Leaf endophytes mediate fertilizer effects on plant yield and traits in northern oat grass (Trisetum spicatum)
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Symbiotic fungi commonly increase plant acquisition of soil nutrients. Because prior work has focused on root fungi, we examined how leaf endophytes (Epichloë) influenced plant responses to fertilization and altered plant traits that may cascade to food webs and ecosystem processes.
We manipulated endophyte presence/absence in two populations of Trisetum spicatum, a wild relative of oat, under a 2 × 2 addition of soil nitrogen (N) and phosphorus (P) in the greenhouse.
Endophyte symbiosis altered how plant biomass responded to soil N and how plant traits responded to soil P. Endophytes boosted the biomass gains from N-fertilization in one population. Plants from a second population had weak benefits of symbiosis, but the endophyte altered plant traits, by increasing specific leaf area under P-fertilization, root diameter under low P, and concentration of the fungal alkaloid AcAP under N fertilization. Endophyte presence suppressed the typically observed increase in root hair density in response to soil P limitation. Under low P, symbiotic plants from both populations had improved forage quality relative to symbiont-free plants, although N-fertilization had a larger effect size on forage quality than did symbiosis. Finally, the two populations differed in production of fungal alkaloids, which generally increased in response to fertilization.
Predicting how microbial symbionts mediate plant acquisition of nutrients requires understanding how much their effects vary among plant and endophyte genotypes. Here, the magnitude and direction of leaf symbionts’ effects on plant yield and traits varied between populations and with soil nutrient availability.
KeywordsEpichloë Mutualism Nitrogen Phosphorus Poaceae Mountain ecosystem
Thanks to Terri Tobias and Andrea Porras-Alfaro for providing seeds from Niwot Ridge, CO. Thanks to Josh Lynn for assistance with SLA measurements. Thanks to Bonnie Watson and David Huhman (Analytical Chemistry Core Facility) at the Noble Research Institute for evaluating the chanoclavine and peramine, and Christopher Schardl at University of Kentucky for advice on analysis of foliar aminopyrrolizidines. Comments from two anonymous reviewers and Section Editor Thomas W. Kuyper improved the manuscript. This work was funded by NSF DEB#1354972 and support from the Rocky Mountain Biological Laboratory to J.R. and supported the undergraduate thesis work of H.B.
- Bacon CW, White JF Jr (1994) Stains, media, and procedures for analyzing endophytes. In: Bacon CW, White JF Jr (eds) Biotechnology of endophytic fungi of grasses. CRC Press, Boca RatonGoogle Scholar
- Barkworth ME, Capels KM, Long S, Anderton LK, Piep MB (eds) (2007) Flora of North America volume 24: North of Mexico: Magnoliophyta: Commelinidae (in part): Poaceae, part 1. In: Flora of North America Editorial Committee, eds. 1993+. Flora of North America North of Mexico, New York.Google Scholar
- Bell-Dereske L, Takacs-Vesbach C, Kivlin SN, Emery SM, Rudgers JA (2017) Leaf endophytic fungus interacts with precipitation to alter belowground microbial communities in primary successional dunes. FEMS Microbiology Ecology 93(6). https://doi.org/10.1093/femsec/fix036
- Clarke KR, Gorley RN (2009) Primer version 6.1.10 user manual and tutorial. Primer-E, PlymouthGoogle Scholar
- Craven KD, Blankenship JD, Leuchtmann A, Hignight K, Schardl CL (2001) Hybrid fungal endophytes symbiotic with the grass Lolium pratense. Sydowia 53:44–73Google Scholar
- Garcia-Parisi PA, Lattanzi FA, Grimoldi AA, Druille M, Omacini M (2017) Three symbionts involved in interspecific plant-soil feedback: epichloid endophytes and mycorrhizal fungi affect the performance of rhizobia-legume symbiosis. Plant Soil 412:151–162. https://doi.org/10.1007/s11104-016-3054-3 CrossRefGoogle Scholar
- Lewis GC (2004) Effects of biotic and abiotic stress on the growth of three genotypes of Lolium perenne with and without infection by the fungal endophyte Neotyphodium lolii. Ann Appl Biol 144:53–63. https://doi.org/10.1111/j.1744-7348.2004.tb00316.x CrossRefGoogle Scholar
- Malinowski DP, Brauer DK, Belesky DP (1999) The endophyte Neotyphodium coenophialum affects root morphology of tall fescue grown under phosphorus deficiency. J Agron Crop Sci 183:53–60Google Scholar
- Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, de Vos AC, Buchmann N, Funes G, Quetier F, Hodgson JG, Thompson K, Morgan HD, ter Steege H, van der Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234. https://doi.org/10.1071/bt12225 CrossRefGoogle Scholar
- Rasmussen S, Lane GA, Mace W, Parsons AJ, Fraser K, Xue H (2011) The use of genomics and metabolomics methods to quantify fungal endosymbionts and alkaloids in grasses. In: Hardy N, Hall R (eds) Plant Metabolomics. Methods in Molecular Biology. Methods and Protocols, vol 860. Humana Press.Google Scholar
- Rogers JK, Young CA, Mosali J, Norton SL, Hopkins AA (2014) Stockpiled forage yield and nutritive value of summer-dormant and summer-active tall fescue in a marginal environment. Forage and Grazinglands 12:1–9. https://doi.org/10.2134/FG-2014-0065-RS
- Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd Edition. Academic Press, p 800.Google Scholar
- Vazquez-de-Aldana BR, Garcia-Ciudad A, Garcia-Criado B, Vicente-Tavera S, Zabalgogeazcoa I (2013) Fungal endophyte (Epichloe festucae) alters the nutrient content of Festuca rubra regardless of water availability. PLoS One 8:e84539. https://doi.org/10.1371/journal.pone.0084539 CrossRefGoogle Scholar