “ (with pattern design)] of the aphid Rhopalosiphum padi after growing for 21 days on Lolium multiflorum progeny plants symbiotic (E+) and non-symbiotic (E−) with fungal endophyte Epichloë occultans, whose mother plants were exposed to tropospheric ozone [with ozone ≈120 ppb (O₃⁺)] or not [without ozone ≈0 ppb (O₃⁻)]. Different letters indicate significant differences based on Tukey’s test at <0.05. For total number of aphids, values are means ± S.E. (n = 20).

Figure 3

Variation in total phenolic compounds in seeds and progeny plants of Lolium multiflorum plants symbiotic (E+) and non-symbiotic (E−) with fungal endophyte Epichloë occultans, whose mother plants were exposed to tropospheric ozone [with ozone ≈ 120 ppb (O₃⁺)] or not [without ozone ≈ 0 ppb (O₃⁻)]. Values are expressed relative to control condition [no endophyte (E−) and no ozone (O₃⁻)] for each category independently. Different letters indicate significant differences (Tukey’s test, p < 0.05); lack of letters in a response variable means there were no significant effects. Values are means ± S.E. (n _seeds = 12, and n _plants = 23).

Figure 4

Shoot biomass (g dry weight) of Lolium multiflorum progeny plants symbiotic (E+) and non-symbiotic (E−) with fungal endophyte Epichloë occultans, whose mother plants were exposed to tropospheric ozone [with ozone ≈120 ppb (O₃⁺)] or not [without ozone ≈0 ppb (O₃⁻)] at the experiment (21 days after the herbivory treatment with Rhopalosiphum padi). Different letters indicate significant differences among means (Tukey’s test, p < 0.05). Values are means ± S.E. (n = 20).