Skip to main content
SpringerLink
Log in

Neotyphodium fungal endophyte in tall fescue (Schedonorus phoenix): a comparison of three Northern European wild populations and the cultivar Kentucky-31

  • Published:
Fungal Diversity Aims and scope Submit manuscript

Abstract

Pooideae grasses may be colonized by systemic fungal endophytes. The fitness of endophyte depends entirely on resources and seed transmission from the host plant, while colonized plants may gain increased survival, growth, and reproduction relative to their uncolonized conspecifics. Most research of endophyte-grass interactions have been carried out on few cultivars of tall fescue (Schedonorus phoenix) and their symbiont Neotyphodium coenophialum. Lack of studies using wild populations of tall fescue across the species natural distribution range, however, limits the understanding of the ecological and evolutionary role of the symbiosis in nature. We performed a common garden experiment in Southern Finland with three wild, tall fescue populations from northern Europe and the forage cultivar Kentucky-31 (KY-31). For each population, we used naturally endophyte-colonized, naturally endophyte-colonized but endophyte removed (decolonized), and naturally uncolonized plants to separate effects due to the host genotype from the endophyte. We evaluated growth variables and survival in four environmental treatments of varying water and nutrients. Supply of water and nutrients increased plant biomass and reproductive effort in all populations. This effect was higher for KY-31 plants which produced on average 55 % more seeds than wild plants, indicating better adaptation to high resource environments. However, the higher incidence of Claviceps sp. and the low winter survival indicated KY-31 tall fescue is mal-adapted to Northern European conditions. Naturally colonized plants had greater plant biomass (≈12 %), reproductive effort (≈22 %) and seed mass (≈29 %) than naturally uncolonized and decolonized plants. Nonetheless, endophyte colonization did not affect plant survival, and the effects of endophyte colonization on tiller number, panicle/tiller ratio and Claviceps sp. incidence depended on the population origin. In the wild populations, endophyte removal only reduced the number of tillers (≈29 % lower), while the difference between naturally colonized and naturally uncolonized plants was not significant. Our results show that endophyte symbiont increases tall fescue performance in general, but the differences between wild populations and cultivars indicate adaptation to local habitats and agronomic management, respectively. The comparison of naturally endophyte-colonized and decolonized plants suggests certain plant genotype-endophyte combinations found within populations result from local selection pressures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bacon CW, Porter JK, Robbins JD, Luttrell ES (1977) Epichloe typhina from toxic tall fescue grasses. Appl Environ Microbiol 34(5):576–581

    PubMed  CAS  Google Scholar 

  • Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes. R-project.org. R package version 0.999375-39

  • Belesky DP, Devine OJ, Pallas JE Jr, Stringer WC (1987) Photosynthetic activity of tall fescue as influenced by fungal endophyte. Photosynthetica 21:82–87

    Google Scholar 

  • Bouton JH, Gates RN, Hoveland CS (2001) Selection for persistence in Endophyte-free Kentucky 31 tall fescue. Crop Sci 41:1026–1028

    Article  Google Scholar 

  • Brosi GB, McCulley RL, Bush LP, Nelson JA, Classen AT, Norby RJ (2010) Effects of multiple climate change factors on the tall fescue–fungal endophyte symbiosis: infection frequency and tissue chemistry. New Phytol 189(3):797–805

    Article  PubMed  Google Scholar 

  • Cheplick GP (2008) Host genotype overrides fungal endophyte infection in influencing tiller and spike production of Lolium perenne (Poaceae) in a common garden experiment. Am J Bot 95:1063–1071

    Article  PubMed  Google Scholar 

  • Cheplick GP (2011) Endosymbiosis and population differentiation in wild and cultivated Lolium perenne (Poaceae). Am J Bot 98(5):829–838

    Article  PubMed  Google Scholar 

  • Cheplick GP, Faeth SH (2009) Ecology and evolution of the Grass-endophyte symbiosis. Oxford University Press, NY

    Book  Google Scholar 

  • Cheplick GP, Clay K, Wray S (1989) Interactions between fungal endophyte infection and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytol 111:89–97

    Article  Google Scholar 

  • Clay K, Holah J (1999) Fungal endophyte symbiosis and plant diversity in successional fields. Science 285:1742–1744

    Article  PubMed  CAS  Google Scholar 

  • Clay K, Schardl CL (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127

    Article  PubMed  Google Scholar 

  • Clay K, Holah J, Rudgers JA (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc Natl Acad Sci U S A 102:12465–12470

    Article  PubMed  CAS  Google Scholar 

  • Clement SL, Elberson LR, Youssef NN, Davitt CM, Doss RP (2001) Incidence and diversity of Neotyphodium fungal endophytes in tall fescue from Morocco, Tunisia, and Sardinia. Crop Sci 41:570–576

    Article  Google Scholar 

  • Denison RF, Kiers ET, West SA (2003) Darwinian agriculture: when can humans find solutions beyond the reach of natural selection? Q Rev Biol 78:145–168

    Article  PubMed  Google Scholar 

  • Dierking RM, Young CA, Kallenbach RL (2012) Mediterranean and continental tall fescue: I. effects of endophyte status on leaf extension, proline, monoand disaccharides, fructan, and freezing survivability. Crop Sci 52:451–459

    Article  Google Scholar 

  • Easton HS (2007) Grasses and Neotyphodium endophytes: co-adaptation and adaptive breeding. Euphytica 154:295–306

    Article  Google Scholar 

  • Ewald PW (1987) Transmission modes and evolution of the parasitism-mutualism continuum. Ann N Y Acad Sci 503:295–306

    Article  PubMed  CAS  Google Scholar 

  • Faeth SH, Hamilton CE (2006) Does an asexual endophyte symbiont alter life stage and long-term survival in a perennial host grass? Microb Ecol 52:748–755

    Article  PubMed  Google Scholar 

  • Faeth SH, Sullivan TJ (2003) Mutualistic asexual endophytes in a native grass are usually parasitic. Am Nat 161(2):310–325

    Article  PubMed  Google Scholar 

  • Gibson DJ (2009) Grasses and grassland ecology. Oxford University Press, NY

    Google Scholar 

  • Gibson DJ, Newman JA (2001) Festuca arundinacea Schreber (F. elatior subsp. arundinacea (Schreber) Hackel). J Ecol 89:304–324

    Article  Google Scholar 

  • Gundel PE, Batista WB, Texeira M, Martínez-Ghersa MA, Omacini M, Ghersa CM (2008) Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency. Proc Roy Soc Lond B 275:897–905

    Article  Google Scholar 

  • Gundel PE, Garibaldi LA, Tognetti PM, Aragón R, Ghersa CM, Omacini M (2009) Imperfect vertical transmission of the endophyte Neotyphodium in exotic grasses in grasslands of the Flooding Pampa. Microb Ecol 57:740–748

    Article  PubMed  Google Scholar 

  • Gundel PE, Omacini M, Sadras VO, Ghersa CM (2010) The interplay between the effectiveness of the grass-endophyte mutualism and the genetic variability of the host plant in an agronomic context. Evol Appl 3(5–6):538–546

    Article  Google Scholar 

  • Gundel PE, Rudgers JA, Ghersa CM (2011) Incorporating the process of vertical transmission into understanding of host-symbiont dynamics. Oikos 120(8):1121–1128

    Article  Google Scholar 

  • Hamilton CE, Bauerle TL (2012) A new currency for mutualism? Fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Divers. doi:10.1007/s13225-012-0156-y

  • Hamilton CE, Dowling TE, Faeth SH (2010) Hybridization in endophyte symbionts alters host response to moisture and nutrient treatments. Microb Ecol 59:768–775

    Article  PubMed  Google Scholar 

  • Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers. doi:10.1007/s13225-012-0158-9

  • Hand ML, Cogan NO, Stewart AV, Forster JW (2010) Evolutionary history of tall fescue morphotypes inferred from molecular phylogenetics of the Lolium-Festuca species complex. BMC Evol Biol 10:303

    Article  PubMed  Google Scholar 

  • Heide OM (1994) Control of flowering and reproduction in temperate grasses. New Phytol 128(2):347–362

    Article  CAS  Google Scholar 

  • Hesse U, Schöberlein W, Wittenmayer L, Förster K, Warnstorff K, Diepenbrock W, Merbach W (2003) Effects of Neotyphodium endophytes on growth, reproduction and drought-stress tolerance of three Lolium perenne L. genotypes. Grass Forage Sci 58:407–415

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P, Heiberger RM (2008) Multcomp: Simultaneous Inference for General Linear Hypotheses. R-project.org. R package version 0.993-1

  • Inda LA, Segarra-Moragues JG, Müller J, Peterson PM, Catalán P (2008) Dated historical biogeography of the temperate Loliinae (Poaceae, Pooideae) grasses in the northern and southern hemispheres. Mol Phylogenet Evol 46:932–957

    Article  PubMed  CAS  Google Scholar 

  • Malinowski DP, Belesky DP (2006) Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassl Sci 52:1–14

    Article  Google Scholar 

  • Marks S, Clay K (1996) Physiological responses of Festuca arundinacea to fungal endophyte infection. New Phytol 133(4):727–733

    Article  Google Scholar 

  • Mattingly WB, Swedo BL, Reynolds HL (2010) Interactive effects of resource enrichment and resident diversity on invasion of native grassland by Lolium arundinaceum. Plant Ecol 207:203–212

    Article  Google Scholar 

  • Morse LJ, Faeth SH, Day TA (2007) Neotyphodium interactions with a wild grass are driven mainly by endophyte haplotype. Funct Ecol 21:813–822

    Article  Google Scholar 

  • Pecetti L, Romani M, Carroni AM, Annicchiarico P, Piano E (2007) The effect of endophyte infection on persistence of tall fescue (Festuca arundinacea Schreb.) populations in two climatically contrasting Italian locations. Aust J Agric Res 58:893–899

    Article  Google Scholar 

  • Piano E, Bertoli FB, Romani M, Tava A, Riccioni L, Valvassori M, Carroni AM, Pecetti L (2005) Specificity of host-endophyte association in tall fescue populations from Sardinia, Italy. Crop Sci 45:1456–1463

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2009) Mixed-effects models in S and S-PLUS. Springer, NY

    Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rudgers JA, Clay K (2007) Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biol Rev 21:107–124

    Article  Google Scholar 

  • Saari S, Helander M, Faeth SH, Saikkonen K (2010) The effects of endophytes on seed production and seed predation of tall fescue and meadow fescue. Microb Ecol 60:928–934

    Article  PubMed  Google Scholar 

  • Saha DC, Jackson MA, Johonson-Cicalese JM (1988) A rapid staining method for detection of endophytic fungi in turf and forage grasses. Phytopathology 78:237–239

    Article  CAS  Google Scholar 

  • Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Evol Syst 29:319–343

    Article  Google Scholar 

  • Saikkonen K, Wäli P, Helander M, Faeth SH (2004) Evolution of endophyte-plant symbioses. Trends Plant Sci 9:275–280

    Article  PubMed  CAS  Google Scholar 

  • Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH (2006) Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci 11:428–433

    Article  PubMed  CAS  Google Scholar 

  • Saikkonen K, Wäli PR, Helander M (2010a) Genetic compatibility determines endophyte-grass combinations. PLoS One 5(6):e11395. doi:10.1371/journal.pone.0011395

    Article  PubMed  Google Scholar 

  • Saikkonen K, Saari S, Helander M (2010b) Defensive mutualism between plants and endophytic fungi? Fungal Divers 41:101–113

    Article  Google Scholar 

  • Saikkonen K, Taulavuori K, Hyvönen T, Gundel PE, Hamilton CE, Vänninen I, Nissinen A, Helander M (2012) Climate change-driven species’ range shifts filtered by photoperiodism. Nat Clim Chang 2:239–242

    Article  Google Scholar 

  • Schardl CL (2010) The Epichloae, symbionts of the grass subfamily Poöideae. Ann MO Bot Gard 97(4):646–665

    Article  Google Scholar 

  • Spyreas G, Gibson DJ, Middleton BA (2001) Effects of endophyte infection in tall fescue (Festuca arundinacea: Poaceae) on community diversity. Int J Plant Sci 162:1237–1245

    Article  Google Scholar 

  • Sullivan TJ, Faeth SH (2008) Local adaptation in Festuca arizonica infected by hybrid and nonhybrid Neotyphodium endophytes. Microb Ecol 55:697–704

    Article  PubMed  CAS  Google Scholar 

  • Tadych M, Ambrose KV, Bergen MS, Belanger FC, White JF Jr (2012) Taxonomic placement of Epichloë poae sp. nov. and horizontal dissemination to seedlings via conidia. Fungal Divers. doi:10.1007/s13225-012-0170-0

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  • Tutin TG et al (1980) Flora Europea. Cambridge University Press, New York, pp 132–133

    Google Scholar 

  • Vesterlund S-R, Helander M, Faeth SH, Hyvönen T, Saikkonen K (2011) Environmental conditions and host plant origin override endophyte effects on invertebrate communities. Fungal Divers 47:109–118

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, NY

    Book  Google Scholar 

Download references

Acknowledgements

This study was financially supported by Finnish Academy grants 213401 and 209210, and Turku University Foundation. We thank Sini Isola, Anna Suuronen, Elina Vainio, Minna Jokela, the staff at Turku University Botanical Garden and numerous other people who have helped at different stages of the research. Finally, we thanks to a reviewer for his fruitful comments on the manuscript.

Author information

Authors and Affiliations

  1. MTT Agrifood Research Finland, Plant Production Research, 31600, Jokioinen, Finland

    Pedro E. Gundel, Cyd E. Hamilton & Kari Saikkonen

  2. IFEVA - CONICET – Faculty of Agronomy, Buenos Aires University (UBA), Buenos Aires, Argentina

    Pedro E. Gundel

  3. Department of Biology, Section of Ecology, University of Turku, 20014, Turku, Finland

    Marjo Helander

  4. Soil Science Division, Faculty of Agronomy, Buenos Aires University (UBA), Buenos Aires, Argentina

    Cecilia Casas

  5. Department of Biology, University of North Carolina, Greensboro, NC, 27402-6170, USA

    Stanley H. Faeth

Authors
  1. Pedro E. Gundel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marjo Helander
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecilia Casas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cyd E. Hamilton
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stanley H. Faeth
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kari Saikkonen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pedro E. Gundel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 26 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gundel, P.E., Helander, M., Casas, C. et al. Neotyphodium fungal endophyte in tall fescue (Schedonorus phoenix): a comparison of three Northern European wild populations and the cultivar Kentucky-31. Fungal Diversity 60, 15–24 (2013). https://doi.org/10.1007/s13225-012-0173-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13225-012-0173-x

Keywords

Search

Navigation