Grass-endophyte symbiosis: A neglected aboveground interaction with multiple belowground consequences

Applied Soil Ecology

Volumn 61, Issue , 2012, Pages 273-279

  Omacini, Marina ^a   Semmartin, Maria ^a   Pérez, Luis I ^a   Gundel, Pedro E ^a,b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b FINNISH FOREST RESEARCH INSTITUTE   (Finland)

Author keywords

AM fungi; Mutualism; Neotyphodium endophytes; Soil biota; Soil processes

Indexed keywords

BACTERIA (MICROORGANISMS); CLAVICIPITACEAE; FUNGI; NEOTYPHODIUM; POACEAE;

EID: 84865854217     PISSN: 09291393     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.apsoil.2011.10.012     Document Type: Article

References (85)

1. Antunes P., Miller J., Carvalho L., Klironomos J.N., Newman J. Even after death the endophytic fungus of Schedonorus phoenix reduces the arbuscular mycorrhizas of other plants. Funct. Ecol. 2008, 22:912-918.
2. Bacon C.W., Hill N.S. Neotyphodium/Grass Interactions 1997, Plenum, NY.
3. Belesky D.P., Fedders J.M. Tall fescue development in response to Acremonium coenophialum and soil acidity. Crop Sci. 1995, 35:529-533.
4. Bever J.D. Feedback between plants and their soil communities in an old field community. Ecology 1994, 75:1965-1977.
5. Brundrett M.C. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 2009, 320:37-77.
6. Casas C., Omacini M., Montecchia M., Correa O. Soil microbial community responses to the fungal endophyte Neotyphodum in Italian ryegrass. Plant Soil 2010, 340:347-355.
7. Cheplick G.P., Faeth S. Ecology and Evolution of the Grass-Endophyte Symbiosis 2009, Oxford University Press.
8. Chu-Chou M., Guo B., An Z.Q., Hendrix J.W., Ferriss R., Siegel D.I., Dougherty C., Burrus P. Suppression of mycorrhizal fungi in fescue by the Acremonium coenophialum endophyte. Soil Biol. Biochem. 1992, 24:633-637.
9. Clay K. Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 1988, 69:10-16.
10. Clay K., Holah J. Fungal endophyte symbiosis and plant diversity in successional fields. Science 1999, 285:1742-1744.
11. Clay K., Schardl C.L. Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am. Midl. Nat. 2002, 160:99-127.
12. Coleman D.C., Crossley D.A., Hendrix P.F. Fundamentals of Soil Ecology 2004, Elsevier Academic Press, San Diego. 2nd ed.
13. Cook R., Lewis G.C. Fungal endophytes and nematodes of agricultural and amenity grasses. Biotic Interactions in Plant-Pathogen Associations 2001, 35-61. CABI Publishing, Wallingford. M.J. Jeger, N.J. Spence (Eds.).
14. Cook R., Lewis G.C., Mizen K.A. Effects on plant-parasitic nematodes of infection of perennial ryegrass, Lolium perenne, by the endophytic fungus, Acremonium lolii. Crop Prot. 1991, 10:403-407.
15. Davitt A.J., Chen C., Rudgers J.A. 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. 2011, 71:137-145.
16. De Battista J.P., Bouton J.H., Bacon C.W., Siegel M.C. Rhizome and herbage production of endophyte-removed tall fescue clones and populations. Agron. J. 1990, 82:651-654.
17. Douglas A. The Symbiotic Habit 2010, Princeton University Press, Princeton, NJ.
18. Easton H. Grasses and Neotyphodium endophytes: co-adaptation and adaptative breeding. Euphytica 2007, 154:295-306.
19. Eerens J.P.J., Lucas R.J., Easton H.S., White J.G.H. Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool-moist environment. III. Interaction with white clover. N. Z. J. Agric. Res. 1998, 41:201-207.
20. Eerens J.P.J., Visker M.H.P.W., Lucas R.J., Easton H.S., White J.G.H. Influence of the ryegrass endophyte (Neotyphodium lolii) in a cool moist environment. IV. Plant parasitic nematodes. N. Z. J. Agric. Res. 1998, 41:209-217.
21. Elmi A.A., West C.P., Robbins R.T., Kirkpatrick T.L. Endophyte effects on reproduction of a root-knot nematode (Meloidogyne marylandi) and osmotic adjustment in tall fescue. Grass Forage Sci. 2000, 55:166-172.
22. Faeth S.H., Helander M.L., Saikkonen K.T. Asexual Neotyphodium endophytes in a native grass reduce competitive abilities. Ecol. Lett. 2004, 7:304-313.
23. Franzluebbers A.J. Short-term responses of soil C and N fractions to tall fescue endophyte infection. Plant Soil 2006, 282:153-164.
24. Franzluebbers A.J., Hill N.S. Soil carbon, nitrogen, and ergot alkaloids with short- and long-term exposure to endophyte-infected and endophyte-free tall fescue. Soil Sci. Soc. Am. J. 2005, 69:404-412.
25. Franzluebbers A.J., Nazih N., Stuedemann J.A., Fuhrmann J.J., Shomberg H.H., Hartel P.G. Soil carbon and nitrogen pools under low- and high-endophyte-infected tall fescue. Soil Sci. Soc. Am. J. 1999, 63:1687-1694.
26. Franzluebbers A.J., Stuedemann J.A. Soil carbon and nitrogen pools in response to tall fescue endophyte infection, fertilization, and cultivar. Soil Sci. Soc. Am. J. 2005, 69:396-403.
27. Freeman E.M. The seed fungus of Lolium temulentum L., the darnel. Philos. Trans. Royal Soc. Lond. Ser. B 1904, 196:1-27.
28. Glenn A., Bacon C., Price R., Hanlin R. Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 1996, 88:369-383.
29. Guo B., Hendrix J., An Z., Ferriss R. Role of Acremonium endophyte of Fescue on inhibition of colonization and reproduction of mycorrhizal fungi. Mycologia 1992, 84:882-885.
30. Hartley S., Gange A.C. Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu. Rev. Entomol. 2009, 54:323-342.
31. Hedges L.V., Olkin I. Statistical Methods for Meta-Analysis 1985, Academic Press, Orlando, FL.
32. Heil M. Plant-mediated interactions between above- and below-ground communities at mutliple trophic levels. J. Ecol. 2011, 99:2-6.
33. Humphries S.S., Gwinn K.D., Stewart A.J. Effects of endophyte status of tall fescue tissues on the earthworm (Eisenia fetida). Environ. Toxicol. Chem. 2001, 20:1346-1350.
34. Iannone L.J., Cabral D., Schardl C.L., Rossi M.S. Phylogenetic divergence, morphological and physiological differences distinguish a new Neotyphodium endophyte species in the grass Bromus auleticus from South America. Mycologia 2009, 101:340-351.
35. Iannone L., White J., Giussani L., Cabral D., Novas M.V. Diversity and distribution of Neotyphodium-infected grasses in Argentina. Mycol. Progr. 2011, 10:9-19.
36. Johnson M.T.J. Evolutionary ecology of plant defences against herbivores. Funct. Ecol. 2011, 25:305-311.
37. Kannadan S., Rudgers J.A. Endophyte symbiosis benefits a rare grass under low water availability. Funct. Ecol. 2008, 22:706-713.
38. Kiers T., Palmer T.M., Ives A.R., Bruno J.F., Bronstein J.L. Mutualisms in a changing world: an evolutionary perspective. Ecol. Lett. 2010, 13:1459-1474.
39. Kimmons C.A., Gwinn K.D., Bernard E.C. Nematode reproduction on endophyte-infected and endophyte-free tall fescue. Plant Dis. 1990, 74:757-761.
40. Larimer A.L., Bever J.D., Clay K. The interactive effect of plant microbial symbionts: a review and meta-anlysis. Symbiosis 2010, 51:139-148.
41. Lehtonen P., Helander M., Saikkonen K. Are endophyte-mediated effects on herbivores conditional on soil nutrients?. Oecologia 2005, 142:38-45.
42. Lemons A., Clay K., Rudgers J.A. Connecting plant-microbial interactions above and belowground: a fungal endophyte affects decomposition. Oecologia 2005, 145:595-604.
43. Mack K., Rudgers J. Balancing multiple mutualists: asymmetric interactions among plants, arbuscular mycorrhizal fungi and fungal endophytes. Oikos 2008, 117:310-320.
44. Malinowski D.P., Zuo H., Belesky D.P., Alloush G.A. Evidence for copper binding by extracellular root exudates of tall fescue but not perennial ryegrass infected with Neotyphodium spp. endophytes. Plant Soil 2004, 267:1-12.
45. Malinowski D.A., Alloush G.A., Belesky D.P. Evidence for chemical changes on the root surface of tall fescue in response to infection with the fungal endophyte Neotyphodium coenophialum. Plant Soil 1998, 205:1-12.
46. Malinowski D.P., Belesky D.P. Adaptations of endophyte-infected cool-season grasses to environmental stresses: mechanisms of drought and mineral stress tolerance. Crop Sci. 2000, 40:923-940.
47. Malinowski D.P., Belesky D.P. Ecological importance of Neotyphodium spp. grass endophytes in agroecosystems. Grassland Sci. 2006, 52:1-14.
48. Matthews J.W., Clay K. Influence of fungal endophyte infection on plant/soil feedback and community interactions. Ecology 2001, 82:500-509.
49. Moon C.D., Scott B., Schardl C.L., Christensen M.J. Evolutionary origins of Epichloë endophytes from annual ryegrasses. Mycologia 2000, 92:1103-1118.
50. Müller J. Artificial infection by endophytes affects growth and mycorrhizal colonization of Lolium perenne. Funct. Plant Biol. 2003, 30:419-424.
51. Novas M.V., Cabral D., Godeas A.M. Interaction between grass endophytes and mycorrhizas in Bromus setifolius from Patagonia, Argentina. Symbiosis 2005, 40:23-30.
52. Novas M.V., Iannone L., Godeas A., Cabral D. Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass. Mycol. Progr. 2009, 8:75-81.
53. Omacini M., Chaneton E.J., Ghersa C.M., Muller C.B. Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 2001, 409:78-81.
54. Omacini M., Chaneton E., Bush L., Ghersa C.M. A fungal endosymbiont affects host plant retruitment through seed- and litter-mediated mechanisms. Funct. Ecol. 2009, 23:1148-1156.
55. Omacini M., Chaneton E., Ghersa C.M., Otero P. Do foliar endophytes affect grass litter decomposition?. A microcosm approach using Lolium multiflorum. Oikos 2004, 104:581-590.
56. Omacini M., Chaneton E.J., Ghersa C.M. A framework for understanding the ecosystem consequences of endophyte grass symbioses. Neotyphodium in Cool-season Grasses Current Research & Applications 2005, 141-161. Blackwell Publishing. C. Roberts, C.P. West, D. Spiers (Eds.).
57. Omacini M., Eggers T., Bonkowsky M., Gange A., Jones T.H. Leaf endophytes affect mycorrhizal status and growth of co-infected and neighbouring plants. Funct. Ecol. 2006, 20:226-232.
58. Pedersen J., Rodriguez-kabana R., Shelby R. Ryegrass cultivars and endophyte in tall fescue affect nematodes in grass and succeeding soybean. Agron. J. 1988, 80:811-814.
59. Pennell C.G.L., Popay A.J., Ball O.J.P., Hume D.E., Baird D.B. Occurrence and impact of pasture mealybug (Balanococcus poae) and root aphid (Aploneura lentisci) on ryegrass (Lolium spp.) with and without infection by Neotyphodium fungal endophytes. N. Z. J. Agric. Res. 2005, 48:329-337.
60. Ponce M.A., Bompadre M.J., Scervino J.M., Ocampo J.A., Chaneton E.J., Godeas A.M. Flavonoids, benzoic acids and cinnamic acids isolated from shoots and roots of Italian rye grass (Lolium multiflorum Lam.) with and without endophyte association and arbuscular mycorrhizal fungus. Biochem. Syst. Ecol. 2009, 37:245-253.
61. Popay A., Gerard P.J. Cultivar and endophyte effects on a root aphid. Aploneura lentisci, in perennial ryegrass. N. Z. Plant Prot. 2007, 60:223-227.
62. Popay A.I., Bonos S.A. Biotic responses in endophytic grasses. Neotyphodium in Cool-season Grasses Current Research & Applications 2005, 163-185. Blackwell Publishing. C. Roberts, C.P. West, D. Spiers (Eds.).
63. Popay A.J., Jensen J.G. Soil biota associated with endophyte-infected tall fescue in the field. N. Z. Plant Prot. 2005, 58:117-121.
64. Rasmussen S., Parsons A., Poppy A., Xue H., Newman J. Plant-endophyte-herbivore interactions: more than just alkaloids?. Plant Signal. Behav. 2008, 3:974-977.
65. Ren A.Z., Gao Y.B., Wang W., Wang J.L., Zhao N.X. Influence of nitrogen fertilizer and endophyte infection on ecophysiological parameters and mineral element content of perennial ryegrass. J. Integr. Plant Biol. 2009, 51:75-83.
66. Ren A., Li C., Gao Y. Endophytic fungus improves growth and metal uptake of Lolium arundinaceum Darbyshire Ex. Schreb. Int. J. Phytorem. 2011, 13:233-243.
67. Rodriguez R., White J., Arnold A., Redman R. Fungal endophytes: diversity and functional roles. New Phytol. 2009, 182:314-330.
68. Rosenberg M.S. The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 2005, 59:464-468.
69. Rosenberg M.S., Adams D.C., Gurevitch J. MetaWin: Statistical Software for Meta-Analysis, Version 2.0 2000, Sinauer Associates, Sunderland.
70. Rudgers J., Clay K. Endophyte symbiosis with tall fescue: how strong are the impacts on communities and ecosystems?. Fungal Biol. Rev. 2007, 21:107-124.
71. Rudgers J., Orr S. Non-native grass alters growth of native tree species via leaf and soil microbes. J. Ecol. 2009, 97:247-255.
72. Saikkonen K., Lehtonen P., Helander M., Koricheva J., Faeth S. Model systems in ecology: dissecting the endophyte-grass literature. Trends Plant Sci. 2006, 11:428-433.
73. Siegrist J., Mcculley R., Bush L., Phillips T. Alkaloids may not be responsible for endophyte-associated reductions in tall fescue decomposition rates. Funct. Ecol. 2010, 24:460-468.
74. Steinkellner S., Lendzemo V., Langer I., Schweiger P., Khaosaad T., Toussaint J.P., Vierheilig H.M. Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 2007, 12:1290-1306.
75. Tikhonovich I., Provorov N. Cooperation of plants and microorganisms: getting closer to the genetic construction of sustainable agro-systems. Biotechnology 2007, 2:833-848.
76. Van der Heijden M.G.A., Sanders I.R. Mycorrhizal Ecology: synthesis and perspectives. Mycorrhizal Ecology 2002, 441-456. Springer-Verlag, Berlin, Heidelberg. M.G.A. Van der Heijden, I.R. Sanders (Eds.).
77. van der Putten W.H., Bardgett R.D., De Ruiter P.C., Hol W., Meyer K., Bezemer T., Bradford M., Christensen S., Eppinga M., Fukami T., Hemerik L., Molofsky J., Schadler M., Scherber C., Strauss S.Y., Vos M., Wardle D.A. Empirical and theorical challenges in aboveground-belowground ecology. Oecologia 2009, 161:1-14.
78. van Hecke M., Treonis A., Kaufman J. How does the fungal endophyte Neotyphodium coenophialum affect tall fescue (Lolium arundinacea) rhizodeposition and soil microorganisms?. Plant Soil 2005, 275:101-109.
79. Vicari M., Hatcher P., Ayres A. Combined efect of foliar and mycorrhizal endophytes on an insect herbivore. Ecology 2002, 83:2452-2464.
80. Vila Aiub M.M., Ghersa C.M., Carceller M. Effect of herbicide diclofop-methyl on proton extrusion from Lolium multiflorum seedlings differing in resistance and in fungal endophyte (Neotyphodium sp.) infection. Phys. Planta. 2003, 119:429-439.
81. Wardle D. Communities and Ecosystems: Linking the Aboveground and Belowground Components 2002, Princeton University press.
82. Wardle D., Bardgett R., Klironomos J., Setala H., Van der Putten W.H., Wall D. Ecological linkages between aboveground and belowground biota. Science 2004, 304:1629-1633.
83. West C.P., Izekor E., Oosterhuis D.M., Robbins R.T. The effect of Acremonium coenophialum on the growth and nematode infestation of tall fescue. Plant Soil 1988, 112:3-6.
84. White J.F. Widespread distribution of endophytes in the Poaceae. Plant Dis. 1987, 71:340-342.
85. White J.F., Torres M. Defensive Mutualism in Microbial Symbiosis 2009, CRC Press/Taylor and Francis Group, Boca Raton.