Asexual Neotyphodium endophytes in Arizona fescue: A test of the seed germination and pathogen resistance hypothesis

Symbiosis

Volumn 38, Issue 1, 2005, Pages 69-85

  Hamilton, Cyd E ^a   Faeth, Stanley H ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Endophytes; Fungal pathogens; Germination; Mutualism; Neotyphodium; Seedlings; Seeds; Symbiosis

Indexed keywords

DISEASE RESISTANCE; ENDOPHYTE; FUNGAL DISEASE; GERMINATION; GRASS; MUTUALISM;

FESTUCA ARIZONICA; FUNGI; NEOTYPHODIUM; POACEAE;

EID: 13444309518     PISSN: 03345114     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (57)

1. Arnold, A.E., Mejia, L.C., Kyllo, D., Rojas, E.I., Maynard, Z. Robbins, N., and Herre, E.A. 2003. Fungal endophytes limit pathogen damage in a tropical tree. Proceedings of the National Academy of Science 100: 15649-15654.
2. Bacon, C. 1993. Abiotic stress tolerances (moisture, nutrients) and photosynthesis in endophyte-infected tall fescue. Agriculture, Ecosystems, & Environment 44: 123-141.
3. Baskin, C.C. and Baskin, J.M. 1998. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. Academic Press, San Diego.
4. Burpee, L.L. and Bouton, J.H. 1993. Effect of eradication of the endophyte Acremonium coenophialum on epidemics of Rhizoctonia blight in tall fescue. Plant Disease 77: 157-159.
5. Carroll, G.C. 1988. Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69: 2-9.
6. Christensen, M.J. 1995. Variation in the ability of Acremonium endophytes of perennial rye-grass (Lolium perenne), tall fescue (Festuca arundinacea) and meadow fescue (F. pratensis) to form compatible associations in three grasses. Mycological Research 99: 466-470.
7. Christensen, M.J. 1996. Antifungal activity in grasses infected with Acremonium and Epichloë endophytes. Australian Journal of Plant Pathology 25: 186-191.
8. Christensen, M.J., Bennett, R.J., and Schmid, J. 2002. Growth of Epichloë/Neotyphodium and p-endophytes in leaves of Lolium and Festuca grasses. Mycological Research 106: 93-106.
9. Clay, K. 1987. Effects of fungal endophyte on the seed and seedling biology of Lolium perenne and Festuca arundinacea. Oecologia 73: 358-362.
10. Clay, K. 1988. Clavicipitaceous fungal endophytes of grasses: coevolution and the change from parasitism to mutualism. In: Coevolution of Fungi with Plants and Animals. Pirozynsky, K.A. and Hawksworth, D.L., eds. Academic Press, San Diego, pp. 79-106.
11. Clay, K. 1990. Fungal endophytes of grasses. Annual Review of Ecology & Systematics 21: 275-297.
12. Clay, K. 1998. Fungal endophyte infection and the population biology of grasses. In: Population Biology of Grasses. Cheplick, G.P., ed. Cambridge University Press, Cambridge, pp. 255-285.
13. Clay, K. and Schardl, C. 2002. Evolutionary origins and ecological consequences of endophytic symbioses with grasses. The American Naturalist 160: S99-127.
14. Connor, R.C. 1995. The benefits of mutualism: a conceptual framework. Biological Review 70: 427-457.
15. Faeth, S.H. 2002. Are endophytic fungi defensive plant mutualists? Oikos 98: 25-36.
16. Faeth, S.H. and Bultman T.L. 2002. Endophytic fungi and interactions among host plants, herbivores and natural enemies. In: Multitrophic Level Interactions. Tscharnkte, T. and Hawkins, B.A., eds. Cambridge University Press, Cambridge, pp. 89-123.
17. Faeth, S.H. and Pagan, W.F. 2002. Fungal endophytes: common host plant symbionts but uncommon mutualists. Integrative and Comparative Biology 42: 360-368.
18. Faeth, S.H. and Sullivan, T.J. 2003. Mutualistic, asexual endophytes in a native grass are usually parasitic. The American Naturalist 161: 310-325.
19. Faeth, S.H., Haase S.H., Sackett, S.S., Sullivan, T.J., Keithley, R.K., and Hamilton, C.E. 2002a. Does fire maintain systemic endophyte infections in native grasses? Symbiosis 32: 211-228.
20. Faeth, S.H., Bush L.P., and Sullivan, T.J. 2002b. Peramine alkaloid variation in Neotyphodium-infected Arizona fescue: effects of endophyte and host genotype and environment. Journal of Chemical Ecology 28: 1511-1526.
21. Faeth, S.H., Saikkonen, K., and Helander, M. 2004. Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecology Letters 7: 304-313.
22. Farr, D.F., Bills, G.F., Chamuris, G.P., and Rossman, A.Y. 1989. Fungi on Plants and Plant Products in The United States. APS Press, St. Paul, MN.
23. Frank, S.A. 1994. Genetics of mutualisms: the evolution of altruism between species. Journal of Theoretical Biology 170: 393-400.
24. Glenn, A.E., Bacon, C.W., Price R., and Hanlin, R.T. 1996. Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88: 369-383.
25. Gwinn, K.D. and Gavin, A.M. 1992. Relationship between endophyte infection level of tall fescue seed lots and Rhizoctonia zeae seedling disease. Plant Disease 76: 911-914.
26. Hamilton, C.E. 2002. Maintenance of Systemic Neotyphodium Infections in Arizona Fescue: A Test of Three Hypotheses. MS Thesis. Arizona State University, Tempe, Arizona.
27. Kearney, T.H. and Peebles, R.H. 1960. Arizona Flora. University California Press, Berkeley, CA.
28. Knoch, T.R., Faeth, S.H., and Arnott, D.L. 1993. Endophytic fungi alter foraging and dispersal by desert seed-harvesting ants. Oecologia 95: 470-475.
29. Law, R. 1985. Evolution in a mutualistic environment. In: The Biology of Mutualisms. Boucher, D.H., ed. Croom Helm, London, pp. 145-170.
30. Leuchtmann, A. 1992. Systematics, distribution, and host specificity of grass endophytes. Natural Toxins 1: 150-162.
31. Leuchtmann, A. 1997. Ecological diversity in Neotyphodium-infected grasses as influenced by the host and fungus characteristics. In: Neotyphodium/Grass Interactions. Bacon, C.W. and Hill, N.S., eds. Plenum Press, New York, pp. 93-108.
32. Leuchtmann, A., Schmidt, D., and Bush, L.P. 2000. Different levels of protective alkaloids in grasses with stroma-forming and seed-transmitted Epichloë/Neotyphodium endophytes. Journal of Chemical Ecology 26: 1025-1036.
33. Li, B., Zheng, X., and Suichang, S. 1997. Survey of endophytic fungi in some late forage grasses of Northwestern China. In: Proceedings of the 3rd International Neotyphodium/Grass Interactions Symposium. Athens, GA, Bacon, C.W. and Hill, N.S., eds., Plenum Press, New York, pp. 69-72.
34. Morse, L.J., Day, T.A., and Faeth, S.H. 2002. Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability regimes. Environmental & Experimental Botany 48: 257-268.
35. Neil, K.L., Tiller, R.L., and Faeth S.H. 2003. Germination of big Sacaton and endophyte-infected Arizona fescue under water stress. Journal of Range Management 56: 616-622.
36. Powell, R.G. and Petroski, R.J. 1992. Alkaloid toxins in endophyte-infected grasses. Natural Toxins 1: 163-170.
37. Ravel, C., Michalakis, Y., and Charmet, G. 1997. The effect of imperfect transmission on the frequency of mutualistic seed-borne endophytes in natural populations of grasses. Oikos 80: 18-24.
38. Saikkonen, K., Faeth, S.H., Helander, M., and Sullivan, T.J. 1998. Fungal endophytes: A continuum of interactions with host palnts. Annual Review of Ecology & Systematics 29: 319-343.
39. Saikkonen, K., Helander, M., Faeth, S.H., Schulthess, F., and Wilson, D. 1999. Neotyphodium endophytes in native grass populations: against herbivory-based defensive mutualism. Oecologia 121: 411-420.
40. Saikkonen, K., Ion, D., and Gyllenberg, M. 2002. The persistence of vertically transmitted fungi in grass metapopulations. Proceedings of the Royal Society of London B 26: 1397-1403.
41. Schardl, C.L. and Phillips, T.D. 1997. Protective grass endophytes: where are they from and where are they going? Plant Disease 81: 30-438.
42. Schardl, C.L., Leuchtmann A., Chung, K-R., Penny, D., and Siegel, M.R. 1997. Coevolution by common descent of fungal symbionts (Epichloë spp.) and grass hosts. Molecular Biology & Evolution 14: 133-143.
43. Schulthess, F.M. and Faeth, SH. 1998. Distribution, abundances, and associations of the endophytic fungal community of Arizona fescue (Festuca arizonica). Mycologia 90: 569-578.
44. Siegel, M.R., Varney, D.R., Johnson, M.C., Nesmith, W.C., Buckner, R.C., Bush, L.P., Burris, II, P.B., and Hardison, J.R. 1984. A fungal endophyte of tall fescue: evaluation of control methods. Phytopathology 74: 937-941.
45. Siegel, M.R. and Bush, L.P. 1996. Defensive chemicals in grass-fungal endophyte associations. Recent Advances in Phytochemistry 30: 81-119.
46. Sullivan, T.J. and Faeth, S.H. 2004. Gene flow in the endophyte Neotyphodium and implications for coevolution with Festuca arizonica. Molecular Ecology 13: 649-656.
47. SYSTAT. 2000. SYSTAT Version 10.2, SPSS Inc, Chicago, Illinois, USA.
48. Tan, Y.Y., Spierling, M. J., Scott, V., Lane, G.A., Christensen, M. J., and Schmid, J. 2001. In planta regulation of extension of an endophytic fungus and maintenance of high metabolic rates in its mycelium in the absence of apical extension. Applied & Environmental Microbiology 67: 5377-5383.
49. Tibbets, T.M. and Faeth, S.H. 1999. Neotyphodium endophytes in grasses: deterrents or promoters of herbivory by leaf-cutting ants? Oecologia 118: 297-305.
50. Trevathan, L.E. 1996. Performance of endophyte-free and endophyte infected tall fescue seedlings in soil infected with Cochiobolus sativus. Canadian Journal of Plant Pathology 18: 415-418.
51. Weis, A.E. and Hochberg, M.E. 2000. The diverse effects of intraspecific competition on the selective advantage to resistance: a model and its predictions. The American Naturalist 156: 276-292.
52. Werren, J.H. and O'Neill, S.L. 1997. The evolution of heritable symbionts. In: Influential Passengers. O'Neill, S.L., Hoffman, A.A., and Werren, J.H., eds. Oxford University Press, Oxford, pp. 1-41.
53. White, J.F., Jr. and Cole, G.T. 1985. Endophyte associations in forage grasses. III. In vitro inhibition by Acremonium coenophialum. Mycologia 77: 487-489.
54. White, J.F., Jr., Martin T.I., and Cabral, D. 1996. Endophyte-host associations in grasses XXII. Conidia formation by Acremonium endophytes on the phylloplanes of Agrostis hiemalis and Poa rigidifolia. Mycologia 88: 174-178.
55. Wilkinson, H.H. and Schardl, C.L. 1997. The evolution of mutualism in grass-endophyte associations. In: Neotyphodium/Grass Interactions. Bacon, C.W. and Hill, N.S., eds. Plenum Press, New York, pp. 13-26.
56. Wolock-Madej, C. and Clay, K. 1991. Avian seed preference and weight loss experiment: the role of fungal-infected fescue seeds. Oecologia 88: 296-302.
57. Yue, Q., Miller, C.J., White, J.F., Jr., and Richardson, M.D. 2000. Isolation and characterization of fungal inhibitors from Epichloë festucae. Journal of Agriculture and Food Chemistry 48: 4687-4692.