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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.)

The symbiotic Epichloë festucae var. lolii endophyte produces alkaloids which can provide its host grass, perennial ryegrass (Lolium perenne L), with a selective advantage in both natural and agricultural managed ecosystems. This study focuses on understanding the alkaloid concentrations that occur in endophyte-infected perennial ryegrass during the early establishment phase. In a glasshouse experiment fungal alkaloid concentrations (peramine, lolitrem B, ergovaline, and epoxy-janthitrems) were measured in perennial ryegrass seedlings infected with E. festucae var. lolii proprietary strains AR1, AR37, NEA2, and NZ common toxic for 69 days after sowing. The endophyte becomes metabolically active, starting alkaloid production, as early as 6 days after sowing. Alkaloid concentrations peaked in 8- to 10- day-old seedlings due to a seedling growth slowdown. This study provides data showing that the loss of insect protection in endophyte-infected seedlings is linked to a reduction in chemical defence after seed-stored, maternally synthesised alkaloids are diluted by seedling dry matter accumulation.

This study investigated effects of seed aging and imbibition on sugar metabolite concentrations in Epichloë endophyte-infected and endophyte-free seed of tall fescue ( Festuca arundinacea Schreb.). Two treatments, namely, accelerated aging and imbibition, were applied to the seeds, with embryo and endosperm tissues analyzed separately. Gas chromatography with flame ionization detection was employed for analysis of sugar metabolites within the seed tissues. Mannitol, ribitol, and trehalose were more abundant in embryo than endosperm tissues and were identified at consistently higher concentrations within endophyte-infected compared to endophyte-free seeds. The ratio of raffinose to sucrose significantly increased with seed aging in both endophyte-free and endophyte-infected embryo tissues, while significantly lower concentrations of trehalose were detected in tissues dissected from aged-seed regardless of endophyte status. This research provides fundamental insight into the metabolic details of endophyte survival in seed and provides a first evaluation of key carbohydrates present in the fungal-plant symbiosis.

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.)

Asexual cool-season grass endophytes of the genus Epichloë (Ascomycota: Clavicipitaceae) are strictly vertically disseminated. The hosts of these mutualistic fungi express no symptoms during the fungal lifecycle that takes place entirely within the plant, while their hosts receive beneficial outcomes. These fungi are distributed in two major locations within the mature seeds of their hosts; namely, within the embryo (including the scutellum, coleoptile, plumule, radicle, and coleorhiza tissues) and between the aleurone and pericarp layers, with the latter hyphae playing no role in transmission of the fungus to the next plant generation. Conflicting evidence remains in the literature on the timing of embryo colonization. In a detailed investigation, utilizing confocal microscopy to observe the distribution of Epichloë coenophiala strain AR601 in tall fescue (Lolium arundinaceum), we tracked endophyte hyphal colonization in the ovary (pre-fertilization) through to the fully mature seed stage. Confocal microscopy images revealed that at the early and mature developmental stages of the embryo sac, before host grass fertilization, there were large quantities of endophyte mycelium present, especially around the antipodal cells, indicating that this endophyte enters the embryo sac before the fertilization stage. After host fertilization, fungal hyphae could be seen in the true embryo and early nonstarchy endosperm. Understanding the mechanisms of transmission to the seed is important for commercial seed producers and end users.

Genotyping by sequencing (GBS) was used to reveal the inherent genetic variation within the haploid fungi Sarocladium zeae isolated from diverse Zea germplasm, including modern Zea mays and its wild progenitors—the teosintes. In accordance with broad host relationship parameters, GBS analysis revealed significant host lineages of S. zeae genetic diversity, indicating that S. zeae genetic variation may associate with different evolutionary histories of host species or varieties. Based on a recently identified PKS-NRPS gene responsible for pyrrocidine biosynthesis in S. zeae fungi, a novel PCR assay was developed to discriminate pyrrocidine-producing S. zeae strains. This molecular method for screening bioactive strains of S. zeae is complementary to other approaches, such as chemical analyses. An eGFP-labelled S. zeae strain was also developed to investigate the endophytic transmission of S. zeae in Z. mays seedlings, which has further improved our understanding of the transmission modes of S. zeae endophytes in maize tissues. [ABSTRACT FROM AUTHOR]

Grasses have developed a wide range of morphological and physiological mechanisms to resist herbivory. For instance, they accumulate silicon (Si) in tissue, as physical defence, and associate symbiotically with foliar Epichloë‐endophytes that provide chemical defence via antiherbivore alkaloids. Recent evidence showed that some Epichloë‐endophytes increase foliar Si in forage grasses; however, whether this impacts insect herbivores is unknown. Furthermore, while Si is primarily a physical defence, it also affects production of plant defensive secondary metabolites; Si supply might therefore affect Epichloë‐alkaloids, although this remains untested.We grew endophyte‐free (Nil) and Epichloë‐infected tall fescue and perennial ryegrass in a factorial combination with or without Si supplementation, in the absence or presence of Helicoverpa armigera. Epichloë‐endophyte strains were AR584 for tall fescue, and AR37, AR1 or Wild‐type (WT) for perennial ryegrass. We assessed how Si supply and Epichloë‐endophytes in interaction with herbivory affected foliar Si and mutualist‐derived alkaloid concentrations. Subsequently, their effects on H. armigera relative growth rates (RGRs) were evaluated.Endophytes generally increased Si concentrations in Si‐supplied plants. In tall fescue AR584 and perennial ryegrass AR37, endophytes increased constitutive (herbivore‐free) and induced (herbivore‐inoculated) Si concentrations by at least 25%; in contrast, in perennial ryegrass, the AR1 endophyte only increased constitutive levels. Si supply did not affect alkaloids produced by AR584 or AR1/WT endophytes; however, in the presence of herbivory, Si supply decreased the induction of alkaloids produced by AR37 endophytes by 33%. For tall fescue, Si supply reduced H. armigera RGR by at least 76%, regardless of endophytic status, whereas, endophyte‐alkaloids played a secondary role only reducing herbivore growth in the absence of Si supply. Conversely, in perennial ryegrass, both Si and endophyte‐alkaloids (regardless of Si supply) reduced herbivore RGR although not synergised.Novel interactions between constitutive and induced Si‐ and alkaloid‐based antiherbivore defences in grasses were observed. Overall, Si had a greater effect on the folivore than endophytes in both grasses. Endophyte defences contributed more to herbivore resistance in perennial ryegrass than tall fescue. We demonstrate that Si and endophytes were not antagonistic and highlight that the protective nature of their interaction varies with the grass‐endophyte species tested. A free Plain Language Summary can be found within the Supporting Information of this article. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Earthworms are not a direct pest of turf grass but they are considered a problem on many sports fields, disrupting playability and aesthetics due to the castings they deposit on the playing surface. Also, a number of slug species are well-known foliage destroying pests of a number of agriculturally important crop species. Perennial ryegrass and tall fescue cultivars associated with selected Epichloë endophytes, originally developed for bird management at airports, were assessed to determine their deterrent properties towards worms and slugs. Plots sown with endophyte-free ryegrass had significantly higher numbers of worms and slugs than plots containing the same grass cultivar infected with the endophyte strain AR95. Also, plots sown with endophyte-free tall fescue had significantly higher numbers of slugs (but not worms) than plots containing the same grass cultivar infected with the endophyte strain AR601. Although more research is required on the exact mechanism of action, these results suggest selected novel endophyte-infected grass associations, such as those including the endophyte AR95, may substantially reduce populations of worms and slugs in areas where these grasses are sown. [ABSTRACT FROM AUTHOR]

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To improve Neotyphodium endophyte-mediated resistance to black cutworm Agrotis ipsilon (Hufnagel) (BCW), a series of experiments was conducted by using several different cultivars of tall fescue, Schedonorus arundinaceus (Schreb.) Dumort. in combination with several different haplotypes of the endophyte Neotyphodium coenophialum (Morgan-Jones & Cams) (plant cultivar X endophyte haplotype = plant line), each producing unique alkaloid profiles. BCW settling response, survival at 5 and 10 d, and larval biomass varied significantly among plant lines. In general, greater variation BCW performance was observed within a single plant cultivar infected with different endophyte haplotypes than among different plant cultivars infected with the same endophyte haplotype, but comparisons among the former were far more numerous. Although five endophytemediated alkaloids representing three alkaloid classes were quantified in the plants, the pyrrolizidine alkaloid N-acetyl norloline was consistently the single best predictor of BCW performance. BCW settling response, 5-d survival, and 10-d survival decreased as levels of the alkaloid N-acetyl norloline increased. The same three response variables also decreased with increasing levels of peramine, but increased with increasing levels of ergovaline. Minor variation in endophyte infection levels occurring among infected plant lines bad no significant influence on BCW performance. Results indicate a potentially important role for N-acetyl norloline and peramine in providing resistance to black cutworm whereas ergovaline appears to be much less important. Therefore, endophyte haplotypes expressing high levels of N-acetyl norloline and peramine may be of particular importance for developing 'friendly' endophyte-enhanced turf and pasture grasses that resist challenging lepidopteran pests, although remaining safe for wildlife and grazing mammals. [ABSTRACT FROM AUTHOR]

The root-feeding scarab insect Costelytra giveni causes severe damage to pasture ecosystems in New Zealand. Loline alkaloids produced by some Epichloë endophytes deter this insect. In two experiments, tall fescue infected with E. coenophiala, strain AR584, and endophyte-free (Nil) controls were subjected to pulse drought stress (DS) or well-watered conditions (WW). The second experiment also included meadow fescue infected with E. uncinata. After 4–6 weeks exposure to the different conditions, roots were excised and fed to C. giveni larvae for 7 days. Relative root consumption (RC), frass production, and relative weight change (RWC) of larvae were measured and the loline content of roots determined. RC and frass output were higher for larvae feeding on Nil DS tall fescue than WW and reduced by AR584. RWC was also greater on DS than on WW Nil plants but reduced by endophyte only in DS plants. RC, frass output, and RWC of larvae were reduced by endophyte in DS and WW meadow fescue, but the effect was greater for WW plants. Loline alkaloid concentration in roots was significantly higher in DS than WW tall fescue in Experiment I but higher in WW than DS meadow fescue in Experiment II. These experiments have demonstrated that moisture status interacts with endophyte to differentially affect root herbivory in tall fescue and meadow fescue. [ABSTRACT FROM AUTHOR]