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Ground‐level ozone is a global air pollutant with high toxicity and represents a threat to plants and microorganisms. Although beneficial microorganisms can improve host performance, their role in connecting environmentally induced maternal plant phenotypes to progeny (transgenerational effects [TGE]) is unknown. We evaluated fungal endophyte‐mediated consequences of maternal plant exposure to ozone on performance of the progeny under contrasting scenarios of the same factor (high and low) at two stages: seedling and young plant. With no variation in biomass, maternal ozone‐induced oxidative damage in the progeny that was lower in endophyte‐symbiotic plants. This correlated with an endophyte‐mediated higher concentration of proline, a defence compound associated with stress control. Interestingly, ozone‐induced TGE was not associated with reductions in plant survival. On the contrary, there was an overall positive effect on seedling survival in the presence of endophytes. The positive effect of maternal ozone increasing young plant survival was irrespective of symbiosis and only expressed under high ozone condition. Our study shows that hereditary microorganisms can modulate the capacity of plants to transgenerationally adjust progeny phenotype to atmospheric change. Ozone induced positive transgenerational effects (TGE) by increasing plant survival. It depended on fungal endophytes symbiosis, progeny size, and current ozone condition. Endophytes were determinant for seedlings, while current ozone allowed TGE to express in young plants. Our results give insights on the role of seed‐borne fungi into environmentally induced transgenerational responses of plants. [ABSTRACT FROM AUTHOR]

Ozone is an increasing tropospheric contaminant of climate change. Exposure to ozone may affect the symbiotic relationship between plants and beneficial microorganisms. In particular, the herbivore resistance mechanism conferred by fungal endophytes (defensive mutualism) may be affected, as any of the ozone-triggered effects (such as elicitation of defence mechanisms against biotrophic fungi or oxidative stress in the apoplastic space) may target the symbiont., Symbiotic and non-symbiotic Lolium multiflorum plants were exposed to ozone for two consecutive days (2 h per day), after which half were infested with 10 aphids ( Rhopalosiphum padi). We measured variables related to performance of plants, the endophyte symbiont (alkaloids) and the herbivores., Aphid populations were smaller on symbiotic plants than in non-symbiotic plants in low-ozone conditions. However, this difference disappeared in exposed plants to high-ozone conditions. Under low-ozone conditions, structure of aphid populations on endophyte-symbiotic plants was characterized by a low number of nymphs and a high number of adults. This pattern was not observed with high-ozone exposure. Level of fungal alkaloids (lolines) was not affected by either ozone or herbivory., Results indicate that ozone impairs the grass-endophyte symbiosis without affecting production of alkaloids generally linked with aphids' response to endophyte presence. Since neither plant biomass nor alkaloid level were affected by ozone, other ozone-mediated mechanisms at molecular or biochemical level may underlie plant-herbivore interaction mediated by fungal endophytes. Thus, the mechanism behind this effect must be determined in future experiments. [ABSTRACT FROM AUTHOR]

Tropospheric ozone is among the global change factors that pose a threat to plants and microorganisms. Symbiotic microorganisms can assist plants to cope with stress, but their role in the tolerance of plants to ozone is poorly understood. Here, we subjected endophyte-symbiotic and non-symbiotic plants of Lolium multiflorum , an annual species widely distributed in temperate grasslands, to high and low (i.e., charcoal-filtered air) ozone levels at vegetative and reproductive phases. Exposure to high ozone reduced leaf photochemical efficiency and greenness in both symbiotic and non-symbiotic plants. However, ozone-induced oxidative damage at biochemical level (i.e., lipid peroxidation) was mostly detected in symbiotic plants. Ozone exposure at the vegetative phase did not affect the reproductive investment in seeds, indicating full recovery from stress. Ozone exposure at the reproductive phase reduced biomass and seed production only in symbiotic plants indicating a symbiont-associated cost. At low ozone, endophyte-symbiotic plants showed a steeper slope in the relationship between seed number and seed weight (i.e., a number-weight trade-off) compared to non-symbiotic plants. However, when plants were treated at the reproductive phase, ozone increased the imbalance between seed number and seed weight in both endophyte-symbiotic and non-symbiotic plants. Plants with endophytes at the reproductive stage produced fewer seeds, which were not compensated by increased seed weight. Thus, fungal mycelium growing within ovaries or ozone-induced antioxidant systems may result in costs that finally depress the fitness of plants. Despite ozone pollution could destabilize plant-endophyte mutualisms and render them dysfunctional, other endophyte-mediated benefits (e.g., resistance to herbivory, tolerance to drought) could over-compensate these losses and explain the high incidence of the symbiosis in nature. • Symbiotic and non-symbiotic plants were exposed to low and high ozone (O 3). • Plant fitness was more sensitive to O 3 at reproductive than vegetative stages. • Symbiotic plants exposed to O 3 at flowering displayed reduced investment in reproduction. • O 3 caused a seed number−seed weight trade-off of non-symbiotic plants without compromising fitness. • Low frequency of symbiotic plants may be found in populations under O 3 pollution. [ABSTRACT FROM AUTHOR]

Simple Summary: Global change is driving the incidence of novel stress factors such as the tropospheric pollutant ozone. Plants can overcome the environmental challenges by adjusting their phenotypes that eventually, can be transmitted to the progeny. Plants also establish symbiotic interactions with beneficial fungal endophytes, some of which can be transmitted to the progeny through the seeds. We worked with the grass Lolium multiflorum and its common endophyte, Epichloë occultans that benefits the host by coffering resistance to herbivores. Specifically, we studied the effect of exposing endophyte-symbiotic and non-symbiotic plants to ozone on the level of resistance to herbivorous aphids in the progeny. The ozone history impaired the endophyte-conferred resistance to aphids in progeny. This was evident at individual weight level of aphids but not so at population level. Defensive compounds were higher in endophyte-symbiotic seeds but depressed by mother plants exposure to ozone. Despite the negative effect of maternal ozone on the resistance level of plants, symbiotic plants showed a superior biomass compared to endophyte-free plants. Our work illustrates how the environment explored by parent plants can persist transgenerationally and, depending on the symbiotic state, will affect the fate of the progeny. 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. [ABSTRACT FROM AUTHOR]

• Parental environment affects functional characteristics of seeds. • Seed-transmitted fungal endophytes mediate transgenerational effects in plants. • Negative effects of transgenerational ozone were detected in endophyte-symbiotic seeds but not in non-symbiotic seeds. • Parental ozone impacted seed progeny when it occurs close to reproductive phase of the plant. • Under accelerated ageing conditions, endophyte-symbiotic seeds showed deteriorated physiological state and reduced longevity. The transition from mother plant seed production to seedlings recruitment is critical for annual plant species but also for vertically transmitted microbial symbionts. Evidence indicates that microbial symbionts play important roles in plant response to environmental changes. However, their role in plant facing gaseous tropospheric pollutants such as the highly reactive and phytotoxic ozone, have been scarcely studied. Here, we experimentally tested the consequences of maternal plant exposure to ozone on the longevity of Lolium mutiflorum seeds mediated by a vertically-transmitted fungal endophyte (Epichloë occultans). Seeds were produced by mother plants exposed to contrasting levels of ozone (low and high concentrations) in two phases of the life cycle (vegetative and reproductive). We first characterized the consequences of plant exposure to ozone on the state of the antioxidant glutathione in the seeds. Then, we examined viability dynamics of the seeds through an accelerated ageing trial and followed the physiological variables seed water content (SWC) and electrical conductivity (EC). Irrespectively of maternal ozone, seeds produced by endophyte-symbiotic plants presented higher contents of the oxidised form of glutathione. In the same direction, the fungal endophyte presence was associated with a dramatic reduction in seed longevity. The SWC was higher in endophyte-symbiotic seeds that in endophyte-free seeds. As time under accelerated ageing condition advanced, EC increased more in endophyte-symbiotic seeds than in endophyte-free seeds. Mother plant exposure to ozone tended to have a negative synergistic effect with the endophyte symbiosis. Ozone transgenerational effect was not detected on endophyte-free seeds. Our work contributes to understand the transgenerational effects of vertically transmitted fungal endophytes in plants in response to a currently important factor of stress. [ABSTRACT FROM AUTHOR]