Mutualism effectiveness and vertical transmission of symbiotic fungal endophytes in response to host genetic backround

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Sipha maydis sensitivity to defences of Lolium multiflorum and its endophytic fungus Epichloë occultans

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, endophytesymbiotic 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.Fil: Bastias, Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. Grasslands Research Centre; Nueva ZelandaFil: Martinez-Ghersa, Maria Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Newman, Jonathan A.. Wilfrid Laurier University; CanadáFil: Card, Stuart D.. Grasslands Research Centre; Nueva ZelandaFil: Mace, Wade J.. Grasslands Research Centre; Nueva ZelandaFil: Gundel, Pedro Emilio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentin

Jasmonic acid regulation of the anti-herbivory mechanism conferred by fungal endophytes in grasses

The most studied mechanism of protection against herbivores in grasses associated with Epichloë fungal endophytes has been the fungal production of alkaloids. However, the contribution of the plant immune response on the level of resistance to herbivores in symbiotic grasses has been poorly explored. We studied the relationship between the plant hormone, jasmonic acid (JA) and Epichloë fungal endophytes on herbivore defences in symbiotic grasses. We hypothesized that an exogenous application of methyl jasmonate (MeJA), an activator of the plant JA defence response, would increase the level of resistance of endophyte-symbiotic and non-symbiotic plants to a chewing insect. As Epichloë endophytes produce alkaloids, an enhancement of the JA defence would complement the resistance given by these alkaloids. Lolium multiflorum plants symbiotic and non-symbiotic with the endophyte Epichloë occultans were subjected to an exogenous application of MeJA followed by a challenge with the generalist chewing insect Spodoptera frugiperda. We measured the level of plant resistance to chewing insects, and the defences conferred by host plants and fungal endophytes. Symbiotic plants were more resistant to S. frugiperda than their non-symbiotic counterparts. However, despite the fact that the concentration of JA significantly increased in all plants exposure to MeJA, neither endophyte-symbiotic nor non-symbiotic plants showed an enhanced resistance to insects. Unexpectedly, the exposure of endophyte-symbiotic plants to MeJA led to a reduction in the concentration of loline alkaloids (i.e. N-formyllolines and N-acetylnorlolines), consequently decreasing the level of plant resistance to the herbivore. Synthesis. Our results suggest that, rather than complementing the alkaloid-based defence, the jasmonic acid hormone weakens the anti-herbivore mechanism conferred by Epichloë endophytes. The present study highlights that the interaction between the jasmonic acid hormone and the presence of leaf fungal endophytes can be of importance for the effectiveness of the anti-herbivore defences of symbiotic plants.Fil: Bastias Campos, Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Martinez-Ghersa, Maria Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Newman, Jonathan A.. University of Guelph; CanadáFil: Card, Stuart D.. AgResearch; Nueva ZelandaFil: Mace, Wade J.. AgResearch; Nueva ZelandaFil: Gundel, Pedro Emilio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentin

Maternal exposure to ozone modulates the endophyte-conferred resistance to aphids in lolium multiflorum plants

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.Fil: Bubica Bustos, Ludmila Micaela. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Ueno, Andrea Celeste. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Di Leo, Tara D.. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Crocco, Carlos Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Martinez-Ghersa, Maria Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Molina Montenegro, Marco A.. Universidad de Talca; Chile. Universidad Católica del Norte; Chile. Universidad Católica de Maule; ChileFil: Gundel, Pedro Emilio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. Universidad de Talca; Chil

Getting ready for the ozone battle: Vertically transmitted fungal endophytes have transgenerational positive effects in plants

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.Fil: Ueno, Andrea Celeste. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Gundel, Pedro Emilio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Molina Montenegro, Marco A.. Universidad de Talca; ChileFil: Ramos, Patricio. Universidad de Talca; ChileFil: Ghersa, Claudio Marco. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Martinez-Ghersa, Maria Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentin

Aphid and episodic O3 injury in arugula plants (Eruca sativa Mill) grown in open-top field chambers

Aphid attacks and tropospheric ozone (O3) cause stress and considerable damage in both wild and cultivated plants. Induced defense responses to aphid attacks and O3 exposure share signaling pathways with common points. We investigated the plant-aphid interaction under O3 exposure using open-top O3 chambers. Ozone leaf injury was lower in aphid-infested plants than in aphid-free plants, although herbivore damage was not evident. Aphid population growth was strongly affected by previous exposure to O3 but no direct effect of O3 was observed. The possibility that during O3 episodes, herbivores may reduce O3 damage on host plants and that the offspring of the exposed aphids have lower population growth rates opens new and intriguing questions about potential effects of future increased tropospheric O3 levels on plant-insect interactions. © 2009 Elsevier B.V. All rights reserved.Fil: Menéndez, Analía. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía; ArgentinaFil: Romero, Ana María. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Producción Vegetal; ArgentinaFil: Folcia, A. M.. Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Producción Vegetal; ArgentinaFil: Martinez-Ghersa, Maria Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía; Argentin

Tolerance to ozone might impose restrictions to plant disease management in tomato

Tropospheric ozone (O3) is considered a major air pollutant having negative effects on plant growth and productivity. Background concentrations are expected to rise in several regions of the world in the next 50 years, affecting plant responses to diseases, thus requiring new management strategies for food production. The effects of elevated O3 on the severity of a bacterial disease, and the effectiveness of a chemical defence inducer, were examined in two cultivars of tomato, Roma and Moneymaker, which present different tolerance to this pollutant. The two cultivars differ in their ability to produce and accumulate reactive oxygen species (ROS) in leaf tissues. Tomato plants were challenged with a strain of Xanthomonas vesicatoria, Xv9, which is pathogenic on tomato. Ozone consistently increased severity of the disease by over 40% in both cultivars. In the more tolerant cultivar, O3 pollution increased disease intensity, even after applying a commercially available product to enhance resistance (acibenzolar-S-methyl, BTH). In the more susceptible cultivar, level of disease attained depended on the oxidative balance that resulted from other stress factors. The antioxidant capacity of the plant at the time of infection was relevant for controlling development of the disease. Our results suggest that development of O3 tolerance in commercial crops might impose a penalty cost in terms of disease management under projected higher O3 concentrations.Fil: Romero, Ana M.. Universidad de Buenos Aires. Facultad de Agronomía; ArgentinaFil: Menéndez, A. I.. Universidad de Buenos Aires. Facultad de Agronomía; ArgentinaFil: Folcia, Ana María. Universidad de Buenos Aires. Facultad de Agronomía. Departamento de Producción Vegetal; ArgentinaFil: Martinez-Ghersa, Maria Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentin

Impact of ozone exposure of the maternal environment on the viability and antioxidant content of grass seeds is affected by a vertically transmitted symbiotic fungus

Ozone gas is a rising pollutant in the troposphere and is a consequence of human-driven global change. As a novel environmental stressor, interest in the impact of ozone on symbiotic systems is increasing. Focusing on the symbiosis between grasses and Epichloe species, we evaluated the effect of ozone exposure on the relative fitness of symbiotic and endophyte free plants and its transgenerational effects including seed performance and endophyte persistence. Endophyte symbiotic and endophyte free Lolium multiflorum plants were exposed to high ozone concentration at pre-anthesis. Seed production of symbiotic plants was 23% higher than that of endophyte free plants, being positively correlated with number of spikes and independent of ozone. Seed viability was negatively affected by the endophyte and improved by ozone. A dramatic negative effect of ozone on endophyte viability was manifested only after 25-day seed storage under accelerating ageing conditions. On average, seeds from plants exposed to ozone had higher levels of reduced glutathione (GSH), whilst seeds from symbiotic plants were associated with higher content of glutathione disulfide (GSSG). Consistent with the pattern of seed viability dynamics, the glutathione half-cell reduction potential (EGSSG/2GSH) was higher (i.e. less negative) in E+ seeds and slightly lower (i.e. more negative) in seeds from plants exposed to high ozone. The relationship between endophyte symbiosis and ozone stress with the levels of tocochromanol antioxidants was unclear, and irrespective of seed or endophyte viability. The concentration of some tocochromanols were not affected, whereas others were positively (b-tocopherol) or negatively (a-tocotrienol and g-tocopherol) affected by the endophyte, or positively affected (g-tocopherol) by ozone alone. The fungal symbiont modified the effect of ozone exposure in the maternal environment and thus, grass seed viability and antioxidant content. Although the grass-endophyte symbiosis may promote plant yield under rising ozone levels associated with global change, it may be at the expense of seed viability and endophyte persistence.Fil: Gundel, Pedro Emilio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Sorzoli, N.. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Ueno, Andrea Celeste. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Ghersa, Claudio Marco. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Seal, C. E.. Royal Botanic Gardens. Department of Comparative Plant and Fungal Biology; Reino UnidoFil: Bastias, D. A.. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Martinez-Ghersa, Maria Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentin

Impact of plant and aphid stress history on infestation in arugula plants

Plants can activate inducible defence mechanisms against pests, pathogens, or chemical elicitors, such as ozone, mediated by reactive oxygen species (ROS), particularly hydrogen peroxide (H2O2). An unfavourable balance between ROS production and the plant antioxidant capacity seems to be responsible for the resulting susceptibility of the plant to insect attack. Arugula plants [Eruca sativa Mill. (Brassicaceae)] and green peach aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae), were used in this study to test the hypothesis that the growth of an aphid population depends on both plant and insect stress history. We investigated the impact of density and duration of a previous aphid infestation, and the time lag before re-infestation, on aphid population growth. In a second experiment, we assessed the effect on aphid population growth of previous ozone exposure of arugula plants in open top chambers receiving a continuous O3 fumigation of 100–120 p.p.b., 90 min per day during 3 days. A third experiment was conducted to study the effect of aphid density during a previous infestation on the population growth on an uninfested host. Both previous herbivory and ozone changed the oxidative status of plant tissues and facilitated aphid population growth, which increased with the duration and density of a previous infestation by aphids. Colonization success also depended on the aphids' own history. Aphids coming from high-density populations and/or longer infestation periods produced larger populations on an (initially) uninfested plant. Pest outbreaks in a polluted environment might be expected to be modulated by the hosts' spatial-temporal heterogeneity related to the ozone exposure and previous herbivory.Fil: Menéndez, A. I.. Universidad de Buenos Aires. Facultad de Agronomia. Departamento de Recursos Naturales y Ambiente; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Folcia, A. M.. Universidad de Buenos Aires. Facultad de Agronomia. Departamento de Producción Vegetal. Cátedra de Produccion Vegetal; ArgentinaFil: Vizgarra, L.. Universidad de Buenos Aires. Facultad de Agronomia. Departamento de Producción Vegetal. Cátedra de Produccion Vegetal; ArgentinaFil: Romero, Ana María. Universidad de Buenos Aires. Facultad de Agronomia. Departamento de Producción Vegetal. Cátedra de Produccion Vegetal; ArgentinaFil: Martinez-Ghersa, Maria Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentina. Universidad de Buenos Aires. Facultad de Agronomia. Departamento de Recursos Naturales y Ambiente; Argentin

The plant hormone salicylic acid interacts with the mechanism of anti‐herbivory conferred by fungal endophytes in grasses

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.Fil: Bastias Campos, Daniel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Martinez-Ghersa, Maria Alejandra. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; ArgentinaFil: Newman, Jonathan A.. University of Guelph; CanadáFil: Card, Stuart D.. Grasslands Research Centre; Nueva ZelandaFil: Mace, Wade J.. Grasslands Research Centre; Nueva ZelandaFil: Gundel, Pedro Emilio. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Parque Centenario. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura. Universidad de Buenos Aires. Facultad de Agronomía. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura; Argentin