Fungal Endophytes in Lolium and Festuca Species

  • Christopher L. Schardl


The epichloë endophytes (fungal genera Epichloë and Neotyphodium) are symbionts of many temperate pasture grasses, and are particularly important in Festuca and Lolium species. Many epichloae are known to protect host grasses against a wide range of insects, but some of the anti-insect alkaloids that they produce can negatively affect the health and reproduction of livestock. Here I review the evolutionary relationships and origins of Epichloë and Neotyphodium species, and what is known of the biosynthetic pathways and genetics of protective alkaloids that they produce.


Tall Fescue Perennial Ryegrass Ergot Alkaloid Fungal Endophyte Lysergic Acid 
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  1. Blankenship JD, Houseknecht JB, Pal S, Bush LP, Grossman RB, Schardl CL (2005) Biosynthetic precursors of fungal pyrrolizidines, the loline alkaloids. Chembiochem 6:1016–1022CrossRefPubMedGoogle Scholar
  2. Bluett SJ, Thom ER, Dow BW, Burggraaf VT, Hume DE, Davies E, Tapper BA (2004) Effects of natural reseeding and establishment method on contamination of a novel endophyte-infected perennial ryegrass dairy pasture with other ryegrass/endophyte associations. N Z J Agric Res 47:333–344Google Scholar
  3. Bluett SJ, Thom ER, Clark DA, Macdonald KA, Minnee EMK (2005) Effects of perennial ryegrass infected with either AR1 or wild endophyte on dairy production in the Waikato. N Z J Agric Res 48:197–212Google Scholar
  4. Bouton JH, Latch GCM, Hill NS, Hoveland CS, McCann MA, Watson RH, Parish JA, Hawkins LL, Thompson FN (2002) Reinfection of tall fescue cultivars with non-ergot alkaloid-producing endophytes. Agron J 94:567–574Google Scholar
  5. Bultman TL, Leuchtmann A (2003) A test of host specialization by insect vectors as a mechanism for reproductive isolation among entomophilous fungal species. Oikos 103:681–687CrossRefGoogle Scholar
  6. Chung KR, Hollin W, Siegel MR, Schardl CL (1997) Genetics of host specificity in Epichloë typhina. Phytopathology 87:599–605CrossRefPubMedGoogle Scholar
  7. Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21:275–295CrossRefGoogle Scholar
  8. Clay K (1994) Hereditary symbiosis in the grass genus Danthonia. New Phytol 126:223–231CrossRefGoogle Scholar
  9. Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160 Suppl.:S99–S127CrossRefPubMedGoogle Scholar
  10. Coyle CM, Panaccione DG (2005) An ergot alkaloid biosynthesis gene and clustered hypothetical genes from Aspergillus fumigatus. Appl Environ Microbiol 71:3112–3118CrossRefPubMedGoogle Scholar
  11. Darbyshire SJ (1993) Realignment of Festuca. subgenus Schedonorus with the genus Lolium (Poaceae) Novon 3:239–243CrossRefGoogle Scholar
  12. Faulkner JR, Hussaini SR, Blankenship JD, Pal S, Branan BM, Grossman RB, Schardl CL (2006) On the sequence of bond formation in loline alkaloid biosynthesis. Chembiochem 7:1078–1088CrossRefPubMedGoogle Scholar
  13. Fleetwood DJ, Scott B, Lane GA, Tanaka A, Johnson RD (2007) A complex ergovaline gene cluster in Epichloë endophytes of grasses. Appl Environ Microbiol 73:2571–2579CrossRefPubMedGoogle Scholar
  14. Freeman EM (1904) The seed fungus of Lolium temulentum L., the darnel. Philos Trans R Soc Lond B 196:1–27CrossRefGoogle Scholar
  15. Gröger D, Floss HG (1998) Biochemistry of ergot alkaloids – achievements and challenges. In Cordell GA (ed). Alkaloids. Vol. 50. Academic Press, New York: pp. 171–218Google Scholar
  16. Haarmann T, Machado C, Lübbe Y, Correia T, Schardl CL, Panaccione DG, Tudzynski P (2005) The ergot alkaloid gene cluster in Claviceps purpurea. : extension of the cluster sequence and intra species evolution. Phytochemistry 66:1312–1320CrossRefPubMedGoogle Scholar
  17. Lewis GC, Ravel C, Naffaa W, Astier C, Charmet G (1997) Occurrence of Acremonium endophytes in wild populations of Lolium. spp. in European countries and a relationship between level of infection and climate in France. Annu Appl Biol 130:227–238CrossRefGoogle Scholar
  18. Li W, Ji Y-l, Yu H-S, Wang Z-W (2006) A new species of Epichloë. symbiotic with Chinese grasses. Mycologia 98:560–570CrossRefPubMedGoogle Scholar
  19. Lorenz N, Wilson EV, Machado C, Schardl C, Tudzynski P (2007). Comparison of ergot alkaloid biosynthesis gene clusters in Claviceps species indicate loss of late pathway steps in evolution of C fusiformis . Appl Environ Microbiol 73:7185–7191CrossRefGoogle Scholar
  20. Malinowski DP, Belesky DP (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci 40:923–940Google Scholar
  21. McMillan LK, Carr RL, Young CA, Astin JW, Lowe RGT, Parker EJ, Jameson GB, Finch SC, Miles CO, McManus OB, Schmalhofer WA, Garcia ML, Kaczorowski GJ, Goetz M, Tkacz JS, Scott B (2003) Molecular analysis of two cytochrome P450 monooxygenase genes required for paxilline biosynthesis in Penicillium paxilli. , and effects of paxilline intermediates on mammalian maxi-K ion channels. Mol Genet Genomics 270:9–23CrossRefPubMedGoogle Scholar
  22. Moon CD, Craven KD, Leuchtmann A, Clement SL, Schardl CL (2004) Prevalence of interspecific hybrids amongst asexual fungal endophytes of grasses. Mol Ecol 13:1455–1467CrossRefPubMedGoogle Scholar
  23. Moon CD, Guillaumin J-J, Ravel C, Li C, Craven KD, Schardl CL (2007) New Neotyphodium endophyte species from the grass tribes Stipeae and Meliceae. Mycologia 99:895–905CrossRefPubMedGoogle Scholar
  24. Panaccione DG, Johnson RD, Wang JH, Young CA, Damrongkool P, Scott B, Schardl CL (2001). Elimination of ergovaline from a grass-Neotyphodium endophyte symbiosis by genetic modification of the endophyte. Proc Natl Acad Sci U S A 98:12820–12825CrossRefGoogle Scholar
  25. Panaccione DG, Kotcon JB, Schardl CL, Johnson RD, Morton JB (2006) Ergot alkaloids are not essential for endophytic fungus-associated population suppression of the lesion nematode, Pratylenchus scribneri. , on perennial ryegrass. Nematology 8:583–590CrossRefGoogle Scholar
  26. Philipson MN, Christey MC (1986) The relationship of host and endophyte during flowering, seed formation, and germination of Lolium perenne. N Z J Bot 24:125–134Google Scholar
  27. Riedell WE, Kieckhefer RE, Petroski RJ, Powell RG (1991) Naturally occurring and synthetic loline alkaloid derivatives: insect feeding behavior modification and toxicity. J Entomol Sci 26:122–129Google Scholar
  28. Rowan DD (1993) Lolitrems, paxilline and peramine: mycotoxins of the ryegrass/endophyte interaction. Agric Ecosyst Environ 44:103–122CrossRefGoogle Scholar
  29. Schardl CL, Leuchtmann A (2005) The epichloë endophytes of grasses and the symbiotic continuum. In: Dighton J, White JF, Oudemans P (eds). The Fungal Community: its organization and role in the ecosystem. Vol. 23. CRC Press, Boca Raton, FL: pp. 475–503Google Scholar
  30. Schardl CL, Leuchtmann A, Spiering MJ (2004) Symbioses of grasses with seedborne fungal endophytes. Annu Rev Plant Biol 55:315–340CrossRefPubMedGoogle Scholar
  31. Schardl CL, Panaccione DG, Tudzynski P (2006) Ergot alkaloids-biology and molecular biology. Alkaloids Chem Biol 63:45–86CrossRefPubMedGoogle Scholar
  32. Schardl CL, Grossman RB, Nagabhyru P, Faulkner JR, Mallik UP (2007) Loline alkaloids: currencies of mutualism. Phytochemistry 68:980–996CrossRefPubMedGoogle Scholar
  33. Spatafora JW, Sung GH, Sung JM, Hywel-Jones NL, White JF (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Mol Ecol 16:1701–1711CrossRefPubMedGoogle Scholar
  34. Sullivan RF, Bills GF, Hywel-Jones NL, White JF Jr(2000) Hyperdermium. : a new clavicipitalean genus for some tropical epibionts of dicotyledonous plants. Mycologia 92:908–918CrossRefGoogle Scholar
  35. Tanaka A, Tapper BA, Popay A, Parker EJ, Scott B (2005) A symbiosis expressed non-ribosomal peptide synthetase from a mutualistic fungal endophyte of perennial ryegrass confers protection to the symbiotum from insect herbivory. Mol Microbiol 57:1036–1050CrossRefPubMedGoogle Scholar
  36. Wang J, Machado C, Panaccione DG, Tsai H-F, Schardl CL (2004) The determinant step in ergot alkaloid biosynthesis by an endophyte of perennial ryegrass. Fungal Genet Biol 41:189–198CrossRefPubMedGoogle Scholar
  37. Young CA, Felitti S, Shields K, Spangenberg G, Johnson RD, Bryan GT, Saikia S, Scott B (2006) A complex gene cluster for indole-diterpene biosynthesis in the grass endophyte Neotyphodium lolii. Fungal Genet Biol 43:679–693CrossRefPubMedGoogle Scholar

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© Springer Science + Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Plant PathologyUniversity of KentuckyUSA

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