journal article Open Access Sep 28, 2022

A First Draft of the Core Fungal Microbiome of Schedonorus arundinaceus with and without Its Fungal Mutualist Epichloë coenophiala

Journal of Fungi Vol. 8 No. 10 pp. 1026 · MDPI AG
View at Publisher Save 10.3390/jof8101026
Abstract
Tall fescue (Schedonorus arundinaceus) is a cool-season grass which is commonly infected with the fungal endophyte Epichloë coenophiala. Although the relationship between tall fescue and E. coenophiala is well-studied, less is known about its broader fungal communities. We used next-generation sequencing of the ITS2 region to describe the complete foliar fungal microbiomes in a set of field-grown tall fescue plants over two years, and whether these fungal communities were affected by the presence of Epichloë. We used the Georgia 5 cultivar of tall fescue, grown in the field for six years prior to sampling. Plants were either uninfected with E. coenophiala, or they were infected with one of two E. coenophiala strains: The common toxic strain or the AR542 strain (sold commerically as MaxQ). We observed 3487 amplicon sequence variants (ASVs) across all plants and identified 43 ASVs which may make up a potential core microbiome. Fungal communities did not differ strongly between Epichloë treatments, but did show a great deal of variation between the two years. Plant fitness also changed over time but was not influenced by E. coenophiala infection.
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References
68
[1]
Gibson "Festuca arundinacea Schreber (F. elatior L. ssp. arundinacea (Schreber) Hackel)" J. Ecol. (2001) 10.1046/j.1365-2745.2001.00561.x
[2]
Leuchtmann "Nomenclatural realignment of Neotyphodium species with genus Epichloë" Mycologia (2014) 10.3852/13-251
[3]
Newman "Costs, benefits, parasites and mutualists: The use and abuse of the mutualism-parasitism continuum concept for Epichloë fungi" Philos. Theory, Pract. Biol. (2022)
[4]
Rasmussen "Metabolomics analysis of the Lolium perenne–Neotyphodium lolii symbiosis: More than just alkaloids?" Phytochem. Rev. (2009) 10.1007/s11101-009-9136-6
[5]
Gundel "Epichloë fungal endophytes and plant defenses: Not just alkaloids" Trends Plant Sci. (2017) 10.1016/j.tplants.2017.08.005
[6]
Fernando, K., Reddy, P., Spangenberg, G.C., Rochfort, S.J., and Guthridge, K.M. (2022). Metabolic potential of Epichloë endophytes for host grass fungal disease resistance. Microorganisms, 10. 10.3390/microorganisms10010064
[7]
Schardl "The Epichloae, symbionts of the grass subfamily Poöidae" Ann. Mo. Bot. Gard. (2010) 10.3417/2009144
[8]
Nagabhyru, P., Dinkins, R.D., Wood, C.L., Bacon, C.W., and Schardl, C.L. (2013). Tall fescue endophyte effects on tolerance to water-deficit stress. BMC Plant Biol., 13. 10.1186/1471-2229-13-127
[9]
West "Susceptibility of tall fescue to Rhizoctonia zeae infection as affected by endophyte symbiosis" Ann. Appl. Biol. (2013) 10.1111/aab.12051
[10]
Hunt "Reduced herbivore resistance from a novel grass–endophyte association" J. Appl. Ecol. (2005) 10.1111/j.1365-2664.2005.01061.x
[11]
Bourguignon "Ecophysiological responses of tall fescue genotypes to fungal endophyte infection, elevated temperature, and precipitation" Crop Sci. (2015) 10.2135/cropsci2015.01.0020
[12]
Gwinn "Relationship between endophyte infestation level of tall fescue seed lots and Rhizoctonia zeae seedling disease" Plant Disease (1992) 10.1094/pd-76-0911
[13]
Card, S.D., Bastías, D.A., and Caradus, J.R. (2021). Antagonism to plant pathogens by Epichloë fungal endophytes—A review. Plants, 10. 10.3390/plants10101997
[14]
Kauppinen "Epichloë endophyte effects on leaf blotch pathogen (Rhynchosporium sp.) of tall fescue (Schedonorus phoenix) vary among grass origin and environmental conditions" Plant Ecol. Divers. (2018) 10.1080/17550874.2019.1613451
[15]
Chen "The advantages of endophyte-infected over uninfected tall fescue in the growth and pathogen resistance are counteracted by elevated CO2" Sci. Rep. (2017) 10.1038/s41598-017-07183-y
[16]
Welty "Response of field-grown tall fescue infected by Acremonium coenophialum to Puccinia graminis subsp" graminicola. Plant Dis. (1993) 10.1094/pd-77-0574
[17]
Rojas "Infection with a shoot-specific fungal endophyte (Epichloë) alters tall fescue soil microbial communities" Microb. Ecol. (2016) 10.1007/s00248-016-0750-8
[18]
Mahmud, K., Lee, K., Hill, N.S., Mergoum, A., and Missaoui, A. (2021). Influence of tall fescue Epichloë endophytes on rhizosphere soil microbiome. Microorganisms, 9. 10.21203/rs.3.rs-614409/v1
[19]
Panke-Buisse, K., Cheng, L., Gan, H., Wickings, K., Petrovic, M., and Kao-Kniffin, J. (2020). Root fungal endophytes and microbial extracellular enzyme activities show patterned responses in tall fescues under drought conditions. Agronomy, 10. 10.3390/agronomy10081076
[20]
Mack "Balancing multiple mutualists: Asymmetric interactions among plants, arbuscular mycorrhizal fungi, and fungal endophytes" Oikos (2008) 10.1111/j.2007.0030-1299.15973.x
[21]
Omacini "Grass–endophyte symbiosis: A neglected aboveground interaction with multiple belowground consequences" Appl. Soil Ecol. (2012) 10.1016/j.apsoil.2011.10.012
[22]
Slaughter "Asexual Epichloë endophytes do not consistently alter arbuscular mycorrhizal fungi colonization in three grasses" Am. Midl. Nat. (2018) 10.1674/0003-0031-179.2.157
[23]
Slaughter "Climate change and Epichloë coenophiala association modify belowground fungal symbioses of tall fescue host" Fungal Ecol. (2018) 10.1016/j.funeco.2017.10.002
[24]
Slaughter, L.C., and McCulley, R.L. (2016). Aboveground Epichloë coenophiala-grass associations do not affect belowground fungal symbionts or associated plant, soil parameters. Microb. Ecol., 682–691. 10.1007/s00248-016-0828-3
[25]
Slaughter "Tall fescue and Epichloë coenophiala genetics influence root-associated soil fungi in a temperate grassland" Front. Microbiol. (2019) 10.3389/fmicb.2019.02380
[26]
Nissinen "Heritable Epichloë symbiosis shapes fungal but not bacterial communities of plant leaves" Sci. Rep. (2019) 10.1038/s41598-019-41603-5
[27]
Guerreiro "Knowing your neighbourhood—The effects of Epichloë endophytes on foliar fungal assemblages in perennial ryegrass in dependence of season and land-use intensity" PeerJ (2018) 10.7717/peerj.4660
[28]
Liu "The effect of Epichloë endophyte on phyllosphere microbes and leaf metabolites in Achnatherum inebrians" iScience (2022) 10.1016/j.isci.2022.104144
[29]
Zahn "Foliar fungi alter reproductive timing and allocation in Arabidopsis under normal and water-stressed conditions" Fungal Ecol. (2019) 10.1016/j.funeco.2019.04.002
[30]
Busby "Common foliar fungi of Populus trichocarpa modify Melampsora rust disease severity" New Phytol. (2016) 10.1111/nph.13742
[31]
Christian "Foliar endophytic fungi alter patterns of nitrogen uptake and distribution in Theobroma cacao" New Phytol. (2019) 10.1111/nph.15693
[32]
Bouton "Registration of ‘Georgia 5’ tall fescue" Crop Sci. (1993) 10.2135/cropsci1993.0011183x003300060059x
[33]
ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases

Eva Bellemain, Tor Carlsen, CHRISTIAN BROCHMANN et al.

BMC Microbiology 10.1186/1471-2180-10-189
[34]
New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities

Katarina Ihrmark, Inga T.M. Bödeker, Karelyn Cruz-Martinez et al.

FEMS Microbiology Ecology 2012 10.1111/j.1574-6941.2012.01437.x
[35]
Ryan "Metabolite analysis of the effects of elevated CO2 and nitrogen fertilization on the association between tall fescue (Schedonorus arundinaceus) and its fungal symbiont Neotyphodium coenophialum" Plant Cell Environ. (2014) 10.1111/pce.12146
[36]
DADA2: High-resolution sample inference from Illumina amplicon data

Benjamin J Callahan, Paul J McMurdie, Michael J Rosen et al.

Nature Methods 2016 10.1038/nmeth.3869
[37]
Cutadapt removes adapter sequences from high-throughput sequencing reads

Marcel Martin

EMBnet.journal 2011 10.14806/ej.17.1.200
[38]
Exact sequence variants should replace operational taxonomic units in marker-gene data analysis

Benjamin J Callahan, Paul J McMurdie, Susan P Holmes

The ISME Journal 2017 10.1038/ismej.2017.119
[39]
The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications

Rolf Henrik Nilsson, Karl-Henrik Larsson, Andy F S Taylor et al.

Nucleic Acids Research 2019 10.1093/nar/gky1022
[40]
R Core Team (2020). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing.
[41]
Oksanen, J., Blanchet, F.G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O’Hara, R.B., Simpson, G.L., and Solymos, P. (2020). Vegan: Community Ecology Package, R Foundation for Statistical Computing. R Package Version 2.5-7.
[42]
Martinez Arbizu, P. (2022, August 29). pairwiseAdonis: Pairwise Multilevel Comparison Using Adonis. R Package Version 0.4. Available online: https://github.com/pmartinezarbizu/pairwiseAdonis.
[43]
McMurdie, P.J., and Holmes, S. (2014). Waste not, want not: Why rarefying microbiome data is inadmissible. PLoS Comput. Biol., 10. 10.1371/journal.pcbi.1003531
[44]
Willis "Rarefaction, alpha diversity, and statistics" Front. Microbiol. (2019) 10.3389/fmicb.2019.02407
[45]
Normalization and microbial differential abundance strategies depend upon data characteristics

Sophie Weiss, Zhenjiang Zech Xu, Shyamal Peddada et al.

Microbiome 2017 10.1186/s40168-017-0237-y
[46]
McKnight "Methods for normalizing microbiome data: An ecological perspective" Methods Ecol. Evol. (2019) 10.1111/2041-210x.13115
[47]
Analysis of compositions of microbiomes with bias correction

Huang Lin, Shyamal Das Peddada

Nature Communications 2020 10.1038/s41467-020-17041-7
[48]
Wasserstein "Moving to a world beyond “p < 0.05”" Am. Stat. (2019) 10.1080/00031305.2019.1583913
[49]
[50]
Abarenkov "FungalTraits: A user-friendly traits database of fungi and fungus-like stramenopiles" Fungal Divers. (2020) 10.1007/s13225-020-00466-2

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Published
Sep 28, 2022
Vol/Issue
8(10)
Pages
1026
License
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Funding
Canada Foundation for Innovation
Canadian Natural Sciences and Engineering Research Council
Cite This Article
Jenna C. M. Dale, Jonathan A. Newman (2022). A First Draft of the Core Fungal Microbiome of Schedonorus arundinaceus with and without Its Fungal Mutualist Epichloë coenophiala. Journal of Fungi, 8(10), 1026. https://doi.org/10.3390/jof8101026
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