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Despite their genetic adaptation to local conditions, plants often achieve ecological success through symbiotic associations with fungal endophytes. However, the habitat-specific functionality of these interactions and their potential to drive plant adaptation to new environments remain uncertain. In this study, we tested this using the vascular flora of the Antarctic tundra (Colobanthus quitensis and Deschampsia antarctica), an extreme environment where fungal endophytes are known for playing important ecological roles. After characterizing the root-associated fungal endophyte communities of both species in two distinct Antarctic terrestrial habitats-hill and coast-we experimentally assessed the contribution of fungal endophytes to plant adaptation in each habitat. The field reciprocal transplant experiment involved removing endophytes from a set of plants and crossing symbiotic status (with and without endophytes) with habitat for both species, aiming to assess plant performance and fitness. The diversity of root fungal endophytes was similar between habitats and mainly explained by plant species, although habitat-specific endophyte community structures were identified in D. antarctica. Endophytes significantly influenced C. quitensis homeostatic regulation, including oxidative stress and osmotic control, as well as plant fitness in both environments. By contrast, the effect of endophytes on D. antarctica was particularly evident in coastal sites, suggesting an endophyte-mediated improvement in local adaptation. Altogether, our results suggest that the two Antarctic vascular plant species follow different strategies in recruiting and developing functional symbiosis with root-associated fungal communities. While C. quitensis is more generalist, D. antarctica establishes specific interactions with habitat-specific microbial symbionts, predominantly in the most stressful environmental context., (© 2024 Scandinavian Plant Physiology Society.)

Background: Chlorsulfuron resistance and genetic dominance was evaluated in Raphanus raphanistrum genotypes homozygous (122-RR, 376-RR), heterozygous (122-RS, 376-RS) and compound heterozygous (122-R/376-R) for the target-site resistance mutations Ala-122-Tyr and Asp-376-Glu in the AHAS (acetohydroxyacid synthase) gene., Results: At the AHAS level, 122-RR and 122-RS plants exhibited significantly higher I 50 values than 376-RR and 376-RS plants, respectively. However, plants of the compound heterozygous genotype (122-R/376-R), showed no difference in AHAS activity compared to the 122-RS genotype but lower activity than the 122-RR genotype, and showed a nearly 400-fold greater I 50 value than both genotypes (376-RR and 376-RS) carrying the 376-Glu allele. At the whole-plant level, 100% survival was observed for 122-RR plants at the highest chlorsulfuron dose of 640 g ha -1 , yet 376-RR plants showed no survival at 380 g ha -1 . Thus, this survival difference resulted in different median lethal dose (LD 50 ) estimates [>640 (122-RR) versus 330 g ha -1 (376-RR)]. The effect of chlorsulfuron in reducing aboveground growth of surviving plants also was markedly lower for the homozygous 122-RR (GR 50  = 566 g ha -1 ) than for 376-RR plants (GR 50  = 66). Heterozygous plants carrying the 122-Tyr allele (122-RS) exhibited two- and five-fold higher LD 50 values than both homozygous and heterozygous plants carrying the 376-Glu allele (376-RR, 376-RS), respectively. Along the difference in plant survival, 122-RS plants also showed four-fold higher GR 50 than both 376-RR and 376-RS plants. Survival of plants with the compound heterozygous genotype (122-R/376-R) under increasing chlorsulfuron doses was similar to 122-RR or 122-RS genotypes. However, this compound heterozygous genotype showed two- and six-fold higher LD 50 values than 376-RR or 376-RS genotypes, respectively. However, both resistance 122-Tyr and 376-Glu alleles were dominant or nearly dominant over the wild-type susceptible alleles (ALA-122 and ASP-376), and the resistance 122-Tyr allele was dominant over the 376-Glu allele., Conclusions: These results broaden our understanding of AHAS target-site resistance in R. raphanistrum and strengthens the hypothesis that the AHAS 122-Tyr allele corresponds to a stronger target-site resistance allele than the 376-Glu allele. © 2024 Society of Chemical Industry., (© 2024 Society of Chemical Industry.)

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.)

In agroecosystems, herbicides are the predominant anthropogenic selection pressure for agriculture weed species. While weeds are the primary target, herbicides can have adverse impacts on non-target plant beneficial microorganisms. We aimed to investigate the influence of a foliar endophytic fungus (Epichloë occultans) on the sensitivity of Lolium multiflorum to a graminicide herbicide (diclofop-methyl) during both plant ontogeny and progeny. Susceptible individuals to diclofop-methyl with and without endophyte were pre-exposed to the auxin 2,4-D herbicide. This herbicide is known to stimulate the metabolic detoxification mechanism (CYP-450) of diclofop-methyl. Regardless of the endophyte, 2,4-D pre-treatment increased mother plant survival to nearly 100 % under diclofop treatment but not in the progeny. Furthermore, maternal plant exposure to 2,4-D reduced endophyte transmission to the seeds and from seed-to-seedlings. Our findings suggest that, despite a reduction in diclofop-methyl sensitivity during the ontogeny of mother plants, 2,4-D-mediated induction of likely CYP-450 metabolism is not intergenerationally transmitted and shows detrimental effects on the symbiotic endophyte persistence., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2023 Elsevier B.V. All rights reserved.)

Plants inhabiting environments with stressful conditions often exhibit a low number of flowers, which can be attributed to the energetic cost associated with reproduction. One of the most stressful environments for plants is the Antarctic continent, characterized by limited soil water availability and low temperatures. Induction of dehydrins like those from the COR gene family and auxin transcriptional response repressor genes (IAAs), which are involved in floral repression, has been described in response to water stress. Here, we investigated the relationship between the water deficit-induced stress response and the number of flowers in Colobanthus quitensis plants collected from populations along a latitudinal gradient. The expression levels of COR47 and IAA12 genes in response to water deficit were found to be associated with the number of flowers. The relationship was observed both in the field and growth chambers. Watering the plants in the growth chambers alleviated the stress and stimualted flowering, thereby eliminating the trade-off observed in the field. Our study provides a mechanistic understanding of the ecological constraints on plant reproduction along a water availability gradient. However, further experiments are needed to elucidate the primary role of water availability in regulating resource allocation to reproduction in plants inhibiting extreme environments., (© 2023 John Wiley & Sons Ltd.)

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.

Aphids are important herbivorous insects that can cause significant crop damage, leading to yield reduction and economic loss. One avenue being explored to reduce aphid impacts is the development of aphid-resistant plants. Under projected climate scenarios, it is expected that plants will be exposed to greater biotic and abiotic stress, including increased herbivorous insect infestation and exposure to prolonged periods of environmental stress, particularly drought. In response to these projections, plant-aphid interactions under drought conditions have been a subject of growing interest; however, few studies have looked at the impact of drought stress on plant resistance to aphids despite the potential importance for plant breeding. Here, we examine the latest scientific advances regarding variation in plant resistance to aphids under drought, emphasizing underlying mechanisms and functional trade-offs and propose a conceptual model relating plant tolerance to drought with plant resistance to aphids., (© The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

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., (© 2022 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.)

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.)

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., Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2022 Elsevier Ltd. All rights reserved.)

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.

Seeds commonly harbour diverse bacterial communities that can enhance the fitness of future plants. The bacterial microbiota associated with mother plant's foliar tissues is one of the main sources of bacteria for seeds. Therefore, any ecological factor influencing the mother plant's microbiota may also affect the diversity of the seed's bacterial community. Grasses form associations with beneficial vertically transmitted fungal endophytes of genus Epichloë . The interaction of plants with Epichloë endophytes and insect herbivores can influence the plant foliar microbiota. However, it is unknown whether these interactions (alone or in concert) can affect the assembly of bacterial communities in the produced seed. We subjected Lolium multiflorum plants with and without its common endophyte Epichloë occultans (E+, E-, respectively) to an herbivory treatment with Rhopalosiphum padi aphids and assessed the diversity and composition of the bacterial communities in the produced seed. The presence of Epichloë endophytes influenced the seed bacterial microbiota by increasing the diversity and affecting the composition of the communities. The relative abundances of the bacterial taxa were more similarly distributed in communities associated with E+ than E- seeds with the latter being dominated by just a few bacterial groups. Contrary to our expectations, seed bacterial communities were not affected by the aphid herbivory experienced by mother plants. We speculate that the enhanced seed/seedling performance documented for Epichloë -host associations may be explained, at least in part, by the Epichloë -mediated increment in the seed-bacterial diversity, and that this phenomenon may be applicable to other plant-endophyte associations., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2022 Bastías, Bustos, Jáuregui, Barrera, Acuña-Rodríguez, Molina-Montenegro and Gundel.)

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., (Copyright © 2021 Elsevier Masson SAS. All rights reserved.)

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.)

Symptomless fungal endophytes in the genus Epichloë are repeatedly mentioned to increase tolerance of cool-season grasses to a wide range of environmental stress factors, mainly drought. However, the generality of this idea is challenged because (i) most studies have been conducted on two economically important forage grasses {tall fescue [ Festuca arundinacea (Schreb.) Dumort] and perennial ryegrass ( Lolium perenne L.)}, (ii) endophyte-mediated mechanisms and effects on plant responses to drought have shown to be highly variable across species, and that (iii) symbiosis incidence in plant populations occurring in extremely arid environments is usually low. We question this idea by reviewing the existing information about Epichloë fungal endophyte effects on drought tolerance in cool-season grasses. We combined standard review, vote counting, and calculation of effect sizes to synthesize the literature, identify information gaps, and guide future research. The total number of studies was higher for domesticated than for wild species, a ratio that was balanced when papers with data quality for effect size calculus were considered. After the drought, endophyte-infected plants accumulated more aboveground and belowground biomass than non-infected counterparts, while no effect on tillering was observed. However, these effects remained significant for wild (even on tillering) but not for domesticated species. Interestingly, despite the continuous effort in determining physiological mechanisms behind the endophyte effects, no studies evaluated plant fecundity as a measure of ecological fitness nor vital rates (such as survival) as to escalate individual-level variables to population. Together with the high variability in results, our work shows that generalizing a positive effect of fungal endophytes in plant tolerance to drought may be misleading. Future studies combining field surveys with manipulative experiments would allow us to unravel the role of fungal endophytes in plant adaptation by considering the evolutionary history of species and populations to the different ecological contexts., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2021 Decunta, Pérez, Malinowski, Molina-Montenegro and Gundel.)

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., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2020 Elsevier Ltd. All rights reserved.)

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.)

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.

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 F v /F m ) 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., (© 2020 John Wiley & Sons Ltd/CNRS.)

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.)

Climatic change is pointed as one of the major challenges for global food security. Based on current models of climate change, reduction in precipitations and in turn, increase in the soil salinity will be a sharp constraint for crops productivity worldwide. In this context, root fungi appear as a new strategy to improve plant ecophysiological performance and crop yield under abiotic stress. In this study, we evaluated the impact of the two fungal endophytes Penicillium brevicompactum and P. chrysogenum isolated from Antarctic plants on nutrients and Na + contents, net photosynthesis, water use efficiency, yield and survival in tomato and lettuce, facing salinity stress conditions. Inoculation of plant roots with fungal endophytes resulted in greater fresh and dry biomass production, and an enhanced survival rate under salt conditions. Inoculation of plants with the fungal endophytes was related with a higher up/down-regulation of ion homeostasis by enhanced expression of the NHX1 gene. The two endophytes diminished the effects of salt stress in tomato and lettuce, provoked a higher efficiency in photosynthetic energy production and an improved sequestration of Na + in vacuoles is suggested by the upregulating of the expression of vacuolar NHX1 Na + /H + antiporters. Promoting plant-beneficial interactions with root symbionts appears to be an environmentally friendly strategy to mitigate the impact of climate change variables on crop production.

Functional symbiosis is considered one of the successful mechanisms by which plants that inhabit extreme environment improve their ability to tolerate different types of stress. One of the most conspicuous type of symbiosis is the endophyticism. This interaction has been noted to play a role in the adaptation of the native vascular plant Colobanthus quitensis to the stressful environments of Antarctica, characterized by low temperatures and extreme aridity. Projections of climate change for this ecosystem indicate that abiotic conditions will be less limiting due to an increase in temperature and water availability in the soil. Due to this decrease in stress induced by the climate change, it has been suggested that the positive role of fungal endophytes on performance of C. quitensis plants would decrease. In this study, we evaluated the role of endophytic fungi on osmoprotective molecules (sugar production, proline, oxidative stress) and gene expression ( CqNCED1 , CqABCG25 , and CqRD22 ) as well as physiological traits (stomatal opening, net photosynthesis, and stomatal conductance) in individuals of C. quitensis . Individual plants of C. quitensis with (E+) and without (E-) endophytic fungi were exposed to simulated conditions of increased water availability (W+), having the current limiting water condition (W-) in Antarctica as control. The results reveal an endophyte-mediated lower oxidative stress, higher production of sugars and proline in plants. In addition, E+ plants showed differential expressions in genes related with drought stress response, which was more evident in W- than in W+. These parameters corresponded with increased physiological mechanisms such as higher net photosynthesis, stomatal opening and conductance under presence of endophytes (E+) as well as the projected water condition (W+) for Antarctica. These results suggest that the presence of fungal endophytes plays a positive role in favoring tolerance to drought in C. quitensis . However, this positive role would be diminished if the stress factor is relaxed, suggesting that the role of endophytes could be less important under a future scenario of climate change in Antarctica with higher soil water availability., (Copyright © 2020 Hereme, Morales-Navarro, Ballesteros, Barrera, Ramos, Gundel and Molina-Montenegro.)

Background: Plants possess a sophisticated immune system to defend from herbivores. These defence responses are regulated by plant hormones including salicylic acid (SA) and jasmonic acid (JA). Sometimes, plant defences can be complemented by the presence of symbiotic microorganisms. A remarkable example of this are grasses establishing symbiotic associations with Epichloë fungal endophytes. We studied the level of resistance provided by the grass' defence hormones, and that provided by Epichloë fungal endophytes, against an introduced herbivore aphid. These fungi protect their hosts against herbivores by producing bioactive alkaloids. We hypothesized that either the presence of fungal endophytes or the induction of the plant salicylic acid (SA) defence pathway would enhance the level of resistance of the grass to the aphid., Methods: Lolium multiflorum plants, with and without the fungal endophyte Epichloë occultans , were subjected to an exogenous application of SA followed by a challenge with the aphid, Sipha maydis ., Results: Our results indicate that neither the presence of E. occultans nor the induction of the plant's SA pathway regulate S. maydis populations. However, endophyte-symbiotic plants may have been more tolerant to the aphid feeding because these plants produced more aboveground biomass. We suggest that this insect insensitivity could be explained by a combination between the ineffectiveness of the specific alkaloids produced by E. occultans in controlling S. maydis aphids and the capacity of this herbivore to deal with hormone-dependent defences of L. multiflorum ., Competing Interests: Daniel A. Bastías, Stuart D. Card and Wade J. Mace are employed by Forage Science, AgResearch Limited., (©2019 Bastías et al.)

Background: The effect of plant size (seedlings versus young plants versus adult plants) on the phenotypic level of glyphosate resistance and selection intensity (SI) in Sorghum halepense with and without a reduced glyphosate translocation resistance mechanism was evaluated., Results: Resistance parameters [the 50% lethal dose (LD 50 ) and the dose required to cause a 50% reduction in plant growth (GR 50 )] in adult plants were notably higher than in seedlings regardless of the resistance status. However, under similar plant size increases, populations comprised of glyphosate-resistant (R) individuals showed higher survival and growth when glyphosate treated compared with glyphosate-susceptible (S) plants. An increase in SI was always evident with increasing glyphosate doses. However, the rate of increase in SI was higher under glyphosate selection of young R and S plants, followed by seedlings and adult R and S plants. However, in conditions of R seedlings coexisting with adult S plants under glyphosate treatment (1000-4000 g ha -1 ), selection against glyphosate resistance was observed., Conclusion: Any increase in size from the seedling stage of R plants translates into an amplification of resistance. Depending on the particular size combinations of spatially coexisting R and S plants, selection for glyphosate resistance may be faster, slower or even not evident. © 2018 Society of Chemical Industry., (© 2018 Society of Chemical Industry.)

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., (© 2017 John Wiley & Sons Ltd.)

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.

Information on whole community responses is needed to predict direction and magnitude of changes in plant and animal abundance under global changes. This study quantifies the effect of past ozone exposure on a weed community structure and arthropod colonization. We used the soil seed bank resulting from a long-term ozone exposure to reestablish the plant community under a new low-pollution environment. Two separate experiments using the same original soil seed bank were conducted. Plant and arthropod richness and species abundance was assessed during two years. We predicted that exposure to episodic high concentrations of ozone during a series of growing cycles would result in plant assemblies with lower diversity (lower species richness and higher dominance), due to an increase in dominance of the stress tolerant species and the elimination of the ozone-sensitive species. As a consequence, arthropod-plant interactions would also be changed. Species richness of the recruited plant communities from different exposure histories was similar (≈ 15). However, the relative abundance of the dominant species varied according to history of exposure, with two annual species dominating ozone enriched plots (90 ppb: Spergula arvensis, and 120 ppb: Calandrinia ciliata). Being consistent both years, the proportion of carnivore species was significantly higher in plots with history of higher ozone concentration (≈3.4 and ≈7.7 fold higher in 90 ppb and 120 ppb plots, respectively). Our study provides evidence that, past history of pollution might be as relevant as management practices in structuring agroecosystems, since we show that an increase in tropospheric ozone may influence biotic communities even years after the exposure.

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.

Plant responses to competition have often been described as passive consequences of reduced resource availability. However, plants have mechanisms to forage for favorable conditions and anticipate competition scenarios. Despite the progresses made in understanding the role of light signaling in modulating plant-plant interactions, little is known about how plants use and integrate information gathered by their photoreceptors aboveground to regulate performance belowground. Given that the phytochrome family of photoreceptors plays a key role in the acquisition of information about the proximity of neighbors and canopy cover, it is tempting to speculate that changes in the red:far-red (R:FR) ratio perceived by aboveground plant parts have important implications shaping plant behavior belowground. Exploring data from published experiments, we assess the neglected role of light signaling in the control of root function. The available evidence indicates that plant exposure to low R:FR ratios affects root growth and morphology, root exudate profiles, and interactions with beneficial soil microorganisms. Although dependent on species identity, signals perceived aboveground are likely to affect root-to-root interactions. Root systems could also be guided to deploy new growth predominantly in open areas by light signals perceived by the shoots. Studying interactions between above- and belowground plant-plant signaling is expected to improve our understanding of the mechanisms of plant competition.

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.

Tropospheric ozone is one of the major drivers of global change. This stress factor alters plant growth and development. Ozone could act as a selection pressure on species communities composition, but also on population genetic background, thus affecting life history traits. Our objective was to evaluate the consequences of prolonged ozone exposure of a weed community on phenotypic traits of Spergulaarvensis linked to persistence. Specifically, we predicted that the selection pressure exerted by high ozone concentrations as well as the concomitant changes in the weed community would drive population adaptive changes which will be reflected on seed germination, dormancy and longevity. In order to test seed viability and dormancy level, we conducted germination experiments for which we used seeds produced by S. arvensis plants grown within a weed community exposed to three ozone treatments during four years (0, 90 and 120 ppb). We also performed a soil seed bank experiment to test seed longevity with seeds coming from both the four-year ozone exposure experiment and from a short-term treatment conducted at ambient and added ozone concentrations. We found that prolonged ozone exposure produced changes in seed germination, dormancy and longevity, resulting in three S. arvensis populations. Seeds from the 90 ppb ozone selection treatment had the highest level of germination when stored at 75% RH and 25 °C and then scarified. These seeds showed the lowest dormancy level when being subjected to 5 ºC/5% RH and 25 ºC/75% followed by 5% RH storage conditions. Furthermore, ozone exposure increased seed persistence in the soil through a maternal effect. Given that tropospheric ozone is an important pollutant in rural areas, changes in seed traits due to ozone exposure could increase weed persistence in fields, thus affecting weed-crop interactions, which could ultimately reduce crop production.

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.)

Defensive mutualism is widely accepted as providing the best framework for understanding how seed-transmitted, alkaloid producing fungal endophytes of grasses are maintained in many host populations. Here, we first briefly review current knowledge of bioactive alkaloids produced by systemic grass-endophytes. New findings suggest that chemotypic diversity of the endophyte-grass symbiotum is far more complex, involving multifaceted signaling and chemical cross-talk between endophyte and host cells (e.g., reactive oxygen species and antioxidants) or between plants, herbivores, and their natural enemies (e.g., volatile organic compounds, and salicylic acid and jasmonic acid pathways). Accumulating evidence also suggests that the tight relationship between the systemic endophyte and the host grass can lead to the loss of grass traits when the lost functions, such as plant defense to herbivores, are compensated for by an interactive endophytic fungal partner. Furthermore, chemotypic diversity of a symbiotum appears to depend on the endophyte and the host plant life histories, as well as on fungal and plant genotypes, abiotic and biotic environmental conditions, and their interactions. Thus, joint approaches of (bio)chemists, molecular biologists, plant physiologists, evolutionary biologists, and ecologists are urgently needed to fully understand the endophyte-grass symbiosis, its coevolutionary history, and ecological importance. We propose that endophyte-grass symbiosis provides an excellent model to study microbially mediated multirophic interactions from molecular mechanisms to ecology.

Background: Glyphosate resistance in populations of the C(4) perennial Sorghum halepense (Johnsongrass) and C(3) annual Lolium rigidum (rigid ryegrass) has evolved and been documented in many cropping areas around the globe. In S. halepense and in the majority of reported cases in L. rigidum the glyphosate resistance trait has been associated with a mechanism that reduces glyphosate translocation within plants. Here, the significant decrease in the glyphosate resistance level when resistant plants of S. halepense and L. rigidum are grown at suboptimal cool temperature conditions is reported., Results: Lowering temperature from 30 to 19 °C in S. halepense and from 19 to 8 °C in L. rigidum significantly reduced both plant survival and above-ground biomass produced by glyphosate-resistant plants. Thus, glyphosate resistance parameters significantly decreased when glyphosate-treated resistant plants of both species were grown under non-optimal temperature conditions. The results suggest that the resistance mechanism against glyphosate damage is less efficient at sub-optimal [corrected] growing temperatures., Conclusion: It is possible to increase the control of glyphosate-resistant S. halepense and L. rigidum populations by treatment with glyphosate during growing conditions at suboptimal low temperatures. Conversely, glyphosate failure will continue to occur on glyphosate-resistant populations treated during periods of higher temperatures, (Copyright © 2012 Society of Chemical Industry.)

Certain species of the Pooideae subfamily develop stress tolerance and herbivory resistance through symbiosis with vertically transmitted, asexual fungi. This symbiosis is specific, and genetic factors modulate the compatibility between partners. Although gene flow is clearly a fitness trait in allogamous grasses, because it injects hybrid vigor and raw material for evolution, it could reduce compatibility and thus mutualism effectiveness. To explore the importance of host genetic background in modulating the performance of symbiosis, Lolium multiflorum plants, infected and noninfected with Neotyphodium occultans, were crossed with genetically distant plants of isolines (susceptible and resistant to diclofop-methyl herbicide) bred from two cultivars and exposed to stress. The endophyte improved seedling survival in genotypes susceptible to herbicide, while it had a negative effect on one of the genetically resistant crosses. Mutualism provided resistance to herbivory independently of the host genotype, but this effect vanished under stress. While no endophyte effect was observed on host reproductive success, it was increased by interpopulation plant crosses. Neither gene flow nor herbicide had an important impact on endophyte transmission. Host fitness improvements attributable to gene flow do not appear to result in direct conflict with mutualism while this seems to be an important mechanism for the ecological and contemporary evolution of the symbiotum.

Neotyphodium endophytic fungi, the asexual state of Epichloë species, protect cool-season grasses against stresses. The outcomes of Neotyphodium-grass symbioses are agronomically relevant as they may affect the productivity of pastures. It has been suggested that the mutualism is characteristic of agronomic grasses and that differential rates of gene flow between both partners' populations are expected to disrupt the specificity of the association and, thus, the mutualism in wild grasses. We propose that compatibility is necessary but not sufficient to explain the outcomes of Neotyphodium-grass symbiosis, and advance a model that links genetic compatibility, mutualism effectiveness, and endophyte transmission efficiency. For endophytes that reproduce clonally and depend on allogamous hosts for reproduction and dissemination, we propose that this symbiosis works as an integrated entity where gene flow promotes its fitness and evolution. Compatibility between the host plant and the fungal endophyte would be high in genetically close parents; however, mutualism effectiveness and transmission efficiency would be low in fitness depressed host plants. Increasing the genetic distance of mating parents would increase mutualism effectiveness and transmission efficiency. This tendency would be broken when the genetic distance between parents is high (out-breeding depression). Our model allows for testable hypotheses that would contribute to understand the coevolutionary origin and future of the endophyte-grass mutualism.

Abstract: Associations between fungal endophytes and grasses have served as particularly useful systems for exploring the nature and significance of hereditary symbiosis. Here, we propose alternative explanations for recent work by Faeth, in which endophytes were proposed to function as reproductive parasites. Faeth argued that his data demonstrated a symbiosis-induced shift to earlier host reproduction that could generate parasitism through life-history trade-offs with growth/survival. We contend that identifying a symbiosis as mutualistic or parasitic requires studies that incorporate both correlations among demographic pathways and rates of symbiont transmission; such work can advance understanding of the ecology and evolution of symbiosis.

Cool-season grasses establish symbioses with vertically transmitted Neotyphodium endophytes widespread in nature. The frequency of endophyte-infected plants in closed populations (i.e., without migrations) depends on both the differential fitness between infected and non-infected plants, and the endophyte-transmission efficiency. Most studies have been focused on the first mechanism ignoring the second. Infection frequency and endophyte transmission from vegetative tissues to seeds were surveyed in two grasses growing in vegetation units that differ in flood and grazing regimes, and soil salinity. Transmission efficiency and infection frequency for tall fescue did not vary significantly and were 0.98 and 1.00, respectively. For Italian ryegrass, transmission efficiency and infection frequency were 0.88 and 0.57 in humid prairies, and 0.96 and 0.96 in the other vegetation units. Only in humid mesophytic meadows, the observed pattern was irrespective of the presence or absence of grazers. Our results suggest that selection forces for endophyte infection are different for both species. Imperfect transmission was only compensated in tall fescue through an increased fitness of infected plants. Interpreting variations of infection frequency only in terms of differential fitness can be misleading, considering that endophyte transmission can be imperfect and variable in nature. Therefore, this study highlights the importance of measuring transmission efficiency.

Persistence and ubiquity of vertically transmitted Neotyphodium endophytes in grass populations is puzzling because infected plants do not consistently exhibit increased fitness. Using an annual grass population model, we show that the problems for matching endophyte infection and mutualism are likely to arise from difficulties in detecting small mutualistic effects, variability in endophyte transmission efficiency and an apparent prevalence of non-equilibrium in the dynamics of infection. Although endophytes would ultimately persist only if the infection confers some fitness increase to the host plants, such an increase can be very small, as long as the transmission efficiency is sufficiently high. In addition, imperfect transmission limits effectively the equilibrium infection level if the infected plants exhibit small or large reproductive advantage. Under frequent natural conditions, the equilibrium infection level is very sensitive to small changes in transmission efficiency and host reproductive advantage, while convergence to such an equilibrium is slow. As a consequence, seed immigration and environmental fluctuation are likely to keep local infection levels away from equilibrium. Transient dynamics analysis suggests that, when driven by environmental fluctuation, infection frequency increases would often be larger than decreases. By contrast, when due to immigration, overrepresentation of infected individuals tends to vanish faster than equivalent overrepresentation of non-infected individuals.

Herbicide resistance is an evolutionary event resulting from intense herbicide selection over genetically diverse weed populations. In South America, orchard, cereal and legume cropping systems show a strong dependence on glyphosate to control weeds. The goal of this report is to review the current knowledge on cases of evolved glyphosate-resistant weeds in South American agriculture. The first reports of glyphosate resistance include populations of highly diverse taxa (Lolium multiflorum Lam., Conyza bonariensis L., C. canadensis L.). In all instances, resistance evolution followed intense glyphosate use in fruit fields of Chile and Brazil. In fruit orchards from Colombia, Parthenium hysterophorus L. has shown the ability to withstand high glyphosate rates. The recent appearance of glyphosate-resistant Sorghum halepense L. and Euphorbia heterophylla L. in glyphosate-resistant soybean fields of Argentina and Brazil, respectively, is of major concern. The evolution of glyphosate resistance has clearly taken place in those agroecosystems where glyphosate exerts a strong and continuous selection pressure on weeds. The massive adoption of no-till practices together with the utilization of glyphosate-resistant soybean crops are factors encouraging increase in glyphosate use. This phenomenon has been more evident in Argentina and Brazil. The exclusive reliance on glyphosate as the main tool for weed management results in agroecosystems biologically more prone to glyphosate resistance evolution., (Copyright (c) 2007 Society of Chemical Industry.)