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.

Ozone disrupts the communication between plants and insects in urban and suburban areas: an updated insight on plant volatiles

“…In the field, leaf beetles grazed Japanese white birch individuals in ambient O 3 plots more than in elevated O 3 plots, although it would have been expected that the ozonated leaves would have been preferred based on laboratory assays (Sakikawa et al 2016 ; Agathokleous et al 2017 ; Abu ElEla et al 2018 ). To date, much research of O 3 effects on herbivory insects has focused on the relationship between the physiological response (photosynthesis, allocation of carbon products and nutrients) of plants and insect grazing (Manninen et al 2000 ; Holton et al 2003 ; Kopper and Lindroth 2003 ; Agrell et al 2005 ; Hamilton et al 2005 ; Matyssek et al 2012 ; Agathokleous et al 2017 ; Bubica Bustos et al 2020 ). However, it is difficult to explain herbivory based on only foliage quality.…”

Global Change Factors Influence Plant-Epichloë Associations

“…Ozone did not affect either the concentration of alkaloids nor the biomass of fungal mycelia within plant green tissues or seed [32,34]. Despite the lack of effect of the ozone on alkaloids, the level of resistance to herbivores in symbiotic plants was reduced by the pollutant, and this effect persisted in the next plant generation [34,37,38].…”

“…The global change factors were not necessarily applied at the same plant stage that the plant performance was measured (e.g., factor applied at seedling stage, but performance measured at reproductive stage). The column 'References' refers to articles that contain experimental results associated with the effects of the factors carbon dioxide (CO 2 ), ozone (O 3 ), cold and heat/warm temperatures, drought, flooding, and salinity on plantendophyte symbioses [18,25,29,32,37,42,51,53,64,68,70,74,79].…”

Environmental interference of plant−microbe interactions

“…Interestingly, the detrimental effect of stresses on the endophyte‐derived benefits can be transmitted intergenerationally. Daughter symbiotic plants of L. multiflorum produced from mothers that were exposed to ozone exhibited lower levels of resistance to insects compared to mother plants that were not exposed to the stress (Bubica Bustos et al, 2020 ).…”