GIORGIO LALLI, MARCO LEONARDI, MARILENA ODDIS, GIOVANNI PACIONI, ELENA SALERNI, MIRCO IOTTI, ALESSANDRA ZAMBONELLI

Expanding the understanding of a forest ectomycorrhizal community by combining root tips and fruiting bodies: a case study of Tuber magnatum stands

A survey of both ectomycorrhizal (ECM) root tips and fruiting bodies of ECM fungi was carried out during a four-year period (2009-2012) in two similar forest stands in central Italy, previously investigated in detail being habitats of the Italian white truffle Tuber magnatum Pico. This research is one of the few conducted in mixed forest stands and, for the first time, it took into account the cryptic fungi (corticiaceous, hypogeous, and sclerotia). This survey led to an exhaustive description of the ECM community by integrating all the 197 taxa recorded (147 species as fruiting bodies, 65 as ectomycorrhizas, and 15 overlapping taxa recorded by both systems), and it also revealed a discrepancy between the results obtained using these two different approaches. In fact, a prevalence of Russulaceae, Inocybaceae, and Cortinariaceae resulted from fruiting body observations, whereas Thelephoraceae and Sebacinaceae dominated the ECM root tips. This result suggests a probable flaw in the sampling methodology. There may be several causes of this phenomenon, including the different nutritional strategies of ectomycorrhizal fungi and their seasonal turnover. Some species that could be candidates as bioindicators of T. Magnatum habitat in mixed forest were identified.

Anahtar Kelimeler:

Biodiversity, forest ecology, fungal community, mycorrhizal symbiosis, white truffle

Expanding the understanding of a forest ectomycorrhizal community by combining root tips and fruiting bodies: a case study of Tuber magnatum stands

Keywords:

Biodiversity, forest ecology, fungal community, mycorrhizal symbiosis, white truffle,

PDF

___

Agerer R (1987–2008). Colour Atlas of Ectomycorrhizae (1st–14th delivery). Germany: Einhorn-Verlag, Schwäbisch Gmünd.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.
Amicucci A, Zambonelli A, Giomaro G, Potenza L, Stocchi V (1998). Identification of ectomycorrhizal fungi of the genus Tuber by species-specific ITS primers. Mol Ecol 7: 273–277.
Ashkannejhad S, Horton TR (2006). Ectomycorrhizal ecology under primary succession on coastal sand dunes: interactions involving Pinus contorta, suilloid fungi and deer. New Phytol 169: 345–354.
Baciarelli-Falini L, Rubini A, Riccioni C, Paolocci F (2006). Morphological and molecular analyses of ectomycorrhizal diversity in a man-made Tuber melanosporum plantation: description of novel truffle-like morphotypes. Mycorrhiza 16: 475–484.
Badalyan SM, Hovsepyan, RA, Iotti M, Zambonelli A (2005). On the presence of truffles in Armenia. Flora Mediterranea 15: 683–692.
Bertini L, Rossi I, Zambonelli A, Amicucci A, Sacchi A, Cecchini M, Gregori G, Stocchi V (2006). Molecular identification of Tuber magnatum ectomycorrhizas in the field. Microbiol Res 161: 59–64.
Bonito G, Brenneman T, Vilgalys R (2011). Ectomycorrhizal fungal diversity in orchards of cultivated pecan (Carya illinoinensis; Juglandaceae). Mycorrhiza 21: 601–612.
Bray JR, Curtis JT (1957). An ordination of upland forest communities of southern Wisconsin. Ecol Monog 27: 325–349.
Brundett M (2004). Diversity and classification of mycorrhizal associations. Biol Rev 79: 473–495.
Buée M, De Boer W, Martin F, van Overbeek L, Jurkevitch E (2009). The rhizosphere zoo: An overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil 321: 189–212.
Courty P-E, Franc A, Pierrat J-C, Garbaye J (2008). Temporal changes in the ectomycorrhizal community in two soil horizons of a temperate oak forest. Appl Environ Microb 74: 5792–5801.
Gardes M, Fortin J, White TJ, Bruns TD, Taylor JW (1991). Identification of indigenous and introduced symbiotic fungi in mycorrhizae by amplification of the internal transcribed spacer. Can J Bot 69: 180–190.
Gardes M, Bruns TD (1993). ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113–118.
Gardes M, Bruns TD (1996). Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above- and belowground views. Can J Bot 74: 1572–1583.
Giovannetti G (1983). Nella coltivazione il futuro del tartufo bianco. Informatore Agrario 39: 27464–27466 (in Italian). Gryndler M, Černá L, Bukovská P, Hršelová H, Jansa J (2014). Tuber aestivum association with non-host roots. Mycorrhiza 24: 603–610.
Imhof S (2009). Arbuscular, ecto-related, orchid mycorrhizas - three independent structural lineages towards mycoheterotrophy: implications for classification? Mycorrhiza 19: 357–363.
Iotti M, Zambonelli A (2006). A quick and precise technique for identifying ectomycorrhizas by PCR. Mycol Res 110: 60–65.
Koide RT, Xu B, Sharda J (2005). Contrasting below-ground views of an ectomycorrhizal fungal community. New Phytol 166: 251–262.
Krpata D, MühlmannO, Kuhnert R, Ladurner H, Göbl F, Peintner U (2007). High diversity of ectomycorrhizal fungi associated with Arctostaphylos uva-ursi in subalpine and alpine zones: potential inoculum for afforestation. Forest Ecol Manag 250: 167–175.
Laganà A, Salerni E, Barluzzi C, Perini C, De Dominicis V (1999). Mycocoenological studies in Mediterranean forest ecosystems: calcicolous deciduous oak woods of central-southern Tuscany (Italy). Czech Mycology 52: 1–16.
Lancellotti E, Iotti M, Zambonelli A, Franceschini A (2014). Characterization of Tuber borchii and Arbutus unedo mycorrhizas. Mycorrhiza 24: 481–486.
Landeweert R, Leeflang P, Kuyper TW, Hoffland E, Rosling A, Wernars K, Smit E (2003). Molecular identification of ectomycorrhizal mycelium in soil horizons. Appl Environ Microb 69: 327–333.
Leonardi M, Iotti M, Oddis M, Lalli G, Pacioni G, Leonardi P, Maccherini S, Perini C, Salerni E, Zambonelli A (2013).
Assessment of ectomycorrhizal fungal communities in the natural habitats of Tuber magnatum (Ascomycota, Pezizales). Mycorrhiza 23: 349–358.
McCune B, Grace JB (2002). Analysis of ecological communities. Gleneden Beach, OR, USA: MjM Software Design.
Mühlmann O, Bacher M, Peintner U (2008). Polygonum viviparum mycobionts on an alpine primary successional glacier forefront. Mycorrhiza 18: 87–95.
Murat C, Vizzini A, Bonfante P, Mello A (2005). Morphological and molecular typing of the below-ground fungal community in a natural Tuber magnatum truffle-ground. FEMS Microbiol Lett 245: 307–313.
Nara K, Nakaya H, Hogetsu T (2003). Ectomycorrhizal sporocarp succession and production during early primary succession on Mount Fuji. New Phytol 158: 193–206.
Nara K (2008). Community development patterns and ecological functions of ectomycorrhizal fungi: implications from primary succession. In: Varma A, editor. Mycorrhiza: State of the Art, Genetics and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure and Systematics. Berlin, Germany: Springer-Verlag, pp. 581–599.
Pacioni G (1991). Wet-sieving and decanting technique for spore extraction. In: Varma AK, Trappe JM, Fortin JA, Norris JR, editors. Methods in Microbiology, Vol. 23, Experiments with Mycorrhizae. London, UK: Academic Press, pp. 317–322.
Pacioni G, Comandini O, Rinaldi AC (2001). An assessment of below-ground ectomycorrhizal diversity of Abies alba Miller in central Italy. Plant Biosyst 135: 337–350.
Paolocci F, Rubini A, Granetti B, Arcioni S (1999). Rapid molecular approach for a reliable identification of Tuber spp. ectomycorrhizas. FEMS Microbiol Ecol 28: 23–30.
Peintner U, Iotti M, Klotz P, Bonuso E, Zambonelli A (2007). Soil fungal communities in a Castanea sativa (chestnut) forest producing large quantities of Boletus edulis sensu lato (porcini): where is the mycelium of porcini? Environ Microbiol 9: 880– 889.
Rinaldi AC, Comandini O, Kuyper TW (2008). Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33: 1–45.
Selosse MA, Faccio A, Scappaticci G, Bonfante P (2004). Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microb Ecol 47: 416–426.
Smith ME, Douhan GW, Rizzo DM (2007). Ectomycorrhizal community structure in a xeric Quercus woodland based on rDNA sequence analysis of sporocarps and pooled roots. New Phytol 174: 847–863.
Taylor AFS (2002). Fungal diversity in ectomycorrhizal communities: sampling effort and species detection. Plant Soil 244: 19–28.
Tedersoo L, Kõljalg U, Hallenberg N, Larsson K-H (2003). Fine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest. New Phytol 159: 153–165.
Urban A, Puschenreiter M, Strauss J, Gorfer M (2008). Diversity and structure of ectomycorrhizal and co-associated fungal communities in a serpentine soil. Mycorrhiza 18: 339–354.
Van der Heijden MGA, Bardgett RD, van Straalen NM (2008). The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11: 296–310.
Vogt KA, Bloomfield J, Ammirati JF, Ammirati SR (1992). Sporocarp production by basidiomycetes with emphasis of forest ecosystems. In: Carroll GC, Wicklow DT, editors. The Fungal Community, Its Organization and Role in the Ecosystem. 2nd ed. New York, NY, USA: Marcel Dekker Inc., pp. 563–581.
White TJ, Bruns TD, Lee S, Taylor J (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR Protocols: a Guide to Methods and Applications. San Diego, CA, USA: Academic Press, pp. 315–322.