Environmental stresses mediate endophyte-grass interactions in a boreal archipelago

Journal of Ecology

Volumn 98, Issue 2, 2010, Pages 470-479

  Saona, Nora M ^a   Albrectsen, Benedicte Riber ^b   Ericson, Lars ^b   Bazely, Dawn R ^a  

^a YORK UNIVERSITY   (Canada)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Antagonist mutualist continuum; Endophyte; Epichlo festucae; Festuca rubra; Grass; Herbivory; Nutrient stress; Sweden; Symbiosis; Water stress

Indexed keywords

ARCHIPELAGO; ENDOPHYTE; ENVIRONMENTAL STRESS; EVOLUTIONARY BIOLOGY; EXPERIMENTAL STUDY; FUNGUS; GRASS; GRAZING PRESSURE; GROWTH RESPONSE; HERBIVORY; NUTRIENT AVAILABILITY; POPULATION DENSITY; SOIL MOISTURE; SYMBIOSIS; WATER STRESS;

SWEDEN;

ANSER; BRANTA CANADENSIS; EPICHLOE; EPICHLOE FESTUCAE; FESTUCA RUBRA; POACEAE;

EID: 77749279690     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/j.1365-2745.2009.01613.x     Document Type: Article

References (77)

1. Afkhami ME, Rudgers JA. Symbiosis lost: imperfect vertical transmission of fungal endophytes in grasses. American Naturalist 2008, 172:405-416.
2. Ahlholm JU, Helander M, Lehtimäki S, Wäli P, Saikkonen K. Vertically transmitted fungal endophytes: different responses of host-parasite systems to environmental conditions. Oikos 2002, 99:173-183.
3. Bazely DR, Vicari M, Emmerich S, Filip L, Lin D, Inman A. Interactions between herbivores and endophyte-infected Festuca rubra from the Scottish islands of St. Kilda, Benbecula and Rum. Journal of Applied Ecology 1997, 34:847-860.
4. Bazely DR, Ball JP, Vicari M, Tanentzap AJ, Berenger M, Rakocevic T, Koh S. Broad-scale geographic patterns in the distribution of vertically-transmitted, asexual endophytes in four naturally-occurring grasses in Sweden. Ecography 2007, 30:367-374.
5. Belesky DP, Stringer WC, Hill NS. Influence of endophyte and water regime upon tall fescue accessions. I. Growth characteristics. Annals of Botany 1989, 63:495-503.
6. Burdon JJ, Thrall PH, Ericson L. The current and future dynamics of disease in plant communities. Annual Review of Phytopathology 2006, 44:19-39.
7. Carlsson U, Elmqvist E, Wennström A, Ericson L. Infection by pathogens and population age of host plants. Journal of Ecology 1990, 78:1094-1105.
8. Carroll G. Fungal endophytes in stems and leaves - from latent pathogen to mutualistic symbiont. Ecology 1988, 69:2-9.
9. Cheplick GP. Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environmental and Experimental Botany 2007, 60:202-210.
10. Cheplick GP, Clay K. Acquired chemical defenses in grasses - the role of fungal endophytes. Oikos 1988, 52:309-318.
11. Cheplick GP, Perera A, Koulouris K. Effect of drought on the growth of Lolium perenne genotypes with and without fungal endophytes. Functional Ecology 2000, 14:657-667.
12. Clay K. Fungal endophytes of grasses - a defensive mutualism between plants and fungi. Ecology 1988, 69:10-16.
13. Clay K. Interactions among fungal endophytes, grasses and herbivores. Researches on Population Ecology 1996, 38:191-201.
14. Clay K, Schardl C. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. American Naturalist 2002, 160:S99-S127.
15. Conover MR. Impact of the consumption of endophyte-infected perennial ryegrass by meadow voles. Agriculture Ecosystems & Environment 2003, 97:199-203.
16. Conover MR, Messmer TA. Feeding preferences and changes in mass of Canada geese grazing endophyte-infected tall fescue. Condor 1996, 98:859-862.
17. Ekman M. A consistent map of the postglacial uplift of Fennoscandia. Terra Nova 1996, 8:158-165.
18. Ericson L, Wallentinus H-G. Sea-shore vegetation around the Gulf of Bothnia. Wahlenbergia 1979, 5:1-118.
19. Eriksson OE. The Non-lichenized Pyrenomycetes of Sweden 1992, SBT-förlaget, Lund
20. Ewald PW. Host-parasite relations, vectors, and the evolution of disease severity. Annual Review of Ecology and Systematics 1983, 14:465-485.
21. Ewald PW. Transmission modes and evolution of the parasitism-mutualism continuum. Annals of the New York Academy of Sciences 1987, 503:295-306.
22. Faeth SH. Are endophytic fungi defensive plant mutualists? Oikos 2002, 98:25-36.
23. Faeth SH. Asexual fungal symbionts alter reproductive allocation and herbivory over time in their native perennial grass hosts. American Naturalist 2009, 173:554-565.
24. Faeth SH, Fagan WF. Fungal endophytes: common host plant symbionts but uncommon mutualists. Integrative and Comparative Biology 2002, 42:360-368.
25. Faeth SH, Helander ML, Saikkonen KT. Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecology Letters 2004, 7:304-313.
26. Faeth SH, Sullivan TJ. Mutualistic asexual endophytes in a native grass are usually parasitic. American Naturalist 2003, 161:310-325.
27. Metapopulation Dynamics: Emperical and Theoretical Investigations 1991, Gilpin MHanski I. eds, Harcourt Brance Jovanovich, London, UK
28. Granath G, Vicari M, Bazely DR, Ball JP, Puentes A, Rakocevic T. Variation in the abundance of fungal endophytes in fescue grasses along altitudinal and grazing gradients. Ecography 2007, 30:422-430.
29. Gundel PE, Maseda PH, Vila- Aiub MM, Ghersa CM, Benech-Arnold R. Effects of Neotyphodium fungi on Lolium multiflorum seed germination in relation to water availability. Annals of Botany 2006, 97:571-577.
30. Gundel PE, Omacini M, Martinez-Ghersa MA, Ghersa CM. Herbivory mediates grass-endophyte relationships: comment. Ecology 2008, 89:3542-3545.
31. Harri SA, Krauss J, Müller CB. Fungal endosymbionts of plants reduce lifespan of an aphid secondary parasitoid and influence host selection. Proceedings of the Royal Society B-Biological Sciences 2008, 275:2627-2632.
32. Harri SA, Krauss J, Müller CB. Extended larval development time for aphid parasitoids in the presence of plant endosymbionts. Ecological Entomology 2009, 34:20-25.
33. Hochberg ME, Gomulkiewicz R, Holt RD, Thompson JN. Weak sinks could cradle mutualistic symbioses - strong sources should harbour parasitic symbioses. Journal of Evolutionary Biology 2000, 13:213-222.
34. Hultén E, Fries M. Atlas of North European Vascular Plants, North of the Tropic of Cancer 1986, Koeltz Scientific Books, Königstein
35. Jensen AMD, Mikkelsen L, Roulund N. Variation in genetic markers and ergovaline production in endophyte (Neotyphodium)-infected fescue species collected in Italy, Spain, and Denmark. Crop Science 2007, 47:139-147.
36. Ju HJ, Hill NS, Abbott I, Ingram KT. Temperature influences on endophyte growth in tall fescue. Crop Science 2006, 46:404-412.
37. Koh S, Hik DS. Herbivory mediates grass-endophyte relationships. Ecology 2007, 88:2752-2757.
38. Koh S, Hik DS. Herbivory mediates grass-endophyte relationships: reply. Ecology 2008, 89:3545-3549.
39. Koh S, Vicari M, Ball JP, Rakocevic T, Zaheer S, Hik DS, Bazely DR. Rapid detection of fungal endophytes in grasses for large-scale studies. Functional Ecology 2006, 20:736-742.
40. Lehtonen PT, Helander M, Siddiqui SA, Lehto K, Saikkonen K. Endophytic fungus decreases plant virus infections in meadow ryegrass (Lolium pratense). Biology Letters 2006, 2:620-623.
41. Lewis GC, Ravel C, Naffaa W, Astier C, Charmet G. Occurrence of Acremonium endophytes in wild populations of Lolium spp. in European countries and a relationship between level of infection and climate in France. Annals of Applied Biology 1997, 130:227-238.
42. Malinowski DP, Belesky DP, Fedders JM. Endophyte infection may affect the competitive ability of tall fescue grown with red clover. Journal of Agronomy and Crop Science-Zeitschrift für Acker und Pflanzenbau 1999, 183:91-101.
43. Markgraff-Dannenberg I. Festuca, Flora Europaea 1980, Cambridge University Press, Cambridge
44. Meister B, Krauss J, Harri SA, Schneider MV, Müller CB. Fungal endosymbionts affect aphid population size by reduction of adult life span and fecundity. Basic and Applied Ecology 2006, 7:244-252.
45. Monnet F, Vaillant N, Hitmi A, Coudret A, Sallanon H. Endophytic Neotyphodium lolii induced tolerance to Zn stress in Lolium perenne. Physiologia Plantarum 2001, 113:557-563.
46. Morse LJ, Day TA, Faeth SH. Effect of Neotyphodium endophyte infection on growth and leaf gas exchange of Arizona fescue under contrasting water availability regimes. Environmental and Experimental Botany 2002, 48:257-268.
47. Müller CB, Krauss J. Symbiosis between grasses and asexual fungal endophytes. Current Opinion in Plant Biology 2005, 8:450-456.
48. Novas MV, Collantes M, Cabral D. Environmental effects on grass-endophyte associations in the harsh conditions of south Patagonia. Fems Microbiology Ecology 2007, 61:164-173.
49. Ohgushi T. Herbivore-induced effects through trait change in plants. Annual Review of Ecology, Evolution, and Systematics 2005, 36:81-105.
50. Olejniczak P, Lembicz M. Age-specific response of the grass Puccinellia distans to the presence of a fungal endophyte. Oecologia 2007, 152:485-494.
51. Piano E, Bertoli FB, Romani M, Tava A, Riccioni L, Valvassori M, Carroni AM, Pecetti L. Specificity of host-endophyte association in tall fescue populations from Sardinia, Italy. Crop Science 2005, 45:1456-1463.
52. Ravel C, Michalakis Y, Charmet G. The effect of imperfect transmission on the frequency of mutualistic seed-borne endophytes in natural populations of grasses. Oikos 1997b, 80:18-24.
53. Ravel C, Courty C, Coudret A, Charmet G. Beneficial effects of Neotyphodium lolii on the growth and the water status in perennial ryegrass cultivated under nitrogen deficiency or drought stress. Agronomie 1997a, 17:173-181.
54. Richmond DS, Grewal PS, Cardina J. Competition between Lolium perenne and Digitaria sanguinalis: ecological consequences for harbouring an endosymbiotic fungus. Journal of Vegetation Science 2003, 14:835-840.
55. Rudgers JA, Holah J, Orr SP, Clay K. Forest succession suppressed by an introduced plant-fungal symbiosis. Ecology 2007, 88:18-25.
56. Saikkonen K, Faeth SH, Helander M, Sullivan TJ. Fungal endophytes: a continuum of interactions with host plants. Annual Review of Ecology and Systematics 1998, 29:319-343.
57. Saikkonen K, Helander M, Faeth SH, Schulthess F, Wilson D. Endophyte-grass-herbivore interactions: the case of Neotyphodium endophytes in Arizona fescue populations. Oecologia 1999, 121:411-420.
58. Saikkonen K, Ahlholm J, Helander M, Lehtimäki S, Niemeläinen O. Endophytic fungi in wild and cultivated grasses in Finland. Ecography 2000, 23:360-366.
59. Saikkonen K, Wäli P, Helander M, Faeth SH. Evolution of endophyte-plant symbioses. Trends in Plant Science 2004, 9:275-280.
60. Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth SH. Model systems in ecology: dissecting the endophyte-grass literature. Trends in Plant Science 2006, 11:428-433.
61. de Sassi C, Müller CB, Krauss J. Fungal plant endosymbionts alter life history and reproductive success of aphid predators. Proceedings of the Royal Society B-Biological Sciences 2006, 273:1301-1306.
62. Schulz B, Boyle C. The endophytic continuum. Mycological Research 2005, 109:661-686.
63. Shiba T, Sugawara K. Resistance to the rice leaf bug, Trigonotylus caelestialium, is conferred by Neotyphodium endophyte infection of perennial ryegrass, Lolium perenne. Entomologia Experimentalis et Applicata 2005, 115:387-392.
64. Sjörs H. The background: geology, climate and zonation. Acta Phytogeographica Suecica 1999, 84:5-14.
65. Sokal RR, Rohlf FJ. Biometry: The Principles and Practice of Statistics in Biological Research 1995, 3rd edn, W. H. Freemand and Company, New York
66. Spyreas G, Gibson DJ, Basinger M. Endophyte infection levels of native and naturalized fescues in Illinois and England. Journal of the Torrey Botanical Society 2001, 128:25-34.
67. Thompson JN. The Geographic Mosaic of Coevolution 2005, Chicago University Press, Chicago IL
68. Väre H. Festuca rubra ssp. arctica in Finland. Lutukka 2007, 23:120-126. (in Finnish, English summary)
69. Vazquez de Aldana BR, Zabalgogeazcoa I, Ciudad AG, Criado BG. Ergovaline occurrence in grasses infected by fungal endophytes of semi-arid pastures in Spain. Journal of the Science of Food and Agriculture 2003, 83:347-353.
70. Vazquez de Aldana BR, Zabalgogeazcoa I, Garcia Ciudad A, Garcia Criado B. Fungal alkaloids in populations of endophyte-infected Festuca rubra subsp pruinosa. Grass and Forage Science 2007, 62:364-371.
71. Wäli PR, Ahlholm JU, Helander M, Saikkonen K. Occurrence and genetic structure of the systemic grass endophyte Epichloë festucae in fine fescue populations. Microbial Ecology 2007, 53:20-29.
72. Wäli P, Helander M, Saloniemi I, Ahlholm J, Saikkonen K. Variable effects of endophytic fungus on seedling establishment of fine fescues. Oecologia 2009, 159:49-57.
73. West CP, Izekor E, Turner KE, Elmi AA. Endophyte effects on growth and persistence of tall fescue along a water-supply gradient. Agronomy Journal 1993, 85:264-270.
74. Wilkinson HH, Siegel MR, Blankenship JD, Mallory AC, Bush LP, Schardl CL. Contribution of fungal loline alkaloids to protection from aphids in a grass-endophyte mutualism. Molecular Plant-Microbe Interactions 2000, 13:1027-1033.
75. Wilson D. Endophyte - the evolution of a term, and clarification of its use and definition. Oikos 1995, 73:274-276.
76. Zabalgogeazcoa I, de Aldana BRV, Criado BG, Ciudad AG. The infection of Festuca rubra by the fungal endophyte Epichloë festucae in Mediterranean permanent grasslands. Grass and Forage Science 1999, 54:91-95.
77. Zabalgogeazcoa I, Romo M, Keck E, de Aldana BRV, Ciudad AG, Criado BG. The infection of Festuca rubra subsp. pruinosa by Epichloë festucae. Grass and Forage Science 2006, 61:71-76.