Land-use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants

New Phytologist

Volumn 205, Issue 4, 2015, Pages 1577-1586

  Vályi, Kriszta ^a,b   Rillig, Matthias C ^a,b   Hempel, Stefan ^a,b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b BERLIN BRANDENBURG INSTITUTE OF ADVANCED BIODIVERSITY RESEARCH BBIB   (Germany)

Author keywords

Arbuscular mycorrhizal fungi (AMF); Community ecology; Glomeromycota; Host plant identity; Land use; Massively parallel multitag pyrosequencing; Mycorrhiza

Indexed keywords

ABUNDANCE; ARBUSCULAR MYCORRHIZA; COMMUNITY STRUCTURE; COMPETITION (ECOLOGY); FUNGUS; GRASSLAND; HOST PLANT; LAND USE CHANGE;

FUNGI; GLOMEROMYCOTA;

BIODIVERSITY; DNA SEQUENCE; ECOSYSTEM; GERMANY; GLOMEROMYCOTA; GRASSLAND; MICROBIOLOGY; MYCORRHIZA; PHYSIOLOGY; PLANT; PLANT ROOT; SPECIES DIFFERENCE; SYMBIOSIS;

BIODIVERSITY; ECOSYSTEM; GERMANY; GLOMEROMYCOTA; GRASSLAND; MYCORRHIZAE; PLANT ROOTS; PLANTS; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; SYMBIOSIS;

EID: 84922814218     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13236     Document Type: Article

References (75)

1. Allen MF. 1987. Re-establishment of mycorrhizas on Mount St Helens: migration vectors. Transactions of the British Mycological Society 88: 413-417.
2. Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32-46.
3. Atmar W, Patterson BD. 1993. The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96: 373-382.
4. Barto K, Rillig MC. 2010. Does herbivory really suppress mycorrhiza? A meta-analysis. Journal of Ecology 98: 745-753.
5. Becklin KM, Hertweck KL, Jumpponen A. 2012. Host identity impacts rhizosphere fungal communities associated with three alpine plant species. Microbial Ecology 63: 682-693.
6. Berry D, Ben Mahfoudh K, Wagner M, Loy A. 2011. Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Applied and Environmental Microbiology 77: 7846-7849.
7. Bethlenfalvay GJ, Dakessian S. 1984. Grazing effects on mycorrhizal colonization and floristic composition of the vegetation on a semiarid range in northern Nevada. Journal of Range Management 37: 312-316.
8. Bik HM, Porazinska DL, Creer S, Caporaso JG, Knight R, Thomas WK. 2012. Sequencing our way towards understanding global eukaryotic biodiversity. Trends in Ecology & Evolution 27: 233-243.
9. Blüthgen N, Dormann C, Prati D, Klaus VH, Kleinebecker T, Hölzel N, Alt F, Boch S, Gockel S, Hemp A et al. 2012. A quantitative index of land-use intensity in grasslands: integrating mowing, grazing and fertilization. Basic and Applied Ecology 13: 207-220.
10. Borsch T, Quandt D. 2009. Mutational dynamics and phylogenetic utility of noncoding chloroplast DNA. Plant Systematics and Evolution 282: 169-199.
11. Bowyer P. 1999. Plant disease caused by fungi. In: Oliver RP, Schweizer M, eds. Molecular fungal biology. Cambridge, UK: University Press, 301.
12. Camenzind T, Hempel S, Homeier J, Horn S, Velescu A, Wilcke W, Rillig MC. 2014. Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Global Change Biology 20: 3546-3659.
13. Daniell TJ, Husband R, Fitter AH, Young JPW. 2001. Molecular diversity of arbuscular mycorrhizal fungi colonising arable crops. FEMS Microbiology Ecology 36: 203-209.
14. Davison J, Öpik M, Daniell TM, Moora M, Zobel M. 2011. Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. FEMS Microbiology Ecology 78: 103-115.
15. Dormann CF, Gruber B, Fruend J. 2008. Introducing the bipartite package: analysing ecological networks. R News 8: 8-11.
16. Douds DD, Galvez L, Janke RR, Wagoner P. 1995. Effect of tillage and farming system upon populations and distribution of vesicular-arbuscular mycorrhizal fungi. Agriculture Ecosystems & Environment 52: 111-118.
17. Douds DD, Millner PD. 1999. Biodiversity of arbuscular mycorrhizal fungi in agroecosystems. Agriculture Ecosystems & Environment 74: 77-93.
18. Dray S. 2013. spacemakeR: spatial modelling. R package version 0.0-5/r113. [WWW document] URL http://R-Forge.R-project.org/projects/sedar [accessed 6 February 2013].
19. Dufrene M, Legendre P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67: 345-366.
20. Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH. 2010a. Relative roles of niche and neutral processes in structuring a soil microbial community. ISME Journal 4: 337-345.
21. Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH. 2010b. Idiosyncrasy and overdominance in the structure of natural communities of arbuscular mycorrhizal fungi: is there a role for stochastic processes? Journal of Ecology 98: 419-428.
22. Ellenberg H. 1974. Zeigerwerte der Gefäßpflanzen Mitteleuropas. Scripta Geobotanica 9: 1-97.
23. Fischer M, Bossdorf O, Gockel S, Hänsel F, Hemp A, Hessenmöller D, Korte G, Nieschulze J, Pfeiffer S, Prati D et al. 2010. Implementing large-scale and long-term functional biodiversity research: the biodiversity exploratories. Basic and Applied Ecology 11: 473-485.
24. Frank DA, Gehring CA, Machut L, Phillips M. 2003. Soil community composition and the regulation of grazed temperate grassland. Oecologia 137: 603-609.
25. Gollotte A, van Tuinen D, Atkinson D. 2004. Diversity of arbuscular mycorrhizal fungi colonising roots of the grass species Agrostis capillaris and Lolium perenne in a field experiment. Mycorrhiza 14: 111-117.
26. Gosling P, Mead A, Proctor M, Hammond JP, Bending GD. 2013. Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytologist 198: 546-556.
27. Grime JP. 2001. Plant strategies, vegetation processes, and ecosystem properties. Chichester, UK: J. Wiley.
28. Grman E. 2012. Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93: 711-718.
29. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW. 1998. Ploughing up the wood-wide web? Nature 394: 431.
30. Hempel S, Renker C, Buscot F. 2007. Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environmental Microbiology 9: 1930-1938.
31. Henwood WD. 1998. An overview of protected areas in the temperate grasslands biome. Parks 8: 3-8.
32. HilleRisLambers J, Adler PB, Harpole WS, Levine JM, Mayfield MM. 2012. Rethinking community assembly through the lens of coexistence theory. Annual Review of Ecology and Systematics 43: 227-248.
33. Horn S, Caruso T, Verbruggen E, Rillig MC, Hempel S. 2014. Arbuscular mycorrhizal fungal communities are phylogenetically clustered at small scales. ISME Journal 8: 2231-2242.
34. Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC. 2011. Integrative analysis of environmental sequences using MEGAN 4. Genome Research 21: 1552-1560.
35. Ihrmark K, Bödeker ITM, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, Strid Y, Stenlid J, Brandström-Durling M, Clemmensen KE et al. 2012. New primers to amplify the fungal ITS2 region - evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiology Ecology 82: 666-677.
36. Johnson NC. 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185: 631-647.
37. Klaus V, Blüthgen N. 2013. LUI grasslands 2006-2010 (5-year-index) DETAILS. Biodiversity Exploratories information system (BEXIS). Max Planck Society for the Advancement of Science e.V. [WWW document] URL http://exploratories.bgc-jena.mpg.de [accessed 1 November 2013].
38. Klotz S, Kühn I, Durka W. 2002. BIOLFLOR - Eine Datenbank zu biologisch-ökologischen Merkmalen der Gefäßpflanzen in Deutschland. Schriftenreihe für Vegetationskunde 38. Bonn, Germany: Bundesamt für Naturschutz. [WWW document] URL http://www.biolflor.de [accessed 30 January 2014].
39. rd English edn. Amsterdam, the Netherlands: Elsevier Science BV.
40. Liu Y, Shi G, Mao L, Cheng G, Jiang S, Ma X, An L, Du G, Johnson NC, Feng H. 2012. Direct and indirect influences of 8-yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytologist 194: 523-535.
41. Moora M, Berger S, Davison J, Berger S, Opik M, Berger S, Bommarco R, Bruelheide H, Kuhn I, Kunin WE et al. 2011. Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. Journal of Biogeography 38: 1305-1317.
42. Morris EK, Buscot F, Herbst C, Meiners T, Obermaier E, Wäschke NW, Wubet T, Rillig MC. 2013. Land use and host neighbor identity effects on arbuscular mycorrhizal fungal community composition in focal plant rhizosphere. Biodiversity and Conservation 22: 2193-2205.
43. Nilsson RH, Bok G, Ryberg M, Kristiansson E, Hallenberg N. 2009. A software pipeline for processing and identification of fungal ITS sequences. Source Code for Biology and Medicine 4: 1.
44. Oehl F, Sieverding E, Mader P, Dubois D, Ineichen K, Boller T, Wiemken A. 2004. Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138: 574-583.
45. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H. 2013. vegan: community ecology package. R package version 2.0-10. [WWW document] URL http://CRAN.R-project.org/package=vegan [accessed 13 December 2013].
46. Öpik M, Metsis M, Daniell TJ, Zobel M, Moora M. 2009. Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytologist 184: 424-437.
47. Öpik M, Moora M, Liira J, Zobel M. 2006. Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. Journal of Ecology 94: 778-790.
48. Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier Ü, Zobel M. 2010. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist 188: 223-241.
49. Öpik M, Zobel M, Cantero JJ, Davison J, Facelli JM, Hiiesalu I, Jairus T, Kalwij JM, Koorem K, Leal ME et al. 2013. Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza 23: 411-430.
50. R Core Team. 2013. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL http://www.R-project.org/ [accessed 1 December 2013].
51. Renker C, Zobel M, Öpik M, Allen MF, Allen EB, Vosátka M, Rydlová J, Buscot F. 2004. Structure, dynamics, and restoration of plant communities: do arbuscular mycorrhizae matter? In: Temperton VM, Hobbs RJ, Nuttle T, Halle S, eds. Assembly rules and restoration ecology. Washington, DC, USA: Island Press, 195.
52. Rillig MC, Treseder KK, Allen MF. 2002. Global change and mycorrhizal fungi. In: van der Heijden MGA, Sanders IR, eds. Mycorrhizal ecology, ecologial studies, Vol. 157. Berlin, Heidelberg, Germany: Springer-Verlag, 143.
53. Roberts DW. 2013. labdsv: ordination and multivariate analysis for ecology. R package version 1.6-1. [WWW document] URL http://CRAN.R-project.org/package=labdsv [accessed 8 January 2014].
54. Rodríguez-Gironés MA, Santamaría L. 2006. A new algorithm to calculate the nestedness temperature of presence-absence matrices. Journal of Biogeography 33: 924-935.
55. Sanders IR. 2002. Specificity in the arbuscular mycorrhizal symbiosis. In: van der Heijden MGA, Sanders IR, eds. Mycorrhizal ecology, ecological studies, Vol. 157. Berlin Heidelberg, Germany: Springer-Verlag, 416.
56. Santos-Gonzalez JC, Finlay RD, Tehler A. 2007. Seasonal dynamics of arbuscular mycorrhizal fungal communities in roots in a seminatural grassland. Applied and Environmental Microbiology 73: 5613-5623.
57. Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A. 2005. Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycological Research 109: 789-794.
58. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology 75: 7537-7541.
59. Schmitt B, Prati D, Fischer M. 2011. Vegetation relevés in 150 grassland EP-s. Biodiversity Exploratories Information System (BEXIS). Max Planck Society for the Advancement of Science e.V. [WWW document] URL http://exploratories.bgc-jena.mpg.de [accessed 4 May 2012].
60. Schmitz AM, Harrison MJ. 2014. Signaling events during initiation of arbuscular mycorrhizal symbiosis. Journal of Integrative Plant Biology 56: 250-261.
61. Schöning I, Solly E, Kloetzing T, Trumbore S. 2012. MinSoil_2011_Mineral_Soil_pH. Biodiversity Exploratories Information System (BEXIS). Max Planck Society for the Advancement of Science e.V. [WWW document] URL http://exploratories.bgc-jena.mpg.de [accessed 19 November 2013].
62. Schöttner S, Hoffmann F, Cárdenas P, Rapp HT, Boetius A, Ramette A. 2013. Relationships between host phylogeny, host type and bacterial community diversity in cold-water coral reef sponges. PLoS ONE 8: e55505.
63. Schüßler A, Schwarzott D, Walker C. 2001. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 105: 1413-1421.
64. Šmilauer P. 2001. Communities of arbuscular mycorrhizal fungi in grassland: seasonal variability and effects of environment and host plants. Folia Geobotanica 36: 243-263.
65. Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. Cambridge, UK: Academic Press.
66. Stammers M, Harris J, Evans GM, Hayward MD, Forster JW. 1995. Use of random PCR (RAPD) technology to analyse phylogenetic relationships in the Lolium/Festuca complex. Heredity 74: 19-27.
67. Taberlet P, Gielly L, Pautou G, Bouvet J. 1991. Universal primers for amplification of 3 noncoding regions of chloroplast DNA. Plant Molecular Biology 17: 1105-1109.
68. Treseder KK, Cross A. 2006. Global distributions of arbuscular mycorrhizal fungi. Ecosystems 9: 305-316.
69. Vandenkoornhuyse P, Mahe S, Ineson P, Staddon P, Ostle N, Cliquet JB, Francez AJ, Fitter AH, Young JPW. 2007. Active root-inhabiting microbes identified by rapid incorporation of plant-derived carbon into RNA. Proceedings of the National Academy of Sciences, USA 104: 16970-16975.
70. Vandenkoornhuyse P, Ridgway KP, Watson IJ, Fitter AH, Young JPW. 2003. Co-existing grass species have distinctive arbuscular mycorrhizal communities. Molecular Ecology 12: 3085-3095.
71. Verbruggen E, Röling WFM, Gamper HA, Kowalchuk GA, Verhoef HA, van der Heijden MGA. 2010. Positive effects of organic farming on below-ground mutualists: large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytologist 186: 968-979.
72. Verbruggen E, Van Der Heijden MGA, Weedon JT, Kowalchuk GA, Röling WFM. 2012. Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Molecular Ecology 21: 2341-2353.
73. Veresoglou SD, Rillig MC. 2014. Do closely related plants host similar arbuscular mycorrhizal fungal communities? A meta-analysis. Plant and Soil 377: 395-406.
74. Wilson JM. 1984. Competition for infection between vesicular-arbuscular mycorrhizal fungi. New Phytologist 97: 427-435.
75. Wilson SD, Tilman D. 1991. Interactive effects of fertilization and disturbance on community structure and resource availability in an old-field plant community. Oecologia 88: 61-71.