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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]

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]

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]

Neotyphodium frequently occurs as an endophyte in grasses. Evidence shows enhanced fitness of endophyte infected grasses relative to non-infected ones. Some studies of seed germination show endophyte enhancement of plant fitness in various environments, but inconsistent results indicate that further studies are needed. So far, experiments have failed to separate the confounded effects of population origin and seed management. For this reason, we evaluated the effects of endophyte infection on seed dormancy and germination in Lolium multiflorum using an experimental design controlling these factors. Depending on the year of seed production, endophyte infection modified seed response to light quality, affecting predominantly seed dormancy levels. Nevertheless, the endophyte did not affect base temperature or thermal time of germination. We concluded that endophytes were not a strong influence on germination behaviour. We speculate from our results that the presence of the endophyte changes germination by an indirect effect, in extending growth of the maternal plant during seed development and ripening. The direct effect of hyphae in the seed on seed behaviour was disregarded, because the difference between infected and non-infected seed varied within the year of seed production. Future experiments should focus on effects of the endophyte on the canopy of parent plants during seed production and ripening, and, hence, on subsequent dormancy and germination of the seeds. [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]

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]

Environmental stresses can compromise the interactions of plants with beneficial microbes. In the present review, experimental results showing that stresses negatively affect the abundance and/or functionality of plant beneficial microbes are summarized. It is proposed that the environmental interference of these plant−microbe interactions is explained by the stress‐mediated induction of plant signalling pathways associated with defence hormones and reactive oxygen species. These plant responses are recognized to regulate beneficial microbes within plants. The direct negative effect of stresses on microbes may also contribute to the environmental regulation of these plant mutualisms. It is also posited that, in stress situations, beneficial microbes harbour mechanisms that contribute to maintain the mutualistic associations. Beneficial microbes produce effector proteins and increase the antioxidant levels in plants that counteract the detrimental effects of plant stress responses on them. In addition, they deliver specific stress‐protective mechanisms that assist to their plant hosts to mitigate the negative effects of stresses. Our study contributes to understanding how environmental stresses affect plant−microbe interactions and highlights why beneficial microbes can still deliver benefits to plants in stressful environments. SUMMARY STATEMENT: Here, it is proposed that the environmental interference of plant‐microbe interactions is explained by the stress‐mediated induction of certain plant signalling pathways and that specific mechanisms harboured by beneficial microbes assist in maintaining the mutualisms in stress situations. [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]

Abstract: Temperate grasses frequently acquire resistance to herbivores through a symbiosis with epichloid fungi that produces alkaloids of variable deterrent effects. However, in those cases without apparent endophyte negative effects on domestic herbivores, it is not clear whether plant consumption or preference is affected or not. We performed three experiments with 1‐year‐old steers (Bos taurus, Aberdeen Angus) and the annual grass Lolium multiflorum, infected or not by Epichloë occultans to evaluate preference and to identify the underlying tolerance mechanisms. The first experiment evaluated steer preference for L. multiflorum cultivated in plots with three endophyte infection frequencies (low, medium and high), and investigated the role of canopy structure and plant nutritional traits on preference. The second experiment evaluated preference for chopped grass, offered in individual trays with contrasting infection frequencies (low and high), to discard possible effects associated with canopy structure and to focus on nutritional traits. The third experiment was performed with a tray + basket design that separated visual and olfactory stimuli from nutritional traits. High endophyte infection frequencies reduced consistently animal preference, even after short (~10 min) feeding events. However, we did not find significant evidence of plant structural, nutritional, visual or olfactory traits. Our results discarded several potential mechanisms; therefore, the dissuasive effect of fungal endophytes on animal consumption might be related to other mechanisms, including, likely, alkaloids and changes on grass metabolome. [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]