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1.
J Fungi (Basel) ; 10(8)2024 Jul 23.
Artigo em Inglês | MEDLINE | ID: mdl-39194838

RESUMO

Exploitation of the symbiotic relationship between endophytic fungi and ryegrass is a crucial technique for reducing the incidence of insect pests. This is primarily due to the production of alkaloids, such as peramine, by the fungi. This alkaloid has been reported as both a deterrent and toxic to a variety of insects. However, insects have developed various strategies to counteract plant defenses. One of the most studied methods is their ability to sequester toxic compounds from plants. In this study, we examined the feeding preferences and adaptation to peramine in Chilesia rudis, a native Chilean larva. Using a no-choice assay, we assessed larval feeding preferences and mass gain on seven experimental lines and two commercial cultivars of endophyte-infected and non-infected ryegrass. Pupal development time and adult performance were evaluated post-assay. Additionally, we measured peramine content in larval carcasses, feces, and ryegrass leaves. Jumbo was the most preferred cultivar with 32 mm2 of leaf tissues consumed. The longest pupal development time was observed in L161 and ALTO AR1, both at 28 days. Wing length in adults was greatest in the Jumbo and L163 cultivars, measuring 1.25 cm and 1.32 cm, respectively. Peramine concentrations were detected in the bodies of C. rudis. In conclusion, this larva can adapt to endophyte-infected ryegrass and develop counter-adaptation mechanisms to mitigate the effects of peramine.

2.
J Chem Ecol ; 48(11-12): 867-881, 2022 Dec.
Artigo em Inglês | MEDLINE | ID: mdl-36372818

RESUMO

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.


Assuntos
Alcaloides , Afídeos , Epichloe , Animais , Endófitos , Poaceae , Herbivoria , Afídeos/fisiologia , Epigênese Genética , Simbiose , Alcaloides/farmacologia
3.
Plant Cell Environ ; 44(8): 2716-2728, 2021 08.
Artigo em Inglês | MEDLINE | ID: mdl-33721328

RESUMO

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.


Assuntos
Endófitos/fisiologia , Epichloe/fisiologia , Lolium/fisiologia , Ozônio , Biomassa , Lolium/efeitos dos fármacos , Lolium/microbiologia , Ozônio/farmacologia , Plântula/fisiologia , Simbiose
4.
Ann Bot ; 125(6): 981-991, 2020 05 13.
Artigo em Inglês | MEDLINE | ID: mdl-32010946

RESUMO

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.


Assuntos
Epichloe , Poa , Endófitos , Herbivoria , Poaceae , Simbiose
5.
PeerJ ; 7: e8257, 2019.
Artigo em Inglês | MEDLINE | ID: mdl-31976166

RESUMO

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.

6.
Plant Cell Environ ; 41(2): 395-405, 2018 02.
Artigo em Inglês | MEDLINE | ID: mdl-29194664

RESUMO

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.


Assuntos
Endófitos/metabolismo , Herbivoria , Lolium/fisiologia , Reguladores de Crescimento de Plantas/metabolismo , Ácido Salicílico/metabolismo , Alcaloides/metabolismo , Epichloe/metabolismo , Cromatografia Gasosa-Espectrometria de Massas , Lolium/microbiologia , Reguladores de Crescimento de Plantas/fisiologia
7.
Am J Bot ; 104(5): 787-792, 2017 May.
Artigo em Inglês | MEDLINE | ID: mdl-28515076

RESUMO

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.


Assuntos
Epichloe , Poaceae/microbiologia , Simbiose , Endófitos , Genótipo , Fenótipo
8.
Oecologia ; 184(1): 237-245, 2017 05.
Artigo em Inglês | MEDLINE | ID: mdl-28315955

RESUMO

Plants interact with a myriad of microorganisms that modulate their interactions within the community. A well-described example is the symbiosis between grasses and Epichloë fungal endophytes that protects host plants from herbivores. It is suggested that these symbionts could play a protective role for plants against pathogens through the regulation of their growth and development and/or the induction of host defences. However, other endophyte-mediated ecological mechanisms involved in disease avoidance have been scarcely explored. Here we studied the endophyte impact on plant disease caused by the biotrophic fungus, Claviceps purpurea, under field conditions through (1) changes in the survival of the pathogen´s resistance structure (sclerotia) during overwintering on the soil surface, and (2) effects on insects responsible for the transportation of pathogen spores. This latter mechanism is tested through a visitor exclusion treatment and the measurement of plant volatile cues. We found no significant effects of the endophyte on the survival of sclerotia and thus on disease inocula. However, both pathogen incidence and severity were twofold lower in endophyte-symbiotic plants than in non-symbiotic ones, though when insect visits were prevented this difference disappeared. Endophyte-symbiotic and non-symbiotic plots presented different emission patterns of volatiles suggesting that they can play a role in this protection. We show a novel indirect ecological mechanism by which endophytes can defend host grasses against diseases through negatively interacting with intermediary vectors of the epidemic process.


Assuntos
Endófitos , Simbiose , Animais , Epichloe , Herbivoria , Poaceae/microbiologia
9.
Mycologia ; 106(2): 339-52, 2014.
Artigo em Inglês | MEDLINE | ID: mdl-24782501

RESUMO

In this work we performed morphological and molecular phylogenetic analyses (based on sequences of calmodulin M [calM], translation-elongation factor 1-α [tefA] and ß-tubulin [tubB] genes) to characterize the diversity of Epichloë endophytes in Bromus setifolius and Phleum alpinum. The phylogenies obtained from the three genes were congruent and allowed differentiation of three lineages of endophytes that also presented morphological differences. One lineage corresponds to the previously described species Epichloë tembladerae, which is present in a wide range of native grasses from Argentina including B. setifolius and P. alpinum. Another genotype isolated only from B. setifolius is a non-hybrid endophyte, a rare condition for the South American Epichloë endophytes. Isolates of this genotype, described herein as a new variety, Epichloë typhina var. aonikenkana, presented waxy colonies at maturity and a low production of conidia. The third lineage, exclusively found in isolates from P. alpinum, is a hybrid between E. typhina and a common ancestor of E. amarillans and E. baconii. Isolates of this lineage produce abundant conidia that are variable in shape and size. Based on its unique phylogenetic position and morphology, we propose the new species, Epichloë cabralii for this lineage. The new combinations Epichloë tembladerae and E. pampeana also are proposed for the previously described Neotyphodium tembladerae and Neotyphodium pampeanum species.


Assuntos
Epichloe/isolamento & purificação , Neotyphodium/isolamento & purificação , Poaceae/microbiologia , Biodiversidade , DNA Fúngico/genética , DNA Espaçador Ribossômico/genética , Epichloe/classificação , Epichloe/genética , Epichloe/crescimento & desenvolvimento , Dados de Sequência Molecular , Neotyphodium/classificação , Neotyphodium/genética , Neotyphodium/crescimento & desenvolvimento , Filogenia , Poaceae/fisiologia , Esporos Fúngicos/classificação , Esporos Fúngicos/genética , Esporos Fúngicos/crescimento & desenvolvimento , Esporos Fúngicos/isolamento & purificação , Simbiose
10.
Evol Appl ; 3(5-6): 538-46, 2010 Sep.
Artigo em Inglês | MEDLINE | ID: mdl-25567945

RESUMO

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.

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