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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.)

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.

We propose that symbiotically modified organisms (SMOs) should be taken into account in sustainable agriculture. In this opinion article, we present the results of a meta-analysis of the literature, with a particular focus on the potential of SMOs in forage and turf grass production, to determine the impact of endophytes in grasses on livestock, the grassland ecosystems, and associated environments. SMOs can be incorporated into breeding programs to improve grass yield, resistance to pests and weeds, and forage quality for livestock by decreasing the level of toxic alkaloids. However, the benefits of these selected grass-endophyte symbiota appear to be highly dependent on grass cultivar, fungal strain, and environmental conditions, requiring a comprehensive understanding of the genetic bases and phenotypic plasticity of the traits of the plant-microbe unit in different environments., (Copyright © 2013 Elsevier Ltd. 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. 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]

Summary: 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. [ABSTRACT FROM AUTHOR]

Our hypothesis is that I Epichloë i endophytes may uncouple the growth-defence trade-off by simultaneously inducing plant growth-related hormones and producing defence compounds (alkaloids) that circumvent the need for host defence-related hormones (Fig. As a final note, it is important to remark that we put forward that endophytes I can i eliminate the growth-defence trade-off, proving our point with I Epichloë i endophytes but acknowledging that not all endophytes would possess the ability to decouple the trade-off. Keywords: alkaloids; endophytes; growth-defence trade-off; phytohormones; symbiosis EN alkaloids endophytes growth-defence trade-off phytohormones symbiosis 388 390 3 06/20/22 20220715 NES 220715 Acknowledgements We thank Víctor M. Escobedo and Christina D. Moon for critical contributions to earlier versions of the manuscript. How and when fungal endophytes can eliminate the plant growth-defence trade-off: mechanistic perspectives. [Extracted from the article]

In this review, we examine the functional roles of microbial symbionts in plant tolerance to cold and freezing stresses. The impacts of symbionts on antioxidant activity, hormonal signaling and host osmotic balance are described, including the effects of the bacterial endosymbionts Burkholderia, Pseudomonas and Azospirillum on photosynthesis and the accumulation of carbohydrates such as trehalose and raffinose that improve cell osmotic regulation and plasma membrane integrity. The influence of root fungal endophytes and arbuscular mycorrhizal fungi on plant physiology at low temperatures, for example their effects on nutrient acquisition and the accumulation of indole‐3‐acetic acid and antioxidants in tissues, are also reviewed. Meta‐analyses are presented showing that aspects of plant performance (shoot biomass, relative water content, sugar and proline concentrations and Fv/Fm) are enhanced in symbiotic plants at low (−1 to 15 °C), but not at high (20–26 °C), temperatures. We discuss the implications of microbial symbionts for plant performance at low and sub‐zero temperatures in the natural environment and propose future directions for research into the effects of symbionts on the cold and freezing tolerances of plants, concluding that further studies should routinely incorporate symbiotic microbes in their experimental designs. [ABSTRACT FROM AUTHOR]

Abstract: The plant hormone salicylic acid (SA) is recognized as an effective defence against biotrophic pathogens, but its role as regulator of beneficial plant symbionts has received little attention. We studied the relationship between the SA hormone and leaf fungal endophytes on herbivore defences in symbiotic grasses. We hypothesize that the SA exposure suppresses the endophyte reducing the fungal‐produced alkaloids. Because of the role that alkaloids play in anti‐herbivore defences, any reduction in their production should make host plants more susceptible to herbivores. Lolium multiflorum plants symbiotic and nonsymbiotic with the endophyte Epichloë occultans were exposed to SA followed by a challenge with the aphid Rhopalosiphum padi. We measured the level of plant resistance to aphids, and the defences conferred by endophytes and host plants. Symbiotic plants had lower concentrations of SA than did the nonsymbiotic counterparts. Consistent with our prediction, the hormonal treatment reduced the concentration of loline alkaloids (i.e., N‐formyllolines and N‐acetylnorlolines) and consequently decreased the endophyte‐conferred resistance against aphids. Our study highlights the importance of the interaction between the plant immune system and endophytes for the stability of the defensive mutualism. Our results indicate that the SA plays a critical role in regulating the endophyte‐conferred resistance against herbivores. [ABSTRACT FROM AUTHOR]

Symbiosis between cool-season grasses and vertically transmitted fungal endophytes are common and significantly impact on ecosystem function. This makes the understanding of the underlying mechanisms to symbiotic individuals frequency in local populations much more interesting. Most studies have been focused on the differential fitness between symbiotic and non-symbiotic counterparts (relative fitness), barely considering other mechanisms. We performed a microcosms experiment to evaluate whether grazing alters the dynamics of the endophyte Neotyphodium occultans in the annual grass Lolium multiflorum by simultaneously modifying the relative fitness and the endophyte efficiency to be transmitted from host plants to seeds. Grazing was simulated by means of clipping and trampling on symbiotic and non-symbiotic plants growing separately, in soils obtained from paddocks, differing in their agronomic management history (natural grassland vs. ryegrass promotion). Seed production showed a complex pattern as it depended on the symbiotic status of the plants, the level of grazing and the agro-ecological context. Grazed plants produced three times fewer seeds than ungrazed plants only in microcosms with endophyte-symbiotic plants in soils from ryegrass promotion. Endophyte benefits on seed production were exclusively observed in ungrazed plants in the same soil. Symbiotic plants produced symbiotic and non-symbiotic seeds in all the treatments. While the production of non-symbiotic seeds by these plants was not affected by grazing and the soil, grazing reduced the production of symbiotic seeds in both contexts. Grazing negative effect on the density of fully infected spikes determined a significant increment in the transmission failures which were not modified by agro-ecological contexts. Therefore, grazing can modulate symbiosis dynamics through reducing seed production and endophyte transmission efficiency. Transmission has been disregarded, but it is a context-dependent process that could lead to a gradual reduction in the symbiotic plants frequency in a population if the mutualism effectiveness does not outweigh transmission failures. [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]

Abstract: Most terrestrial plants form symbiosis with a large variety of microorganisms that can be major determinants of morphological and physiological host traits that, ultimately, affect the structure and function of communities. Epichloae fungal endophytes (Clavicipitaceae) are widespread symbionts of grasses that asymptomatically inhabit aerial host tissues, and confer defense to herbivores and tolerance to multiple stresses. Research on symbionts of plants has focused on soil organisms such as nitrogen-fixing bacteria and mycorrhizal fungi, although recent studies suggest that endophytes of great agronomic interest can also generate major shifts in the belowground subsystem. We conducted a meta-analysis to examine the available knowledge on the effects of endophytes on the soil. Our objective was to provide a synthesis of existing data that, comprehensively and quantitatively, evaluates the different pathways by which the grass–endophyte symbiosis may affect belowground components and processes, and highlights gaps in knowledge relevant to agroecosystem management. The presence of endophyte was found to reduce root biomass and mycorrhizal colonization of plants. In turn, a significant stimulation of root exudates by endophytes was detected. Effects of endophytes on soil respiration and litter decomposition were not significant. No pattern was found in the response of the soil fauna to endophyte presence. Our review revealed that we still need to improve our understanding about the impact of endophytes on other mutualistic symbionts. The grass–endophyte symbiosis is a promising interaction that, like those involving nitrogen-fixing bacteria and mycorrhizal fungi, may become an important tool for sustainable agriculture. [Copyright &y& Elsevier]