Foundation plants shape the composition of local biotic communities and abiotic environments, but the impact of a plant's intraspecific variations on these processes is poorly understood. We examined these links in the alpine cushion moss campion (Silene acaulis) on two neighboring mountain ranges in the French Alps. Genotyping of cushion plants revealed two genetic clusters matching known subspecies. The exscapa subspecies was found on both limestone and granite, while the longiscapa one was only found on limestone. Even on similar limestone bedrock, cushion soils from the two S. acaulis subspecies deeply differed in their impact on soil abiotic conditions. They further strikingly differed from each other and from the surrounding bare soils in fungal community composition. Plant genotype variations accounted for a large part of the fungal composition variability in cushion soils, even when considering geography or soil chemistry, and particularly for the dominant molecular operational taxonomic units (MOTUs). Both saprophytic and biotrophic fungal taxa were related to the MOTUs recurrently associated with a single plant genetic cluster. Moreover, the putative phytopathogens were abundant, and within the same genus (Cladosporium) or species (Pyrenopeziza brassicae), MOTUs showing specificity for each plant subspecies were found. Our study highlights the combined influences of bedrock and plant genotype on fungal recruitment into cushion soils and suggests the coexistence of two mechanisms, an indirect selection resulting from the colonization of an engineered soil by free-living saprobes and a direct selection resulting from direct plant-fungi interactions.

Laboratoire d'Ecologie Alpine University Grenoble Alpes University Savoie Mont Blanc CNRS LECA Grenoble France

Present address Aix Marseille Univ Univ Avignon CNRS IMBE Marseille France

Present address CARRTEL INRA Université Savoie Mont Blanc Thonon les Bains France

Present address Centre for Polar Ecology University of South Bohemia Ceske Budejovice Czech Republic

Present address Institut für Biologie Ökologie der Pflanzen Freie Universität Berlin Germany

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Aeschimann, D. , Lauber, K. , Moser, D. M. , & Theurillat, J.‐P. (2004). Flora alpina. Paris, France: Belin.

Anderson, M. J. , Crist, T. O. , Chase, J. M. , Vellend, M. , Inouye, B. D. , Freestone, A. L. , … Swenson, N. G. (2011). Navigating the multiple meanings of β diversity: A roadmap for the practicing ecologist. Ecology Letters, 14, 19–28. 10.1111/j.1461-0248.2010.01552.x PubMed DOI

Arrigo, N. , Tuszynski, J. W. , Ehrich, D. , Gerdes, T. , & Alvarez, N. (2009). Evaluating the impact of scoring parameters on the structure of intra‐specific genetic variation using RawGeno, an R package for automating AFLP scoring. BMC Bioinformatics, 10, 14 10.1186/1471-2105-10-33 PubMed DOI PMC

Badano, E. I. , Jones, C. G. , Cavieres, L. A. , & Wright, J. P. (2006). Assessing impacts of ecosystem engineers on community organization: A general approach illustrated by effects of a high‐Andean cushion plant. Oikos, 115, 369–385. 10.1111/j.2006.0030-1299.15132.x DOI

Bailey, J. K. , Deckert, R. , Schweitzer, J. A. , Rehill, B. J. , Lindroth, R. L. , Gehring, C. , & Whitham, T. G. (2005). Host plant genetics affect hidden ecological players: Links among Populus, condensed tannins, and fungal endophyte infection. Canadian Journal of Botany‐Revue Canadienne De Botanique, 83, 356–361. 10.1139/b05-008 DOI

Bangert, R. K. , Turek, R. J. , Rehill, B. , Wimp, G. M. , Schweitzer, J. A. , Allan, G. J. , … Whitham, T. G. (2006). A genetic similarity rule determines arthropod community structure. Molecular Ecology, 15, 1379–1391. 10.1111/j.1365-294X.2005.02749.x PubMed DOI

Bangert, R. K. , & Whitham, T. G. (2007). Genetic assembly rules and community phenotypes. Evolutionary Ecology, 21, 549–560. 10.1007/s10682-006-9135-7 DOI

Bates, D. , Maechler, M. , Bolker, B. , & Walker, S. (2015). Fitting Linear Mixed‐Effects Models Using lme4. Journal of Statistical Software, 67, 1–48.

Benjamini, Y. , & Hochberg, Y. (1995). Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological), 57, 289–300.

Bensch, K. , Braun, U. , Groenewald, J. Z. , & Crous, P. W. (2012). The genus Cladosporium. Studies in Mycology, 72, 1–401. 10.3114/sim0003 PubMed DOI PMC

Berendsen, R. L. , Pieterse, C. M. J. , & Bakker, P. A. H. M. (2012). The rhizosphere microbiome and plant health. Trends in Plant Science, 17, 478–486. 10.1016/j.tplants.2012.04.001 PubMed DOI

Bertness, M. D. , & Callaway, R. (1994). Positive interactions in communities. Trends in Ecology & Evolution, 9, 191–193. 10.1016/0169-5347(94)90088-4 PubMed DOI

Bever, J. D. , Platt, T. G. , & Morton, E. R. (2012). Microbial Population and Community Dynamics on Plant Roots and Their Feedbacks on Plant Communities. Annual Review of Microbiology, 66, 265–283. 10.1146/annurev-micro-092611-150107 PubMed DOI PMC

Bock, C. (1983). Quelques aspects de la variation infraspécifique chez le Silene acaulis (L.) Jacq. Compt‐Rendus 108è, , Sect Sci, Fasc, 2nd ed. Grenoble: : Congrès National Soc Savantes.

Bonanomi, G. , Stinca, A. , Chirico, G. B. , Ciaschetti, G. , Saracino, A. , & Incerti, G. (2016). Cushion plant morphology controls biogenic capability and facilitation effects of Silene acaulis along an elevation gradient. Functional Ecology, 30, 1216–1226. https://doi:10.1111/1365-2435.12596 DOI

Boyer, F. , Mercier, C. , Bonin, A. , Le Bras, Y. , Taberlet, P. , & Coissac, E. (2016). Obitools: A unix‐inspired software package for DNA metabarcoding. Molecular Ecology Resources, 16, 176–182. https://doi:10.1111/1755-0998.12428 PubMed DOI

Brundrett, M. C. (2002). Coevolution of roots and mycorrhizas of land plants. New Phytologist, 154, 275–304. 10.1046/j.1469-8137.2002.00397.x PubMed DOI

Buée, M. , Reich, M. , Murat, C. , Morin, E. , Nilsson, R. H. , Uroz, S. , & Martin, F. (2009). 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytologist, 184, 449–456. 10.1111/j.1469-8137.2009.03003.x PubMed DOI

Butterfield, B. J. , Cavieres, L. A. , Callaway, R. M. , Cook, B. J. , Kikvidze, Z. , Lortie, C. J. , … Brooker, R. W. (2013). Alpine cushion plants inhibit the loss of phylogenetic diversity in severe environments. Ecology Letters, 16, 478–486. 10.1111/ele.12070 PubMed DOI

Chappell, T. M. , & Rausher, M. D. (2016). Evolution of host range in Coleosporium ipomoeae, a plant pathogen with multiple hosts. Proceedings of the National Academy of Sciences, 113, 5346. PubMed PMC

Clément, J. , Robson, T. , Guillemin, R. , Saccone, P. , Lochet, J. , Aubert, S. , & Lavorel, S. (2012). The effects of snow‐N deposition and snowmelt dynamics on soil‐N cycling in marginal terraced grasslands in the French Alps. Biogeochemistry, 108, 297–315. 10.1007/s10533-011-9601-3 DOI

Coissac, E. , Riaz, T. , & Puillandre, N. (2012). Bioinformatic challenges for DNA metabarcoding of plants and animals. Molecular Ecology, 21, 1834–1847. 10.1111/j.1365-294X.2012.05550.x PubMed DOI

Cordier, T. , Robin, C. , Capdevielle, X. , Desprez‐Loustau, M.‐L. , & Vacher, C. (2012). Spatial variability of phyllosphere fungal assemblages: Genetic distance predominates over geographic distance in a European beech stand (Fagus sylvatica). Fungal Ecology, 5, 509–520. 10.1016/j.funeco.2011.12.004 DOI

Cripps, C. L. , & Eddington, L. H. (2005). Distribution of Mycorrhizal Types among Alpine Vascular Plant Families on the Beartooth Plateau, Rocky Mountains, U.S.A., in Reference to Large‐Scale Patterns in Arctic‐Alpine Habitats. Arctic, Antarctic, and Alpine Research, 37, 177–188. 10.1657/1523-0430(2005)037[0177:DOMTAA]2.0.CO;2 DOI

Crowther, T. W. , Maynard, D. S. , Crowther, T. R. , Peccia, J. , Smith, J. R. , & Bradford, M. A. (2014). Untangling the fungal niche: The trait‐based approach. Frontiers in Microbiology, 5, 579 10.3389/fmicb.2014.00579 PubMed DOI PMC

Crutsinger, G. M. , Rodriguez‐Cabal, M. A. , Roddy, A. B. , Peay, K. G. , Bastow, J. L. , Kidder, A. G. , … Rudgers, J. A. (2014). Genetic variation within a dominant shrub structures green and brown community assemblages. Ecology, 95, 387–398. 10.1890/13-0316.1 PubMed DOI

De Deyn, G. B. , Cornelissen, J. H. C. , & Bardgett, R. D. (2008). Plant functional traits and soil carbon sequestration in contrasting biomes. Ecology Letters, 11, 516–531. 10.1111/j.1461-0248.2008.01164.x PubMed DOI

de Mazancourt, C. , & Loreau, M. (2000). Grazing optimization, nutrient cycling, and spatial heterogeneity of plant‐herbivore interactions: Should a palatable plant evolve? Evolution, 54, 81–92. 10.1554/0014-3820(2000)054[0081:GONCAS]2.0.CO;2 PubMed DOI

Defossez, E. , Courbaud, B. , Marcais, B. , Thuiller, W. , Granda, E. , & Kunstler, G. (2011). Do interactions between plant and soil biota change with elevation? A study on Fagus sylvatica. Biology Letters, 7, 699–701. 10.1098/rsbl.2011.0236 PubMed DOI PMC

Dray, S. , & Dufour, A.‐B. (2007). The ade4 Package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22, 1–20.

Dumbrell, A. J. , Nelson, M. , Helgason, T. , Dytham, C. , & Fitter Alastair, H. (2009). 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. 10.1111/j.1365-2745.2009.01622.x DOI

Epp, L. S. , Boessenkool, S. , Bellemain, E. P. , Haile, J. , Esposito, A. , Riaz, T. , … Brochmann, C. (2012). New environmental metabarcodes for analyzing soil DNA: Potential for studying past and present ecosystems. Molecular Ecology, 21, 1821–1833. 10.1111/j.1365-294X.2012.05537.x PubMed DOI

Ferrier, S. , Manion, G. , Elith, J. , & Richardson, K. (2007). Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Diversity and Distributions, 13, 252–264. 10.1111/j.1472-4642.2007.00341.x DOI

Geremia, R. A. , Pușcaș, M. , Zinger, L. , Bonneville, J.‐M. , & Choler, P. (2016). Contrasting microbial biogeographical patterns between anthropogenic subalpine grasslands and natural alpine grasslands. New Phytologist, 209, 1196–1207. 10.1111/nph.13690 PubMed DOI

Gilbert, G. S. , & Webb, C. O. (2007). Phylogenetic signal in plant pathogen–host range. Proceedings of the National Academy of Sciences, 104, 4979–4983. 10.1073/pnas.0607968104 PubMed DOI PMC

Hanson, C. A. , Allison, S. D. , Bradford, M. A. , Wallenstein, M. D. , & Treseder, K. K. (2008). Fungal Taxa Target Different Carbon Sources in Forest Soil. Ecosystems, 11, 1157–1167. 10.1007/s10021-008-9186-4 DOI

Hawkes, C. V. , Kivlin, S. N. , Rocca, J. D. , Huguet, V. , Thomsen, M. A. , & Suttle, K. B. (2011). Fungal community responses to precipitation. Global Change Biology, 17, 1637–1645. 10.1111/j.1365-2486.2010.02327.x DOI

Hayes, M. A. (2012). The Geomyces Fungi: Ecology and Distribution. BioScience, 62, 819–823. 10.1525/bio.2012.62.9.7 DOI

Jones, C. G. , Lawton, J. H. , & Shachak, M. (1994). Organisms as Ecosystem Engineers. Oikos, 69, 373–386. 10.2307/3545850 DOI

Jumpponen, A. , & Jones, K. (2009). Massively parallel 454 sequencing indicates hyperdiverse fungal communities in temperate Quercus macrocarpa phyllosphere. New Phytologist, 184, 438–448. 10.1111/j.1469-8137.2009.02990.x PubMed DOI

Kia, S. H. , Glynou, K. , Nau, T. , Thines, M. , Piepenbring, M. , & Maciá‐Vicente, J. G. (2016). Influence of phylogenetic conservatism and trait convergence on the interactions between fungal root endophytes and plants. The Isme Journal, 11, 777 10.1038/ismej.2016.140 PubMed DOI PMC

Lamit, L. J. , Lau, M. K. , Sthultz, C. M. , Wooley, S. C. , Whitham, T. G. , & Gehring, C. A. (2014). Tree genotype and genetically based growth traits structure twig endophyte communities. American Journal of Botany, 101, 467–478. 10.3732/ajb.1400034 PubMed DOI

Legendre, P. , & Legendre, L. F. (2012). Numerical ecology. Amsterdam: Elsevier.

Lentendu, G. , Zinger, L. , Manel, S. , Coissac, E. , Choler, P. , Geremia, R. A. , & Melodelima, C. (2011). Assessment of soil fungal diversity in different alpine tundra habitats by means of pyrosequencing. Fungal Diversity, 49, 113–123. 10.1007/s13225-011-0101-5 DOI

Maillet, N. , Lemaitre, C. , Chikhi, R. , Lavenier, D. , & Peterlongo, P. (2012). Compareads: Comparing huge metagenomic experiments. BMC Bioinformatics, 13, S10. PubMed PMC

Meudt, H. M. , & Clarke, A. C. (2007). Almost forgotten or latest practice? AFLP applications, analyses and advances. Trends in Plant Science, 12, 106–117. 10.1016/j.tplants.2007.02.001 PubMed DOI

Millard, P. , & Singh, B. (2010). Does grassland vegetation drive soil microbial diversity? Nutr Cycl Agroecosys, 88, 147–158. 10.1007/s10705-009-9314-3 DOI

Molenda, O. , Reid, A. , & Lortie, C. J. (2012). The Alpine Cushion Plant Silene acaulis as Foundation Species: A Bug’s‐Eye View to Facilitation and Microclimate. PLOS ONE, 7, e37223. PubMed PMC

Molina‐Montenegro, M. A. , Oses, R. , Torres‐Díaz, C. , Atala, C. , Núñez, M. A. , & Armas, C. (2015). 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, 17, 218–226. 10.1016/j.ppees.2015.02.003 DOI

Morris, W. F. , & Doak, D. F. (1998). Life history of the long‐lived gynodioecious cushion plant Silene acaulis (Caryophyllaceae), inferred from size‐based population projection matrices. American Journal of Botany, 85, 784–793. 10.2307/2446413 PubMed DOI

Mouhamadou, B. , Puissant, J. , Personeni, E. , Desclos‐Theveniau, M. , Kastl, E. M. , Schloter, M. , … Lavorel, S. (2013). Effects of two grass species on the composition of soil fungal communities. Biology and Fertility of Soils, 49, 1131–1139. 10.1007/s00374-013-0810-x DOI

Nguyen, N. H. , Song, Z. , Bates, S. T. , Branco, S. , Tedersoo, L. , Menke, J. , … Kennedy, P. G. (2016). FUNGuild: An open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology, 20, 241–248. 10.1016/j.funeco.2015.06.006 DOI

Oksanen, J. , Blanchet, F. G. , Kindt, R. , Legendre, P. , Minchin, P. R. , O'Hara, R. B. , …Wagner, H. (2013) vegan: Community Ecology Package. R package version 2.3‐1.

Osono, T. (2002). Phyllosphere fungi on leaf litter of Fagus crenata: Occurrence, colonization, and succession. Canadian Journal of Botany‐Revue Canadienne De Botanique, 80, 460–469. 10.1139/b02-028 DOI

Pearson, W. R. (2000). Flexible sequence similarity searching with the FASTA3 program package. Methods in Molecular Biology (Clifton, NJ), 132, 185–219. PubMed

Pellissier, L. , Niculita‐Hirzel, H. , Dubuis, A. , Pagni, M. , Guex, N. , Ndiribe, C. , … Guisan, A. (2014). Soil fungal communities of grasslands are environmentally structured at a regional scale in the Alps. Molecular Ecology, 23, 4274–4290. 10.1111/mec.12854 PubMed DOI

Pompanon, F. , Bonin, A. , Bellemain, E. , & Taberlet, P. (2005). Genotyping errors: Causes, consequences and solutions. Nature Reviews Genetics, 6, 847–859. 10.1038/nrg1707 PubMed DOI

Pritchard, J. K. , Stephens, M. , & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959. PubMed PMC

Prober, S. M. , Leff, J. W. , Bates, S. T. , Borer, E. T. , Firn, J. , Harpole, W. S. , … Fierer, N. (2015). Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecology Letters, 18, 85–95. 10.1111/ele.12381 PubMed DOI

R_Development_Core_Team,, (2011). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Rawlinson, C. J. , Sutton, B. C. , & Muthyalu, G. (1978). Taxonomy and biology of Pyrenopeziza brassicae sp.nov. (Cylindrosporium concentricum), a pathogen of winter oilseed rape (Brassica napus ssp. oleifera). Transactions of the British Mycological Society, 71, 425–439. 10.1016/S0007-1536(78)80070-9 DOI

Robertson, G. , Coleman, D. , Bledsoe, C. , & Sollins, P. (1999). Standard soil methods for long‐term ecological research. Oxford University Press.

Rodriguez, R. J. , Redman, R. S. , & Henson, J. M. (2004). The Role of Fungal Symbioses in the Adaptation of Plants to High Stress Environments. Mitigation and Adaptation Strategies for Global Change, 9, 261–272. 10.1023/B:MITI.0000029922.31110.97 DOI

Rousk, J. , Baath, E. , Brookes, P. C. , Lauber, C. L. , Lozupone, C. , Caporaso, J. G. , … Fierer, N. (2010). Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME Journal, 4, 1340–1351. 10.1038/ismej.2010.58 PubMed DOI

Roy, J. , Albert, C. H. , Choler, P. , Clément, J.‐C. , Ibanez, S. , Lavergne, S. , … Geremia, R. A. (2013). Microbes on the cliff: Alpine cushion plants structure bacterial and fungal communities. Frontiers in Microbiology, 4, 1–14. 10.3389/fmicb.2013.00064 PubMed DOI PMC

Saunders, M. , & Kohn, L. M. (2009). Evidence for alteration of fungal endophyte community assembly by host defense compounds. New Phytologist, 182, 229–238. 10.1111/j.1469-8137.2008.02746.x PubMed DOI

Schmidt, S. K. , Sobieniak‐Wiseman, L. C. , Kageyama, S. A. , Halloy, S. R. P. , & Schadt, C. W. (2008). Mycorrhizal and Dark‐Septate Fungi in Plant Roots Above 4270 Meters Elevation in the Andes and Rocky Mountains. Arctic, Antarctic, and Alpine Research, 40, 576–583. 10.1657/1523-0430(07-068)[SCHMIDT]2.0.CO;2 DOI

Talbot, J. M. , Bruns, T. D. , Taylor, J. W. , Smith, D. P. , Branco, S. , Glassman, S. I. , … Peay, K. G. (2014). Endemism and functional convergence across the North American soil mycobiome. Proceedings of the National Academy of Sciences, 111, 6341–6346. 10.1073/pnas.1402584111 PubMed DOI PMC

Tedersoo, L. , Bahram, M. , Põlme, S. , Kõljalg, U. , Yorou, N. S. , Wijesundera, R. , … Abarenkov, K. (2014). Global diversity and geography of soil fungi. Science, 346, 1078–1088. 10.1126/science.1256688 PubMed DOI

Treseder, K. K. , & Lennonb, J. T. (2015). Fungal Traits That Drive Ecosystem Dynamics on Land. Microbiology and Molecular Biology Reviews, 79, 243–262. 10.1128/MMBR.00001-15 PubMed DOI PMC

van Dongen, S. (2000). Graph clustering by flow simulation. Utrecht, The Netherlands: : University of Utrecht.

van Molken, T. , & Stuefer, J. F. (2008). Virulence in clonal plants: Conflicting selection pressures at work? Evolutionary Ecology, 22, 467–470.

Voriskova, J. , & Baldrian, P. (2013). Fungal community on decomposing leaf litter undergoes rapid successional changes. Isme Journal, 7, 477–486. 10.1038/ismej.2012.116 PubMed DOI PMC

Vos, P. , Hogers, R. , Bleeker, M. , Reijans, M. , Vandelee, T. , Hornes, M. , … Zabeau, M. (1995). AFLP ‐ A new technique for DNA‐fingerprinting. Nucleic Acids Research, 23, 4407–4414. 10.1093/nar/23.21.4407 PubMed DOI PMC

Weiß, M. , Waller, F. , Zuccaro, A. , & Selosse, M.‐A. (2016). Sebacinales – one thousand and one interactions with land plants. New Phytologist, 211, 20–40. 10.1111/nph.13977 PubMed DOI

Whitham, T. G. , Young, W. P. , Martinsen, G. D. , Gehring, C. A. , Schweitzer, J. A. , Shuster, S. M. , … Kuske, C. R. (2003). Community and ecosystem genetics: A consequence of the extended phenotype. Ecology, 84, 559–573. 10.1890/0012-9658(2003)084[0559:CAEGAC]2.0.CO;2 DOI

Zhang, T. , & Yao, Y.‐F. (2015). Endophytic Fungal Communities Associated with Vascular Plants in the High Arctic Zone Are Highly Diverse and Host‐Plant Specific. PLOS ONE, 10, e0130051 10.1371/journal.pone.0130051 PubMed DOI PMC

Zhou, D. , & Hyde, K. D. (2001). Host‐specificity, host‐exclusivity, and host‐recurrence in saprobic fungi* *Paper presented at the Asian Mycological Congress 2000 (AMC 2000) incorporating the 2nd Asia‐Pacific Mycological Congress on Biodiversity and Biotechnology, and held at the University of Hong Kong on 9–13 July 2000. Mycological Research, 105, 1449–1457. 10.1017/S0953756201004713 DOI

Zinger, L. , Lejon, D. P. , Baptist, F. , Bouasria, A. , Aubert, S. , Geremia, R. A. , & Choler, P. (2011). Contrasting diversity patterns of crenarchaeal, bacterial and fungal soil communities in an alpine landscape. PLoS One, 6, e19950 10.1371/journal.pone.0019950 PubMed DOI PMC

Zinger, L. , Shahnavaz, B. , Baptist, F. , Geremia, R. A. , & Choler, P. (2009). Microbial diversity in alpine tundra soils correlates with snow cover dynamics. ISME Journal, 3, 850–859. 10.1038/ismej.2009.20 PubMed DOI

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