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A trade-off between growth and defence against biotic stresses is common in plants. Fungal endophytes of the genus Epichloë may relieve this trade-off in their host grasses since they can simultaneously induce plant growth and produce antiherbivore alkaloids that circumvent the need for host defence. The Epichloë ability to decouple the growth-defence trade-off was evaluated by subjecting ryegrass with and without Epichloë endophytes to an exogenous treatment with gibberellin (GA) followed by a challenge with Rhopalosiphum padi aphids. In agreement with the endophyte-mediated trade-off decoupling hypothesis, the GA-derived promotion of plant growth increased the susceptibility to aphids in endophyte-free plants but did not affect the insect resistance in endophyte-symbiotic plants. In line with the unaltered insect resistance, the GA treatment did not reduce the concentration of Epichloë-derived alkaloids. The Epichloë mycelial biomass was transiently increased by the GA treatment but at the expense of hyphal integrity. The response of the phyllosphere bacterial microbiota to both GA treatment and Epichloë was also evaluated. Only Epichloë, and not the GA treatment, altered the composition of the phyllosphere microbiota and the abundance of certain bacterial taxa. Our findings clearly demonstrate that Epichloë does indeed relieve the plant growth-defence trade-off., (© 2024 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.)

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., (© The Author(s) 2024. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.)

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., (© 2022. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.)

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., (Copyright © 2021 Elsevier Inc. All rights reserved.)

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., (© 2021 John Wiley & Sons Ltd.)

A trade-off between growth and defence functions is commonly observed in plants. We propose that the association of plants with Epichloë fungal endophytes may eliminate this trade-off. This would be a consequence of the double role of these endophytes in host plants: the stimulation of plant growth hormones (e.g. gibberellins) and the fungal production of antiherbivore alkaloids. We put forward a model that integrates this dual effect of endophytes on plant growth and defence and test its predictions by means of meta-analysis of published literature. Our results support the notion that the enhanced plant resistance promoted by endophytes does not compromise plant growth. The limits and ecological benefits of this endophyte-mediated lack of plant growth-defence trade-off are discussed., (© 2021 The Authors New Phytologist © 2021 New Phytologist Foundation.)

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., (© 2020 John Wiley & Sons Ltd.)

Background and Aims: The processes that maintain variation in the prevalence of symbioses within host populations are not well understood. While the fitness benefits of symbiosis have clearly been shown to drive changes in symbiont prevalence, the rate of transmission has been less well studied. Many grasses host symbiotic fungi (Epichloë spp.), which can be transmitted vertically to seeds or horizontally via spores. These symbionts may protect plants against herbivores by producing alkaloids or by increasing tolerance to damage. Therefore, herbivory may be a key ecological factor that alters symbiont prevalence within host populations by affecting either symbiont benefits to host fitness or the symbiont transmission rate. Here, we addressed the following questions: Does symbiont presence modulate plant tolerance to herbivory? Does folivory increase symbiont vertical transmission to seeds or hyphal density in seedlings? Do plants with symbiont horizontal transmission have lower rates of vertical transmission than plants lacking horizontal transmission?, Methods: We studied the grass Poa autumnalis and its symbiotic fungi in the genus Epichloë. We measured plant fitness (survival, growth, reproduction) and symbiont transmission to seeds following simulated folivory in a 3-year common garden experiment and surveyed natural populations that varied in mode of symbiont transmission., Key Results: Poa autumnalis hosted two Epichloë taxa, an undescribed vertically transmitted Epichloë sp. PauTG-1 and E. typhina subsp. poae with both vertical and horizontal transmission. Simulated folivory reduced plant survival, but endophyte presence increased tolerance to damage and boosted fitness. Folivory increased vertical transmission and hyphal density within seedlings, suggesting induced protection for progeny of damaged plants. Across natural populations, the prevalence of vertical transmission did not correlate with symbiont prevalence or differ with mode of transmission., Conclusions: Herbivory not only mediated the reproductive fitness benefits of symbiosis, but also promoted symbiosis prevalence by increasing vertical transmission of the fungus to the next generation. Our results reveal a new mechanism by which herbivores could influence the prevalence of microbial symbionts in host populations., (© The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Although the role of fungal alkaloids in protecting grasses associated with Epichloë fungal endophytes has been extensively documented, the effects of the symbiont on the host plant's immune responses have received little attention. We propose that, in addition to producing protective alkaloids, endophytes enhance plant immunity against chewing insects by promoting endogenous defense responses mediated by the jasmonic acid (JA) pathway. We advance a model that integrates this dual effect of endophytes on plant defenses and test its predictions by means of a standard meta-analysis. This analysis supports a role of Epichloë endophytes in boosting JA-mediated plant defenses. We discuss the ecological scenarios where this effect of endophytes on plant defenses would be most beneficial for increasing plant fitness., (Copyright © 2017 Elsevier Ltd. All rights reserved.)

Plant-herbivore interactions are often mediated by plant microorganisms, and the "defensive mutualism" of epichloid fungal endophytes of grasses is an example. These endophytes synthesize bioactive alkaloids that generally have detrimental effects on the performance of insect herbivores, but the underlying mechanisms are not well understood. Our objective was to determine whether changes in the physiology and/or behavior of aphids explain the changes in performance of insects feeding on endophytic plants. We studied the interaction between the aphid Rhopalosiphum padi and the annual ryegrass Lolium multiflorum symbiotic (E+) or not symbiotic (E-) with the fungus Epichloë occultans that can synthesize loline alkaloids. We hypothesized that aphids feeding on E+ plants have higher energetic demands for detoxification of fungal alkaloids, thereby negatively impacting the individual performance, population growth, and structure. Aphids growing on E+ plants had lower values in morphometric and functional variables of individual performance, displayed lower birth rate, smaller population size, and dramatic structural changes. However, aphids exhibited lower values of standard metabolic rate (SMR) on E+ plants, which suggests no high costs of detoxification. Behavioral variables during the first 8 h of feeding showed that aphids did not change the phloem sap ingestion with the presence of fungal endophytes. We hypothesize that aphids may maintain phloem sap ingestion according to their fungal alkaloid tolerance capacity. In other words, when alkaloid concentrations overcome tolerance threshold, ingestion of phloem should decrease, which may explain the observed lower values of SMR in E+ feeding aphids.

Premise of the Study: A transgenerational effect occurs when a biotic or abiotic environmental factor acts on a parental individual and thereby affects the phenotype of progeny. Due to the importance of transgenerational effects for understanding plant ecology and evolution, their underlying mechanisms are of general interest. Here, we introduce the concept that inherited symbiotic microorganisms could act as mechanisms of transgenerational effects in plants., Methods: We define the criteria required to demonstrate that transgenerational effects are microbially mediated and review evidence from the well-studied, vertically transmitted plant-fungal symbiosis (grass- Epichloë spp.) in support of such effects. We also propose a basic experimental design to test for the presence of adaptive transgenerational effects mediated by plant symbionts., Key Results: An increasingly large body of literature shows that vertically transmitted microorganisms are common in plants, with potential to affect the phenotypes and fitness of progeny. Transgenerational effects could occur via parental modification of symbiont presence/absence, symbiont load, symbiont products, symbiont genotype or species composition, or symbiont priming. Several of these mechanisms appear likely in the grass- Epichloë endophytic symbiosis, as there is variation in the proportion of the progeny that carries the fungus, as well as variation in concentrations of mycelia and secondary compounds (alkaloids and osmolytes) in the seed., Conclusions: Symbiont-mediated transgenerational effects could be common in plants and could play large roles in plant adaptation to changing environments, but definitive tests are needed. We hope our contribution will spark new lines of research on the transgenerational effects of vertically transmitted symbionts in plants., (© 2017 Botanical Society of America.)

Polyploidy and symbiotic Epichloë fungal endophytes are common and heritable characteristics that can facilitate environmental range expansion in grasses. Here we examined geographic patterns of polyploidy and the frequency of fungal endophyte colonized plants in 29 Festuca rubra L. populations from eight geographic sites across latitudes from Spain to northernmost Finland and Greenland. Ploidy seemed to be positively and negatively correlated with latitude and productivity, respectively. However, the correlations were nonlinear; 84% of the plants were hexaploids (2n = 6x = 42), and the positive correlation between ploidy level and latitude is the result of only four populations skewing the data. In the southernmost end of the gradient 86% of the plants were tetraploids (2n = 4x = 28), whereas in the northernmost end of the gradient one population had only octoploid plants (2n = 8x = 56). Endophytes were detected in 22 out of the 29 populations. Endophyte frequencies varied among geographic sites, and populations and habitats within geographic sites irrespective of ploidy, latitude or productivity. The highest overall endophyte frequencies were found in the southernmost end of the gradient, Spain, where 69% of plants harbored endophytes. In northern Finland, endophytes were detected in 30% of grasses but endophyte frequencies varied among populations from 0% to 75%, being higher in meadows compared to riverbanks. The endophytes were detected in 36%, 30% and 27% of the plants in Faroe Islands, Iceland and Switzerland, respectively. Practically all examined plants collected from southern Finland and Greenland were endophyte-free, whereas in other geographic sites endophyte frequencies were highly variable among populations. Common to all populations with high endophyte frequencies is heavy vertebrate grazing. We propose that the detected endophyte frequencies and ploidy levels mirror past distribution history of F. rubra after the last glaciation period, and local adaptations to past or prevailing selection forces such as vertebrate grazing., Competing Interests: The authors have declared that no competing interests exist.

Plants employ various strategies to mitigate the impact of herbivory and one such strategy involves the associations with fungal endophytes. Some cool‐season forage grasses benefit from protection against herbivores by Epichloë fungal endophytes. However, since the maintenance of symbiosis relies on the plant, costs of hosting endophytes have been also observed. This becomes particularly crucial when forage varieties, inoculated with endophytes that are nontoxic to livestock but still protect host against insect herbivores, experience significant foliage loss (defoliation). We investigated the impact of a nontoxic Epichloë endophyte on the responses of tall fescue plants to defoliation across two morphotype varieties, Continental and Mediterranean, and different seasonal contexts. Under specific defoliation treatments, endophyte‐symbiotic plants showed reduced postdefoliation recovery, indicating the costs of hosting the endophyte for host plants. However, these conditions were not the most severe for plant growth. Regardless of the endophyte's presence, plants from Continental morphotype exhibited superior recovery than those from Mediterranean morphotype, an effect that was more pronounced in summer. Notably, the endophyte promoted plant growth after defoliation in winter for both morphotypes. Our study offers insights into mitigating endophyte‐associated costs on plant recovery postdefoliation by strategically managing cutting intensity and frequency, considering the seasonal variation. [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]

Bromus auleticus is a winter wild species with promissory characteristics for domestication as forage that inhabits temperate‐warm grasslands from a wide region from South America. Populations from regions with different environmental conditions are considered as ecotypes and are associated with different seedborne Epichloë fungal endophytes. Association with Epichloë provides B. auleticus with increased growth capacity and resistance against pathogens. The seeds mature at the end of spring and germinate in autumn, remaining dormant during wet and warm summer. As the persistence of Epichloë endophytes in the seed is highly sensitive to temperature and humidity, we studied how the endophytes modulate seed germination in response to these factors in two B. auleticus ecotypes named La Pampa (LP) and El Palmar (EP). We also studied how environmental factors during germination affect endophyte survival. In the LP ecotype, adapted to coldest temperatures in autumn, Epichloë improved final germination under alternating temperatures, but had no effects on germination inhibition imposed by low water availability. In the EP ecotype, adapted to warm humid summer and autumn, the endophyte promoted germination at constant 25°C and alternating 15/25°C temperatures, and prevented germination at low water potentials. At 30°C, seed germination was inhibited and whereas seeds remained viable, endophyte survival was significantly lowered. The effect of Epichloë on B. auleticus seed germination was ecotype‐specific: promoting germination at alternating temperatures in La Pampa ecotype or at high temperatures in El Palmar ecotype, while inhibiting it at low water availabilities, could be an endophyte‐mediated ecotypic strategy minimising endophyte mortality and increasing seedling establishment. [ABSTRACT FROM AUTHOR]

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1. The strength of many interactions between plants and other organisms changes across regional gradients. For example, the relevance of plant-herbivore interactions increases with primary production. Likewise, biotic interactions collectively become more intense from the poles to the equator. Yet, the regional variation of the interaction between grasses and systemic fungal endophytes, which provide resistance to biotic and abiotic environmental factors (i.e. herbivory and drought), is poorly understood. 2. We compiled 1008 records of the incidence level of fungal endophytes (Epichloë, Ascomycetes: Clavicipitaceae) on wild populations of 48 cool season grasses, encompassing 10 biomes across a broad latitudinal expanse and primary production gradient. Symbiosis incidence was analysed as a function of mean primary production, precipitation, temperature and latitude of each site, which in turn were obtained from climatic and satellital sources. 3. Across a 30-fold variation of mean primary production, average symbiosis incidence increased from 20% to 70%. The pattern became stronger when the analysis was restricted to the single grass genus Festuca, which accounted for half of the total data. 4. The number of grass populations showing no symbiosis incidence (0%) decreased as primary production increased, whereas those with 100% of incidence increased. 5. Primary production at the regional scale was negatively correlated with latitude but positively with mean annual temperature and precipitation. Symbiosis incidence was similarly correlated with latitude and temperature, and it was not with mean annual precipitation. 6. Synthesis. Different descriptors of this grass-fungus symbiosis show that average incidence in wild populations world-wide increases with mean primary production. As at large spatial scales herbivory and temperature increase and aridity decreases with primary production, our results suggest that, at broad-scales, these biotic and abiotic factors may be important drivers of the symbiosis success. [ABSTRACT FROM AUTHOR]

Epichloë endophytes are common symbionts living asymptomatically in pooid grasses and may provide chemical defences against herbivorous insects. While the mechanisms underlying these fungal defences have been well studied, it remains unknown whether endophyte presence affects the host's own defences. We addressed this issue by examining variation in the impact of Epichloë on constitutive and herbivore-induced emissions of volatile organic compounds (VOC), a well-known indirect plant defence, between two grass species, Schedonorus phoenix (ex. Festuca arundinacea; tall fescue) and Festuca pratensis (meadow fescue). We found that feeding by a generalist aphid species, Rhopalosiphum padi, induced VOC emissions by uninfected plants of both grass species but to varying extents, while mechanical wounding failed to do so in both species after one day of damage. Interestingly, regardless of damage treatment, Epichloë uncinata-infected F. pratensis emitted significantly lower quantities of VOCs than their uninfected counterparts. In contrast, Epichloë coenophiala-infected S. phoenix did not differ from their uninfected counterparts in constitutive VOC emissions but tended to increase VOC emissions under intense aphid feeding. A multivariate analysis showed that endophyte status imposed stronger differences in VOC profiles of F. pratensis than damage treatment, while the reverse was true for S. phoenix. Additionally, both endophytes inhibited R. padi population growth as measured by aphid dry biomass, with the inhibition appearing greater in E. uncinata-infected F. pratensis. Our results suggest, not only that Epichloë endophytes may play important roles in mediating host VOC responses to herbivory, but also that the magnitude and direction of such responses may vary with the identity of the Epichloë–grass symbiosis. Whether Epichloë-mediated host VOC responses will eventually translate into effects on higher trophic levels merits future investigation. [ABSTRACT FROM AUTHOR]