Abstract
Aims
The arbuscular mycorrhizal symbiosis is a widespread symbiosis in terrestrial biomes with functional implications for the ecology of both plants and soil organisms. We here asked whether phylogenetic host specificity (PHS) in arbuscular mycorrhizal (AM) fungal communities exists.
Methods
Data were retrieved from the online database MaarjAM and AM fungal sequences were clustered into taxa to allow us to compute community similarity indices. The phylogenetic reconstruction of the plant hosts allowed us to obtain an objective index of host relatedness. PHS was assessed through mixed effects linear models with community similarity as dependent variable, host relatedness as independent variable and with ecosystem type as covariate.
Results
To our surprise not only did we not find evidence of PHS, but we detected evidence that more closely related plants hosted more dissimilar AM fungal communities. Results differed for different ecosystems.
Conclusions
We highlight the importance of ecosystem type when assessing PHS. Moreover, we argue for potential causes of the unique PHS patterns that are detected in the AM association.
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References
Adams DC, Gurevitch J, Rosenberg MS (1997) Resampling tests for meta-analysis of ecological data. Ecology 78:1277–1283
Akashi H (1997) Codon bias evolution in Drosphila. Population genetics of mutation-selection drift. Gene 205:269–278
Alguacil MM, Lumini E, Roldan A, Salinas-Garcia JR, Bonfante P, Bianciotto V (2008) The impact of tillage practices on arbuscular mycorrhizal fungal diversity in subtropical crops. Ecol Appl 18:527–536
Alguacil MM, Roldan A, Torres MP (2009) Assessing the diversity of AM fungi in arid gypsophilous plant communities. Environ Microbiol 11:2649–2659
Alguacil MM, Torrecillas E, Caravaca F, Fernandez DA, Azcon R, Roldan A (2011) The application of an organic amendment modifies the arbuscular mycorrhizal fungal communities colonizing native seedlings grown in a heavy-metal-polluted soil. Soil Biol Biochem 43:1498–1508
Alguacil MM, Torrecillas E, Roldan A, Diaz G, Torres MP (2012) Perennial plant species from semiarid gypsum soils support higher AMF diversity in roots than the annual Bromus rubens. Soil Biol Biochem 49:132–138
Angelard C, Colard A, Niculita-Hirzel H, Croll D, Sanders IR (2010) Segregation in a mycorrhizal fungus alters rice growth and symbiosis-specific gene transcription. Curr Biol 20:1216–1221
Butcher M, Wegmüller S, Drissner D (2009) Chasing the structures of small molecules in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 12:500–507
Cadotte MW, Strauss SY (2011) Phylogenetic patterns of colonization and extinction in experimentally assempled plant communities. PLoS One 6:e19363
Caruso T, Rillig MC, Garlaschelli D (2012) On the application of network theory to arbuscular mycorrhizal fungi–plant interactions: the importance of basic assumptions. New Phytol 194:891–894
Chao A, Chazdon RL, Colwell RK, Shen TJ (2006) Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 62:361–371
Chase JM, Myers JA (2011) Disentangling the importance of ecological niches from stochastic processes across scales. Philos Trans R Soc Lond B Biol Sci 366:2351–2363
Cooper N, Griffin R, Franz M, Omotayo M, Nunn CL (2012) Phylogenetic host specificity and understanding parasite sharing in primates. Ecol Lett 15:1370–1377
Davison J, Öpik M, Daniell TJ, Moora M, Zobel M (2011) Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiol Ecol 78:103–115
Douhan GW, Petersen C, Bledsoe CS, Rizzo DM (2005) Contrasting root associated fungi of three common oak-woodland plant species based on molecular identification: host specificity or non-specific amplification? Mycorrhiza 15:365–372
Drummond A, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgason T (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804
Dunlap PV, Ast JC, Kimura S, Fukui A, Yoshino T, Endo H (2007) Phylogenetic analysis of host-symbiont specificity and codivergence in bioluminescent symbiosis. Cladistics 23:507–532
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high through put. Nucleic Acids Res 32:1792–1797
Edgar RC (2011) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608
Embar K, Kotler BP, Mukherjee S (2011) Risk management in optimal foragers: the effect of sightlines and predator type of patch use, time allocation, and vigilance in gerbils. Oikos 120:1657–1666
Eom AH, Hartnett DC, Wilson GWT (2000) Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122:435–444
Gilbert GS, Webb CO (2007) Phylogenetic signal in plant pathogen—host range. Proc Natl Acad Sci U S A 104:4979–4983
Gómez JM, Verdú M, Perdectti F (2010) Ecological interactions are evolutionarily conserved across the entire tree of life. Nature 465:918–921
Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823
Gribaldo S, Philippe H (2002) Ancient phylognetic relationships. Theor Popul Biol 61:391–408
Hammer EC, Pallon J, Wallander H, Olsson PA (2011) Tit for tat? A mycorrhizal fungus accumulates P under low plant C availability. FEMS Microbiol Ecol 76:236–244
Hartmann S, Vision TJ (2008) Using ESTs for phylogenomics: can one accurately infer a phylogenetic tree from a gappy alignment? BMC Evol Biol 8:95
Helgason T, Daniell T, Husband R, Fitter AH, Young JPW (1998) Ploughing up the worldwide web? Nature 394:431
Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384
Hoeksema JD, Forde SE (2008) A meta-analysis of factors affecting local adaptation between interacting species. Am Nat 171:275–290
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabiski C, Bever JD, Moore JC et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407
Husband R, Herre EA, Turner SL, Gallery R, Young JPW (2002) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Mol Ecol 11:2669–2678
Jacquemyn H, Merckx V, Brys R, Tytec D, Cammue BPA, Honnay O, Lievens B (2011) Analysis of network architecture reveals phylogenetic constraints on mycorrhizal specificity in the genus Orchis (Orchidaceae). New Phytol 192:518–528
Jansen RK, Cal Z, Raubeson LA, Daniell H, de Pamphills CW, Leebens-Mack J, Müller KF, Guisinger-Bellian M, Haberle RC, Hansen AK, Chumley TW, Lee SB, Peery R, McNeal JR, Kuehl JV, Boore JL (2007) Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. Proc Natl Acad Sci U S A 49:19369–19374
Kawakita A, Okamoto T, Goto R, Kato M (2010) Mutualism favours higher host specificity than does antagonism in plant-herbivore interaction. Proc R Soc Lond B Biol Sci 277:2765–2774
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum C, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882
Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol 168:189–204
Lekberg Y, Koide R, Pohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105
Lekberg Y, Schnoor T, Kjøller R, Gibbons SM, Hansen LH, Al-Soud WA, Sørensen SJ, Rosendahl S (2012) 454-sequencing reveals stochastic local reassembly and high disturbance tolerance within arbuscular mycorrhizal fungal communities. J Ecol 100:151–160
Liu Y, He J, Shi G, An L, Opik M, Feng H (2011) Diverse communities ofarbuscular mycorrhizal fungi inhabit sites with very high altitude in Tibet Plateau. FEMS Microbiol Ecol 78:355–365
Macek I, Dumbrell AJ, Nelson M, Fitter AH, Vodnik D, Helgason T (2011) Local adaptation to soil hypoxia determines the structure of an arbuscular mycorrhizal fungal community in roots from natural CO2 springs. Appl Environ Microbiol 77:4770–4777
McIntosh ME (2002) Flowering phenology and reproductive output in two sister species of Ferocasctus. Plant Ecol 159:1–13
Montesinos-Navarro A, Segarra-Moragues JG, Valiente-Banuet A, Verdú M (2012) Plant facilitation occurs between species differing in their associated arbuscular mycorrhizal fungi. New Phytol 196:835–844
Mooney KA, Halitschke R, Kessler A, Agrawal AA (2010) Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science 327:1642–1644
Nava S, Guglielmone AA (2013) A meta-analysis of host specificity in Neotropical hard ticks (Acari: Ixodidae). Bull Entomol Res 103:216–224
O’Brien HE, Miadlikowska J, Lutzoni F (2005) Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungus Peltigera. Eur J Phycol 40:363–378
Öpik M, Moora M (2012) Missing nodes and links in mycorrhizal networks. New Phytol 194:304–306
Öpik M, Moora M, Liira J, Zobel M (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol 94:778–790
Öpik M, Moora M, Zobel M, Saks U, Wheatley R, Wright F, Daniell T (2008) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Phytol 179:867–876
Öpik M, Metsis M, Daniell T, Zobel M, Moora M (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184:424–437
Orrock JL, Watling JI (2010) Local community size mediates ecological drift and competition in metacommunities. Proc R Soc Lond B Biol Sci 277:2185–2191
Pendergast TH, Burke DJ, Carson WP (2013) Belowground biotic complexity drives aboveground dynamics: a test of the soil community feedback model. New Phytol 197:1300–1310
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princenton
Poulin R, Krasnov BR, Mouillot D (2011) Host specificity in phylogenetic and geographical space. Trends Parasitol 27:355–361
Powell JR, Monaghan MT, Öpik M, Rillig MC (2011) Evolutionary criteria outperform operational approaches in producing ecologically-relevant fungal species inventories. Mol Ecol 20:655–666
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process, and rate. Syst Biol 57:591–601
Sanchez-Castro I, Ferrol N, Barea JM (2012) Analyzing the community composition of arbuscular mycorrhizal fungi colonizing the roots of representative shrubland species in a Mediterranean ecosystem. J Arid Environ 80:1–9
Santos-Gonzalez JC, Finlay RD, Tehler A (2007) Seasonal dynamics of arbuscular mycorrhizal fungal communities in roots in a seminatural grassland. Appl Environ Microbiol 73:5613–5623
Scheublin TR, Ridgway KP, Young JPW, van der Heijden MG (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246
Small RL, Cronn RC, Wendel JF (2004) Use of nuclear genes for phylogeny reconstruction of plants. Aust Syst Bot 17:145–170
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Elsevier Science Ltd., London
Stoll P, Prati D (2001) Intraspecific aggregation alters competitive interactions in experimental plant communities. Ecology 82:319–327
Sukumaran J, Holder MT (2010) DendroPy: a python library for phylogenetic computing. Bioinformatics 26:1569–1571
Sykorova Z, Ineichen K, Wiemken A, Redecker D (2007) The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18:1–14
Torrecillas E, Alguacil MM, Roldan A (2012) Host preferences of arbuscular mycorrhizal fungi colonizing annual herbaceous plant species in semiarid mediterranean prairies. Appl Environ Microbiol 78:6180–6186
Valiente-Banuet A, Verdú M (2008) Temporal shifts from facilitation to competition occur between closely related taxa. J Ecol 96:489–494
van der Heijden MGA (2004) Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol Lett 7:293–303
Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck JM, Fitter AH, Young JPW (2002) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11:1555–1564
Veresoglou SD, Halley JM (2012) A model that explains diversity patterns of arbuscular mycorrhizas. Ecol Model 231:146–152
Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8:214–217
Wilde P, Manal A, Stodden M, Sieverding E, Hildebrandt U, Bothe H (2009) Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environ Microbiol 11:1548–1561
Wubet T, Kottke I, Teketay D, Oberwinkler F (2009) Arbuscular mycorrhizal fungal community structures differ between co-occurring tree species of dry Afromontane tropical forest, and their seedlings exhibit potential to trap isolates suited for reforestation. Mycol Prog 8:317–328
Yamato M, Ikeda S, Iwase K (2008) Community of arbuscular mycorrhizal fungi in a coastal vegetation on Okinawa island and effect of the isolated fungi on growth of sorghum under salt treated conditions. Mycorrhiza 18:241–249
Acknowledgments
We thank Dr Jeff Powell for advice with phylogenetic methods. SDV was supported by a Marie Curie fellowship.
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Veresoglou, S.D., Rillig, M.C. Do closely related plants host similar arbuscular mycorrhizal fungal communities? A meta-analysis. Plant Soil 377, 395–406 (2014). https://doi.org/10.1007/s11104-013-2008-2
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DOI: https://doi.org/10.1007/s11104-013-2008-2