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There is an increasing interest in determining the influence of global change on plant–microorganism interactions. We review the results of experiments that evaluated the effects of the global change factors carbon dioxide, ozone, temperature, drought, flooding, and salinity on plant symbioses with beneficial Epichloë endophytes. The factors affected the performance of both plants and endophytes as well as the frequency of plants symbiotic with the fungus. Elevated carbon dioxide levels and low temperatures differentially influenced the growth of plants and endophytes, which could compromise the symbioses. Furthermore, we summarise the plant stage in which the effects of the factors were quantified (vegetative, reproductive, or progeny). The factors ozone and drought were studied at all plant stages, but flooding and carbon dioxide were studied in just a few of them. While only studied in response to ozone and drought, evidence showed that the effects of these factors on symbiotic plants persisted trans-generationally. We also identified the putative mechanisms that would explain the effects of the factors on plant–endophyte associations. These mechanisms included the increased contents of reactive oxygen species and defence-related phytohormones, reduced photosynthesis, and altered levels of plant primary metabolites. Finally, we describe the counteracting mechanisms by which endophytes would mitigate the detrimental effects of the factors on plants. In presence of the factors, endophytes increased the contents of antioxidants, reduced the levels of defence-related phytohormones, and enhanced the plant uptake of nutrients and photosynthesis levels. Knowledge gaps regarding the effects of global change on plant–endophyte associations were identified and discussed. [ABSTRACT FROM AUTHOR]

Plants have evolved mechanisms to survive herbivory. One such mechanism is the induction of defences upon attack that can operate intergenerationally. Cool-season grasses (sub-family Pooideae) obtain defences via symbiosis with vertically transmitted fungal endophytes (genus Epichloë) and can also show inducible responses. However, it is unknown whether these herbivore-induced responses can have intergenerational effects. We hypothesized that herbivory by aphids on maternal plants induces the intergenerational accumulation of endophyte-derived defensive alkaloids and resistance intensification in the progeny. We subjected mother plants symbiotic or not with Epichloë occultans, a species known for its production of anti-insect alkaloids known as lolines, to the aphid Rhopalosiphum padi. Then, we evaluated the progeny of these plants in terms of loline alkaloid concentration, resistance level (through herbivore performance), and shoot biomass. Herbivory on mother plants did not increase the concentration of lolines in seeds but it tended to affect loline concentration in progeny plants. There was an overall herbivore-induced intergenerational effect increasing the endophyte-conferred defence and resistance. Symbiotic plants were more resistant to aphids and had higher shoot biomass than their non-symbiotic counterparts. Since maternal herbivory did not affect the loline concentrations in seeds, the greater resistance of the progeny could have resulted from an inherited mechanism of epigenetic regulation. It would be interesting to elucidate the origin of this regulation since it could come from the host or the fungal symbiont. Thus, endophyte-driven differential fitness between symbiotic and non-symbiotic plants might be higher as generations pass on in presence of herbivores. [ABSTRACT FROM AUTHOR]

Context. Tall fescue (Schedonorus arundinaceus) is one of the most important cultivated forage grasses in temperate regions but its association with some Epichloë fungal endophytes usually makes it unsuitable for livestock feeding due to toxic alkaloids. However, re-inoculation of plants with non-toxic endophytes can result in positive effects for livestock feeding. Aims. Assess the effects of the non-toxic AR584 endophyte on seed viability and germination in two tall fescue cultivars. Methods. The effects of AR584 endophyte (presence/absence) and tall fescue cultivar (INIA Aurora/Taita) were evaluated on seed viability and germination responses across a range of temperature and water availability regimes. Response to constant temperature and water availability was characterised by the thermal-time and hydro-time models, respectively. Key results. Under accelerated aging conditions, endophyte presence reduced seed viability in cultivar Taita. For both cultivars, endophyte-infected seeds showed a lower germination rate than endophyte-free seeds, except for INIA Aurora under low incubation temperatures. Also, endophyte-infected seeds in both cultivars displayed lower germination rates and final germination as the water potential was lowered. Conclusions. A strong cultivar-by-endophyte interaction for seed germination indicates the need to understand how specific cultivarendophyte combinations best fit a given environmental condition, as defined by temperature and water availability. Implications. The information we present can be valuable not only for farmers who have to decide what to cultivate but also for seed companies that have to preserve seed quality. [ABSTRACT FROM AUTHOR]

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]

Tropospheric ozone is an abiotic stress of increasing importance in the context of global climate change. This greenhouse gas is a potent phytotoxic molecule with demonstrated negative effects on crop yield and natural ecosystems. Recently, oxidative stress has been proposed as a mechanism that could regulate the interaction between cool‐season grasses and Epichloë endophytes. We hypothesized that exposure of Lolium multiflorum plants, hosting endophytes to an ozone‐polluted environment at different ontogenetic phases, would impact the trans‐generational dynamics of the vertically transmitted fungal symbiont. Here, we found that the ozone‐induced stress on the mother plants did not affect the endophyte vertical transmission but it impaired the persistence of the fungus in the seed exposed to artificial ageing. Endophyte longevity in seed was reduced by exposure of the mother plant to ozone. Although ozone exposure did not influence either the endophyte mycelial concentration or their compound defences (loline alkaloids), a positive correlation was observed between host fitness and the concentration of endophyte‐derived defence compounds. This suggests that fungal defences in grass seeds were not all produced in situ but remobilized from the vegetative tissues. Our study reveals ozone trans‐generational effects on the persistence of a beneficial symbiont in a host grass. Mother plant exposure to ozone did not affect the growth and the transmission of fungal endophytes into host seeds. Seed alkaloid concentration correlated with endophyte mycelial concentration and host fitness. However, ozone‐induced stress on mother plants did impair the longevity of the endophytes in the seeds. [ABSTRACT FROM AUTHOR]

Background and Aims In the subfamily Poöideae (Poaceae), certain grass species possess anti-herbivore alkaloids synthesized by fungal endophytes that belong to the genus Epichloë (Clavicipitaceae). The protective role of these symbiotic endophytes can vary, depending on alkaloid concentrations within specific plant–endophyte associations and plant parts. Methods We conducted a literature review to identify articles containing alkaloid concentration data for various plant parts in six important pasture species, Lolium arundinaceum , Lolium perenne , Lolium pratense , Lolium multiflorum | Lolium rigidum and Festuca rubra , associated with their common endophytes. We considered the alkaloids lolines (1-aminopyrrolizidines), peramine (pyrrolopyrazines), ergovaline (ergot alkaloids) and lolitrem B (indole-diterpenes). While all these alkaloids have shown bioactivity against insect herbivores, ergovaline and lolitrem B are harmful for mammals. Key Results Loline alkaloid levels were higher in the perennial grasses L. pratense and L. arundinaceum compared to the annual species L. multiflorum and L. rigidum , and higher in reproductive tissues than in vegetative structures. This is probably due to the greater biomass accumulation in perennial species that can result in higher endophyte mycelial biomass. Peramine concentrations were higher in L. perenne than in L. arundinaceum and not affected by plant part. This can be attributed to the high within-plant mobility of peramine. Ergovaline and lolitrem B, both hydrophobic compounds, were associated with plant parts where fungal mycelium is usually present, and their concentrations were higher in plant reproductive tissues. Only loline alkaloid data were sufficient for below-ground tissue analyses and concentrations were lower than in above-ground parts. Conclusions Our study provides a comprehensive synthesis of fungal alkaloid variation across host grasses and plant parts, essential for understanding the endophyte-conferred defence extent. The patterns can be understood by considering endophyte growth within the plant and alkaloid mobility. Our study identifies research gaps, including the limited documentation of alkaloid presence in roots and the need to investigate the influence of different environmental conditions. [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]