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Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition.

ABSTRACT: Tall fescue [Lolium arundinaceum (Schreb.)] is a cool-season perennial grass used in pastures throughout the Southeastern United States. The grass can harbor a shoot-specific fungal endophyte (Epichloë coenophiala) thought to provide the plant with enhanced resistance to biotic and abiotic stresses. Because alkaloids produced by the common variety of the endophyte cause severe animal health issues, focus has been on replacing the common-toxic strain with novel varieties that do not produce the mammal-toxic alkaloids but maintain abiotic and biotic stress tolerance benefits. Little attention has been given to the influence of the plant-fungal symbiosis on rhizosphere processes. Therefore, our objective was to study the influence of this relationship on plant biomass production and root exudate composition in tall fescue cultivars PDF and 97TF1, which were either not infected with the endophyte (E-), infected with the common toxic endophyte (CTE+) strain or with one of two novel endophytes (AR542E+, AR584E+). Plants were grown sterile for 3 weeks after which plant biomass, total organic carbon, total phenolic content and detailed chemical composition of root exudates were determined. Plant biomass production and exudate phenolic and organic carbon content were influenced by endophyte status, tall fescue cultivar, and their interaction. GC-TOF MS identified 132 compounds, including lipids, carbohydrates and carboxylic acids. Cluster analysis showed that the interaction between endophyte and cultivar resulted in unique exudate profiles. This is the first detailed study to assess how endophyte infection, notably with novel endophytes, and tall fescue cultivar interact to influence root exudate composition. Our results illustrate that tall fescue cultivar and endophyte status can influence plant growth and root exudate composition, which may help explain the observed influence of this symbiosis on rhizosphere biogeochemical processes.

SUBMITTER: Guo J

PROVIDER: S-EPMC4391242 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition.

Guo Jingqi J McCulley Rebecca L RL McNear David H DH

Frontiers in plant science 20150409

Tall fescue [Lolium arundinaceum (Schreb.)] is a cool-season perennial grass used in pastures throughout the Southeastern United States. The grass can harbor a shoot-specific fungal endophyte (Epichloë coenophiala) thought to provide the plant with enhanced resistance to biotic and abiotic stresses. Because alkaloids produced by the common variety of the endophyte cause severe animal health issues, focus has been on replacing the common-toxic strain with novel varieties that do not produce the m ...[more]

PMID: 25914697

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Project description:Tall fescue KY-31 is an important primary forage for beef cattle. It carries a fungal endophyte that produces ergovaline, the main cause of tall fescue toxicosis that leads to major revenue loss for livestock producers. The MaxQ, an engineered cultivar, hosts an ergovaline nonproducing strain of the fungus and consequently is nontoxic. However, it is less attractive economically. It is not known how rumen microbiome processes these two forages towards nutrient generation and ergovaline transformation. We have analysed the rumen microbiome compositions of cattle that grazed MaxQ with an intervening KY-31 grazing period using the 16S rRNA-V4 element as an identifier and found that KY-31 remodelled the microbiome substantially, encompassing both cellulolytic and saccharolytic functions. The effect was not evident at the whole microbiome levels but was identified by analysing the sessile and planktonic fractions separately. A move from MaxQ to KY-31 lowered the Firmicutes abundance in the sessile fraction and increased it in planktonic part and caused an opposite effect for Bacteroidetes, although the total abundances of these dominant rumen organisms remained unchanged. The abundances of Fibrobacter , which degrades less degradable fibres, and certain cellulolytic Firmicutes such as Pseudobutyrivibrio and Butyrivibrio 2, dropped in the sessile fraction, and these losses were apparently compensated by increased occurrences of Eubacterium and specific Ruminococcaceae and Lachnospiraceae . A return to MaxQ restored the original Firmicutes and Bacteroidetes distributions. However, several KY-31 induced changes, such as the low abundance of Fibrobacter and Butyrivibrio two remained in place, and their substitutes maintained significant presence. The rumen microbiome was distinct from previously reported faecal microbiomes. In summary, KY-31 and MaxQ were digested in the cattle rumen with distinct consortia and the KY-31-specific features were dominant. The study also identified candidate ergovaline transforming bacteria. It highlighted the importance of analysing sessile and planktonic fractions separately.

Project description:The objective of this study was to quantitatively summarize literature reporting endophyte-infected (Neotyphodium coenophialum) tall fescue (Festuca arundinacea) effects on cattle ADG. This meta-analysis evaluated endophyte infection level, climate, and forage yield using a literature dataset of 138 treatments from 20 articles. Three infection level measurements were tested: endophyte infection as a percentage of infected tillers (E%); ergovaline concentration in ppb ([E]); and total ergot alkaloid concentration ([TEA]). Three types of climate variables were used: base values (temperature, humidity, and relative humidity), climate indices (heat index and temperature-heat index [THI]), and novel climate variables accounting for duration of climate effects. Mixed effect models, weighted by 1/SEM, including a random effect of study were built for each factorial combination of measurement method and climate variable group. Because many studies were missing SEM, two datasets were used: one containing only data with SEM reported and one that also included missing-SEM data. For the complete-SEM dataset (CSD), models were weighted by 1/SEM. In the missing-SEM dataset (MSD) the mean reported 1/SEM was assigned as the weight for all missing SEM treatments. Although 18 initial models were created (2 × 3 × 3 factorial approach), the backward stepwise derivation resulted in models that included only endophyte infection level, suggesting a negative relationship between infection level and ADG. The CSD models predicted ADG to decrease 39 and 33 g/d with each increase of 100 ppb of [TEA] and [E], and by 39 g/d for each increase of 10% E%. In the MSD dataset, predicted ADG decreased by 39 and 33 g/d with each increase of 100 ppb of [TEA] and [E], and by 47 g/d for each increase of 10% E%. All relationships reported had P < 0.05. After visual inspection of the data, piecewise regression was used to identify an infection threshold (IT) of 60 ppb [E] and 11 E%, where the effect of infection level was constant on either side of the IT. The ADG was 40% and 49% greater for infection levels below the IT for [E] and E%, respectively. Across THI values in the analysis, ADG decreases ranged from 11.2% to 45.0% for cattle grazing endophyte-infected tall fescue compared to non-ergot alkaloid endophyte infected tall fescue. Pasture E%, [E], and [TEA] have a negative relationship with ADG in growing cattle, and increasing temperature decreases ADG when infection level is greater than the IT.

Project description:The plant breeding program has developed many cultivars of tall fescue (Festuca arundinacea) with low maintenance and stress tolerance. While the root-associated microbial community helps confer stress tolerance in the host plant, it is still largely unknown how the microbiota varies with plant cultivars under water stress. The study aimed to characterize drought-responsive bacteria and fungi in the roots and rhizosphere of different tall fescue cultivars. Intact grass-soil cores were collected from six cultivars grown in a field trial under no-irrigation for 3 years. Tall fescue under irrigation was also sampled from an adjacent area as the contrast. Bacterial and fungal communities in roots, rhizosphere, and bulk soil were examined for abundance, diversity, and composition using quantitative-PCR and high-throughput amplicon sequencing of 16S rRNA gene and ITS regions, respectively. Differences in microbial community composition and structure between non-irrigated and irrigated samples were statistically significant in all three microhabitats. No-irrigation enriched Actinobacteria in all three microhabitats, but mainly enriched Basidiomycota in the root endosphere and only Glomeromycota in bulk soil. Tall fescue cultivars slightly yet significantly modified endophytic microbial communities. Cultivars showing better adaptability to drought encompassed more relatively abundant Actinobacteria, Basidiomycota, or Glomeromycota in roots and the rhizosphere. PICRUSt2-based predictions revealed that the relative abundance of functional genes in roots related to phytohormones, antioxidant enzymes, and nutrient acquisition was enhanced under no-irrigation. Significant associations between Streptomyces and putative drought-ameliorating genes underscore possible mechanics for microbes to confer tall fescue with water stress tolerance. This work sheds important insight into the potential use of endophytic microbes for screening drought-adaptive genotypes and cultivars.

Project description:Tall fescue (Schedonorus arundinaceus) is a cool-season perennial grass that is widely used as a forage for many livestock species including sheep. An endophyte (Neotyphodium coenophialum) in tall fescue produces ergot alkaloids that enhance plant survival but produce toxicosis in animals. The objective of this study was to investigate the rumen microbiota from gestation and lactation in ewes grazing tall fescue pastures with high (HA) or moderate (MA) levels of endophyte infection, and their relationship with serum parameters. Data were collected at the beginning of the study (d1), the week before initiation of lambing (d51), and at the end of the trial (d115). The rumen microbiota was evaluated using 16S rRNA gene sequencing. Ewes grazing HA had greater serum non-esterified fatty acid (NEFA) (P = 0.024) levels compared with ewes in MA pasture at d115. Both the number of observed OTUs and Shannon diversity index tended (P = 0.08, P = 0.06) to be greater for HA than for MA on d115. At the genus level, Prevotella relative abundance increased with time in both MA and HA (on d1, d51, and d115: 15.17, 25.59, and 24.78% in MA; 14.17, 18.10, and 19.41% in HA). Taxa unclassified at the genus level including (unclassified) Lachnospiraceae, Coriobacteriaceae, and Veillonellaceae exhibited higher abundances in HA at d51 (3.72, 2.07, and 11.22%) compared with MA (2.06, 1.28, and 7.42%). The predictor microbiota for HA and MA were identified by a random forest classification model. The HA predictors included bacteria associated with unclassified Coriobacteriaceae and Ruminococcaceae. Other OTUs classified as Prevotella and Clostridiales could be microbial predictors for MA. The OTUs classified as Prevotella and Lachnospiraceae were negatively correlated with serum concentration of prolactin. Negative correlations with NEFA were observed in the microbiota such as species affiliated to unclassified Clostridiales and Prevotella. OTUs classified as Bacteroidetes and Coriobacteriaceae exhibited a positive correlation with NEFA. Our study confirmed that the rumen microbiota populations were affected by high levels of toxins in endophyte-infected tall fescue and were associated with host hormone and energy metabolism.

Project description:A constitutive, host-specific symbiosis exists between the aboveground fungal endophyte Epichloë coenophiala (Morgan-Jones & W. Gams) and the cool-season grass tall fescue (Lolium arundinaceum (Schreb.) Darbysh.), which is a common forage grass in the United States, Australia, New Zealand, and temperate European grasslands. New cultivars of tall fescue are continually developed to improve pasture productivity and animal health by manipulating both grass and E. coenophiala genetics, yet how these selected grass-endophyte combinations impact other microbial symbionts such as mycorrhizal and dark septate fungi remains unclear. Without better characterizing how genetically distinct grass-endophyte combinations interact with belowground microorganisms, we cannot determine how adoption of new E. coenophiala-symbiotic cultivars in pasture systems will influence long-term soil characteristics and ecosystem function. Here, we examined how E. coenophiala presence and host × endophyte genetic combinations control root colonization by belowground symbiotic fungi and associated plant nutrient concentrations and soil properties in a 2-year manipulative field experiment. We used four vegetative clone pairs of tall fescue that consisted of one endophyte-free (E-) and one E. coenophiala-symbiotic (E+) clone each, where E+ clones within each pair contained one of four endophyte genotypes: CTE14, CTE45, NTE16, or NTE19. After 2 years of growth in field plots, we measured root colonization of arbuscular mycorrhizal fungi (AMF) and dark septate endophytes (DSE), extraradical AMF hyphae in soil, total C, N, and P in root and shoot samples, as well as C and N in associated soils. Although we observed no effects of E. coenophiala presence or symbiotic genotype on total AMF or DSE colonization rates in roots, different grass-endophyte combinations altered AMF arbuscule presence and extraradical hyphal length in soil. The CTE45 genotype hosted the fewest AMF arbuscules regardless of endophyte presence, and E+ clones within NTE19 supported significantly greater soil extraradical hyphae compared to E- clones. Because AMF are often associated with improved soil physical characteristics and C sequestration, our results suggest that development and use of unique grass-endophyte combinations may cause divergent effects on long-term ecosystem properties.

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Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition.

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Tall fescue cultivar and fungal endophyte combinations influence plant growth and root exudate composition.

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