Research :: Endophyte Symbiosis & Biodiversity

Summary

A unique symbiotic interaction between grasses and systemic fungal endophytes has received much research attention over the past 30 years. In cool-season (C3) grasses, the fungus occurs intercellularly in all above-ground plant parts. When the host grass flowers, the endophyte grows into the ovules and then seeds, and recolonizes the seedling following its germination. This is an example of vertical transmission where the symbiont is passed from generation to generation through the maternal line, analogous to chloroplasts or mitochondria. Theory predicts that these associations should be mutualistic since the fitness of the fungus is directly tied to the fitness of the host. One potential basis for mutualism is the production of ergot and other alkaloids by the fungus, which serve to defend the host plant against grazing animals. One major line of research is to test this hypothesis and examine the relationship between herbivores, endophyte infection and grassland vegetation. Much of our work focuses on tall fescue, the most widespread grass in the eastern United States.

We have contributed to the Web page (forages.oregonstate.edu/tallfescuemonograph/) which specifically addresses the tall fescue-endophyte interaction.

Research by students and post-docs in the lab has investigated the chemical, ecological, evolutionary and physiological interactions between a wide range of grasses (and sedges) and fungal endophytes. Closely related to vertically-transmitted endophytes of cool-season grasses are a range of more pathogenic endophytes that infect both cool-season and warm-season grasses. Unlike the seed-transmitted endophytes, these endophytes produce fruiting bodies on their hosts and typically result in the sterilization or castration of host inflorescences. Nevertheless, infected plants are often vegetatively vigorous and possibly defended by endophyte-produced alkaloid compounds. We are interested in the dynamics of infection in nature, and how infected plants perform under a variety of circumstances.

Recent endophyte research has been conducted in collaboration with former PhD students Jean Pan (www.uakron.edu), Tammy Tintjer (www.smwc.edu) and post-doc Jenn Rudgers (www.ruf.rice.edu).

This research has been funded by multiple NSF grants, most recently by DDIG awards to Jean Pan (Pan Abstract PDF) and Tammy Tintjer (Tintjer Abstract PDF).

Representative Endophyte Publications (Download PDF)

Representative Endophyte publications

Larimer, A.L., Bever, J. B. and K. Clay. 2010. Meta-analysis of the interactive effects of plant microbial symbionts. Symbiosis (in press).

Rudgers, J. A., Davitt, A. J., Clay, K., Gundel, P. and M. Omacini. 2010. Searching for evidence against the mutualistic nature of hereditary symbiosis: A comment on Faeth (2009). The American Naturalist 176: 99-103.

Rudgers, J. A., Fischer, S, and K. Clay. 2010. Managing plant symbiosis: Fungal endophyte genotype alters plant community composition. Journal of Applied Ecology 47: 468-477.

Clay, K. 2008. Defensive Mutualism and Grass Endophytes: Still Valid After All These Years? Pp. 9-20, In Defensive Mutualism in Microbial Symbiosis (J. White and M. Torres, Eds.), Taylor & Francis Group Publishers, Boca Raton.

Ren, A. and K. Clay. 2008. Impact of a horizontally transmitted endophyte, Balansia henningsiana, on growth and drought tolerance of Panicum rigidulum. International Journal of Plant Science 599-608.

Rudgers, J. and K. Clay. 2008. An invasive plant-fungal mutualism reduces arthropod diversity. Ecology Letters 11: 831-840.

Tintjer, T., A. Leuchtmann and K. Clay. 2008. Variation in horizontal and vertical transmission of the endophyte Epichloë elymi infecting the grass Elymus hystrix. New Phytologist 179:236-246.

Finlay, R. D. and K. Clay. 2007. Fungal endophytes in forests, woody plants and grassland ecosystems: diversity, functional ecology and evolution. Fungal Biology Reviews 21: 49-50.

Marks, S. and K. Clay. 2007. Low resource availability affects the interaction between fungal endophytes and two host grasses. International Journal of Plant Science 168: 1269-1277.

Rudgers, J. A. and K. Clay. 2007. Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems? Fungal Biology Reviews 21: 107- 124.

Rudgers, J. A., Holah, J., Orr, S. P. and K. Clay. 2007. Forest succession suppressed by an introduced plant-fungal symbiosis. Ecology 88: 18-25.

Finkes, L. K., J. A. Rudgers, A.B. Cady, K. Clay, and J. C. Mulroy. 2006. A fungal mutualist affects the composition of spiders in an old field. Ecology Letters 9: 347-356.

Orr, S. P., Rudgers, J. A. and K. Clay. 2005. Invasive plants can inhibit native tree seedlings: Testing mechanisms of allelopathy. Plant Ecology 181: 153-165.

Lemons, A., K. Clay, and J. A. Rudgers. 2005. Connecting plant-microbial interactions above- and belowground: a fungal endophyte affects decomposition. Oecologia 145:595-604.

Clay, K., Holah, J. and J. A. Rudgers. 2005. Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proceedings of the National Academy of Science USA 102:12465-12470.

Rudgers, J. A., Koslow, J.M. and K. Clay. 2004. Endophytic fungi alter relationships between diversity and ecosystem processes. Ecology Letters 7: 42-51.

Pan, J. J. and K. Clay. 2004. Epichloë glyceriae infection and carbon translocation in the clonal grass Glyceria striata. New Phytologist 164: 467-475.

Pan, J. J. and K. Clay. 2003. Infection by the systemic fungus, Epichloë glyceriae, alters clonal growth of its grass host, Glyceria striata. Proceedings of the Royal Society of London B 270: 1585-1591.

Clay, K. and C. L. Schardl. 2002. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist 160:S99-S127.

Pan, J. J. and K. Clay. 2002. Infection by the systemic fungus Epichloë glyceriae and clonal growth of its host grass Glyceria striata. Oikos 98:37-46.

Matthews, J. and K. Clay. 2001. Influence of fungal endophyte infection on plant-soil feedback and community interactions. Ecology 82: 500-509.

Fortier, G., Bard, N., Jansen, M. and K. Clay. 2000. Effects of tall fescue infection and vole population density on the growth and reproduction of the prairie vole. Journal of Wildlife Management 64:122-128.

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

Kover, P.X. and K. Clay. 1998. Trade-off between virulence and vertical transmission and the maintenance of a virulent plant pathogen. American Naturalist 152:165-175.

Kover, P.X., T. E. Dolan, and K. Clay. 1997. Potential versus realized transmission rates of a vertically and horizontally transmitted plant pathogen. Proceedings of the Royal Society of London B 264:903-909.

Clay, K. and V.K. Brown. 1997. Infection of Holcus lanatus and H. mollis by Epichloë in experimental grasslands. Oikos 79:363-370.

Leuchtmann, A. and K. Clay. 1996. Isozyme evidence for host races of the fungus Atkinsonella hypoxylon (Clavicipitaceae) infecting the Danthonia (Poaceae) complex in the southern Appalachians. American Journal of Botany 83:1144-1152.

Marks, S. and K. Clay. 1996. Physiological responses of Festuca arundinacea (Poaceae) to fungal endophyte infection. New Phytologist 133:727-733.

Fowler, N.F. and K. Clay. 1995. Environmental heterogeneity, fungal parasitism and the demography of the grass Stipa leucotricha. Oecologia 103:55-62.

Van Horn, R. and K. Clay. 1995. mtDNA variation in the fungus Atkinsonella hypoxylon infecting sympatric Danthonia grasses. Evolution 49:360-371.

Clay, K. 1994. Hereditary symbiosis in the grass genus Danthonia. New Phytologist 126:223-231.

Clay, K. and I. Frentz. 1993. Balansia pilulaeformis, another epiphytic "endophyte." Mycologia 85:527-534.

Leuchtmann, A. and K. Clay. 1993. Nonreciprocal compatibility between Epichloë typhina and four host grasses. Mycologia 85:157-63.

Clay, K., S. Marks and G.P. Cheplick. 1993. Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74:1767-1777.

Powell, R.G., R.J. Petroski and K. Clay. 1992. Alkaloids of Stipa robusta (Sleepygrass) infected with an Acremonium endophyte. Natural Toxins 1:84-88.

Madej, C.W. and K. Clay. 1991. Avian seed preference and weight loss experiments: the effect of fungal endophyte-infected tall fescue seeds. Oecologia 88:296-302.

Clay, K. 1991. Parasitic castration of plants by fungi. Trends in Ecology and Evolution 6:162-166.

Powell, R.G., R.D. Plattner, S.G. Yates, K. Clay and A. Leuchtmann. 1990. Ergobalansine, a new ergot-type peptide alkaloid from Cenchrus echinatus (sandbur grass) infected with Balansia obtecta, and produced in liquid culture of B. obtecta and B. cyperi. Journal of Natural Products 53:1272-1279.

Clay, K. 1990. The impact of mutualistic and pathogenic fungi on competitive relationships among plants. In Perspectives on Plant Competition. pp. 391-412. (D. Tilman and J. Grace, eds.) Academic Press, NY.

Clay, K. 1990. Fungal endophytes of grasses. Annual Review of Ecology and Systematics 21:275-297.

Plowman, T.C., A. Leuchtmann, C. Blaney and K. Clay. 1990. Significance of the fungus Balansia cyperi infecting medicinal species of Cyperus from Amazonia. Economic Botany 44: 452-462.

Marks, S. and K. Clay. 1990. Effects of fungal endophyte infection, CO2 and nutrients on the growth of two grasses. Oecologia 84:207-214.

Leuchtmann, A. and K. Clay. 1990. Isozyme variation in the Acremonium/Epichloë fungal endophyte complex. Phytopathology 80:1133-1139.

Clay, K. 1990. Comparative demography of three graminoids infected by systemic, clavicipitaceous fungi. Ecology 71:558-570.

Leuchtmann, A. and K. Clay. 1989. Isozyme variation in the fungus Atkinsonella hypoxylon within and among populations of its host grasses. Canadian Journal of Botany 67:2600-2607.

Clay, K., G.P. Cheplick, and S.M. Wray. 1989. Impact of the fungus Balansia henningsiana on the grass Panicum agrostoides: frequency of infection, plant growth, and reproduction, and resistance to pests. Oecologia 80:374-380.

Cheplick, G.P., K. Clay and S. Wray. 1989. Interactions between fungal endophyte infection and nutrient limitation in the grasses Lolium perenne and Festuca arundinacea. New Phytologist 111:89-97.

Cheplick, G.P. and K. Clay. 1988. Acquired chemical defenses of grasses: the role of fungal endophytes. Oikos 52:309-318.

Leuchtmann, A. and K. Clay. 1988. Atkinsonella hypoxylon and Balansia cyperi, epiphytic members of the Balansiae. Mycologia 80:192-199.

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

Clay, K. 1988. Clavicipitaceous fungal endophytes of grasses: Coevolution and the change from parasitism to mutualism. In Co-Evolution of Fungi with Plants and Animals. pp. 79-105. (K. Pirozynski and D.L. Hawksworth, Eds.). Academic Press.

Clay, K. 1986. Induced vivipary in Cyperus virens and the transmission of the fungus Balansia cyperi. Can. J. Bot. 64:2984-2988.

Clay, K., T.N. Hardy and A.M. Hammond, Jr. 1985. Fungal endophytes of Cyperus and their effect on an insect herbivore. Amer. J. Bot. 72:1284-1289.

Clay, K., T.N. Hardy and A.M. Hammond, Jr. 1985. Fungal endophytes of grasses and their effects on an insect herbivore. Oecologia 66:1-6.

Clay, K. 1984. The effect of the fungus Atkinsonella hypoxylon (Clavicipitaceae) on the reproductive system and demography of the grass Danthonia spicata. New Phytologist 98:165-175.

Representative Photos



Keith Clay  |  Phone: (812) 855-8158  |  Fax: (812) 855-6705  |  clay@indiana.edu