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Plants harbor a wide diversity of microorganisms in their tissues. Some of them have a long co-evolutionary history with their hosts, likely playing a pivotal role in regulating the plant interaction with other microbes such as pathogens. Some cool-season grasses are symbiotic with Epichloë fungal endophytes that grow symptomless and systemically in aboveground tissues. Among the many benefits that have been ascribed to endophytes, their role in mediating plant interactions with pathogens has been scarcely developed. Here, we explored the effects of Epichloë fungal endophytes on the interaction of host grasses with fungal pathogens. We made a meta-analysis that covered a total of 18 host grass species, 11 fungal endophyte species, and 22 fungal pathogen species. We observed endophyte-mediated negative effects on pathogens in vitro and in planta. Endophyte negative effects on pathogens were apparent not only in laboratory but also in greenhouse and field experiments. Epichloë fungal endophytes had negative effects on pathogen growth and spores' germination. On living plants, endophytes reduced both severity and incidence of the disease as well as colonization and subsequent infection of seeds. Symbiosis with endophytes showed an inhibitory effect on debilitator and killer pathogens, but not on castrators, and this effect did not differ among biotrophic or necrotrophic lifestyles. We found that this protection can be direct through the production of fungistatic compounds, the competition for a common resource, or the induction of plant defenses, and indirect associated with endophyte-generated changes in the abiotic or the biotic environment. Several mechanisms operate simultaneously and contribute differentially to the reduction of disease within grass populations. • Epichloë fungal endophytes protect host plants against fungal pathogens. • This protection against pathogens can be either direct or indirect. • Endophytes reduce pathogen incidence and severity in host plant populations. • In seeds, the association with endophytes reduced pathogen colonization and infection. • Endophyte protection seems to be clear on debilitator and killer pathogens but not on castrators. [ABSTRACT FROM AUTHOR]

Highlights: [•] Symbiotically modified organisms (SMOs) can improve grass yield, and resistance to pests and weeds. [•] SMOs can improve forage quality for livestock. [•] Toxicity can be caused by uncharacterized plant or fungal metabolites. [•] Feasibility of SMOs depends on the cultivar and fungal strain. [ABSTRACT FROM AUTHOR]

Driven by human activities, air pollution and soil degradation are threatening food production systems. Rising ozone in the troposphere can affect several physiological processes in plants and their interaction with symbiotic microorganisms. Plant responses to ozone may depend on both soil fertility and the ontogenetic stage in which they are exposed. In this work, we studied the effects of ozone episodes and soil fertility on soybean plants. We analysed soybean plant responses in the production of aboveground and belowground biomass, structural and functional attributes of rhizobia, and seed production and quality. The experiment was performed with plants grown in two substrates with different fertility (commercial soil, and soil diluted (50%, v/v) with sand). Plants were exposed to acute episodes of ozone during vegetative and reproductive stages. We observed that ozone significantly reduced belowground biomass (≈25%), nodule biomass (≈30%), and biological nitrogen fixation (≈21%). Plants exposed to ozone during reproductive stage growing in soil with reduced fertility had lower seed production (≈10% lower) and seed protein (≈12% lower). These responses on yield and quality can be explained by the observed changes in belowground biomass and nitrogen fixation. The negative impact of ozone on the symbiotic interaction with rhizobia, seed production and quality in soybean plants were greater in soils with reduced fertility. Our results indicate that food security could be at risk in the future if trends in ozone concentration and soil degradation processes continue to increase. Image 1 • Ozone reduced belowground biomass, nodulation and biological nitrogen fixation in soybean plants. • Soybean plants exposed to ozone during reproductive stage had lower seed production and quality. • These ozone effects were significant in soybean plants growing on low fertility soils. Tropospheric ozone episodes reduce nodulation, biological nitrogen fixation, seed production and quality in soybean plants growing on reduced fertility soils. [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]

Expansins are proteins involved in cell wall metabolism that play an important role in plant growth, development, fruit ripening and abiotic stress tolerance. In the present study, we analyzed putative expansins that respond to drought stress. Five expansin genes were identified in cDNA libraries isolated from Colobanthus quitensis gown either with or without endophytic fungi under hydric stress. A differential transcript abundance was observed by qPCR analysis upon drought stress. To compare these expansin genes, and to suggest a possible mechanism of action at the molecular level, the structural model of the deduced proteins was obtained by comparative modeling methodology. The structures showed two domains and an open groove on the surface of the proteins was observed in the five structural models. The proteins were evaluated in terms of their protein-ligand interactions using four different ligands. The results suggested differences in their mode of protein-ligand interaction, in particular concerning the residues involved in the protein-ligand interaction. The presented evidence supports the participation of some members of the expansin multiprotein family in the response to drought stress in C. quitensis and suggest that the response is modulated by endophytic fungi. [Display omitted] • Antarctic plant lives in stressing environment in symbiosis with fungal endophytes. • Expansin encoding genes are differentially expressed in response to drought stress. • Expansin are differentially modulated by fungal endophytes presence. • Expansin proteins display variable substrate affinity to polysaccharides. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

[Display omitted] • Plant-fungal symbiotic interaction drives improvements in the performance of plants exposed to environmental stresses. • One of the mechanisms triggered by symbiosis under stress is flavonoids accumulation. • Some endophytes establish symbiosis with non-original hosts promoting their growth. • Eco-friendly strategies are key to improve plant performance and yield under stress. Climate change is threatening human activities, but the combination of water scarcity and heat waves are particularly challenging agriculture. Accumulating literature shows that beneficial fungal endophytes improve plant performance, a condition that seems to be magnified in presence of stress. Because evidence points out to an endophytic mediation of antioxidant activity in plants, we here focused on flavonoids for two main reasons: (i) they are involved in plant tolerance to abiotic stress, and (ii) they are known to be healthy for human consumption. With these two premises as guidance, we explored the literature trying to link mechanistically the relationship between endophytes and plant responses to stress as well as identifying patterns and knowledge gaps. Overall, fungal endophytes improve plant growth and tolerance to environmental stresses. However, evidence for endophytes boosting flavonoid mediated responses in plants is relatively scarce. Reports showing endophytes promoting flavonoid contents in grains and fresh fruits are rather limited which may be related to (long) length of the required experiments for testing it. The use of endophytes isolated from extreme environments (e.g., dry and cold deserts, acid lakes, etc.) is proposed to be better in conferring tolerance to plants under very stressful conditions. However, the real challenge is to test the capacity of these endophytes to established and maintain persistent and functional symbiosis under productive conditions. In summary, there is a clear potential for symbiotically modifying crop plants as a strategy to develop more tolerant varieties to face the stress and eventually increase the quality of the agricultural products. [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]