Tulostoma dunense Finy, Jeppson, L. Albert, Oelvedi , Dima & V. Papp, 2023

Finy, Peter, Jeppson, Mikael, Knapp, Daniel G., Papp, Viktor, Albert, Laszlo, Oelvedi, Istvan, Boka, Karoly, Varga, Dora, Kovacs, Gabor M. & Dima, Balint, 2023, Exploring diversity within the genus Tulostoma (Basidiomycota, Agaricales) in the Pannonian sandy steppe: four fascinating novel species from Hungary, MycoKeys 100, pp. 153-170 : 153

Tulostoma dunense Finy, Jeppson, L. Albert, Oelvedi, Dima & V. Papp sp. nov.

Fig. 3

Holotype.

Hungary, Tolna, Németkér, open sandy grassland, 18 Oct 2020, P. Finy, I. Ölvedi, FP-2020-10-18 (BP112640, isotype GB). GenBank: ITS OR722622, LSUOR722648, tef1 OR707014.

Etymology.

The epithet refers to the continental, open, bare sandy habitat of this species, similar to coastal dunes.

Description.

Spore-sac subglobose, depressed-globose, 10-20 mm. Exoperidium hyphal, encrusting sand only at the base of the spore-sac. Endoperidium tough, chalky white or dirty-dingy white, with age becoming greyish, young basidiomata with velvety surface. Mouth prominent, fibrillose-lacerate, irregular sometimes remains unopened for a long time and splits later due to mechanical pressure (wind or trampling). Socket distantly separated from the stem. Stem 35-80 × 1.5-5 mm, initially white, then ochraceous, with age greyish-blackish, longitudinally furrowed, at the base with a volva and a prominent, easily broken pseudorhiza. Gleba ferruginous to brick-red brown, usually scattered on the surface of the spore-sac. Capillitium brown, 2.5-10 µm in diameter with walls 0.7-2.5 µm in diameter, fragile, breaking up at septal levels in 40-350 µm long segments with rounded, not widened ends, rarely branching. Spores subglobose to oval, 4.6-5.2 × 4.0-4.8 µm (av. 4.4 × 4.9 µm), smooth under LM and SEM.

Habitat and distribution.

The psammophilous species Tulostoma dunense known so far only from sandy areas of the Great Hungarian Plain of Hungary. It occurs on both sides of the Danube ( Kiskunság, Dél-Mezőföld), where open dunes appear. It mainly grows solitary, deep in the sand in large, open sandy areas to bare spots.

Notes.

Tulostoma dunense was previously recorded in Hungary by Hollós (1904), Siller and Vasas (1995), Babos (1999), Siller et al. (2005), Siller et al. (2006) and Rimóczi et al. (2011) under the names of T. volvulatum , T. obesum and T. aff. cretaceum . Hollós (1904) included both T. giovanellae and T. dunense under the name T. volvulatum (nom. rej., Altés et al. (1999)) and recorded it in urban places in the City of Kecskemét (now T. giovanellae ) as well as in sand dunes (now the new species, T. dunense ). The brownish colour of the capillitium characteristic of specimens from sand dunes and largely absent in those from urban habitats, was considered a result of the maturation process. Later ( Hollós 1913) corrected his earlier concept and concluded that some of the synonyms he had listed under T. volvulatum in his publication ( Hollós 1904), in fact belonged to a complex of several species. He added illustrations of their different types of capillitia ( Hollós 1913: tables 3 and 4) and concluded that his concept of T. volvulatum from the sand dunes was a synonym of T. kansense , a smooth-spored species with brownish capillitium described from North America. The capillitium in the samples from urban habitats clearly showed the undulating inner walls of the capillitium typical of T. giovanellae ( Hollós 1913: table 3, fig. 6), although Hollós did not identify them under this name. Some 50 years later, Nagy and Babos (1969) recorded T. giovanellae growing on a pavement at the base of a house wall in Budapest. It matched partly the material cited by Hollós (1904) as T. volvulatum , but was decidedly different from the species growing in the sand dunes. Babos (1999) later came to the same conclusion. Altés et al. (1999) studied the holotype material of T. volvulatum and concluded that it was a synonym of T. giovanellae characterised by ornamented spores. They also studied the holotype material of T. obesum with which they identified European collections with completely smooth spores from steppe habitats and the name T. volvulatum was rejected. Rimóczi et al. (2011) accordingly identified the Hungarian species of the sand dunes as T. obesum . Molecular data ( Jeppson et al. 2017) later showed that the Hungarian " T. obesum " was not identical with the American holotype of T. obesum , but was closely related to another American species described as T. cretaceum . It was recovered as T. aff. cretaceum by Jeppson et al. (2017). The T. aff. cretaceum from Hungary belongs to a complex of cryptic species with a strong geographical isolation. The type of T. cretaceum was studied and successfully sequenced by Gube (2009), but the ITS and LSU sequences have remained unpublished. We have kindly received these sequences from Matthias Gube allowing us to include them in the phylogenetic analyses. The phylogenetic analyses showed that the type of T. cretaceum formed a distinct lineage within this complex (Fig. 1 ), proving that this North American species is different from the European and Asian lookalikes. Therefore, the Hungarian collections are proposed here as a novel species, T. dunense , which is closely related to samples of T. aff. cretaceum collected in Hungary, Kazakhstan and in the Russian Federation as well as in Spain (Fig. 1 ). The main features to distinguish T. dunense from the other species in the complex are mainly phylogenetic- and geographical-based data. Tulostoma dunense has been a protected species under Hungarian law since 2005, but to date, it has erroneously been treated under various misinterpreted and dubious names, i.e. T. volvulatum , T. obesum and T. aff. cretaceum . The ITS region of T. dunense differs from its closest clade represented by a single sequence ( T. cf. cretaceum MJ3821, see Fig. 2 ) by at least 13 substitution and indel positions, which is a similarity of 98%. This sequence might represent a different species, but further collections need to be studied to clarify its taxonomic status. In contrast, low intraspecific genetic variation was detected in T. dunense (0-4 substitution and indel positions). The ITS and LSU sequences of an old collection identified by Long (www.mycoportal.org) under the name Schizostoma laceratum (NY834492) collected in 1941 in New Mexico, were provided for us by Matthias Gube. Our phylogenetic analyses indicate that this specimen belongs to the T. cretaceum complex as a distinct lineage. On the other hand, the nomenclature of the genus Schizostoma , as well as the species S. laceratum ( Fries 1829; Léveillé 1846), seems to be problematic and needs further clarification.

Specimens examined.

Hungary, Bács-Kiskun, Ágasegyháza, in open sand, 18 Feb 2021, P. Finy, FP- 2021-02-18 (ELTE); Bócsa, in open sand, 7 Dec 2019, P. Finy, FP- 2019-12-07 (ELTE); Fülöpháza, 11 Apr 2006, T. Knutsson, T. Gunnarsson, J. Jeppson, M. Jeppson, MJ 7759 (GB), Ibidem, in open sand, 5 Jun 2016, P. Finy, FP- 2016-06-05 (ELTE); Izsák (Soltszentimre), in open sand, 21 Nov 2019, A. Nagy, B. Dima, DB- 2021-11-21-2 (ELTE); Kéleshalom, in open sand, 6 Dec 2015, P. Finy, FP- 2015-12-06 (ELTE); Ibidem, in open sand, 2 Jan 2022, P. Finy, I. Ölvedi, FP- 2022-01-02-1 (ELTE); Tázlár, in open sand, 11 Dec 2016, P. Finy, FP- 2016-12-11 (ELTE); Ibidem, in open sand, 2 Jan 2021, P. Finy, FP- 2021-01-02 (ELTE) . Pest, Örkény, former military training field, sand steppe vegetation, in open sand, 5 Nov 2001, J. Jeppson, M. Jeppson, MJ6103 (GB), Ibidem, in open sand, 6 Dec 2020, P. Finy, L. Albert, FP- 2020-12-06 (ELTE) .

Figures

Figure 1. Habitats of Tulostoma species in Hungary: a T. hungaricum in Orgovany b T. sacchariolens in Orgovany c T. dunense in Izsak (Soltszentimre) d T. shaihuludii in Izsak (Soltszentimre). Photos: P. Finy.

Figure 2. Maximum Likelihood (RAxML) tree of concatenated nrDNA ITS, nrDNA LSU and tef 1 - α sequences of representative species of the genus Tulostoma and the four newly-introduced species in the present study. Sequences obtained in this study are shown in bold blue. After the voucher number, the species and the country of origin are shown. Then, the type specimens are indicated. ML bootstrap support values (≥ 70) are shown before slashes and Bayesian posterior probabilities (≥ 0.90) are shown after slashes. Highlighted sections indicate affiliations to the four novel Tulostoma species: T. dunense, T. hungaricum, T. sacchariolens and T. shaihuludii. The illustrations exhibit basidiomata and basidiospore characteristics of the novel species. Tulostoma pulchellum (MJ 7833) and T. striatum (Fritz) served as multiple outgroups. The scale bar indicates expected changes per site per branch.

Figure 3. Tulostoma dunense: a, c-f FP- 2020 - 10 - 18 (BP 112640, holotype), Nemetker b FP- 2021 - 01 - 02, Tazlar a-c basidiocarps d, e basidiospores f capillitium with basidiospores. Scale bars: 1 μm (d); 10 μm (e); 10 µm (f). Photos: a, b, e, f P. Finy c L. Albert d K. Boka.