Root-associated fungal communities are important components in ecosystem processes, impacting plant growth and vigor by influencing the quality, direction, and flow of nutrients and water between plants and fungi. Linkages of plant phenological characteristics with belowground root-associated fungal communities have rarely been investigated, and thus our aim was to search for an interplay between contrasting phenology of host ectomycorrhizal trees from the same location and root-associated fungal communities (ectomycorrhizal, endophytic, saprotrophic and pathogenic root-associated fungi) in young and in adult silver fir trees. The study was performed in a managed silver fir forest site. Twenty-four soil samples collected under two phenologically contrasting silver fir groups were analyzed for differences in root-associated fungal communities using Illumina sequencing of a total root-associated fungal community. Significant differences in beta diversity and in mean alpha diversity were confirmed for overall community of ectomycorrhizal root-associated fungi, whereas for ecologically different non-ectomycorrhizal root-associated fungal communities the differences were significant only for beta diversity and not for mean alpha diversity. At genus level root-associated fungal communities differed significantly between early and late flushing young and adult silver fir trees. We discuss the interactions through which the phenology of host plants either drives or is driven by the root-associated fungal communities in conditions of a sustainably co-naturally managed silver fir forest.

Biotechnical Faculty Department of Agronomy University of Ljubljana Ljubljana Slovenia

Department of Forest Physiology and Genetics Slovenian Forestry Institute Ljubljana Slovenia

Institute of Microbiology of the Czech Academy of Sciences Prague Czechia

Zobrazit více v PubMed

Agerer R. (2008).

Arguelles-Moyao A., Garibay-Orijel R., Marquez-Valdelamar L. M., Arellano-Torres E. (2017). Clavulina- PubMed DOI

Aronesty E. (2011).

Baar J., Horton T. R., Kretzer A. M., Bruns T. D. (1999). Mycorrhizal colonization of DOI

Barrow J. R., Aaltonen R. E. (2001). Evaluation of the internal colonization of

Bengtsson-Palme J., Veldre V., Ryberg M., Hartmann M., Branco S., Wang Z., et al. (2013). ITSx: improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for use in environmental sequencing.

Bödeker I. T. M., Lindahl B. D., Olson Å., Clemmensen K. E. (2016). Mycorrhizal and saprotrophic fungal guild compete for the same organic substrates but affect decomposition differently. DOI

Chen W., Koide R. T., Adams T. S., DeForest J. L., Cheng L., Eissenstat D. M. (2016). Root morphology and mycorrhizal symbiosis together shape nutrient foraging strategies of temperate trees. PubMed DOI PMC

Clemmensen K., Finlay R. D., Dahlberg A., Stenlid J., Wardle D. A., Lindhal B. D. (2014). Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. PubMed DOI

Comandini O., Pacioni G., Rinaldi A. C. (1998). Fungi in ectomycorrhizal associations of silver fir ( DOI

Courty P.-E., Buee M., Diedhiou A. G., Frey-Klett P., Le Tacon F., Rineau F., et al. (2010). The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. DOI

Croft H., Chen J. M., Noland T. L. (2014). Stand age effects on boreal forest physiology using a long time-series of satellite data. DOI

Crous P. W., Schubert K., Braun U., de Hoog G. S., Hocking A. D., Shin H. D., et al. (2007). Opportunistic, human-pathogenic species in the PubMed DOI PMC

Edgar R. C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. PubMed DOI

Egli S., Ayer F., Peter M., Eilmann B., Rigling A. (2010). Is forest mushroom productivity driven by tree growth? Results from a thinning experiment. DOI

Fernandez-Toiran L. M., Agreda T., Olano J. M. (2006). Stand age and sampling year effect on the fungal fruit body community in DOI

Gallaud I. (1905). Études sur les mycorrhizas endotrophes.

Ganley R. J., Brunsfeld S. J., Newcombe G. (2004). A community of unknown, endophytic fungi in western white pine. PubMed DOI PMC

Geml J., Davis D. D., Geiser D. M. (2005). Systematics of the genus PubMed DOI

Gianinazzi-Pearson V. (1984). “Host-Fungus Specificity, Recognition and Compatibility in Mycorrhizae,” in

Gogala N. (1991). Regulation of mycorrhizal infection by hormonal factors produced by hosts and fungi. DOI

Hambleton S., Sigler L. (2005). Meliniomyces, a new anamorph genus for root-associated fungi with phylogenetic affinities to DOI

Hill M. O. (1973). Diversity and evenness: a unifying notation and its consequences. DOI

Hilszczanska D. (2016). Endophytes – characteristics and possibilities of application in forest management. DOI

Hupperts S. F., Karst J., Pritsch K., Landhausser S. M. (2017). Host phenology and potential saprotrophism of ectomycorrhizal fungi in boreal forests. DOI

Igiehon N. O., Babalola O. O. (2018). Below-ground-above-ground plant-microbial interactions: focusing on soybean, rhizobacteria and mycorrhizal fungi. PubMed DOI PMC

Ihrmark K., Bödeker I. T., Cruz-Martinez K., Friberg H., Kubartova A., Schenck J., et al. (2012). New primers to amplify the fungal ITS2 region – evaluation by 454-sequencing of artificial and natural communities. PubMed DOI

Jumpponen A. (2001). Dark septate endophytes – are they mycorrhizal? DOI

Jumpponen A., Mattson K. G., Trappe J. M. (1998). Mycorrhizal functioning of PubMed DOI

Jumpponen A., Trappe J. M. (1998). Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. PubMed DOI

Kaiser C., Koranda M., Kitzler B., Fuchslueger L., Schnecker J., Schweiger P., et al. (2010). Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. PubMed DOI PMC

Katoh K., Asimenos G., Toh H. (2009). “Multiple alignment of DNA sequences with MAFFT,” in PubMed DOI

Kernaghan G., Patriquin G. (2011). Host associations between fungal root endophytes and boreal trees. PubMed DOI

Kõljalg U., Nilsson R. H., Abarenkov K., Tedersoo L., Taylor A. F., Bahram M., et al. (2013). Towards unified paradigm for sequence-based identification of fungi. PubMed DOI

Korkama T., Pakkanen A., Pennanen T. (2006). Ectomycorrhizal community structure varies among Norway spruce ( PubMed DOI

Kraigher H. (1996). Types of ectomycorrhizae – their taxonomy, role and application.

Kraigher H., Grayling A., Wang T. L., Hanke D. E. (1991). Cytokinin production by two ectomycorrhizal fungi in liquid culture. DOI

Kraigher H., Grebenc T., Hanke D. (2008). “Ozone stress and ectomycorrhizal root-shoot signaling,” in

Kyaschenko J., Clemmensen K. E., Hagenbo A., Karltun E., Lindahl B. D. (2017). - Shift in fungal communities and associated enzyme activities along an age gradient of managed PubMed DOI PMC

Last F. T., Dighton J., Mason P. A. (1987). Successions of sheathing mycorrhizal fungi. PubMed DOI

Lodge D. J., Padamsee M., Matheny P. B., Aime M. C., Cantrell S. A., Boertmann D., et al. (2014). Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales). DOI

Lukešova T., Kohout P., Vetrovsky T., Vohnik M. (2015). The potential of dark septate endophytes to form root symbioses with ectomycorrhizal and ericoid mycorrhizal middle European forest plants. PubMed DOI PMC

Mandyam K., Jumpponen A. (2005). Seeking the elusive function of the root-colonising dark septate endophytic fungi. DOI

Newsham K. K. (1999). Phialophora graminicola, a dark septate fungus, is a beneficial associate of the grass PubMed DOI

Oksanen J. F., Blanchet G., Friendly M., Kindt R., Legendre P., McGlinn D., et al. (2018).

Pena R., Offermann C., Simon J., Neumann P. S., Geßler A., Holst J., et al. (2010). Girdling affects ectomycorrhizal fungal (EMF) diversity and reveals functional differences in EMF community composition in a beech forest. PubMed DOI PMC

Peter M., Ayer F., Egli S., Honegger R. (2001). Above- and below-ground community structure of ectomycorrhizal fungi in three Norway spruce ( DOI

Porras-Alfaro A., Bayman P. (2011). Hidden fungi, emergent properties: endophytes and microbiomes. PubMed DOI

Porras-Alfaro A., Liu K. L., Kuske C. R., Xie G. (2014). From genus to phylum: large-subunit and internal transcribed spacer rRNA operon regions show similar classification accuracies influenced by database composition. PubMed DOI PMC

R Core Team (2016).

Rinaldi A. C., Comandini O., Kuyper T. W. (2008). Ectomycorrhizal fungal diversity: separating the wheat from the chaff.

Rognes T., Flouri T., Nichols B., Quince C., Mahé F. (2016). VSEARCH: a versatile open source tool for metagenomics. PubMed DOI PMC

Rudawska M., Pietras M., Smutek I., Strzelinski P., Leski T. (2016). Ectomycorrhizal fungal assemblages of PubMed DOI PMC

Sato H., Morimoto S., Hattori T. (2012). A thirty-year survey reveals that ecosystem function of fungi predicts phenology of mushroom fruiting. PubMed DOI PMC

Sato H., Yumoto T., Murakami N. (2007). Cryptic species and host specificity in the ectomycorrhizal genus PubMed DOI

Sieber T. N. (2007). Endophytic fungi in forest trees. Are they mutualists? DOI

Sigler L., Lumley T. C., Currah R. S. (2000). New species and records of saprophytic ascomycetes (Myxotrichaceae) from decaying logs in the boreal forest. DOI

Simard S. W. (2009). The foundational role of mycorrhizal networks in self-organization of interior Douglas-fir forests. DOI

Smith J. E., Molina R., Huso M. M., Luoma D. L., McKay D., Castellano M. A., et al. (2002). Species richness, abundance, and composition of hypogeous and epigeous ectomycorrhizal fungal sporocarps in young, rotation-age, and old-growth stands of Douglas-fir ( DOI

Smith S. E., Gianinazzi-Pearson V. (1988). Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. DOI

Smith S. E., Read D. J. (2008).

Taylor D. L., Bruns T. D. (1999). Community structure of ectomycorrhizal fungi in a PubMed DOI

Tedersoo L., May T. W., Smith M. E. (2010). Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. PubMed DOI

Toju H., Yamamoto S., Sato H., Tanabe A. S., Gilbert G. S., Kadowaki K. (2013). Community composition of root-associated fungi in a quercus-dominated temperate forests: “codominance” of mycorrhizal and root-endophytic fungi. PubMed DOI PMC

Twieg B. D., Durall D. M., Simard S. W. (2007). Ectomycorrhizal fungal succession in mixed temperate forests. PubMed DOI

van der Heijden M. G. A., Martin F. M., Selosse M.-A., Sanders I. R. (2015). Mycorrhizal ecology and evolution: the pas, the present, and the future. PubMed DOI

Varela-Cervero S., Vasar M., Davison J., Barea J. M., Opik M., Azcon-Aguilar C. (2015). The composition of arbuscular mycorrhizal fungal communities differs among the roots, spores and extraradical mycelia associated with five mediterranean plant species. PubMed DOI

Vaz A. B. M., Fonseca P. L. C., Leite L. R., Badotti F., Salim A. C. M., Araujo F. M. G., et al. (2017). Using Next-Generation Sequencing (NGS) to uncover diversity of wood-decaying fungi in neotropical Atlantic forests. DOI

Větrovský T., Baldrian P. (2013). Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. DOI

Voriškova J., Baldrian P. (2013). Fungal community on decomposing leaf litter undergoes rapid successional changes. PubMed DOI PMC

Walker J. F., Aldrich-Wolfe L., Riffel A., Barbare H., Simpson N. B., Trowbridge J., et al. (2011). Diverse helotiales associated with the roots of three species of artic ericaceae provide no evidence for host specificity. PubMed DOI

Wallander H., Johansson U., Sterkenburg E., Brandstrom Durling M., Lindahl B. D. (2010). Production of ectomycorrhizal mycelium peaks during canopy closure in Norway spruce forests. PubMed DOI

Wang Y., Naumann U., Wright S. T., Warton D. I. (2012). mvabund –An R package for model-based analysis of multivariate abundance data. DOI

Wardle D. A., Bardagett R. D., Klironomos J. N., Setala H., van der Putten W. H., Wall D. H. (2004). Ecological linkages between aboveground and belowground biota. PubMed DOI

Wazny R. (2014). Ectomycorrhizal communities associated with silver fir seedlings ( DOI

Ważny R., Kowalski S. (2017). Ectomycorrhizal fungal communities of silver-fir seedlings regenerating in fir stands and larch forecrops. DOI

Wickham H. (2016). DOI

Železnik P., Hrenko M., Then C., Koch N., Grebenc T., Levanič T., et al. (2007). CASIROZ: root parameters and types of ectomycorrhiza of young beech plants exposed to different ozone and light regimes. PubMed DOI

Železnik P., Vilhar U., Starr M., de Groot M., Kraigher H. (2016). Fine root dynamics in slovenian beech forests in relation to soil temperature and water availability. DOI