Consequences of grazing on the vertical transmission of a fungal Neotyphodium symbiont in an annual grass population

Austral Ecology

Volumn 37, Issue 5, 2012, Pages 620-628

  García Parisi, Pablo A ^a   Casas, Cecilia ^a   Gundel, Pedro E ^a,b   Omacini, Marina ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b FINNISH FOREST RESEARCH INSTITUTE   (Finland)

Author keywords

Grass endophyte symbiosis; Lolium multiflorum; Mutualism effectiveness; Symbiosis dynamics; Transmission efficiency

Indexed keywords

AGROECOLOGY; ANNUAL PLANT; ECOSYSTEM FUNCTION; ENDOPHYTE; FITNESS; FUNGUS; GRASS; GRAZING; HOST PLANT; HOST-SYMBIONT INTERACTION; MICROCOSM; MUTUALISM; SEED PRODUCTION; SYMBIONT;

LOLIUM; LOLIUM MULTIFLORUM; NEOTYPHODIUM; NEOTYPHODIUM OCCULTANS; POACEAE;

EID: 84864142454     PISSN: 14429985     EISSN: 14429993     Source Type: Journal    
DOI: 10.1111/j.1442-9993.2011.02325.x     Document Type: Article

References (62)

1. Afkhami M. & Rudgers J. (2008) Symbiosis lost: imperfect vertical transmission of fungal endophytes in grasses. Am. Nat. 175, 405-16.
2. Bacon C. W. & White J. F. Jr (1994) Biotechnology of Endophytic Fungi of Grasses. CRC Press, Boca Raton.
3. Bardgett R. D., Bowman W. D., Kaufmann R. & Schmidt S. K. (2005) A temporal approach to linking aboveground and belowground ecology. Trends Ecol. Evol. 20, 634-41.
4. Canals R. M., San Emeterio L. & Oreja A. (2008) Chances of loss of fungal endophytes in agronomic grasses: a case-study for Lolium rigidum. Agric. Ecosyst. Environ. 127, 146-52.
5. Cheplick G. P. (2007) Costs of fungal endophyte infection in Lolium perenne genotypes from Eurasia and North Africa under extreme resource limitation. Environ. Exp. Bot. 60, 202-10.
6. Cheplick G. P. & Faeth S. (2009) Ecology and Evolution of the Grass-endophyte Symbiosis. Oxford University Press, Oxford.
7. Christensen M. J., Zhang X. & Scott B. (2008) Regulation switching of Epichloë typhina within elongating perennial ryegrass leaves. Mycol. Res. 112, 1056-62.
8. Clay K. (1990) Fungal endophytes of grasses. Annu. Rev. Ecol. Syst. 21, 275-95.
9. Clay K. (1993) The ecology and evolution of endophytes. Agric. Ecosyst. Environ. 44, 39-64.
10. Clay K. & Schardl C. L. (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Midl. Nat. 160, 99-127.
11. Clay K., Holah J. & Rudgers J. A. (2005) Herbivores cause a rapid increase in hereditary symbiosis and alter plant community composition. Proc. Natl Acad. Sci. USA 102, 12465-70.
12. Davitt A. J., Chen C. & Rudgers J. A. (2011) Understanding context-dependency in plant-microbe symbiosis: The influence of abiotic and biotic contexts on host fitness and the rate of symbiont transmission. Environ. Exp. Bot. 71, 137-45.
13. De Battista J. (2005) Neotyphodium research and application: current trends in South America. In: Neotyphodium in Cool-Season Grasses (eds C. Roberts, C. West & D. Spiers ) pp. 65-71. Blackwell publishing, Ames.
14. Douglas A. E. (2010) The Symbiotic Habit. Princeton University Press, Princeton.
15. Fitter A. H., Heinemeyer A. & Staddon P. L. (2000) The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach. New Phytol. 147, 179-87.
16. Fox J. (2009) Car: companion to applied regression. R package version. R-cran project.
17. Gundel P. E., Batista W. B., Texeira M., Martinez-Ghersa M., Omacini M. & Ghersa C. M. (2008) Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency. Proc. R. Soc. B Biol. Sci. 275, 897-905.
18. Gundel P. E., Garibaldi L. A., Tognetti P., Aragon R., Ghersa C. M. & Omacini M. (2009) Imperfect vertical transmission of the endophyte Neotyphodium in exotic grasses in grasslands of the Flooding Pampa. Microb. Ecol. 57, 740-8.
19. Gundel P. E., Garibaldi L. A., Martínez-Ghersa M. A. & Ghersa C. M. (2011a) Neotyphodium endophyte transmission to Lolium multiflorum seeds depends on the host plant fitness. Environ. Exp. Bot. 71, 359-66.
20. Gundel P. E., Rudgers J. A. & Ghersa C. M. (2011b) Incorporating the process of vertical transmission into understanding of host-symbiont dynamics. Oikos 120, 1121-8.
21. Hartley S. E. & Gange A. C. (2009) Impacts of plant symbiotic fungi on insect herbivores: Mutualism in a multitrophic context. Annu. Rev. Entomol. 54, 323-42.
22. Jensen A. & Roulund N. (2004) Occurrence of Neotyphodium endophytes in permanent grassland with perennial ryegrass (Lolium perenne) in Denmark. Agric. Ecosyst. Environ. 104, 419-27.
23. Ju H.-J., Hill N. S., Abbott T. & Ingram K. T. (2006) Temperature influences on endophyte growth in tall fescue. Crop Sci. 46, 404-12.
24. Kareiva P. (1994) Space - the final frontier for ecological theory. Ecology 75, 1.
25. Kiers E. T., Rousseau R. A., West S. A. & Denlson R. F. (2003) Host sanctions and the legume-rhizobium mutualism. Nature 425, 78-81.
26. Kirkby K. A., Pratley J. E., Hume D. E., An M. & Wu H. (2011a) Viability of seeds and endophyte (Neotyphodium occultans) in annual ryegrass (Lolium rigidum) when buried and in long term storage. Seed Sci. Technol. 39, 452-64.
27. Kirkby K. A., Pratley J. E., Hume D. E., Faville M. J., An M. & Wu H. (2011b) Incidence of endophyte Neotyphodium occultans in Lolium rigidum from Australia. Weed Res. 51, 261-72.
28. Koricheva J., Gange A. C. & Jones T. (2009) Effects of mycorrhizal fungi on insect herbivores: A meta-analysis. Ecology 90, 2088-97.
29. Lewis G., Ravel C., Naffaa W., Astier C. & Charmet G. (1997) Occurence of Acremonium endophytes in wild populations of Lolium spp in Eurpean countries and a relationship between level of infection and climate in France. Ann. Appl. Biol. 130, 227-38.
30. Mack K. & Rudgers J. (2008) Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi an dfungal endophytes. Oikos 117, 310-20.
31. Malinowski D. P. & Belesky D. P. (2000) Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci. 40, 923-40.
32. Miranda M. I., Omacini M. & Chaneton E. J. (2011) Environmental context of endophyte symbioses: interacting effects of watter stress and insect herbivory. Int. J. Plant Sci. 172, 499-508.
33. Moon C. D., Scott B., Schardl C. L. & Christensen M. J. (2000) Evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 92, 1103-18.
34. Müller C. B. & Krauss J. (2005) Symbiosis between grasses and asexual fungal endophytes. Curr. Opin. Plant Biol. 8, 450-6.
35. Novas V. M., Collantes M. & Cabral D. (2007) Environmental effects on grass-endophyte associations in the harsh conditions of south Patagonia. FEMS Microbiol. Ecol. 61, 164-73.
36. Novas M. V., Iannone L., Godeas A. & Cabral D. (2009) Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass. Mycol. Prog. 8, 75-81.
37. Omacini M., Chaneton E. J., Ghersa C. M. & Muller C. B. (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409, 78-81.
38. Omacini M., Chaneton E. J., Ghersa C. M. & Otero P. (2004) Do foliar endophytes affect grass litter decomposition? A microcosm approach using Lolium multiflorum. Oikos 104, 581-90.
39. Omacini M., Chaneton E. J. & Ghersa C. M. (2005) A framework for understanding the ecosystem consequences of endophyte grass symbioses. In: Neotyphodium in Cool-Season Grasses Current Research & Applications (eds C. Roberts, C. West & D. Spiers ) pp. 141-62. Blackwell publishing, Ames.
40. Omacini M., Eggers T., Bonkowski M., Gange A. C. & Jones T. (2006) Leaf endophytes afffect mycorrhizal status and growth of c′-infected and neighbouring plants. Funct. Ecol. 20, 226-32.
41. Omacini M., Chaneton E., Bush L. & Ghersa C. M. (2009) A fungal endosymbiont affects host plant retruitment through seed- and litter-mediated mechanisms. Funct. Ecol. 23, 1148-56.
42. Philipson M. N. & Christey M. C. (1986) The relationship of host and endophyte during flowering, seed formation, and germination of Lolium perenne. NZ J. Bot. 24, 125-34.
43. Piippo S., Markkola A., Härmä E. & Tuomi J. (2011) Do compensatory shoot growth and mycorrhizal symbionts act as competing above- and below-ground sinks after simulated grazing? Plant Ecol. 212, 33-42.
44. Pinheiro J. C. & Bates D. M. (2009) Mixed-Effects Models in S and S-PLUS. Springer, New York.
45. Rasmussen S., Parsons A. J., Bassett S. etal. (2007) High nitrogen supply and carbohydrate content reduce fungal endophyte and alkaloid concentration in Lolium perenne. New Phytol. 173, 787-97.
46. Ravel C., Michalakis Y. & 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.
47. Rodriguez A. M. & Jacobo E. (2010) Glyphosate effects on floristic composition and species diversity in the Flooding Pampa grassland (Argentina). Agric. Ecosyst. Environ. 138, 222-31.
48. Rudgers J. A., Afkhami M. E., Rúa M. A., Davitt A. J., Hammer S. & Huguet V. M. (2009) A fungus among us: broad patterns of endophyte distribution in the grasses. Ecology 90, 1531-9.
49. Rudgers J. A., Davitt A. J., Clay K., Gundel P. E. & Omacini M. (2010) Searching for evidence against the mutualistic nature of hereditary symbioses: a comment on Faeth. Am. Nat. 176, 99-103.
50. Saikkonen K., Ion D. & Gyllenberg M. (2002) The persistence of vertically transmitted fungi in grass metapopulations. Proc. R. Soc. B Biol. Sci. 269, 1397-403.
51. Schardl C. L. (2010) The epichloae, symbionts of the grass subfamily Poideae. Ann. Mo. Bot. Gard. 97, 646-65.
52. Selosse M. A. & Schardl C. L. (2007) Fungal endophytes of grasses: hybrids rescued by vertical transmission? An evolutionary perspective. New Phytol. 173, 452-8.
53. Siegel M. R., Varney D. R., Johnson M. C. etal. (1984) A fungal endophyte of tall fescue: evaluation of control methods. Phytopathology 74, 937-41.
54. Soriano A. (1991) Rio de la Plata grasslands. In: Natural Grasslands: Introduccion and Western Hemisphere. Ecosystem of the World 8 A (ed. R. T. Coupland ) pp. 367-407. Elsevier, Amsterdam.
55. Striker G. G., Insausti P., Grimoldi A. A. & León R. J. C. (2006) Root strength and trampling tolerance in the grass Paspalum dilatatum and the dicot Lotus glaber in flooded soil. Funct. Ecol. 20, 4-10.
56. Tepaske M., Powell R. & Clement S. (1993) Analyses of selected endophyte-infected grasses for the presence of Loline-type and ergot-type alkaloids. J. Agric. Food Chem. 41, 2299-303.
57. Thompson J. N. (2005) The Geographic Mosaic of Coevolution. University of Chigago Press, Chicago.
58. Uchitel A., Omacini M. & Chaneton E. J. (2011) Inherited fungal symbionts enhance establishment of an invasive annual grass across successional habitats. Oecologia 165, 465-75.
59. Wardle D. A., Bardgett R. D., Klironomos J. N., Setälä H., van der Putten W. H. & Wall D. H. (2004) Ecological linkages between aboveground and belowground biota. Science 304, 1629-33.
60. West S. A., Kiers E. T., Simms E. L. & Denison R. F. (2002) Sanctions and mutualism stability: Why do rhizobia fix nitrogen? Proc. R. Soc. B Biol. Sci. 269, 685-94.
61. White J. F. J. & Torres M. S. (2010) Is plant endophyte-mediated defensive mutualism the result of oxidative stress protection? Physiol. Plant. 138, 440-6.
62. Zuur A. F., Ieno E. N., Walker N. J., Saveliev A. A. & Smith G. M. (2009) Mixed Effects Models and Extensions in Ecology with R. Springer, New York.