Differences in the fungal communities nursed bytwo genetic groups of the alpine cushion plant, Silene acaulis Julien Roy, Jean-Marc Bonneville, Patrick Saccone, Sébastian Ibanez, Cécile Albert, Marti Boleda, Maya Gueguen, Marc Ohlmann, Delphine Rioux, Jean-Christophe Clément, et al. To cite this version: Julien Roy, Jean-Marc Bonneville, Patrick Saccone, Sébastian Ibanez, Cécile Albert, et al.. Differences in the fungal communities nursed by two genetic groups of the alpine cushion plant, Silene acaulis. Ecology and Evolution, Wiley Open Access, In press, 8, pp.11568-11581. 10.1002/ece3.4606. hal- 01930654 HAL Id: hal-01930654 https://hal.archives-ouvertes.fr/hal-01930654 Submitted on 22 Nov 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Received: 2 January 2018 Accepted: 14 September 2018 Differences in the fungal communities nursed by two genetic groups of the alpine cushion plant, Silene acaulis Julien Roy* | Jean‐Marc Bonneville* | Patrick Saccone | Sébastian Ibanez | Cécile H. Albert | Marti Boleda | Maya Gueguen | Marc Ohlmann | Delphine Rioux | Jean‐ Christophe Clément | Sébastien Lavergne | Roberto A. Geremia Laboratoire d’Ecologie Alpine (LECA), University Grenoble Abstract Alpes, University Savoie Mont Blanc, CNRS, Foundation plants shape the composition of local biotic communities and abiotic en‐ LECA, Grenoble, France vironments, but the impact of a plant’s intraspecific variations on these processes is Correspondence poorly understood. We examined these links in the alpine cushion moss campion Roberto A. Geremia, Laboratoire d’Ecologie Alpine (LECA), University Grenoble Alpes, (Silene acaulis) on two neighboring mountain ranges in the French Alps. Genotyping University Savoie Mont Blanc, CNRS, LECA, of cushion plants revealed two genetic clusters matching known subspecies. The ex‐ Grenoble, France. Email: [email protected] scapa 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 Present Address Julien Roy, Institut für Biologie, Ökologie der the two S. acaulis subspecies deeply differed in their impact on soil abiotic condi‐ Pflanzen, Freie Universität Berlin, Germany tions. They further strikingly differed from each other and from the surrounding bare Patrick Saccone, Centre for Polar soils in fungal community composition. Plant genotype variations accounted for a Ecology, University of South Bohemia, Ceske Budejovice, Czech Republic large part of the fungal composition variability in cushion soils, even when consider‐ Cécile H. Albert, Aix Marseille Univ, Univ ing geography or soil chemistry, and particularly for the dominant molecular opera‐ Avignon, CNRS, IMBE, Marseille, France tional taxonomic units (MOTUs). Both saprophytic and biotrophic fungal taxa were Jean‐Christophe Clément, CARRTEL, INRA – Université Savoie Mont Blanc, Thonon‐les‐ related to the MOTUs recurrently associated with a single plant genetic cluster. Bains, France Moreover, the putative phytopathogens were abundant, and within the same genus (Cladosporium) or species (Pyrenopeziza brassicae), MOTUs showing specificity for Funding information Labex, Grant/Award Number: 2020 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 coloniza‐ tion of an engineered soil by free‐living saprobes and a direct selection resulting from direct plant–fungi interactions. KEYWORDS community genetics, fungal community, gene‐for‐gene interactions, nurse effect, soil ecosystem engineering 1 INTRODUC TION Chikhi, Lavenier, & Peterlongo, 2012; Molenda et al., 2012), and other plants (Butterfield et al., 2013). To our knowledge, however, Terrestrial plants interact with aboveground and belowground fungal the extent of the abiotic and biotic soil changes induced by various communities (Buée et al., 2009; Jumpponen & Jones, 2009) whose as‐ cushion plant species or subspecies has not been explicitly studied. semblage is influenced both by abiotic factors and by the plant commu‐ Silene acaulis (L.) Jacq is a common circumboreal and alpine cush‐ nity. Through positive or negative plant–soil feedbacks, fungi, in turn, ion plant with slow growth and cushions that can often be older than shape plant community composition (Bever, Platt, & Morton, 2012), 300 years (Morris & Doak, 1998). Its xenogamic reproduction makes playing a major role in their evolution (Brundrett, 2002) and in ecosys‐ that two distinct plant individuals always represent distinct geno‐ tem functioning (Berendsen, Pieterse, & Bakker, 2012). Vascular plants types. Although the evolutionary history of Silene acaulis remains to be provide dead or living organic matter to most soil fungi; thus, they in‐ fully unraveled, two main subspecies have been proposed in the Alps, teract directly with biotrophic fungi but also modify their edaphic en‐ S. acaulis exscapa and S. acaulis longiscapa, exhibiting dense‐ (shorter in‐ vironment (De Deyn, Cornelissen, & Bardgett, 2008), hence, impacting ternodes) and loose‐cushion morphologies, respectively (Aeschimann, the saprotrophic community (Millard & Singh, 2010). Lauber, Moser, & Theurillat, 2004; Bock, 1983). They occur on adjacent Distance can limit fungal distributions since they present bio‐ territories, probably with genetic barriers, longiscapa being restricted geographic patterns at the continental (Prober et al., 2015; Talbot to calcareous bedrock while exscapa is mainly, but not only, found on et al., 2014; Tedersoo et al., 2014) and regional scales (Geremia, siliceous bedrock (Sébastien Ibanez, S. I., unpublished obs.). Subspecies Pușcaș, Zinger, Bonneville, & Choler, 2016; Pellissier et al., 2014). determination can, however, be difficult since intermediate cushion ar‐ Locally, the available pool of fungi then undergoes selection by chitectures may sometimes be found (Figure 1a). soil‐ or plant‐related parameters, including aboveground plant We previously reported that the presence of a cushion affects species composition. Fungal community composition is correlated soil chemical parameters on two bedrocks and that this shift in abi‐ with soil moisture (Hawkes et al., 2011) or pH (Rousk et al., 2010), otic properties comes along with a shift in the fungal community; but also with plant legacies, such as soil C/N ratio (Prober et al., in particular, the fungal turnover from bare soil to cushion soil in‐ 2015) or soil organic matter content (Zinger et al., 2011). The soil creased with environmental stress (high elevation and very low pH; fungal communities are further linked to the present plant com‐ Roy et al., 2013). In the present study, we first established that the munities, and fungal beta diversity (compositional dissimilarity be‐ two plant subspecies corresponded to distinct genotypic clusters, tween sites, see Anderson et al., 2011) is correlated with plant beta which then allowed us to assess the correlation between plant ge‐ diversity (Geremia et al., 2016; Pellissier et al., 2014; Prober et al., netic distances and fungal beta diversity. To disentangle this genetic 2015; Tedersoo et al., 2014). Also, different plant species give rise effect from those of the local environment (geology, elevation), and to diverging fungal communities from the same starting soil in con‐ also to measure abiotic soil engineering by the plant, we sampled trolled experiments, likely due to differences in rhizodeposition soils both beneath cushions and in neighboring bare soils. We finally (Mouhamadou et al., 2013). Plant intraspecific genetic variation examined the fungal functional guilds across the sampling design to can also lead to divergent composition of dependent communities address the distribution, filtering, and recruitment mechanisms. (Bangert & Whitham, 2007; Bangert et al., 2006). For endophytic fungi, this may be mediated directly by the differential production 2 MATERIAL S AND METHODS of defense compounds as shown in maize (Saunders & Kohn, 2009) or in Populus (Bailey et al., 2005; Lamit et al., 2014). However, little 2.1 Plant and soil sampling is known about the influence of plant genetic variation on fungal community composition in soils, which is challenging to disentan‐ The sampling area was located in the French Hautes‐Alpes along gle from confounding factors in natural environments. Here, we replicated ecotones from alpine to subnival environments and en‐ report on a field survey providing insights into this influence. compassed two neighboring mountain massifs: one mostly calcare‐ Alpine cushion plants offer an interesting system to study ous (Cerces) and one siliceous (Combeynot; see Roy et al., 2013 for fungal community assembly and to assess the role of intraspe‐ details). In September 2009, at 19 sites located across six elevation cific plant genetic variation. These foundation