Abstract
There is an urgent need to create new solutions for sustainable agricultural practices that circumvent the heavy use of fertilizers and pesticides and increase the resilience of agricultural systems to environmental change. Beneficial microbial symbionts of plants are expected to play an important role in integrated pest management schemes over the coming decades. Epichloë endophytes, symbiotic fungi of many grass species, can protect plants against several stressors, and could therefore help to increase the productivity of forage grasses and the hardiness of turf grasses while reducing the use of synthetic pesticides. Indeed, Epichloë endophytes have successfully been developed and commercialized for agricultural use in the USA, Australia and New Zealand. Many of the host grass species originate from Europe, which is a biodiversity hotspot for both grasses and endophytes. However, intentional use of endophyte-enhanced grasses in Europe is virtually non-existent. We suggest that the diversity of European Epichloë endophytes and their host grasses should be exploited for the development of sustainable agricultural, horticultural and landscaping practices, and potentially for bioremediation and bioenergy purposes, and for environmental improvement.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Bindi, M. & Olesen, J. E. The responses of agriculture in Europe to climate change. Reg. Environ. Change 11, 151–158 (2011).
Chandler, D. et al. The development, regulation and use of biopesticides for integrated pest management. Phil. Trans. R. Soc. B. 366, 1987–1998 (2011).
FAOSTAT (Food and Agriculture Organization of the UN, 2009); http://faostat.fao.org/
Ramankutty, N., Evan, A. T., Monfreda, C. & Foley, J. A. Farming the planet: 1. Geographic distribution of global agricultural lands in the year 2000. Glob. Biogeochem. Cycles 22, GB1003 (2008).
Soussana, J.-F. et al. in Revitalising Grasslands to Sustain Our Communities: Proc. 22nd Int. Grasslands Congress (eds Michalk, D. L., Millar, G. D., Badgery, W. B. & Broadfoot, K. M. ) 10–27 (New South Wales Department of Primary Industry, Australia, 2013).
Schreinemachers, P. & Tipraqsa, P. Agricultural pesticides and land use intensification in high, middle and low income countries. Food Policy 37, 616–626 (2012).
Chandler, D. et al. The Consequences of the ‘Cut Off’ Criteria for Pesticides: Alternative Methods of Cultivation (The European Parliament's Committee on Agriculture and Rural Development, 2008).
Ambrus, A. & Yang, Y. Z. Global harmonization of maximum residue limits for pesticides. J. Agric. Food Chem. 64, 30–35(2015).
Faust, M. et al. Comparative assessment of plant protection products: how many cases will regulatory authorities have to answer? Environ. Sci. Eur. 26, 11 (2014).
Handford, C. E., Elliot, C. T. & Campbell, K. A review of the global pesticide legislation and the scale of challenge in research the global harmonization of food safety standards. Integr. Environ. Assess. Manage. 11, 525–536 (2015).
Davison, J. GM plants: science, politics and EC regulations. Plant Sci. 178, 94–98 (2010).
Law Library of Congress. Restrictions of Genetically Modified Organisms (2014); http://www.loc.gov/law/help/restrictions-on-gmos/index.php
Iglesias, A., Mougou, R., Moneo, M., Quiroga, S. Towards adaptation of agriculture to climate change in the Mediterranean. Reg. Environ. Change 11, 159–166 (2011).
Gundel, P. E., Perez, L. I., Helander, M. & Saikkonen, K. Symbiotically modified organisms: nontoxic fungal endophytes in grasses. Trends Plant Sci. 18, 420–427 (2013).
Clay, K. Clavicipitaceous endophytes of grasses: their potential as biocontrol agents. Mycol. Res. 92, 1–12 (1989).
Saikkonen, K., Faeth, S. H., Helander, M. & Sullivan, T. J. Fungal endophytes: a continuum of interactions with host plants. Annu. Rev. Ecol. Syst. 29, 319–343 (1998).
Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis (Academic, 2008).
Saharan, B. S. & Nehra, V. Plant growth promoting rhizobacteria: a critical review. Life Sci. Med. Res. 21, 1–30 (2011).
Jensen, A. M. D. Endophyte persistence and toxin (lolitrem b) production in a Danish seed crop of perennial ryegrass. Europ. J. Agronomy 23, 68–78 (2005).
Welty, R. E., Azavedo, M. D. & Cooper, T. M. Influence of moisture content, temperature, and length of storage on seed germination and survival of endophytic fungi in seeds of tall fescue and perennial ryegrass. Phytopathology 77, 893–900 (1987).
Saikkonen, K. Kentucky 31, far from home. Science 287, 1887 (2000).
Saari, S., Lehtonen P., Helander M. & Saikkonen K. High variation in frequency of infection by endophytes in cultivars of meadow fescue in Finland. Grass Forage Sci. 64, 169–176 (2009).
Johnson, L. J. et al. The exploitation of Epichloë endophytes for agricultural benefit. Fungal Divers. 60, 171–188 (2013).
Young, C. A., Hume, D. E. & McCulley, R. L. Fungal endophytes of tall fescue and perennial ryegrass: pasture friend of foe? J. Anim. Sci. 91, 2379–2394 (2013).
Fletcher, L. R. in Epichloë, endophytes of cool season grasses: implications, utilization and biology (eds Young, C. A., Aiken, G. E., McCulley, R. L., Strickland, J. R. & Schardl, C. L. ) 5–13 (Samuel Roberts Noble Foundation, 2012).
Saikkonen, K., Wäli, P., Helander, M. & Faeth, S. H. Evolution of endophyte-plant symbioses. Trends Plant Sci. 6, 275–280 (2004).
Schardl, C. L. Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genet. Biol. 33, 69–82 (2001).
Tadych, M., Ambrose, K. V., Bergen, M. S., Belanger, F. C. & White, J. F. Jr. Taxonomic placement of Epichloë poae sp. nov. and horizontal dissemination to seedlings via conidia. Fungal Divers. 54, 117–131 (2012).
Clay, K. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69, 10–16 (1988).
Clay, K. & Schardl, C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Nat. 160, 99–127 (2002).
Saikkonen, K. et al. Fungal endophytes help prevent weed invasion. Agr. Ecosyst. Environ. 165, 1–5 (2013).
Bao, G. et al. Does endophyte symbiosis resist allelopathic effects of an invasive plant in degraded grassland? Fungal Ecol. 17, 114–125 (2015).
Cheplick, G. P. & Faeth, S. H. Ecology and Evolution of the Grass-Endophyte Symbiosis (Oxford Univ. Press, 2009).
Leuchtmann, A. Systematics, distribution, and host specificity of grass endophytes. Nat. Toxins 1, 150–162 (1992).
Wäli, P. R., Helander, M., Nissinen, O. & Saikkonen, K. Susceptibility of endophyte-infected grasses to winter pathogens (snow molds). Can. J. Botany 84, 1043–1051 (2006).
Mei C. & Flinn B. S. The use of beneficial microbial endophytes for plant biomass and stress tolerance improvement. Recent Pat. Biotechnol. 4, 81–95 (2010).
Compant, S., van der Heijden, M. G. A., Sessitsch, A. Climate change effects on beneficial plant–microorganism interactions. FEMS Microbiol. Ecol. 73, 197–214 (2010).
Bouton, J. H. et al. Re-infection of tall fescue cultivars with non-ergot alkaloid producing endophytes. Agron. J. 94, 567–574 (2002).
Easton, H. S. & Fleher, L. R. in Proc. 6th International Symposium Fungal Endophytes of Grasses (eds Popay, A. J. & Thom, E. R. ) 11–18 (New Zealand Grassland Association, 2007).
Bouton, J. The economic benefit of forage improvement in the United States. Euphytica 154, 263–270 (2007).
Held, D. W. & Potter, D. A. Prospects for managing turfgrass pests with reduced chemical inputs. Annu. Rev. Entomol. 57, 329–354 (2012).
Pennell C. G. L., Rolston M. P., de Bonth A., Simpson W. R. & Hume D. E. Development of a bird-deterrent fungal endophyte in turf tall fescue. New Zeal. J. Agr. Res. 53, 145–150 (2010).
Finch, S. C., Pennell, C. G. L., Kerby, J. W. F. & Cave, V. M. Mice find endophyte-infected seed of tall fescue unpalatable—implications for the aviation industry. Grass Forage Sci. http://dx.doi.org/10.1111/gfs.12203 (2015).
Pennell, C. G. L. et al. Avanex unique endophyte technology: reduced insect food source at airports. Environ. Entomol. http://dx.doi.org/10.1093/ee/nvv145 (2015).
Latch, G. C. M. in Tall Fescue for the Twenty-first Century (eds Fribourg, H. A., Hannaway, D. B. & West, C. P. ) 121–127 (Agron. Monogr. 53, ASA, CSSA and SSSA, 2009).
Clarke, B. B., White, J. F., Hurley, R. H, Torres, M. S. & Huff, D. R. Endophyte-mediated suppression of dollar spot disease if fine fescues. Plant Dis. 90, 994–998 (2006).
Greulich, F., Horio, E., Shimanuki, T. & Yoshihara, T. Field results confirm natural plant protection by the endophytic fungus Epichloë typhina against the pathogenic fungus Cladosporium phlei on timothy leaves. Ann. Phytopathol. Soc. Jpn 65, 454–459 (1999).
Wiewoira, B., Zurek, G. & Zurek, M. Endophyte-mediated disease resistance in wild populations of perennial ryegrass (Lolium perenne). Fungal Ecol. 15, 1–8 (2015).
Lehtonen, P. T., Helander, M., Siddiqui, S. A., Lehto K. & Saikkonen K. Endophytic fungus decreases plant virus infection in meadow ryegrass (Lolium pratense). Biol. Lett. 2, 620–623 (2006).
Shiba, T. & Sugawara, K. Resistance to the rice leaf bug, Trigonotylus caelestialium, is conferred by Neotyphodium endophyte infection of perennial ryegrass, Lolium perenne. Entomol. Exp. Appl. 115, 387–392 (2005).
Simpson, W. R., Faville, M. J., Moraga, R. A., Williams, W. M., McManus, M. T. & Johnson, R. D. Epichloë fungal endophytes and the formation of synthetic symbioses in Hordeeae (= Triticeae) grasses. J. Syst. Evol. 52, 794–806 (2014).
Rudgers, J. A. & Clay, K. Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biol. Rev. 21, 107–124 (2007).
Soleimani, M. et al. Phytoremediation of an aged petroleum contaminated soil using endophyte infected and non-infected grasses. Chemosphere 81, 1084–90 (2010).
Bonnet, M., Camares, O. & Veisseire, P. Effects of zinc and influence of Acremonium lolii on growth parameters, chlorophyll a fluorescence and antioxidant enzyme activities of ryegrass (Lolium perenne L. cv Apollo). J. Exp. Bot. 51, 945–53 (2000).
Ball, D. M. in Neotyphodium/Grass Interactions (eds Bacon, C. W. & Hill, N. S. ) 395–410 (Plenum, 1997).
Brosi, G. B., Nelson, J. A., McCulley, R. L., Classen, A. T. & Norby, R. Global change factors interact with fungal endophyte symbiosis to determine tall fescue litter chemistry (Poster 45-40, The 94th ESA Annual Meeting, 2009).
Hunt, M. G., Rasmussen, S., Newton, P. C. D., Parsons, A. J. & Newman, J. A. Near-term impacts of elevated CO2, nitrogen and fungal endophyte infection on perennial ryegrass: growth, chemical composition and alkaloid production. Plant Cell Environ. 28, 1345–1354 (2005).
Newman, J. A. et al. Effects of elevated CO2, nitrogen and fungal endophyte-infection on tall fescue: growth, photosynthesis, chemical composition and digestibility. Glob. Change Biol. 9, 425–437 (2003).
Hill, N. S., Pachon, J. G. & Bacon, C. W. Acremonium coenophialum-mediated short- and long-term drought acclimation in tall fescue. Crop Sci. 36, 665–672 (1996).
Iqbal, J., Nelson, J. A. & McCulley, R. L. Fungal endophyte presence and genotype affect plant diversity and soil-to-atmosphere trace gas fluxes. Plant Soil 365, 15–27 (2013).
Iqbal, J., Siegrist, J. A., Nelson, J. A. & McCulley, R. L. Fungal endophyte infection increases carbon sequestration potential of southeastern USA tall fescue stands. Soil Biol. Biochem. 44, 81–92 (2012).
Looper, M. L., Aiken, G. E. & Rosenkrans, C. F. Jr. in Epichloë, Endophytes of Cool Season Grasses: Implications, Utilization and Biology (eds Young, C. A., Aiken, G. E., McCulley, R. L., Strickland, J. R. & Schardl, C. L. ) 1–4 (Samuel Roberts Noble Foundation, 2012).
Saikkonen, K., Young, C. A., Helander, M. & Schardl, C. L. Endophytic Epichloë species and their grass hosts: from evolution to applications. Plant Mol. Biol. http://dx.doi.org/10.1007/s11103-015-0399-6 (2015).
Bouton, J. & Easton, S. in Neotyphodium in Cool-Season (eds Roberts, C. A., West, C. P. & Spiers, D. E. ) 327–340 (Blackwell, 2005).
Saikkonen, K., Wäli, P., Helander, M. Genetic compatibility determines endophyte–grass combinations. PLoS ONE 5, e11395 (2010).
Rolston, M. P., Hare, M. D., Moore, K. K. & Christensen, M. J. Viability of Lolium endophyte fungus in seed stored at different seed moist contents and temperatures. New Zeal. J. Exp. Agr. 14, 297–300 (1986).
Saikkonen, K., Saari, S. & Helander, M. Defensive mutualism between plants and endophytic fungi? Fungal Divers. 41, 101–113 (2010).
Lehtonen, P., Helander, M. & Saikkonen K. Are endophyte-mediated effects on herbivores conditional on soil nutrients? Oecologia 142, 38–45 (2005).
Wäwli, P. R., Helander, M., Nissinen, O., Lehtonen P. & Saikkonen K. Endophyte infection, nutrient status of the soil and duration of snow cover influence the performance of meadow fescue in sub-arctic conditions. Grass Forage Sci. 63, 324–330 (2008).
Müller J. Artificial infection by endophytes affects growth and mycorrhizal colonization of Lolium perenne. Funct. Plant Biol. 30, 419–424 (2003).
Saari, S., Helander, M., Lehtonen, P., Wallius, E. & Saikkonen, K. Fungal endophytes reduce regrowth and affect competitiveness of meadow fescue in early succession of pastures. Grass Forage Sci. 65, 287–295 (2010).
Popay, A. J. & Bonos, S. A. in Neotyphodium in Cool-Season Grasses (eds Robert, C., West, C. & Spiers, D. ) 163–185 (Blackwell, 2005).
Hamilton, C. E. & Faeth, S. H. Asexual Neotyphodium endophytes in Arizona fescue: a test of the seed germination and pathogen resistance hypothesis. Symbiosis 38, 69–85 (2005).
Omacini, M., Chaneton, E. J., Ghersa, C. M. & Müller, C. B. Symbiotic fungal endophytes control insect host-parasite interaction web. Nature. 409, 78–81 (2001).
Vázquez-de-Aldana, B. R., Zabalgogeazcoa I., Garcí-Ciudad, A. & García-Criado, B. An Epichloë endophyte affects the competitive ability of Festuca rubra against other grassland species. Plant Soil 362, 201–213 (2013).
Clement, S. L., Elberson, L. R., Youssef, N. N., Davitt, C. M. & Doss, R. P. Incidence and diversity of Neotyphodium fungal endophytes in tall fescue from Morocco, Tunisia, and Sardinia. Crop Sci. 41, 570–576 (2001).
Bazely, D. R. et al. Broad-scale geographic patterns in the distribution of vertically-transmitted, asexual endophytes in four naturally-occurring grasses. Ecography 30, 367–374 (2007).
Pfannmöller, M., Eggstein, S. & Schöberlein, W. in Neotyphodium/Grass Interactions (eds Bacon, C. W. & Hill, N. S. ) 77–80 (Plenum, 1997).
Puentes, A., Bazely, D. R. & Huss-Danell, K. Endophytic fungi in Festuca pratensis grown in Swedish agricultural grasslands with different managements. Symbiosis 44, 121–126 (2007).
Zabalgogeazcoa, I. & Bony, S. in Neotyphodium in Cool-Season Grasses (eds Roberts, C. A., West, C. P. & Spiers, D. E. ) 23–33 (Blackwell, 2005).
Saha, D. C., Johnson-Cicalese, J. M., Halisky, P. M., van Heemstra, M. I. & Funk, C. R. Occurrence and significance of endophytic fungi in the fine fescues. Plant Disease 71, 1021–1024 (1987).
Dobrindt, L., Stroh, H.-G., Isselstein, J. & Vidal, S. Infected–not infected: factors influencing the abundance of the endophyte Neotyphodium lolii in managed grasslands. Agr. Ecosyst. Environ. 175, 54–59 (2013).
Meyer, W. A., Torres, M. S. & White, J. F. Jr. in Turfgrass: Biology, Use, and Management (eds Stier, J. C., Horgan, B. P. & Bonos, S. A. ) 713–732 (Agron. Monogr. 56, ASA, CSSA, SSSA, 2013).
Takach, J. E. et al. Genotypic and chemotypic diversity of Neotyphodium endophytes in tall fescue from Greece. Appl. Environ. Microb. 78, 5501–5510 (2012).
Bouton, J. H., Gates, R. N., Belesky, D. P. & Owsley, M. Yield and persistence of tall fescue in the southeastern coastal plain after removal of its endophyte. Agron. J. 85, 52–55 (1993).
Latch, G. C. M., Hunt, W. F. & Musgrave, D. R. Endophytic fungi affect growth of perennial ryegrass. New Zeal. J. Agr. Res. 28, 165–168 (1985).
Hume, D. E., Ryan, D. L., Cooper, B. M. & Popay, A. J. Agronomic performance of AR37-infected ryegrass in northern New Zealand. Proc. Conf. New Zealand Grassland Assoc. 69, 201–205 (2007).
West, C. P., Izekor, E., Turner, K. E. & Elmi, A. A. Endophyte effects on growth and persistence of tall fescue along a water-supply gradient. Agron. J. 85, 264–270 (1993).
Kane, K. H. Effects of endophyte infection on drought stress tolerance of Lolium perenne accessions from the Mediterranean region. Environ. Exp. Bot. 71, 337–344 (2011).
Panka, D. & Sadowski, C. in Grassland Science in Europe — Multi-function Grasslands, Quality Forages, Animal Products and Landscapes: Proc. 19th General Meeting of the European Grassland Federation (eds Durand, J. L., Emile, J. C., Huyghe, C. & Lemaire, G. ) 540–541 (AFPF, 2002).
Saikkonen, K., Ahlholm, J., Helander, M., Lehtimäki, S. & Niemeläinen, O. Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23, 360–366 (2000).
Latch, G. C. M., Potter, L. R. & Tyler, B. F. Incidence of endophytes in seeds from collections of Lolium and Festuca species. Ann. Appl. Biol. 111, 59–64 (1987).
Takai., S. H. & Fujii, H. in Proc. 4th Int. Neotyphodium /Grass Interactions Symp.: The Grassland Conf. (eds Paul, V. H. & Dapprich, P. D. ) 347–350 (Universität-Gesamthochschule Paderborn, 2001).
Jöngren, C. Endofytiska svampar i vallgräs — levnadssätt, förekomst och effekter på gräs och gräsätare (Examensarbete/Sveriges lantbruksuniversitet, Institutionen för norrländsk jordbruksvetenskap, 2014).
Panka, D. in Sustainable Grassland Productivity: Proc. 21st General Meeting of the European Grassland Federation (eds Lloveras, D. J., González-Rodríguez. A., Vázquez-Yáñez, O., Piñeiro, J. & Santamaría, O. ) 469–471 (SEEP, Madrid, Spain, 2006).
Phannmöller, M., Eggestein, S. T. & Schöberlein, W. in Neotyphodium/Grass Interactions (eds Bacon, C. W. & Hill, N. S. ) 77–80 (Plenum, 1997).
Saari, S., Helander, M., Faeth, S. H. & Saikkonen, K. The effects of endophytes on seed production and seed predation of tall fescue and meadow fescue. Microb. Ecol. 60, 928–934 (2010).
Wäli, P. R., Helander, M. & Saikkonen, K. in Prospects and Applications for Plant-Associated Microbes: A Laboratory Manual, Part B: Fungi (eds Pirttilä, A. M. & Sorvari, S. ) 197–204 (Biobien Innovations, 2011).
Latch, G. C. M. & Christensen, M. J. Artificial infection of grasses with endophytes. Ann. Appl. Biol. 107, 17–24 (1985).
Acknowledgements
We thank P. Watts (University of Oulu, Finland) for critically reading the article. This study was supported by the Finnish Cultural Foundation, the Nordic Centre of Excellence Tundra and the Academy of Finland (project nos 127140, 137909 and 281354).
Author information
Authors and Affiliations
Contributions
All the authors contributed equally to this work.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Rights and permissions
About this article
Cite this article
Kauppinen, M., Saikkonen, K., Helander, M. et al. Epichloë grass endophytes in sustainable agriculture. Nature Plants 2, 15224 (2016). https://doi.org/10.1038/nplants.2015.224
Published:
DOI: https://doi.org/10.1038/nplants.2015.224
This article is cited by
-
Seed Endophytes and Their Roles in Host Plant Stress Resistance
Journal of Soil Science and Plant Nutrition (2023)
-
Effects of endophytic fungi on the secondary metabolites of Hordeum bogdanii under alkaline stress
AMB Express (2022)
-
Root biomass and cumulative yield increase with mowing height in Festuca pratensis irrespective of Epichloë symbiosis
Scientific Reports (2022)
-
Endophytic fungi as direct plant growth promoters for sustainable agricultural production
Symbiosis (2021)
-
Fungal microbiota in seeds, seedlings and mature plants of raspberry (Rubus ideaus L.)
European Journal of Plant Pathology (2021)