Pseudobaeospora pillodii (Quél.) Wasser

Vizzini, Alfredo, Consiglio, Giovanni, Adamčíková, Katarína, Setti, Ledo & Adamčík, Slavomír, 2025, Pseudobaeosporoideae, a new subfamily within the Tricholomataceae for the genus Pseudobaeospora (Agaricales, Tricholomatineae) based on morphological and molecular inference, IMA Fungus 16, pp. e 144994-e 144994 : e144994-

Pseudobaeospora pillodii (Quél.) Wasser , Flora Gribov Ukrainy. Agarikoyve Griby (Kiev): 220 (1980)

Figs 4 d, g , 5 , 6

Pseudobaeospora pillodii (Quél.) E. Horak , Revue Mycol., Paris 29 (1–2): 73 (1964), Nom. inval., Art. 41.3 (Shenzhen Code).

Collybia pillodii Quél. [as ‘ pillodi’] Basionym, C. r. Assoc. Franç. Avancem. Sci. 18 (2): 509 (1890) [1889].

= Pseudobaeospora oligophylla (Singer) Singer , Lilloa 22: 438 (1951) [1949].

Baeospora oligophylla Singer , Basionym, Revue Mycol., Paris 3 (4–5): 194 (1938).

=? Agaricus (Tricholoma) microsporus Ellis sensu Desjardin (2004) non sensu Singer (1942).

Lectotype of Collybia pillodii .

(selected here, MBT 10024681): Quélet’s original plate, 1890, C. R. Ass. franç. Av. Sci. 18: pl. XV, fig. 4. Fig. 4 g

Epitype of Collybia pillodii .

(designated here, MBT 10024682): FRANCE • Savoie , Bourg-Saint-Maurice, Arc 1800, under Alnus alnobetula (Ehrh.) K. Koch , 27 August 2006, leg. P-A Moreau ( LIP PAM 06082703 ) .

Selected iconography.

Ludwig (2000: 152, 70.1); Ronikier and Moreau (2007: 1 b, c); Morozova and Popov (2013: pl. I- 1); Christan and Rexer (2020: 41).

Selected descriptions.

Kühner and Romagnesi (1954: 92, as Collybia pillodii ); Horak (1968: 511–513, as P. oligophylla ); Redhead (1982: 217, as P. pillodii , no data on presence / absence of clamp-connections); Bas (2003: 192–193, as P. pillodii , 194–195 as P. oligophylla ); Morozova and Popov (2013: 129–130, as P. pillodii , in Russian).

Description.

Spores (2.8 –) 3.3–3.7 – 4.2 (– 5.6) × (2.5 –) 2.9–3.1 – 3.4 (– 4.2) µm (288 / 5 / 5), Q = (0.96 –) 1.07–1.19 – 1.32 (– 1.69), V = (10.2 –) 14.6–19.8 – 25.0 (– 46.1) μm 3, globose to subglobose or broadly ellipsoid in frontal and side view, wall up to 0.2–0.3 µm thick, smooth, colorless in L 4; hilar appendix prominent, 0.5–0.8 µm long (Fig. 6 c – f ). Basidia 16–17.5 × 5–6 µm, mostly tetraspored but also bispored, clavate, sterigmata up to 5 µm long. Hymenophoral trama regular to subregular, consisting of up to 8 µm wide hyphae, colorless in L 4. Hymenial cystidia absent. Pileipellis suprapellis as a quite compact (dense) cutis of broadly ellipsoid up to 16 µm wide hyphae mixed with cylindrical, up to 8 µm wide hyphae, with rounded apex, slightly gelatinized, smooth, sometimes ascendant and forming small trichodermic patches; subpellis formed by broadly ellipsoid, densely septate hyphae up to 10 µm wide (Fig. 5 a – h ). Pigments brownish, intracellular. Stipitipellis of cylindrical, up to 6 µm wide hyphae (Fig. 6 a ). Stipititrama of up to 16 µm wide hyphae. Caulocystidia usually present, clustered, versiform, thin-walled, colorless, up to 6 µm wide (Fig. 6 b ). Clamp-connections absent everywhere.

Specimen examined.

FRANCE • Savoie, Bourg-Saint-Maurice, Arc 1800 , under Alnus alnobetula (Ehrh.) K. Koch , 27 August 2006, leg. P-A Moreau ( LIP PAM 06082703 , epitype of C. pillodii ) . NORWAY • Innlandet, Lesja, Joris delta, Flommarkskog med gråor , 12 August 2021, leg. T. E. Brandrud, S. Khalsa & P. G. Larsen (O-F: 258872) . POLAND • Western Tatra Mts., Sarnia Skala massif, northern slope, at the top , alt. 1375 m, Pinetum mugi carpaticum, on litter, 22 August 2001, leg. A. Ronikier ( KRAM-F: 53298 ) ; ibidem, 8 September 2001, leg. A. Ronikier ( KRAM-F: 53314 ) . RUSSIA • Republic of Karachay-Cherkessia, Teberda State Nature Reserve, Dzhemagat Gorge , 1881 m, on the soil on the border of floodplain forest and meadow, 13 August 2009, leg. E. S. Popov, det. O. V. Morozova ( LE 254346 ) .

Notes.

Collybia pillodii was described and illustrated by the French mycologist Lucien Quélet (1890) from Jura hills as a very small entirely violet species with a campanulate to convex pruinose pileus, whitish pileus margin, adnate and distant lamellae paler than the pileus, a fistulous and slender rooting stipe bristling at the base with white and radiant rhizoids, very thin violaceous context, and minute subglobose to ovoid spores. He reported its spores as minutely aculeate (“ finement aculeolée ”), but his observation was probably incorrect because it was not confirmed by all the subsequent authors who observed always smooth spores. The species was later described in detail by Kühner and Romagnesi (1954), who suggested its possibly placement in Tricholoma section Liposperma . Favre (1960) believed that the species was better placed within the tribe Orcellées (see below) in sense of Kühner (see Kühner and Romagnesi 1953, Kühner 1969 = Entolomataceae ).

When Singer (1938) described Baeospora oligophylla he did not compare it to Collybia pillodii described 48 years earlier by Quélet (1890). He merely noted that the latter species probably also belongs to the genus Baeospora Singer. Then , when Singer (1942) established the genus Pseudobaeospora for the species of Baeospora with dextrinoid spores, he included only B. oligophylla . Both in the first and in second edition of “ The Agaricales in modern taxonomy ” ( Singer 1951, 1962), he placed the genus Pseudobaeospora as closely related to Lepiota (following the suggestions by Locquin 1952), and still monotypic with a single species, P. oligophylla ; while Collybia pillodii was classified as a probable member of Collybia section Iocephalae Singer.

The two species were placed together in one genus for the first time by Horak (1964), who made an invalid combination Pseudobaeospora pillodii , validated later by Wasser (1980). In the third and fourth editions of “ The Agaricales in modern taxonomy ”, Singer (1975, 1986) also followed Horak’s opinion including the two names in one genus.

Since type collections of Quélet’s Collybia pillodii and of Baeospora oligophylla (presumably kept in LE) do not exist (Olga Morozova, pers. comm.) and their very concise original descriptions are difficult to interpret there has been some speculation about the relation between P. pillodii and P. oligophylla and depending on the authors these taxa were treated as two independent species ( Singer 1986; Bas 2002, 2003) or just one ( Horak 1964, 1968, 2005; Redhead 1982; Ronikier and Moreau 2007; Morozova and Popov 2013; Desjardin et al. 2014; Voto 2021).

Bas (2003) was the only author who provided a comparison of P. pillodii and P. oligophylla . He mainly relied on his own collections, the original description of P. oligophylla ( Singer 1938) , the exhaustive descriptions of Collybia pillodii by Kühner (in Kühner and Romagnesi 1954) and of the Swiss specimens of P. pillodii by Horak (1968). He distinguished P. oligophylla by a cutis type of pileipellis with cystidioid, repent to ascending, terminal elements compared to a simple undifferentiated cutis of P. pillodii . These conclusions were later questioned by Ronikier and Moreau (2007) who, after finding and studying specimens at various stages of development, proposed to consider both taxa as synonyms, giving the priority to P. pillodii as an older name. They concluded that the cutis-like pileipellis observed by Bas as characteristic of P. pillodii is only the tardive stage of the subtrichodermic pileipellis found in young specimens named as P. oligophylla .

Our analyses, which did not take into account the developmental stage of the basidiomes as they were carried out on only herbarium (fungarium) material, show that regardless of the presence or absence of ascending pileocystidioid terminal elements (which in our opinion depends more on the point of the pileus where the sampling is taken) all the collections are molecularly conspecific (Figs 2 , 3 ), and thus supporting the conclusions of Horak (1964, 1968), Redhead (1982), and Ronikier and Moreau (2007). Accordingly, Quélet’s illustration of Collybia pillodii ( Quélet 1890) is selected above as lectotype and a sequenced French collection ( LIP PAM 06082703), also studied in Ronikier and Moreau (2007), is established as epitype of C. pillodii .

According to the results of our study, P. pillodii is characterized by very small to small, very slender (e. g., pileus 1–15 mm wide, stipe 10–55 (70) × 0.2–2.0 mm), brownish lilac, entirely purplish coloured basidiome except its whitish pileus margin, spaced lamellae (L = 12–19, l = 0–3), a non-striate pileus, a stipe with basal rhizoids, subglobose to broadly ellipsoid spores (on average not exceeding 4 µm in length), basidia prevailingly tetrasporic (few specimens have been found with 2 - spored basidia only, e. g., Kühner and Romagnesi 1953) as well with 2 - and 4 - spored basidia sometimes even on one lamella (e. g., Ronikier and Moreau 2007, our observations), cheilocystidia absent (but reported as basidioliform by Horak 1964 or filiform by Singer 1938), suprapellis as a cutis with (subtrichodermoid) or without ascending terminal (pileocystidioid) elements, that is negative to pallid or turns very pale grayish-greenish in KOH, clamp-connections absent. Kühner (in Kühner and Romagnesi 1954) pointed out that all the specimens he examined were haploparthenogenic (apogamic, with uninucleate hyphae).

Pseudobaeospora pillodii was originally described from a deciduous mountain forest ( Quélet 1890) and is often reported from Alnus Mill. litter (Kühner in Kühner and Romagnesi 1954; Favre 1960; Bas 2003; Ronikier and Moreau 2007; von Bonsdorff et al. 2012 etc.) as well as from subalpine coniferous litter ( Singer 1938; Kühner in Kühner and Romagnesi 1954; Horak 1964, 1968; Bresinsky and Schmid-Heckel 1982; Redhead 1982; Ronikier and Moreau 2007; Læssøe 2008, 2012; Morozova and Popov 2013; Christan and Rexer 2020) or other subalpine plant communities, such as Salix L. shrubs, the Athyrio-Sorbetum association ( Bujakiewicz 2004) or Rhododendron L. shrubs ( Wasser 1980). As suggested by Ronikier and Moreau (2007), it might be a nitrophilic saprotrophic species, to be sought in other nitrogen-rich organic substrates. It is reported from Asia (Siberia), Europe ( France, Germany, Norway, Poland, Switzerland, Russia), and North America ( Canada) ( Singer 1938; Horak 1964, 1968; Redhead 1982; Bas 2003; Ronikier and Moreau 2007; Læssøe 2008, 2012; Morozova and Popov 2013; Christan and Rexer 2020; Voto 2021). Jamoni (1997) described a Pseudobaeospora collection (on only one basidiome in very poor condition) from subalpine Piedmont ( Italy) near Alnus incana which may represent P. pillodii due to its tetrasporic basidia, clampless hyphae and absence of cheilocystidia, but unfortunately the specimen can no longer be found in any fungarium.

There are several interesting observations on P. oligophylla or P. pillodii which were not confirmed by other authors and require further investigation. Favre (1960) and Kühner (1980) reported a lilac-purplish or pinkish spore deposit for P. pillodii . Bon (in Jamoni and Bon 1996) cited some French collections of P. pillodii consisting of only albinotic basidiomes, but these may represent white Pseudobaeospora species which were described later (e. g., Bas 2002, 2003).

For a single collection named P. oligophylla in sense of Bas, the collector, N. Dam, noted that some rhizoids were connected to small ochraceous tubers (presumably sclerotia) in the soil, as in Collybia tuberosa (Bull.) P. Kumm. (cited in Bas 2003; Clitocybaceae Vizzini, Consiglio & M. Marchetti , Tricholomatineae).

The presence of bisporic and / or tetrasporic basidia in basidiomes and / or collections of the same species found in P. pillodii should not be surprising as, apart from P. wipapatiae and Agaricus fuscolilacinus Peck (that according to Desjardin 2004 belongs to Pseudobaeospora ) for which only bisporic basidiomes are known ( Desjardin 2004; Desjardin et al. 2014), some other species, e. g., P. brunnea , P. cyanea , P. lilacina , show a mixture of (1) 2 - and 4 - spored basidia ( Bas 2003; Arauzo 2011 a; Wu et al. 2017; Voto 2021), P. pyrifera collections with 2–4 spored basidia and others only 4 - spored (see below), and for P. taluna three collections from Tasmania are 4 - spored, and one from Victoria, 2 - spored ( Craig et al. 2023).

Pseudobaeospora pillodii was the only clamp-less species reported from Europe so far before this publication (see below). Pseudobaeospora sp. described in Adamčík and Ripková (2004 b) based on a single clamp-less basidiome collected among Molinia sp. under Alnus glutinosa (L.) Gaertn., from Czech Republic, is distinguished mainly by a very minute basidiome (pileus 4.5 mm wide and stipe 20 × 0.6 mm), pileus with 1–1.5 mm long marginal striation, very sparse lamellae (L = 11, l = 0–1), well-developed versiform to irregular cheilocystidia 21–33 × 2.5–6.0 µm, strictly bisporic basidia, a pseudoparenchymatic subpellis of 9–24 µm wide hyphae, and spores longer than 4 µm on average.

Agaricus (Tricholoma) microsporus Ellis (Nom. illegit., Art. 53.1, Shenzhen Code) is, based on the data provided by Desjardin (2004) who examined its holotype collection (“ this species forms violet basidiomes with a thin cutis-type pileipellis that overlays a subcellular hypodermium, has dextrinoid basidiospores 4–5 × 3.5–4.5 µm, lacks cheilocystidia, lacks clamp connections, and does not discolor in KOH ”), and the original description ( Ellis 1874, stipe with “ long, spreading, pale-yellowish hairs at base ”), a possible older synonym of P. pillodii .

Figures

Figure 2. Mid-point rooted Bayesian phylogeny (nrITS, nrLSU, nrSSU, RPB 2 - exons) of the Tricholomataceae s. s. Nodes were annotated with Bayesian PP (left) and ML BP (right) values, with the significance threshold considered as Bayesian PP ≥ 0.95 and / or ML BP ≥ 70 %. Subsignificant support values were annotated in parentheses. Boldface names represent samples sequenced for this study.

Figure 3. Bayesian inference phylogram built with ITS nucleotide sequence of Pseudobaeospora, rooted with Tricholoma inamoenum (Tricholomataceae) as outgroup. Nodes were annotated with Bayesian PP (left) and ML BP (right) values, with the significance threshold considered as Bayesian PP ≥ 0.95 and / or ML BP ≥ 70 %. Subsignificant support values were annotated in parentheses. Boldface names represent samples sequenced for this study. Clades are named following Craig et al. (2023).

Figure 4. Basidiomes of some sequenced Pseudobaeospora collections. a P. calcarea (LIP PAM 06090111 - FR 2013078); b P. cyanea (GDOR M 3986); c P. laguncularis var. denudata (LIP PAM 99101004 - FR 2013079); d P. pillodii (KRAM F- 53314); e P. terrayi (SAV-F: 3317, holotype); f P. terrayi (SAV-F: 20813). Lectotype of. C. pillodii; g Quélet’s original plate, pl. XV, fig. 4. Photos: a, c by P. A. Moreau; b by D. Gisotti; d by A. Ronikier; e, f by S. Jančovičová.

Figure 5. Pseudobaeospora pillodii, microscopic features. Pileipellis. a – c (KRAM F- 53298); d (KRAM F- 53314); e, f (LE 254346); g, h (O-F: 258872); a – h in ammoniacal Congo red. Scale bars: 10 µm (a – c); 20 µm (e – h). Photos by L. Setti.

Figure 6. Pseudobaeospora pillodii, microscopic features. Stipitipellis. a (KRAM F- 53298); b (KRAM F- 53314). Spores; c (KRAM F- 53298); d (KRAM F- 53314); e (LE 254346); f (O-F: 258872); a – f in ammoniacal Congo red. Scale bars: 10 µm (a); 20 µm (b); 5 µm (c – f). Photos by L. Setti.