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Epichloë grass endophytes in sustainable agriculture

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.

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Figure 1: Vertical transmission of Epichloë endophytes in grasses and manipulation of endophyte infection.

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References

  1. Bindi, M. & Olesen, J. E. The responses of agriculture in Europe to climate change. Reg. Environ. Change 11, 151–158 (2011).

    Article  Google Scholar 

  2. Chandler, D. et al. The development, regulation and use of biopesticides for integrated pest management. Phil. Trans. R. Soc. B. 366, 1987–1998 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  3. FAOSTAT (Food and Agriculture Organization of the UN, 2009); http://faostat.fao.org/

  4. 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).

    Article  CAS  Google Scholar 

  5. 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).

    Google Scholar 

  6. Schreinemachers, P. & Tipraqsa, P. Agricultural pesticides and land use intensification in high, middle and low income countries. Food Policy 37, 616–626 (2012).

    Article  Google Scholar 

  7. 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).

  8. Ambrus, A. & Yang, Y. Z. Global harmonization of maximum residue limits for pesticides. J. Agric. Food Chem. 64, 30–35(2015).

    Article  PubMed  CAS  Google Scholar 

  9. 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).

  10. 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).

    Article  Google Scholar 

  11. Davison, J. GM plants: science, politics and EC regulations. Plant Sci. 178, 94–98 (2010).

    Article  CAS  Google Scholar 

  12. Law Library of Congress. Restrictions of Genetically Modified Organisms (2014); http://www.loc.gov/law/help/restrictions-on-gmos/index.php

  13. 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).

    Article  Google Scholar 

  14. 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).

    Article  CAS  PubMed  Google Scholar 

  15. Clay, K. Clavicipitaceous endophytes of grasses: their potential as biocontrol agents. Mycol. Res. 92, 1–12 (1989).

    Article  Google Scholar 

  16. 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).

    Article  Google Scholar 

  17. Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis (Academic, 2008).

    Google Scholar 

  18. Saharan, B. S. & Nehra, V. Plant growth promoting rhizobacteria: a critical review. Life Sci. Med. Res. 21, 1–30 (2011).

    Google Scholar 

  19. 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).

    Article  CAS  Google Scholar 

  20. 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).

    Article  Google Scholar 

  21. Saikkonen, K. Kentucky 31, far from home. Science 287, 1887 (2000).

    Article  CAS  PubMed  Google Scholar 

  22. 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).

    Article  Google Scholar 

  23. Johnson, L. J. et al. The exploitation of Epichloë endophytes for agricultural benefit. Fungal Divers. 60, 171–188 (2013).

    Article  Google Scholar 

  24. 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).

    Article  CAS  PubMed  Google Scholar 

  25. 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).

    Google Scholar 

  26. Saikkonen, K., Wäli, P., Helander, M. & Faeth, S. H. Evolution of endophyte-plant symbioses. Trends Plant Sci. 6, 275–280 (2004).

    Article  CAS  Google Scholar 

  27. Schardl, C. L. Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genet. Biol. 33, 69–82 (2001).

    Article  CAS  PubMed  Google Scholar 

  28. 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).

    Article  Google Scholar 

  29. Clay, K. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69, 10–16 (1988).

    Article  Google Scholar 

  30. Clay, K. & Schardl, C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Nat. 160, 99–127 (2002).

    Article  Google Scholar 

  31. Saikkonen, K. et al. Fungal endophytes help prevent weed invasion. Agr. Ecosyst. Environ. 165, 1–5 (2013).

    Article  Google Scholar 

  32. Bao, G. et al. Does endophyte symbiosis resist allelopathic effects of an invasive plant in degraded grassland? Fungal Ecol. 17, 114–125 (2015).

    Article  Google Scholar 

  33. Cheplick, G. P. & Faeth, S. H. Ecology and Evolution of the Grass-Endophyte Symbiosis (Oxford Univ. Press, 2009).

    Book  Google Scholar 

  34. Leuchtmann, A. Systematics, distribution, and host specificity of grass endophytes. Nat. Toxins 1, 150–162 (1992).

    Article  CAS  PubMed  Google Scholar 

  35. 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).

    Article  Google Scholar 

  36. 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).

    Article  CAS  PubMed  Google Scholar 

  37. 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).

    CAS  PubMed  Google Scholar 

  38. Bouton, J. H. et al. Re-infection of tall fescue cultivars with non-ergot alkaloid producing endophytes. Agron. J. 94, 567–574 (2002).

    Article  Google Scholar 

  39. 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).

    Google Scholar 

  40. Bouton, J. The economic benefit of forage improvement in the United States. Euphytica 154, 263–270 (2007).

    Article  Google Scholar 

  41. Held, D. W. & Potter, D. A. Prospects for managing turfgrass pests with reduced chemical inputs. Annu. Rev. Entomol. 57, 329–354 (2012).

    Article  CAS  PubMed  Google Scholar 

  42. 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).

    Article  CAS  Google Scholar 

  43. 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).

  44. 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).

  45. 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).

    Google Scholar 

  46. 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).

    Article  PubMed  Google Scholar 

  47. 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).

    Article  Google Scholar 

  48. Wiewoira, B., Zurek, G. & Zurek, M. Endophyte-mediated disease resistance in wild populations of perennial ryegrass (Lolium perenne). Fungal Ecol. 15, 1–8 (2015).

    Article  Google Scholar 

  49. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  50. 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).

    Article  Google Scholar 

  51. 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).

    Article  Google Scholar 

  52. 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).

    Article  Google Scholar 

  53. Soleimani, M. et al. Phytoremediation of an aged petroleum contaminated soil using endophyte infected and non-infected grasses. Chemosphere 81, 1084–90 (2010).

    Article  CAS  PubMed  Google Scholar 

  54. 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).

    CAS  PubMed  Google Scholar 

  55. Ball, D. M. in Neotyphodium/Grass Interactions (eds Bacon, C. W. & Hill, N. S. ) 395–410 (Plenum, 1997).

    Book  Google Scholar 

  56. 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).

  57. 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).

    Article  CAS  Google Scholar 

  58. 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).

    Article  Google Scholar 

  59. 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).

    Article  Google Scholar 

  60. 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).

    Article  CAS  Google Scholar 

  61. 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).

    Article  CAS  Google Scholar 

  62. 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).

    Google Scholar 

  63. 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).

  64. Bouton, J. & Easton, S. in Neotyphodium in Cool-Season (eds Roberts, C. A., West, C. P. & Spiers, D. E. ) 327–340 (Blackwell, 2005).

    Google Scholar 

  65. Saikkonen, K., Wäli, P., Helander, M. Genetic compatibility determines endophyte–grass combinations. PLoS ONE 5, e11395 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. 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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  68. Lehtonen, P., Helander, M. & Saikkonen K. Are endophyte-mediated effects on herbivores conditional on soil nutrients? Oecologia 142, 38–45 (2005).

    Article  PubMed  Google Scholar 

  69. 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).

    Article  CAS  Google Scholar 

  70. Müller J. Artificial infection by endophytes affects growth and mycorrhizal colonization of Lolium perenne. Funct. Plant Biol. 30, 419–424 (2003).

    Article  PubMed  Google Scholar 

  71. 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).

    Google Scholar 

  72. Popay, A. J. & Bonos, S. A. in Neotyphodium in Cool-Season Grasses (eds Robert, C., West, C. & Spiers, D. ) 163–185 (Blackwell, 2005).

    Book  Google Scholar 

  73. 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).

    Google Scholar 

  74. 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).

    Article  CAS  PubMed  Google Scholar 

  75. 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).

    Article  CAS  Google Scholar 

  76. 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).

    Article  Google Scholar 

  77. 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).

    Article  Google Scholar 

  78. Pfannmöller, M., Eggstein, S. & Schöberlein, W. in Neotyphodium/Grass Interactions (eds Bacon, C. W. & Hill, N. S. ) 77–80 (Plenum, 1997).

    Book  Google Scholar 

  79. 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).

    Google Scholar 

  80. Zabalgogeazcoa, I. & Bony, S. in Neotyphodium in Cool-Season Grasses (eds Roberts, C. A., West, C. P. & Spiers, D. E. ) 23–33 (Blackwell, 2005).

    Book  Google Scholar 

  81. 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).

    Article  Google Scholar 

  82. 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).

    Article  Google Scholar 

  83. 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).

    Google Scholar 

  84. Takach, J. E. et al. Genotypic and chemotypic diversity of Neotyphodium endophytes in tall fescue from Greece. Appl. Environ. Microb. 78, 5501–5510 (2012).

    Article  CAS  Google Scholar 

  85. 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).

    Article  Google Scholar 

  86. 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).

    Article  Google Scholar 

  87. 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).

    Google Scholar 

  88. 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).

    Article  Google Scholar 

  89. 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).

    Google Scholar 

  90. 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).

    Google Scholar 

  91. Saikkonen, K., Ahlholm, J., Helander, M., Lehtimäki, S. & Niemeläinen, O. Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23, 360–366 (2000).

    Article  Google Scholar 

  92. 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).

    Article  Google Scholar 

  93. 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).

    Google Scholar 

  94. Jöngren, C. Endofytiska svampar i vallgräs — levnadssätt, förekomst och effekter på gräs och gräsätare (Examensarbete/Sveriges lantbruksuniversitet, Institutionen för norrländsk jordbruksvetenskap, 2014).

  95. 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).

    Google Scholar 

  96. Phannmöller, M., Eggestein, S. T. & Schöberlein, W. in Neotyphodium/Grass Interactions (eds Bacon, C. W. & Hill, N. S. ) 77–80 (Plenum, 1997).

    Book  Google Scholar 

  97. 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).

    Article  PubMed  Google Scholar 

  98. 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).

    Google Scholar 

  99. Latch, G. C. M. & Christensen, M. J. Artificial infection of grasses with endophytes. Ann. Appl. Biol. 107, 17–24 (1985).

    Article  Google Scholar 

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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).

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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

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