Fungal endophytes associated with roots of nurse cushion species have positive effects on native and invasive beneficiary plants in an alpine ecosystem

Perspectives in Plant Ecology, Evolution and Systematics

Volumn 17, Issue 3, 2015, Pages 218-226

  Molina Montenegro, Marco A ^a   Oses, Rómulo ^a   Torres Díaz, Cristian ^b   Atala, Cristian ^c   Núñez, Martín A ^d   Armas, Cristina ^e  

^a Universidad Católica del Norte   (Chile)

^b UNIVERSIDAD DEL BÍO BÍO   (Chile)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE VALPARAÍSO   (Chile)

^d LABORATORIO ECOTONO   (Argentina)

^e DEPARTAMENTO DE BIOLOGÍA   (Chile)

Author keywords

Cushion plants; Endophytic fungi; Facilitation; Invasive species; Positive interactions; Taraxacum officinale

Indexed keywords

ALPINE ENVIRONMENT; BIOMASS; ENDOPHYTE; FACILITATION; FITNESS; FUNGUS; HERB; INOCULATION; INVASIVE SPECIES; MICROORGANISM; ROOT SYSTEM; SEED PRODUCTION;

ANDES; CHILE;

FUNGI; TARAXACUM OFFICINALE;

EID: 85010894660     PISSN: 14338319     EISSN: 16180437     Source Type: Journal    
DOI: 10.1016/j.ppees.2015.02.003     Document Type: Article

References (100)

1. Aly, A.H., et al. Fungal endophytes: unique plant inhabitants with great promises. Appl. Microbiol. Biotechnol. 90 (2011), 1829–1845.
2. Anthelme, F., Dangles, O., Plant–plant interactions in tropical alpine environments. Perspect. Plant Ecol. 14 (2012), 363–372.
3. Aschehoug, E.T., et al. Fungal endophyte increases the allelopathic effects of an invasive forb. Oecologia 175 (2014), 285–291.
4. Atala, C., et al. Impact of mycorrhizae and irrigation in the survival of seedlings of Pinus radiata D. Don subject to drought. Gayana Bot. 69 (2012), 296–304.
5. Auge, R.M., Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11 (2001), 3–42.
6. Badano, E.I., et al. Efectos de la planta en cojín Oreopolus glacialis (Rubiaceae) sobre la riqueza y diversidad de especies en una comunidad alto-andina de Chile central. Rev. Chil. Hist. Nat. 75 (2002), 757–765.
7. Bever, J.D., Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol. 157 (2003), 465–473.
8. Bever, J.D., et al. Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25 (2010), 468–478.
9. Booth, M.G., Hoeksema, J.D., Mycorrhizal networks counteract competitive effects of canopy trees on seedling survival. Ecology 91 (2010), 2294–2302.
10. Bruno, J.F., et al. Inclusion of facilitation into ecological theory. Trends Ecol. Evol. 18 (2003), 119–125.
11. Butterfield, B.J., et al. Alpine cushion plants inhibit the loss of phylogenetic diversity in severe environments. Ecol. Lett. 16:4 (2013), 478–486.
12. Callaway, R., Positive Interactions and Interdependence in Plant Communities. 2007, Springer-Verlag.
13. Callaway, R.M., Pugnaire, F.I., Facilitation in plant communities. Pugnaire, F.I., Valladares, F., (eds.) Handbook of Functional Plant Ecology, 2007, Dekker, Boca Raton, FL, 435–455.
14. Callaway, R.M., Aschehoug, E.T., Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290 (2000), 521–523.
15. Callaway, R.M., et al. Positive interactions among alpine plants increase with stress. Nature 417 (2002), 844–848.
16. Callaway, R.M., et al. Soil biota and exotic plant invasion. Nature 427 (2004), 731–733.
17. Callaway, R.M., et al. Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89 (2008), 1043–1055.
18. Callaway, R.M., et al. Effects of soil biota from different ranges on Robinia invasion: acquiring mutualists and escaping pathogens. Ecology 92 (2011), 1027–1035.
19. Casanova-Katny, M.A., et al. The best for the guest: high Andean nurse cushions of Azorella madreporica enhance arbuscular mycorrhizal status in associated plant species. Mycorrhiza 21 (2011), 613–622.
20. Cavieres, L.A., Arroyo, M.T.K., Soil seed banks in Phacelia secunda JF Gmelin (Hydrophyllaceae): altitudinal variation in the Andes of central Chile (33°S). Rev. Chil. Hist. Nat. 72 (1999), 569–577.
21. Cavieres, L.A., Badano, E.I., Do facilitative interactions increase species richness at the entire community level?. J. Ecol. 97 (2009), 1181–1191.
22. Cavieres, L.A., et al. Nurse effect of the native cushion plant Azorella monantha on the invasive non-native Taraxacum officinale in the high-Andes of central Chile. Perspect. Plant Ecol. 7 (2005), 217–226.
23. Cavieres, L.A., et al. Positive interactions between alpine plant species and the nurse cushion plant Laretia acaulis do not increase with elevation in the Andes of central Chile. New Phytol. 169 (2006), 59–69.
24. Cavieres, L.A., et al. Microclimatic modifications of cushion plants and their consequences for seedling survival of native and non-native herbaceous species in the high Andes of central Chile. Arct. Antarct. Alp. Res. 39 (2007), 229–236.
25. Cavieres, L.A., et al. Facilitation of the non-native Taraxacum officinale by native nurse cushion species in the high Andes of central Chile: are there differences between nurses?. Funct. Ecol. 22 (2008), 148–156.
26. Cavieres, L.A., et al. Facilitative plant interactions and climate simultaneously drive alpine plant diversity. Ecol. Lett. 17 (2013), 193–202.
27. Clay, K., Holah, J., Fungal endophyte symbiosis and plant diversity in successional fields. Science 285 (1999), 1742–1745.
28. Collado, J., et al. Fungal endophytes in leaves, twigs and bark of Quercus ilex from Central Spain. Nova Hedwig. 63 (1996), 347–360.
29. De Deyn, G.B., et al. Plant community development is affected by nutrients and soil biota. J. Ecol. 92 (2004), 824–834.
30. Dernoeden, P.H., McIntosh, M.S., Seasonal responses of perennial ryegrass as influenced by fungicides. HortScience 26 (1991), 1181–1183.
31. di Castri, F., Hajek, E., Bioclimatología de Chile. 1976, Ediciones de la Pontificia Universidad Católica de Chile, Santiago.
32. Drummond, A.J., et al. Geneious v5.4. 2011 http://www.geneious.com.
33. Fox, G.A., Failure time analysis: emergence, flowering, survivorship and other waiting times. Scheiner, S.M., Gurevitch, J., (eds.) Design and Analysis of Ecological Experiments, 1993, Oxford University Press, Oxford, 253–289.
34. Gibert, A., et al. Endophytic fungus fine-tunes the persistence strategy of its alpine host grass in response to soil resource levels. Oikos 122 (2012), 367–376.
35. Giovannetti, M., Mosse, B., An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol. 84 (1980), 489–500.
36. Harley, J.L., Smith, S.E., Mycorrhizal Symbiosis. 1983, Academic Press, London, 483.
37. Harris-Valle, C., et al. Tolerancia al estrés hídrico en la interacción planta-hongo micorrízico arbuscular: metabolismo energético y fisiología. Rev. Fitotéc. Mex. 32 (2009), 265–271.
38. Hayes, M.A., The Geomyces fungi: ecology and distribution. Bioscience 62 (2012), 819–823.
39. Hiatt, E.E., et al. Tall fescue endophyte detection: commercial immunoblot test kit compared with microscopic analysis. Crop Sci. 39 (1999), 796–799.
40. Jackson, D., et al. Indirect biological control of the coffee leaf rust, Hemileia vastatrix, by the entomogenous fungus Lecanicillium lecanii in a complex coffee agroecosystem. Biol. Control 61 (2012), 89–97.
41. Johnson, D., et al. The importance of individuals: intraspecific diversity of mycorrhizal plants and fungi in ecosystems. New Phytol. 194 (2012), 614–628.
42. Kardol, P., et al. Temporal variation in plant–soil feedback controls succession. Ecol. Lett. 9 (2006), 1080–1088.
43. Kardol, P., et al. Microbe-mediated plant–soil feedback in pioneer stages of secondary succession causes long-lasting historical contingency effects in plant community composition. Ecol. Monogr. 77 (2007), 147–162.
44. Kipfer, T., et al. Ectomycorrhiza succession patterns in Pinus sylvestris forests after stand-replacing fire in the Central Alps. Oecologia 167 (2011), 219–228.
45. Körner, C., Alpine Plant Life. 2003, Springer, Berlin.
46. Lewis, D.H., Symbiosis and mutualism: crisp concepts and soggy semantics. Boucher, D.H., (eds.) The Biology of Mutualism, 1985, Croom Helm Ltd., London, UK, 29–39.
47. Loreau, M., Microbial diversity, producer–decomposer interactions and ecosystem processes: a theoretical model. Proc. R. Soc. Biol. Sci. 268 (2001), 303–309.
48. Lozano, Y.M., Hortal, S., Armas, C., Pugnaire, F.I., Interactions among soil, plants, and microorganisms drive secondary succession in a dry environment. Soil Biol. Biochem. 78 (2014), 298–306.
49. Mangla, S., et al. Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J. Ecol. 96 (2008), 58–67.
50. Martínez-García, L.B., Pugnaire, F.I., Arbuscular mycorrhizal fungi host preference and site effects in two plant species in a semiarid environment. Appl. Soil Ecol. 48 (2011), 313–317.
51. Maxwell, K., Johnson, G.N., Chlorophyll fluorescence – a practical guide. J. Exp. Bot. 51 (2000), 659–668.
52. Meisner, A., et al. Soil biotic legacy effects of extreme weather events influence plant invasiveness. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 9835–9838.
53. Molenda, O., et al. The alpine cushion plant Silene acaulis as Foundation species: a bug's-eye view to facilitation and microclimate. PLoS ONE, 7, 2012, e37223.
54. Molina-Montenegro, M.A., et al. Cushion plants as microclimatic shelters for two ladybird beetles species in Alpine Zone of Central Chile. Arct. Antarct. Alp. Res. 38 (2006), 224–227.
55. Molina-Montenegro, M.A., et al. Positive interactions among plant species for pollinator service: assessing the magnet effect concept with invasive species. Oikos 117 (2008), 1833–1839.
56. Molina-Montenegro, M.A., et al. Functional differences in response to drought in the alpine invasive Taraxacum officinale from native and introduced habitat ranges. Plant Ecol. Divers. 4 (2011), 37–44.
57. Montesinos-Navarro, A., et al. The network structure of plant–arbuscular mycorrhizal fungi. New Phytol. 194 (2012), 536–547.
58. Newman, E.I., Mycorrhizal links between plants: their functioning and ecological significance. Adv. Ecol. Res. 18 (1988), 243–270.
59. Núñez, C.I., et al. When do nurse plants stop nursing? Temporal changes in water stress levels in Austrocedrus chilensis growing within and outside shrubs. J. Veg. Sci. 20 (2009), 1064–1071.
60. Núñez, M.A., et al. Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90 (2009), 2352–2359.
61. Ortega, U., et al. Effectiveness of mycorrhizal inoculation in the nursery on growth and water relations of Pinus radiata in different water regimes. Tree Physiol. 24 (2004), 65–73.
62. Pendergast, T.H., et al. Belowground biotic complexity drives aboveground dynamics: a test of the soil community feedback model. New Phytol. 197 (2013), 1300–1310.
63. Read, D.J., Development and function of mycorrhizal hyphae in soil. Sylvia, D.M., Hung, L.L., Graham, J.H., (eds.) Proceedings of the 7th North American Conference on Mycorrhizae, 1987, University of Florida, Gainesville, USA, 178–180.
64. Read, D.J., Mycorrhiza – the state of the art. Varma, A., Hock, B., (eds.) Mycorrhiza, 1999, Springer-Verlag, Berlin, 3–34.
65. Redman, R.S., et al. Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science, 298, 2002, 1581.
66. Redman, R.S., et al. Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS ONE, 6, 2011, e14823.
67. Reid, A.M., et al. A systematic review of the recent ecological literature on cushion plants: champions of plant facilitation. Web Ecol. 10 (2010), 44–49.
68. Reinhart, K.O., Callaway, R.M., Soil biota and invasive plants. New Phytol. 170 (2006), 445–457.
69. Reinhart, K.O., et al. Plant–soil biota interactions and spatial distribution of black cherry in its native and invasive ranges. Ecol. Lett. 6 (2003), 1046–1050.
70. Richardson, D.M., et al. Plant invasions – the role of mutualisms. Biol. Rev. 75 (2000), 65–93.
71. Rillig, M.C., et al. Interactive effects of root endophytes and arbuscular mycorrhizal fungi on an experimental plant community. Oecologia 174 (2014), 263–270.
72. Rodriguez, R.J., et al. Fungal endophytes: diversity and functional roles. New Phytol. 182 (2009), 314–330.
73. Rodriguez, R.J., et al. Adaptation and survival of plants in high stress habitats via fungal endophyte conferred stress tolerance. Symbioses Stress 17 (2010), 461–476.
74. Rodríguez-Echeverría, S., et al. A role for below-ground biota in plant–plant facilitation. J. Ecol. 101 (2013), 1420–1428.
75. Rosa, L.H., et al. Endophytic fungal community associated with the dicotyledonous plant Colobanthus quitensis (Kunth) Bartl (Caryophyllaceae) in Antarctica. FEMS Microbiol. Ecol. 73 (2010), 178–189.
76. Santibáñez, F., Uribe, M., Atlas Agroclimático de la V Región y Región Metropolitana. 1990, Ministerio de Agricultura, Santiago.
77. Sapp, J., The dynamics of symbiosis: an historical overview. Can. J. Bot. 82 (2004), 1046–1056.
78. SAS, Statistical Analysis System. 2003, SAS Institute, Cary, NC, USA.
79. Schöb, C., Variability in functional traits mediates plant interactions along stress gradients. J. Ecol. 101 (2013), 753–762.
80. Schöb, C., Consequences of facilitation: one plant's benefit is another plant's cost. Funct. Ecol. 28 (2014), 500–508.
81. Schöb, C., et al. Foundation species influence trait-based community assembly. New Phytol. 196 (2012), 824–834.
82. Schulz, B., Boyle, C., The endophytic continuum. Mycol. Res. 109 (2005), 661–686.
83. Selosse, M.-A., Mycorrhizal networks: des liaisons dangereuses?. Trends Ecol. Evol. 21 (2006), 621–628.
84. Shah, M.A., et al. Arbuscular mycorrhizas: drivers or passengers of alien plant invasion. Bot. Rev. 75 (2009), 397–417.
85. Sikes, B.A., et al. Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J. Ecol. 97 (2009), 1274–1280.
86. Simberloff, D., Von Holle, B., Positive interactions of nonindigenous species: invasional meltdown?. Biol. Invasions 1 (1999), 21–32.
87. Smith, S.E., Read, D.J., Mycorrhizal Symbiosis. third ed., 2010, Academic Press, London, UK.
88. Spiering, M.J., et al. Gene clusters for insecticidal loline alkaloids in the grass-endophytic fungus Neotyphodium uncinatum. Genetics 169 (2005), 1403–1414.
89. Tedersoo, L., et al. Revisiting ectomycorrhizal fungi of the genus Alnus: differential host specificity, diversity and determinants of the fungal community. New Phytol. 182 (2009), 727–735.
90. van der Heijden, M.G.A., et al. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11 (2008), 296–310.
91. van der Heijden, M.G.A., Horton, T.R., Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J. Ecol. 97 (2009), 1139–1150.
92. Van der Putten, W.H., Peters, B.A.M., How soil-borne pathogens may affect plant competition. Ecology 78 (1997), 1785–1795.
93. Van der Putten, W.H., A multitrophic perspective on functioning and evolution of facilitation in plant communities. J. Ecol. 97 (2009), 1131–1138.
94. Van der Putten, W.H., et al. Plant-soil feedback: the past, the present and future challenges. J. Ecol. 101 (2013), 265–276.
95. Vandenkoornhuyse, P., et al. Extensive fungal diversity in plant roots. Science, 295, 2002, 2051.
96. Vilà, M., Weiner, J., Are invasive plant species better competitors than native plant species? – Evidence from pairwise experiments. Oikos 105 (2004), 229–238.
97. Vos, C., et al. Arbuscular mycorrhizal fungi reduce root-knot nematode penetration through altered root exudation of their host. Plant Soil 354 (2012), 335–345.
98. Wagg, C., Bender, S.F., Widmer, F., van der Heijden, M.G.A., Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc. Natl. Acad. Sci. U. S. A. 111 (2014), 5266–5270.
99. Wardle, D.A., et al. Ecological linkages between aboveground and belowground biota. Science 304 (2004), 1629–1633.
100. Wright, A., et al. Living close to your neighbors – the importance of both competition and facilitation in plant communities. Ecology 95 (2014), 2213–2223.