Abstract
Scleroderma is a gasteroid genus in the Boletales (Basidiomycota), with a cosmopolitan distribution. Species of Scleroderma establish ectomycorrhizal (ECM) symbiosis with a range of coniferous and non-coniferous trees and shrubs, both in temperate and tropical regions, with little tendency to host specificity, a feature that might have facilitated the wide distribution of the genus. With the contribution of confocal laser scanning microscopy, we describe the morpho-anatomical features of the ectomycorrhizae formed by Scleroderma meridionale on Halimium halimifolium, a cistaceous plant belonging to a small group of woody shrubs occurring in open vegetation types in the Mediterranean region. The mycobiont and host plant identity in ECM was verified through molecular tools. Mycorrhizal system is very small, up to 1.9 mm, mostly coralloid to irregularly pinnate. The mantle surface is felty, whitish with silver patches. Differentiated rhizomorphs occur infrequently. Mantle surface is characterized by a network of branched hyphae organized in hyphal boundles. Hyphae are frequently covered by granules or warts. These characters, except for the presence of granules, are similar to those reported for the only two naturally-occurring Scleroderma ECM described so far, i.e. S. bovista on Populus and S. citrinum on Betula and Pinus. On the other side, the peculiarity of S. meridionale + Halimium ECM is the particularly small dimension of mycorrhizal system, a character shared with ECM formed by Cistaceae. At the best of our knowledge, this is the first description of an ectomycorrhiza on Halimium, a plant whose mycorrhizal biology deserves to be explored in greater detail.






Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Agerer R (1986) Studies on ectomycorrhizae II. Introducing remarks on characterization and identification. Mycotaxon 26:473–492
Agerer R (ed) (1987–2012) Colour Atlas of Ectomycorrhizae. 15 parts. Einhorn-Verlag, Schwäbisch Gmünd
Agerer R (1991) Characterization of ectomycorrhiza. In: Norris JR, Read DJ, Varma AK (eds) Methods in Microbiology. Vol. 23. Techniques for the Study of Mycorrhiza. Academic Press, San Diego, pp 25–73
Agerer R (1995) Anatomical characteristics of identified ectomycorrhizae: an attempt towards a natural classification. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer-Verlag, Berlin, pp 685–734
Altschul SF, Gish W, Miller W, Myers EW, Lipman D (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Alvarado P, Manjón JL, Matheny PB, Esteve-Raventós F (2010) Tubariomyces, a new genus of Inocybaceae from the Mediterranean region. Mycologia 102:1389–1397
Baseia IG, Silva BDB, Ishikawa NK, Soares JVC, França IF, Ushijima S, Maekawa N, Martín MP (2016) Discovery or extinction of new Scleroderma species in Amazonia? PLoS One 11:e0167879
Beddiar A, Adouane M, Boudiaf I, Fraga A (2015) Mycorrhizal status of main spontaneous or introduced forest trees in el Tarf province (Algerian north-east). The Online Journal of Science and Technology 5:40–45
Brock PM, Doring H, Bidartondo MI (2009) How to know unknown fungi: the role of a herbarium. New Phytol 181:719–724
Brotzu R, Colomo S (2009) I funghi della Sardegna, vol 1–9. Editrice Archivio Fotografico Sardo, Nuoro, Italia
Brotzu R, Peintner U (2009) Cortinarius cedretorum var. halimiorum, a new variety of a Phlegmacium associated with Halimium halimifolium (Cistaceae) in Mediterranean costal sand dunes. Bresadoliana 1:25–44
Buée M, Vairelles D, Garbaye J (2005) Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus silvatica) forest subjected to two thinning regimes. Mycorrhiza 15:235–245
Buscardo E, Rodríguez-Echeverría S, Barrico L, García MÁ, Freitas H, Martín MP, De Angelis P, Muller LAH (2012) Is the potential for the formation of common mycorrhizal networks influenced by fire frequency? Soil Biol Biochem 46:136–144
Camprubi A, Estaun V, Calvet C (2011) Greenhouse inoculation of psammophilic plant species with arbuscular mycorrhizal fungi to improve survival and early growth. Eur J Soil Biol 47:194–197
Civeyrel L, Leclercq J, Demoly J-P, Agnan Y, Quèbre N, Pélissier C, Otto T (2011) Molecular systematics, character evolution, and pollen morphology of Cistus and Halimium (Cistaceae). Plant Syst Evol 295:23–54
Comandini O, Rinaldi AC (2001) Together, but not for ever: ectomycorrhizal symbiosis is an unstable affair. Mycol Res 105:130–131
Comandini O, Rinaldi AC (2008) Lactarius cistophilus Bon & Trimbach + Cistus sp. Descriptions of Ectomycorrhizae 11/12:83–88
Comandini O, Pacioni G, Rinaldi AC (1998) Fungi in ectomycorrhizal associations of silver fir (Abies alba miller) in Central Italy. Mycorrhiza 7:323–328
Comandini O, Haug I, Rinaldi AC, Kuyper TW (2004) Uniting Tricholoma sulphureum and T. bufonium. Mycol Res 108:1162–1171
Comandini O, Contu M, Rinaldi AC (2006) An overview of Cistus ectomycorrhizal fungi. Mycorrhiza 16:381–395
Comandini O, Erős-Honti Z, Jakucs E, Flores Arzú R, Leonardi M, Rinaldi AC (2012a) Molecular and morpho-anatomical description of mycorrhizas of Lactarius rimosellus on Quercus sp., with ethnomycological notes on Lactarius in Guatemala. Mycorrhiza 22:279–287
Comandini O, Rinaldi AC, Kuyper TW (2012b) Measuring and estimating ectomycorrhizal fungal diversity: a continuous challenge. In: Pagano M (ed) Mycorrhiza: occurrence in natural and restored environments. Nova Science Publishers, New York, pp 165–200
Crous PW, Wingfield MJ, Richardson DM, Leroux JJ, Strasberg D, Edwards J, Roets F, Hubka V, Taylor PWJ, Heykoop M, Martín MP, Moreno G, Sutton DA, Wiederhold NP, Barnes CW, Carlavilla JR, Gené J, Giraldo A, Guarnaccia V, Guarro J, Hernández-Restrepo M, Kolařík M, Manjón JL, Pascoe IG, Popov ES, Sandoval-Denis M, Woudenberg JHC, Acharya K, Alexandrova AV, Alvarado P, Barbosa RN, Baseia IG, Blanchette RA, Boekhout T, Burgess TI, Cano-Lira JF, Čmoková A, Dimitrov RA, Dyakov MY, Dueñas M, Dutta AK, Esteve-Raventós F, Fedosova AG, Fournier J, Gamboa P, Gouliamova DE, Grebenc T, Groenewald M, Hanse B, Hardy GESTJ, Held BW, Jurjević Ž, Kaewgrajang T, Latha KPD, Lombard L, Luangsa-ard JJ, Lysková P, Mallátová N, Manimohan P, Miller AN, Mirabolfathy M, Morozova OV, Obodai M, Oliveira NT, Ordóñez ME, Otto EC, Paloi S, Peterson SW, Phosri C, Roux J, Salazar WA, Sánchez A, Sarria GA, Shin HD, Silva BDB, Silva GA, Smith MTH, Souza-Motta CM, Stchigel AM, Stoilova-Disheva MM, Sulzbacher MA, Telleria MT, Toapanta C, Traba JM, Valenzuela-Lopez N, Watling R, Groenewald JZ (2016) Fungal planet description sheets: 400–468. Persoonia 36:316–458
Demoulin V, Malençon G (1970) [1971] Un nouveau Scléroderma méditerranéo-sud-atlantique: Scleroderma meridionale Demoulin & Malençon, spec. nov. Bulletin de la Société Mycologique de France 86:699–704
Dimou DM, Polemis E, Konstantinidis G, Kaounas V, Zervakis GI (2016) Diversity of macrofungi in the Greek islands of Lesvos and Agios Efstratios, NE Aegean Sea. Nova Hedwigia 102:439–475
Eberhardt U, Oberwinkler F, Verbeken A, Pacioni G, Rinaldi AC, Comandini O (2000) Lactarius ectomycorrhizae on Abies alba: morphological description, molecular characterization, and taxonomic remarks. Mycologia 92:860–873
Flores Arzú R, Comandini O, Rinaldi AC (2012) A preliminary checklist of macrofungi of Guatemala, with notes on edibility and traditional knowledge. Mycosphere 3:1–21
Gardes M, Bruns TD (1993) ITS primers with specificity for basidiomycetes: application to the identification of mycorrhizae and rust. Mol Ecol 2:113–118
Guzmán G, Ovrebo CL (2000) New observations on sclerodermataceous fungi. Mycologia 92:174–179
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Ingleby K (1999) Scleroderma sinnamarense Mont. + Gnetum africanum Welw. Descriptions of Ectomycorrhizae 4:127–133
Iotti M, Zambonelli A (2006) A quick and precise technique for identifying ectomycorrhizae by PCR. Mycol Res 110:60–65
Jakucs E, Agerer R (1999) Scleroderma bovista Fr. + Populus alba L. Descriptions of Ectomycorrhizae 4:121–126
Jeffries P (1999) Scleroderma. In: Ectomycorrhizal fungi key genera in profile. Springer, Berlin, pp 187–200
Jeppson M, Piątek M (2005) Scleroderma septentrionale (fungi, basidiomycetes), first records from Central Europe. Pol Bot J 50:15–17
Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518
Kirk PM, Cannon PF, David JC, Stalpers JA (eds) (2008) Ainsworth and Bisby’s Dictionary of the Fungi, 10th edn. CABI Publishing, Wallingford
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Kumla J, Suwannarach N, Bussaban B, Lumyong S (2013) Scleroderma suthepense, a new ectomycorrhizal fungus from Thailand. Mycotaxon 123:1–7
Lee SS, Alexander IJ, Watling R (1997) Ectomycorrhizae and putative ectomycorrhizal fungi of Shorea lerosula Miq. (Dipterocarpaceae). Mycorrhiza 7:63–81
Leonardi M, Paolocci F, Rubini A, Simonini G, Pacioni G (2005) Assessment of inter- and intra-specific variability in the main species of Boletus edulis complex by ITS analysis. FEMS Microbiol Lett 243:411–416
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
Leonardi M, Comandini O, Rinaldi AC (2016) Peering into the Mediterranean black box: Lactifluus rugatus ectomycorrhizae on Cistus. IMA Fungus 7:275–284
Meotto F, Pellegrino S, Craddock JH (1994) Funghi ectomicorrizici del castagno con particolare riferimento ai funghi eduli. Italus Hortus 2:58–64
Moreau PA, Corriol G, Borgarino D, Auber P, Lavoise C, Richard F, Selosse M-A (2007) Contribution à la connaissance des champignons de l’étage thermoméditerranéen Corse II. Bulletin Semestriel de de la Fédération des Associations Mycologiques Méditerranéennes 31:9–31
Mrak T, Kühdorf K, Grebenc T, Štraus I, Münzenberger B, Kraigher H (2016) Scleroderma areolatum ectomycorrhizae on Fagus sylvatica L. Mycorrhiza 27:283–293
Munsell (2000) Soil color charts. Munsell Color Company, Grand Rapids
Nei M, Kumar S (2000) Molecular evolution and Phylogenetics. Oxford University Press, New York
Nuytinck J, Verbeken A, Leonardi M, Pacioni G, Rinaldi AC, Comandini O (2004) Characterization of Lactarius tesquorum ectomycorrhizae on Cistus sp., and molecular phylogeny of related European Lactarius taxa. Mycologia 96:272–282
Oria-de-Rueda JA, Martín-Pinto P, Olaizola J (2008) Bolete productivity of Cistaceous scrublands in northwestern Spain. Econ Bot 62:323–330
Phosri C, Martín MP, Watling R, Jeppson M, Sihanonth P (2009) Molecular phylogeny and re-assessment of some Scleroderma spp. (Gasteromycetes). Anales Jard Bot Madrid 66S1:83–91
Richter DL, Bruhn JN (1989) Pinus resinosa ectomycorrhizae: seven host-fungus combinations synthesized in pure culture. Symbiosis 7:211–228
Rinaldi AC, Comandini O, Kuyper TW (2008) Ectomycorrhizal fungal diversity: separating the wheat from the chaff. Fungal Divers 33:1–45
Roy M, Vasco-Palacios A, Geml J, Buyck B, Delgat L, Giachini A, Grebenc T, Harrower E, Kuhar F, Magnago A, Rinaldi AC, Schimann H, Selosse M-A, Sulzbacher MA, Wartchow F, Neves M-A (2017) The (re)discovery of ectomycorrhizal symbioses in Neotropical ecosystems sketched in Florianópolis. New Phytol 214:920–923
Ruiz-Díez B, Rincón AM, de Felipe MR, Fernández-Pascual M (2006) Molecular characterization and evaluation of mycorrhizal capacity of Suillus isolates from Central Spain for the selection of fungal inoculants. Mycorrhiza 16:465–474
Rusevska K, Karadelevi M, Phosri C, Dueñas M, Watling R, Martín MP (2014) Rechecking of the genus Scleroderma (Gasteromycetes) from Macedonia using barcoding approach. Turk J Bot 38:375–385
Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San Diego
Taudiere A, Munoz F, Lesne A, Monnet A-C, Bellanger J-M, Selosse M-A, Moreau P-A, Richard F (2015) Beyond ectomycorrhizal bipartite networks: projected networks demonstrate contrasted patterns between early- and late-successional plants in Corsica. Front Plant Sci 6:881
Tedersoo L, Jairus T, Horton BM, Abarenkov K, Suvi T, Saar I, Kõljalg U (2008) Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytol 180:479–490
Thorogood C (2016) Field guide to the wild flowers of western Mediterranean. Kew Publishing, Kew
Waller K, Raidl S, Agerer R (1993) Die Ektomykorrhizen von Scleroderma citrinum. Zeitschrift für Mykologie 59:141–153
White TJ, Bruns T, 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 (eds) PCR Protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Wilson AW, Binder M, Hibbett DS (2011) Effects of gasteroid fruiting body morphology on diversification rates in three independent clades of fungi estimated using binary state speciation and extinction analysis. Evolution 65:1305–1322
Wilson AW, Binder M, Hibbett DS (2012) Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota). New Phytol 194:1079–1095
Zunzunegui M, Ain-Lhout F, Díaz Barradas MC, Álvarez-Cansino LA, Esquivias MP, García Novo F (2009) Physiological, morphological and allocation plasticity of a semi-deciduous shrub. Acta Oecol 35:370–379
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Fig. 1S
Identification of the plant host, through analysis of length differences of the chloroplast trnL region. Specific amplicons generated from DNA of Halimium halimifolium leaves (lane 1, positive control) and Scleroderma meridionale ectomycorrhizae (lanes 2 and 3). (JPEG 228 kb)
Rights and permissions
About this article
Cite this article
Leonardi, M., Neves, MA., Comandini, O. et al. Scleroderma meridionale ectomycorrhizae on Halimium halimifolium: expanding the Mediterranean symbiotic repertoire. Symbiosis 76, 199–208 (2018). https://doi.org/10.1007/s13199-018-0548-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13199-018-0548-1


