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Mallocybe heimii ectomycorrhizae with Cistus creticus and Pinus halepensis in Mediterranean littoral sand dunes — assessment of phylogenetic relationships to M. arenaria and M. agardhii

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Abstract

Ectomycorrhizal symbiosis appears extensively in the Northern Hemisphere, where Mediterranean ecosystems constitute an important ecological area of considerable biodiversity value. Littoral sand dunes are among high-risk habitats, and ectomycorrhizal lifestyle contributes significantly to supporting life in such regions. Mallocybe heimii (Bon) Matheny & Esteve-Rav. (Inocybaceae, Basidiomycota) and the very similar M. arenaria (Bon) Matheny & Esteve-Rav. grow in poor, usually sandy soils, in association with angiosperms or gymnosperms. Basidiomata originally identified under these names were collected from littoral sand dunes of Greece, and their morpho-anatomical characteristics were examined in conjunction with material derived from other European regions. Sequences from basidiomata and root tips corresponding to the nuclear rDNA internal transcribed spacer region (ITS) and large subunit (LSU) were obtained and analyzed. Phylogenetic results demonstrated that material identified as M. heimii or M. arenaria form a single well-supported group, while M. agardhii (N. Lund) Matheny & Esteve-Rav. is confirmed to be distinct from M. arenaria (the latter was initially described as a variety of the former, i.e., I. agardhii var. arenaria Bon). A detailed tree of the genus Mallocybe was generated on the basis of concatenated ITS and LSU sequences, and relationships of selected taxa are discussed in the light of morphological and sequence data. In addition, the first morphotype descriptions of M. heimii ectomycorrhizae with Cistus creticus L. and Pinus halepensis Miller are hereby provided. Both morphotypes exhibited the typical characteristics of Inocybe/Mallocybe ectomycorrhizae; however, differences were noted, the most significant being the presence of clamps on mantle hyphae and the type of anastomoses.

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Data availability

Basidiomata examined in this study are deposited in the fungarium (ACAM) of the Agricultural University of Athens, Laboratory of General and Agricultural Microbiology, at the Eötvös Loránd University, Budapest and at the personal collection of D. Bandini. In addition, mycorrhizal material (root tips) is stored at the former Institution. All data and material are available upon request.

References

  • Agerer R (1987–2002) Colour atlas of ectomycorrhizae. Einhorn-Verlag Eduard Dietenberger GmbH, München.

  • Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog 5(2):67–107. https://doi.org/10.1007/s11557-006-0505-x

    Article  Google Scholar 

  • Agerer R, Rambold G (2004–2021) DEEMY – an information system for characterization and determination of ectomycorrhizae. München, Germany. http://www.deemy.de. Accessed 13 January 2021

  • Agerer R, Hartmann A, Pritsch K et al (2012) Plants and their ectomycorrhizosphere: cost and benefit of symbiotic soil organisms. In: Matyssek R, Schnyder H, Oßwald W, Ernst D, Munch JC, Pretzsch H (eds). Growth and Defence in Plants, Ecological Studies 220, Springer-Verlag Berlin Heidelberg:213–242. https://doi.org/10.1007/978-3-642-30645-7_10

  • Agueda B, Parladé J, de Miguel AM, Martínez-Peña F (2006) Characterization and identification of field ectomycorrhizae of Boletus edulis and Cistus ladanifer. Mycologia 98(1):23–30. https://doi.org/10.1080/15572536.2006.11832709

    Article  PubMed  Google Scholar 

  • Ariyawansa HA, Hyde KD, Jayasiri SC, Buyck B et al (2015) Fungal diversity notes 111–252-taxonomic and phylogenetic contributions to fungal taxa. Fungal Divers 75(1):27–274. https://doi.org/10.1007/s13225-015-0346-5

    Article  Google Scholar 

  • Bas C, Kuyper TW, Noordeloos ME, Vellinga EC (1988) Flora Agaricina Neerlandica, vol 1. AA Balkema Publishes, Brookfield

    Google Scholar 

  • Beenken L (1996a) Inocybe fuscomarginata. In: Agerer R. (ed) Colour atlas of ectomycorrhizae. Einhorn–Verlag, Schwäbisch Gmünd, München, table 95

  • Beenken L (1996b) Inocybe terrigena. In: Agerer R. (ed) Colour atlas of ectomycorrhizae. Einhorn–Verlag, Schwäbisch Gmünd, München, table 97

  • Beenken L, Agerer R, Bahnweg G (1996a) Inocybe fuscomarginata Kühn. + Salix spec Populus Nigra l. Descr Ectomyc 1:41–46

    Google Scholar 

  • Beenken L, Agerer R, Bahnweg G (1996b) Inocybe terrigena (Fr.) Kuyper + Pinus sylvestris L. Descr Ectomyc 1:53–58

    Google Scholar 

  • Bon M (1983) Novitates – Validations et taxons nouveaux. Doc Mycol 13(50):27–28

    Google Scholar 

  • Bon M (1984) Macromycètes de la zone maritime picarde (8ème supplément). Les Inocybes Sabulicoles Doc Mycol 14(53):9–40

    Google Scholar 

  • Brugaletta E, Consiglio G, Marchetti M (2017) Inocybe siciliana, una nuova specie del sottogenere Mallocybe. Riv Micol 60(3):195–209

    Google Scholar 

  • Brundrett MC, Murase G, Kendrick B (1990) Comparative anatomy of roots and mycorrhizae of common Ontario trees. Can J Bot 68:551–578. https://doi.org/10.1139/b90-076

    Article  Google Scholar 

  • Buscardo E, Rodríguez-Echeverría S, Barrico L, García MÁ, Freitas H, Martín MP, De Angelis P, Muller LA (2012) Is the potential for the formation of common mycorrhizal networks influenced by fire frequency? Soil Biol Biochem 46:136–144. https://doi.org/10.1016/j.soilbio.2011.12.007

    Article  CAS  Google Scholar 

  • Comandini O, Rinaldi AC (2008) Lactarius cistophilus Bon & Trimbach + Cistus sp. Descr Ectomyc 11(12):83–88

    Google Scholar 

  • Cripps CL, Larsson E, Horak E (2010) Subgenus Mallocybe (Inocybe) in the Rocky Mountain alpine zone with molecular reference to European arctic-alpine material. N Am Fungi 5:97–126. https://doi.org/10.2509/naf2010.005.0057

    Article  Google Scholar 

  • Crous PW, Wingfield MJ, Chooi YH et al (2020) Fungal Planet description sheets: 1042–1111. Persoonia 44:301. https://doi.org/10.3767/persoonia.2020.44.11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daskalopoulos V, Polemis E, Fryssouli V, Kottis L, Zervakis GI (2017) Ectomycorrhizal fungi of the genus Inocybe associated with plants of the genera Pinus and Cistus. In Proceedings of the 7th Congress of the Scientific Society Mikrobiokosmos, p. 194 (abstract). Mikrobiokosmos, Athens

  • Daskalopoulos V, Polemis E, Fryssouli V, Zervakis GI (2019) Diversity of ectomycorrhizal fungi from littoral sand dunes with thermophilous pine forests in Greece. In Proceedings of the 8th Congress of the Scientific Society Mikrobiokosmos, p. 91 (abstract). Mikrobiokosmos, Patras

  • Davies CE, Moss D, Hill MO (2004) EUNIS habitat classification revised 2004. Report to the European Topic Centre on Nature Protection and Biodiversity. European Environment Agency, 307

  • Erős-Honti Z, Jakucs E, Kovács GM (2008) Helianthemirhiza ochraceobrunnescens + Helianthemum canum (L.) Baumg. Descr Ectomyc 11/12:71–75

  • Ferrari E (2010) Inocybe dai litorali alla zona alpina. In: Ferrari E (ed) Fungi non delineati. Edizioni Candusso, Saronno

  • Franchi P, Gorreri L, Marchetti M, Monti G (2001) Funghi di ambienti dunali. Ente Parco Regionale Migliarino San Rossore. Grafiche 2000, Ponsacco

  • Giovannetti G, Fontana A (1982) Mycorrhizal synthesis between Cistaceae and Tuberaceae. New Phytol 92(4):533–537. https://doi.org/10.1111/j.1469-8137.1982.tb03412.x

    Article  Google Scholar 

  • Hahn C (2001) Boletus rhodoxanthus Kallenb. + Cistus cf. ladanifer L. Descr Ectomyc 5:15–22

    Google Scholar 

  • Iotti M, Marchetti M, Bonuso E, Zambonelli A (2005) Morphological and molecular characterization of the mycorrhizas of Inocybe rufuloides and I. splendens. Mycotaxon 94:75–84

    Google Scholar 

  • Jakucs E, Magyar L, Beenken L (1999) Hebeloma ammophilum Bohus + Fumana procumbens (Dun.) Gr. Godr Descr Ectomyc 4:49–54

    Google Scholar 

  • Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20(4):1160–1166. https://doi.org/10.1093/bib/bbx108

    Article  CAS  PubMed  Google Scholar 

  • Kosentka P, Sprague SL, Ryberg M, Gartz J, May AL, Campagna SR, Matheny PB (2013) Evolution of the toxins muscarine and psilocybin in a family of mushroom-forming fungi. PLoS ONE 8(5):64646. https://doi.org/10.1371/journal.pone.0064646

    Article  CAS  Google Scholar 

  • Kovács GM, Jakucs E (2001) Helianthemirhiza hirsuta + Helianthemum ovatum (Viv.) Dun. Descr Ectomyc 5:49–53

    Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuyper TW (1986) A revision of the genus Inocybe in Europe. I. Subgenus Inosperma and the smooth-spored species of subgenus Inocybe. Persoonia-Supplement 3.1:1–247

  • Lantieri A, Gargano ML, Venturella G (2009) The sabulicolous fungi from Sicily (southern Italy): additions and critical review. Mycotaxon 110:151–154. https://doi.org/10.5248/110.151

    Article  Google Scholar 

  • Larsson E, Ryberg M, Moreau PA, Mathiesen AD, Jacobsson S (2009) Taxonomy and evolutionary relationships within species of section Rimosae (Inocybe) based on ITS, LSU and mtSSU sequence data. Persoonia 23:86–98. https://doi.org/10.3767/003158509X475913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larsson E, Vauras J, Cripps CL (2017) Inocybe lemmi, a new species of section Marginatae from the alpine region of Sweden. Karstenia 57:1–9. https://doi.org/10.29203/ka.2017.478

  • Leonardi M, Comandini O, Rinaldi AC (2016) Peering into the Mediterranean black box: Lactifluus rugatus ectomycorrhizas on Cistus. IMA Fungus 7(2):275. https://doi.org/10.5598/imafungus.2016.07.02.07

    Article  PubMed  PubMed Central  Google Scholar 

  • Leonardi M, Neves MA, Comandini O, Rinaldi AC (2018) Scleroderma meridionale ectomycorrhizae on Halimium halimifolium: expanding the Mediterranean symbiotic repertoire. Symbiosis 76(2):199–208. https://doi.org/10.1007/s13199-018-0548-1

    Article  CAS  Google Scholar 

  • Leonardi M, Furtado ANM, Comandini O, Geml J, Rinaldi AC (2020) Halimium as an ectomycorrhizal symbiont: new records and an appreciation of known fungal diversity. Mycol Prog 19(12):1495–1509. https://doi.org/10.1007/s11557-020-01641-0

    Article  Google Scholar 

  • Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucl Acids Res 44(W1):W242–W245. https://doi.org/10.1093/nar/gkw290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ludwig E (2017) Pilzkompendium, vol 4 (parts 1 & 2). Fungicon, Berlin

  • Magyar L, Beenken L, Jakucs E (1999) Inocybe heimii Bon + Fumana procumbens (Dun.) Gr. Godr Descr Ectomyc 4:61–65

    Google Scholar 

  • Maire JC, Sick G (2009) Révision des Inocybe léiosporés (sauf Cervicolores et Lactiferae), En: Compléments à la flore des champignons supérieurs du Maroc de G. Malençon et R. Bertault, Confédération Européenne de Mycologie Méditerranéenne, Nice, pp. 225–227

  • Malençon G, Bertault R (1970) Flore des champignons supérieurs du Maroc, Faculté de Sciences, Rabat

  • Martínez ML, Maun AM, Psuty N (2004) The fragility and conservation of the world’s coastal dunes: geomorphological, ecological and socioeconomic perspectives. In: Martínez ML, Psuty N (eds) Coastal dunes: ecology and conservation. Springer, Heidelberg, pp 355–369. https://doi.org/10.1007/978-3-540-74002-5_21

  • Matheny PB (2005) Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Mol Phylogenet Evol 35(1):1–20. https://doi.org/10.1016/j.ympev.2004.11.014

    Article  CAS  PubMed  Google Scholar 

  • Matheny PB (2009) A phylogenetic classification of the Inocybaceae. McIlvainea 18(1):11–21

    Google Scholar 

  • Matheny PB, Aime MC, Bougher NL, Buyck B, Desjardin DE, Horak E, Kropp BR, Lodge DJ, Soytong K, Trappe JM, Hibbett DS (2009) Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae. J Biogeogr 36(4):577–592. https://doi.org/10.1111/j.1365-2699.2008.02055.x

    Article  Google Scholar 

  • Matheny PB, Bougher NL (2017) Fungi of Australia: Inocybaceae. CSIRO Publishing, Australia

    Google Scholar 

  • Matheny PB, Curtis JM, Hofstetter V et al (2006) Major clades of Agaricales: a multilocus phylogenetic overview. Mycologia 98(6):982–995. https://doi.org/10.3852/mycologia.98.6.982

    Article  PubMed  Google Scholar 

  • Matheny PB, Hobbs AM, Esteve-Raventós F (2020) Genera of Inocybaceae: new skin for the old ceremony. Mycologia 112(1):83–120. https://doi.org/10.1080/00275514.2019.1668906

    Article  PubMed  Google Scholar 

  • Matheny PB, Kudzma LV (2019) New species of Inocybe (Agaricales) from eastern North America. J Torrey Bot Soc 146:213–235. https://doi.org/10.3159/TORREY-D-18-00060.1

    Article  Google Scholar 

  • Matheny PB, Wang Z, Binder M et al (2007) Contributions of rpb2 and tef1 to the phylogeny of mushrooms and allies (Basidiomycota, Fungi). Mol Phylogenet Evol 43(2):430–451. https://doi.org/10.1016/j.ympev.2006.08.024

    Article  CAS  PubMed  Google Scholar 

  • Miller MA (2010) CIPRES Science Gateway survey results. http://www.phylo.org/tools/survey2.html. Accessed 13 June 2021

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501

    Article  CAS  PubMed  Google Scholar 

  • Nilsson RH, Larsson K-H, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I, Kõljalg U, Abarenkov K (2018) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47(D1):D259–D264. https://doi.org/10.1093/nar/gky1022

    Article  CAS  PubMed Central  Google Scholar 

  • Nuytinck J, Verbeken A, Rinaldi AC, Leonardi M, Pacioni G, Comandini O (2004) Characterization of Lactarius tesquorum ectomycorrhizae on Cistus sp. and molecular phylogeny of related European Lactarius taxa. Mycologia 96(2):272–282. https://doi.org/10.2307/3762063

  • Okonechnikov K, Golosova O, Fursov M (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28:1166–1167. https://doi.org/10.1093/bioinformatics/bts091

    Article  CAS  PubMed  Google Scholar 

  • Osmundson TW, Robert VA, Schoch CL, Baker LJ, Smith A, Robich G, Mizzan L, Garbelotto MM (2013) Filling gaps in biodiversity knowledge for macrofungi: contributions and assessment of an herbarium collection DNA barcode sequencing project. PloS One 8(4). https://doi.org/10.1371/journal.pone.0062419

  • Pancorbo F, Ribes MA, Campos JC, Mateo JF, Merino D, Tello S et al (2014) Estudio de la microbiota de los sistemas dunares de la Península Ibérica e Islas Baleares II. Bol Soc Micol Madrid 38:183–214

    Google Scholar 

  • Picón RM (2007) Macromicetos de las dunas del litoral cantábrico II. ZIZAK 4:51–73

    Google Scholar 

  • Piel WH, Chan L, Dominus MJ, Ruan J, Vos RA, Tannen V (2009) TreeBASE v. 2: A Database of Phylogenetic Knowledge. In: e-BioSphere 2009.

  • Polemis E, Dimou DM, Tzanoudakis D, Zervakis GI (2012a) Diversity of Basidiomycota (subclass Agaricomycetidae) in the island of Andros (Cyclades, Greece). Nova Hedwig 95:25–35

    Article  Google Scholar 

  • Polemis E, Dimou DM, Tzanoudakis D, Zervakis GI (2012b) Annotated checklist of Basidiomycota (subclass Agaricomycetidae) from the islands of Naxos and Amorgos (Cyclades, Greece). Ann Bot Fenn 49:145–161. https://doi.org/10.5735/085.049.0301

  • Polemis E, Kottis L, Konstantinidis G, Zervakis GI (2015) Ectomycorrhizal and other sabulicolous macrofungi from sand dune ecosystems of coastal Greece. In Proceedings of XVII Congress of European Mycologists, p. 129 (abstract), Madeira, Portugal

  • Polemis E, Nuytinck J, Fryssouli V, Pera U, Zervakis GI (2019) Phylogeny, ecology and distribution of the rare Mediterranean species Lactarius pseudoscrobiculatus (Basidiomycota, Russulales). Plant Syst Evol 305(9):755–764. https://doi.org/10.1007/s00606-019-01604-3

    Article  CAS  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256. https://doi.org/10.1093/molbev/msn083

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryberg M (2009) An evolutionary view of the taxonomy and ecology of Inocybe (Agaricales) with new perspectives gleaned from GenBank metadata. PhD Thesis, University of Gothenburg, Department of Plant and Environmental Sciences. http://hdl.handle.net/2077/19692

  • Ryberg M, Nilsson RH, Kristiansson E, Töpel M, Jacobsson S, Larsson E (2008) Mining metadata from unidentified ITS sequences in GenBank: a case study in Inocybe (Basidiomycota). BMC Evol Biol 8:50. https://doi.org/10.1186/1471-2148-8-50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryberg M, Larsson E, Jacobsson S (2010) An evolutionary perspective on morphological and ecological characters in the mushroom family Inocybaceae (Agaricomycotina, Fungi). Mol Phylogenet Evolution 55(2):431–442. https://doi.org/10.1016/j.ympev.2010.02.011

    Article  Google Scholar 

  • Saba M, Khalid AN (2020) Mallocybe velutina (Agaricales, Inocybaceae), a new species from Pakistan. Mycoscience 61(6):348–352. https://doi.org/10.1016/j.myc.2020.06.006

    Article  Google Scholar 

  • Seress D, Dima B, Kovács GM (2016) Characterisation of seven Inocybe ectomycorrhizal morphotypes from a semiarid woody steppe. Mycorrhiza 26(3):215–225. https://doi.org/10.1007/s00572-015-0662-3

    Article  PubMed  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taschen E, Sauve M, Taudiere A, Parlade J, Selosse MA, Richard F (2015) Whose truffle is this? Distribution patterns of ectomycorrhizal fungal diversity in Tuber melanosporum brûlés developed in multi-host Mediterranean plant communities. Environ Microbiol 17(8):2747–2761. https://doi.org/10.1111/1462-2920.12741

    Article  PubMed  Google Scholar 

  • Tedersoo L, Brundrett MC (2017) Evolution of ectomycorrhizal symbiosis in plants. In: Tedersoo L. (eds). Biogeography of Mycorrhizal Symbiosis. Ecological Studies (Analysis and Synthesis), vol 230. Springer International Publishing. https://doi.org/10.1007/978-3-319-56363-3_19

  • Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263. https://doi.org/10.1007/s00572-009-0274-x

    Article  PubMed  Google Scholar 

  • Torres P, Roldan A, Lansac AR, Martin A (1995) Ectomycorrhizal formation between Cistus ladanifer and Laccaria laccata. Nova Hedwigia 60:311–315

    Google Scholar 

  • Vauras J, Larsson E (2011) Inocybe myriadophylla, a new species from Finland and Sweden. Karstenia 51:31–36. https://doi.org/10.29203/ka.2011.446

  • Vauras J, Larsson E (2016) Inocybe baltica and I. suecica, two new smooth-spored species from the Baltic Sea region. Karstenia 56:13–26. https://doi.org/10.29203/ka.2016.472

  • Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172(8):4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wenkart S, Roth-Bejerano N, Mills D, Kagan-Zur V (2001) Mycorrhizal associations between Tuber melanosporum mycelia and transformed roots of Cistus incanus. Plant Cell Rep 20(4):369–373. https://doi.org/10.1007/s002990100325

    Article  CAS  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor JW (1990) Amplification and directsequencing 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, San Diego, pp 315–322

    Google Scholar 

  • Zervakis GI, Venturella G, Fryssouli V, Inglese P, Polemis E, Gargano M L (2019) Pleurotus opuntiae revisited – An insight to the phylogeny of dimitic Pleurotus species with emphasis on the P. djamor complex. Fungal Biol 123(3):188–199. https://doi.org/10.1016/j.funbio.2018.12.005

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Acknowledgements

We would like to thank Prof. C. Fasseas for facilitating access to microscopy infrastructure. István Ölvedi and Péter Finy are acknowledged for their assistance in collecting the Hungarian M. heimii specimen.

Funding

This research work was partly funded by the European Union (European Social Fund – ESF) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF) – Research Funding Program entitled “Contribution of mycorrhizae to the sustainability of marginal Mediterranean ecosystems – Development of mycorrhizal inocula (SALTYMYC)” (THALIS – AUA – MIS 380233). The work of Bálint Dima was partly supported by the ELTE Institutional Excellence Program financed by the National Research, Development and Innovation Office (NKFIH-1157–8/2019-DT).

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Authors and Affiliations

  1. Laboratory of General and Agricultural Microbiology, Agricultural University of Athens, Iera Odos 75, 11855, Athens, Greece

    Vassileios Daskalopoulos, Elias Polemis, Vassiliki Fryssouli & Georgios I. Zervakis

  2. Paros, Greece

    Linos Kottis

  3. Wiesenbach, Germany

    Ditte Bandini

  4. Department of Plant Anatomy, Institute of Biology, Eötvös Loránd University, Budapest, Hungary

    Bálint Dima

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  1. Vassileios Daskalopoulos
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  2. Elias Polemis
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  4. Linos Kottis
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  5. Ditte Bandini
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  6. Bálint Dima
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  7. Georgios I. Zervakis
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Contributions

VD, EP and GIZ conceived the study; VD, EP, DB, BD, and LK collected the biological material and evaluated the morpho-anatomical features; VF, DB, and BD provided the sequences of the material examined; VF performed the phylogenetic analyses; VD, EP, VF, DB, BD, and GIZ compiled and examined the data; VD wrote the early draft, and GIZ compiled the final draft with help from all co-authors.

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Correspondence to Georgios I. Zervakis.

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Daskalopoulos, V., Polemis, E., Fryssouli, V. et al. Mallocybe heimii ectomycorrhizae with Cistus creticus and Pinus halepensis in Mediterranean littoral sand dunes — assessment of phylogenetic relationships to M. arenaria and M. agardhii. Mycorrhiza 31, 497–510 (2021). https://doi.org/10.1007/s00572-021-01038-1

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