Tall fescue and E. coenophiala genetics influence root-associated soil fungi in a temperate grassland

Authors: SLAUGHTER, LINDSEY - Texas Tech University; NELSON, JIM - University Of Kentucky; CARLISLE, ELIZABETH - University Of Kentucky; BOURGUIGNON, MARIE - Seminis Vegetable Seeds, Inc; Dinkins, Randy; PHILLIPS, TIMOTHY - University Of Kentucky; MCCULLEY, REBECCA - University Of Kentucky

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/1/2019
Publication Date: 10/15/2019
Citation: Slaughter, L.C., Nelson, J.A., Carlisle, E., Bourguignon, M., Dinkins, R.D., Phillips, T.D., McCulley, R.L. 2019. Tall fescue and E. coenophiala genetics influence root-associated soil fungi in a temperate grassland. Frontiers in Microbiology. 10:2380. https://www.frontiersin.org/articles/10.3389/fmicb.2019.02380/full.
DOI: https://doi.org/10.3389/fmicb.2019.02380/full

Interpretive Summary: With the discovery of endophytic E. coenophiala strains within tall fescue (Lolium arundinaceum) that do not produce toxic ergot alkaloids, it has led to deployment of non-toxic grass-endophyte combinations in pastures, yet little is known about their ecological consequences. We investigated how tall fescue common toxic and non-toxic endophyte associations impacted belowground fungal symbioses and whether these relationships were sensitive to different environmental conditions in a field study. Soil and root samples were collected from four tall fescue clones, one with the endophyte and the same genotype without the endophyte. Two of the plants contained the common toxic endophyte and the other two harbored different non-toxic endophytes. These were evaluated in control plots under ambient conditions and plots that received additional precipitation (plus 30% of the long-term annual mean) after two years under under the above conditions. Root arbuscular mycorrhizal fungi and dark septate endophyte colonization was measured for each of five replications. Root arbuscular mycorrhizal fungi arbuscules, vesicles, and extraradical hyphae length were affected by tall fescue genotype and the presence or absence of the endophyte affected different genotypes differently under the two treatments. Dark septate endophyte colonization was not affected by E. coenophiala presence, tall fescue genotype or treatment. In conclusion, genetically distinct tall fescue-E. coenophiala associations may have distinct long-term impacts on other symbiont interactions and belowground communities under different environmental conditions.

Technical Abstract: A constitutive, host-specific symbiosis exists between the aboveground fungal endophyte Epichloë coenophiala (Morgan-Jones & W. Gams) and the cool-season grass tall fescue (Schedonorus arundinaceus Schreb.), which is a common forage grass in the U.S., 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 beneficial 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 two-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 two years of growth in field plots, we measured root colonization rates of arbuscular mycorrhizal fungi (AMF) and dark septate endophytes (DSE), extraradical AMF hyphae in soil, and total C and N in root, shoot, and soil samples. 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 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.