Squamanitaceae and Three New Species of Squamanita Parasitic on Amanita Basidiomes

doi:10.21203/rs.3.rs-61779/v1

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Squamanitaceae and Three New Species of Squamanita Parasitic on Amanita Basidiomes

https://doi.org/10.21203/rs.3.rs-61779/v1

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published 03 Mar, 2021

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The systematic position of the enigmatic genus Squamanita (Agaricales, Basidiomycota) is largely unknown. Together with Cystoderma and Phaeolepiota, they were categorized as belonging in the tribe Cystodermateae. In this study, with newly generated sequences of the type species of the genus Squamanita, namely S. schreieri, and sequences of a few species of Cystodermateae, the phylogeny of this “tribe” is reinvestigated with a concatenated (28S-5.8S-18S) dataset. Our study reveals that Squamanita and Phaeolepiota-Cystoderma are indeed sister groups with moderate statistic support (MLBS/PP = 80/1), and Squamanita is a monophyletic clade with highly statistic support (MLBS/PP = 92/1). The family name Squamanitaceae is resurrected and emended to accommodate the three genera. Meanwhile, another concatenated (ITS-28S-18S) dataset is used to investigate the phylogenetic relationship and species delimitation in Squamanita. Our data indicated that “S. umbonata” from North America, Europe, East Asia, and Central America harbors a complex of species, and species of Squamanita can parasitize species of Amanita, besides other fungal species. Squamanita mira parasitizes A. kitamagotake (A. sect. Caesareae), while S. orientalis and S. sororcula are parasites of species belonging to the A. sepiacea complex (A. sect. Validae). “Squamanita umbonata” from Italy occurs on A. excelsa (A. sect. Validae). Three new species of Squamanita from East Asia, viz. S. mira, S. orientalis and S. sororcula are documented with morphological, multi-genes phylogenetic, ecological data, line drawings, and photographs and compared with similar species.

Agricultural Engineering

Amanita

New taxa

Parasitic fungi

Squamanita

Host preference

Three new species

The genus Squamanita Imbach (1946) was originally described from riverine forest in Switzerland. After examining the type material, Horak (1968) presented a full re-description of the microscopic characters including features not reported in the protologue. Squamanita is one of the most enigmatic genera of the Agaricales (Halama 2016; Mondiet et al. 2007; Redhead et al. 1994), and the members of this genus are extremely rare and sporadic all over the world (Griffith et al. 2019; Holden 2005; Matheny and Griffith 2010). Almost all the species of Squamanita are biotrophic parasites on other agaric species (Halama 2016; Harmaja 1987; Henrici 2013; Matheny and Griffith 2010; Nagasawa et al. 1990; Redhead et al. 1994; Reid 1983). The basidiomes of Squamanita grow from other agaric species and deform the host agaric basidiomes becoming an enlarged base of the stipe that have been labelled as “sclerotial bodies”, “protocarpic tubers” (Bas 1965; Singer 1986), “galls” (Redhead et al. 1994), “cecidiocarps” (Bas and Læssøe 1999) or “mycocecidia” (Vizzini and Girlanda 1997; Griffith et al. 2019), and sometimes multiple basidiomes come out from a “mycocecidia” (Bas 1965; Mondiet et al. 2007), as a result that the host is completely deformed and finally more or less recognizable (Redhead et al. 1994; Halama 2016). To date, twelve species of Squamanita have been accepted in the current literature (http://www.indexfungorum.org/Names/names.asp). It is reported that these species can parasite more than seven different genera of Agaricales, viz. Amanita Pers. (Bas 1965; Redhead et al. 1994), Cystoderma Fayod (Griffith et al. 2019; Harmaja 1987; Holden 2005; Matheny and Griffith 2010; Redhead et al. 1994; Reid 1983; Singer 1986), Galerina Earle (Redhead et al. 1994), Hebeloma (Fr.) P. Kumm. (Bas and Læssøe 1999; Mondiet et al. 2007; Vesterholt 1991), Inocybe (Fr.) Fr. (Vizzini and Girlanda 1997), Kuehneromyces Singer & A.H. Sm. (Cervini 2008; Gulden et al. 1977), Phaeolepiota Maire ex Konrad & Maubl. (Nagasawa et al. 1990; Redhead et al. 1994), and possibly also Mycena (Pers.) Roussel (Stridvall 1994).

The genus Squamanita was morphologically assigned to different families in the past, including Squamanitaceae Jülich and Cystodermataceae Locq. Based on phylogenetic analysis of combined nuclear ribosomal RNA genes, Matheny and Griffith (2010) suggested that Squamanita, Cystoderma, and Phaeolepiota represent a monophyletic clade and referred to them as forming a tribe, viz. Cystodermateae. In the subsequent molecular works by Matheny et al. (2015), Griffith et al. (2019) and Vizzini et al. (2019) Squamanita and allied genera were referred as Squamanitaceae. Due to lack of molecular phylogenetic evidence of the type species of Squamanita, S. schreieri Imbach (1946), the phylogenetic position of Squamanita remained unresolved. In addition, the host species of Squamanita were identified mainly based on morphological data and ecological evidence (Bas 1965; Mondiet et al. 2007), except for a few studies (Mondiet et al. 2007; Matheny and Griffith 2010; Griffith et al. 2019), which used molecular phylogenetic techniques to identify the hosts.

In the survey of macrofungi in China, we collected three species of Squamanita and two collections of Amanita sect. Caesareae and one collection of A. sect. Validae (Cui et al. 2018) with similar “mycocecidia” of two Squamanita species in the nearby localities respectively. To validate the taxonomical, phylogenetic and ecological traits, detailed morphological and anatomical studies and molecular phylogenetic analyses are carried out. To understand the species recorded in China, additional specimens collected in other parts of the world are examined and included in the present report.

Morphology, Sampling, DNA extraction, PCR amplification and sequencing

Specimens studied are listed in Table 1. For morphological study, we follow Cui et al. (2018) and the references therein. To verify the parasitic features of the target species, routine samples (HKAS100826) for DNA extraction are separately taken both from the basidiome (five samples for basidiome labeled from A1 to A5) and the mycocecidium (six samples labeled from B1 to B6 as illustrated in Fig. 6). In addition, samples of other specimens are taken from different locations from their basidiomes and mycocecidia respectively then mixed for improving the success probability of DNA extraction in case of poor samples quality. Particularly, the volval remnant-like structure on the cap of the Squamanita specimen (HKAS 574862A) was sampled. All Chinese collections are deposited in the Herbarium of Cryptogams of Kunming Institute of Botany, Chinese Academy of Sciences, China (HKAS).

The total genomic DNA of all the materials of the parasitic species and the coexisting Amanita species are extracted by using the Extract-N-Amp kit (Sigma, USA). Universal primer pairs LROR/LR5 (Vilgalys and Hester 1990), ITS1F/ITS4 (Gardes and Bruns 1993; White et al. 1990), PNS1/NS41 (Hibbett 1996; Bruns lab) and NS51/NS8 (Bruns lab; White et al. 1990), and EF1-983F/EF1-1567R (Rehner and Buckley 2005) are used for amplifying the large nuclear ribosomal RNA subunit (28S), the internal transcribed spacers 1 and 2 with the 5.8S rDNA (ITS), the small subunit (18S) region (the former and later segments of 18S amplified with primer pairs PNS1/NS41 and NS51/NS8 will be abbreviated to 18SF and 18SL in the optimal substitution models of Bayesian Inference (BI) analyses), and translation elongation factor 1-α (tef1-α), respectively.

PCR products which failed in direct sequencing were firstly purified with the Cycle-pure-kit (Omega, America) or Gel Extraction and PCR Purification Combo Kit (Spin-column) (Bioteke, China), and then cloned using pClone007 simple vector kit (Tsingke, Beijing). For the recently collected specimen (HKAS 100826) and the volval remnants like structure on the cap of a Squamanita specimen (HKAS 574862A), 10 clones of each ITS and 28S PCR products of each sampling point are randomly selected from 90 mm petri dish for sequencing with primer pair M13-47/M13-48 to investigate the mycelium distribution of hosts and parasiting fungi. The cloning, PCR amplification and sequencing follow the protocols described by Cai et al. (2016) and Cui et al. (2018).

Results of sequencing

For specimen of HKAS 100826, the ITS and 28S sequences were successfully amplified from all eleven sampling points (A1–A5, B1–B6). Among them, there are two bands occurring in gel electrophoresis diagram of each of the PCR products of ITS from six sampling points of mycocecidium (B1, B2, B3, B4, B5, B6), see Fig. 1. By cloning and sequencing all of the purified PCR products of ITS and 28S, a total of 50 ITS and 50 28S sequences were generated from all points (A1–A5). After alignment and comparison, all of them belong to the same species, namely the parasitic species itself. For the mycocecidium, each band of PCR productions with two bands are excised from gel respectively, and then purified and then sequenced, generating a total of 120 ITS and 60 28S sequences from sampling points B1–B6. After analysis, two types of mushroom sequences were detected for each DNA locus. Statistically, 50% ITS, 90% 28S matched to the potential parasitic species and 50% ITS, 10% 28S belong to the potential host species. For the volval remnants on the cap of the Squamanita specimen (HKAS 574862A), 60% ITS, 90% 28S are the potential parasitic species and 20% ITS, 0% 28S are assigned to the potential host species, others are contaminant?? (Trichoderma hirsutum K. Chen & W.Y. Zhuang) or vector sequences. For the other specimens of Squamanita and nearby Amanita, all sequences were amplified then directly sequenced or obtained by cloning from PCR productions. XXX sequences have been submitted to GenBank and used for phylogenetic analyses (Table 1). The sequences of the two potential species of hosts are the same as those of the coexisting Amanita species respectively, and were finally identified to belong to A. kitamagotake N. Endo & A. Yamada (Fig. 4) and A. sepiacea Imai complex (Fig. 5). The potential parasitic species are clustered into the genus Squamanita (Figs. 2–3).

DNA sequence alignment

Sequences downloaded from GenBank are indicated in Figs. 2–5 with their herbarium ID or GenBank numbers (when herbarium ID cannot be found), and the sequences obtained in this study are listed in Table 1. Four datasets, namely 28S-5.8S-18S, ITS-28S-18S, ITS-28S-tef1-α, and ITS, are used in our study to identify the phylogenetic position of the basidiomes and mycocecidia of the parasitic species. Mythicomyces corneipes (Fr.) & A. H. Sm., Cystoderma amianthinum (Scop.) Fayod, A. hemibapha (Berk. & Broome) Sacc., and A. fritillaria Sacc. are chosen as outgroups for the analyses of the basidiomes and the mycocecidia respectively. From the first dataset to the last, a total of 2882, 3398, 1804 and 1878 characters are used in the phylogenetic analyses, respectively.

For each dataset, the sequences are aligned using MAFFT v6.8 (Katoh et al. 2005) and then manually edited with BioEdit v7.0.9 (Hall 1999) and concatenated with Phyutility v2.2.1 (Smith and Dunn 2008). Both Maximum Likelihood (ML) and Bayesian Inference (BI) analyses are used to analyze the datasets with RAxML v8.2.7 (Stamatakis 2014) and MrBayes v3.1.6 (Ronquist et al. 2012), respectively. The optimal substitution models for each dataset are determined by using the Akaike Information Criterion (AIC) implemented in MrModeltest V2.2 (Nylander 2004). The selected models for four datasets are GTR+I+G(28S)-K80(5.8S)-GTR+I+G(18SF)-HKY+I+G(18SL), GTR+I+G(ITS)-GTR+I+G(28S)-GTR+I+G(18SF)-GTR+I(18SL), SYM+G(ITS)-HKY+I(28S)-SYM+G(tef1-α), and GTR+G (ITS) respectively. In ML analyses, the statistical support values are obtained by using the nonparametric bootstrapping with 1000 replicates, and the other parameters use the default settings. BI analyses use the selected models and four chains are conducted, and then stopped when the standard deviation of the split frequencies fell below 0.01 and ESS values > 200. Trees are sampled every 100 generations. Subsequently, trees are summarized and posterior probabilities are obtained by using the sumt and sump command implemented in MrBayes by discarding the first 25% generations as burn-ins.

For the four datasets, topologies of the phylogenetic trees generated from ML and BI analyses are nearly identical with minimal variation in statistical support values, and thus only the trees inferred from the ML analyses are displayed. The tree generated from the 28S-5.8S-18S dataset reveals that Squamanita and Phaeolepiota-Cystoderma are sister groups with moderate measures of support (MLBS/PP = 80/1) and Squamanita is a monophyletic group with high statistic support (MLBS/PP = 92/1) (Fig. 2). Taking the study of Matheny and Griffith (2010) into consideration, the family Squamanitaceae is resurrected to accommodate the above-mentioned three genera. Besides, both trees generated from 28S-5.8S-18S or ITS-28S-18S datasets uncover that the three potential Squamanita species from China are novel (Figs. 2–3), which are described below as S. mira, S. orientalis and S. sororcula respectively. The tree generated from ITS-28S-18S dataset also shows that there are four clades under Squamanita (Fig. 3), and “S. umbonata” from North America, Central America, Europe and East Asia harbors a complex of species, with eight subclades in the phylogenetic tree (Fig. 3). The collection R. E. Halling 7691 (Figs. 13–14) is regarded as S. umbonata because its morphological characteristics are mostly consistent with the descriptions of the holotype by Bas (1965). The other collections of “S. umbonata” formed a monophyletic group with strong support (MLBS /PP = 99/1) (Figs. 3–4). The trees generated from ITS-28S-tef1-α and ITS datasets reveal that the host of S. mira is A. kitamagotake, and those of S. orientalis and S. sororcula are species of the A. sepiacea complex (Figs. 4–5).

TAXONOMY

Squamanitaceae Jülich, Biblthca Mycol 85: 390, 1981 emend.

= Cystodermataceae (Singer) Locq., Mycol. gén. struct. (Paris): 108, 1984 (nom. inval.)

Type: Squamanita Imbach, Mitt. Naturf. Ges. Luzern 15: 81. 1946. —Holotype not designated, full redescription of taxon based on paratype (Herb. G) and authentic topotypic specimens is found in E. Horak (ZT 65-139, ZT 66-010, ZT 2185).

Basidiome lepiotoid to tricholomatoid, small to medium-sized, with pileus and central stipe; lamellae adnexed to adnate, or with decurrent tooth, never free. Stipe with or without annulus, sometimes due parasitism occurring on other agaric fungi (mycocecidia). Mycocecidia, when present, subglobose or subcylindrical to clavate fusiform. Stipe and pileus often with a floccose layer composed of loose sphaerocytes. Hyphal system monomitic. Hyphae cylindrical or slightly inflated, thin-walled, smooth, with clamps. Cystidia absent or present; if present, thin- to slightly thick-walled, smooth. Basidia narrowly clavate, 4-spored. Spores subglobose to ellipsoid or subreniform, rarely angular, thin- to slightly thick-walled, hyaline, mostly smooth, in some taxa finely verrucose to finely echinulate, without germ pore, amyloid or inamyloid, not or slightly dextrinoid. Conidia present or absent.

Substrate: On soil or parasitizing on mycocecidia of agarics.

Genera included: Cystoderma, Squamanita, and Phaeolepiota

Squamanita mira J. W. Liu & Zhu L. Yang, sp. nov. Figs. 6–7

MycoBank MB 836584.

Etymology:—mirus (Lat.): referring to the wonderful basidiome.

Diagnosis: S. mira differs from other species by its mycocecidia with a limbate volva-like structure and absence of cystidia.

Holotype:—CHINA. Yunnan Province: Ailaoshan Natural Reserve, Chuxiong, Nanhua, in the forests dominated by Fagaceae and Pinaceae, 24°54′27.53″N, 100°49′14.91"E, 2235 m elev., 10 Aug. 2017, J. W. Liu 904 (HKAS 100826!, GenBank Acc. No. : 28S = xxxx, ITS = xxxxxx, 18S=xxxxxx ).

Pileus ca. 40 mm in diam, subconical to convex, distinctly umbonate; surface dry, yellowish brown (6C6–7) or honey yellow (6C6–8), or viscid if moist, covered with dark orange (6A8), yellow-tawny (6B7–8) or honey yellow (6C6–8), repent, fibrillose squamules; margin incurved, strongly appendiculate, irregularly and densely corniform and fibriform squamules derived from breaking up of the veil, and the color is slightly lighter than surface of pileus. Lamellae adnexed to adnate, moderately crowded, narrow; edge irregularly serrate-dentate or subundulate; Stipe 43–46 × 12–24 mm, subcylindrical, densely covered with brown (6A7–8), tawny-yellow (6B7–8) to yellowish brown (5A6–8), appressed or recurved fibrillose and villiform squamules, at the upper part of the stipe covered with fluffy and villose, brown (5A6–8), tawny-yellow (6B7–8) to yellowish brown (6C6–7) appressed or erect, fibrillose or obliquely lacerate scales arranged in irregular rings, 4–6 mm from apex, extreme apex off-white (1A1–2) and subglabrous; Mycocecidia subglobose to napiform, 40–46 × 5–16 mm, nearly smooth, whitish (1A1) or locally yellow (6A4–5) on external surface; Volval limb arising from margin of mycocecidia, 6–20 mm tall; context of pileus and stipe white (1A1), with a strong aromatic smell, like that of Tricholoma matsutake (S. Ito & S. Imai) Singer; context of mycocecidia white, unchanging on exposure, odor not distinctive.

Basidiospores [60/1/1] (5.5–) 6–7 (–7.5) × 4–5 (6) μm, (Q = (1.16) 1.33–1.75 (–1.8), Qm = 1.53 ± 0.13), ellipsoid or subreniform, colorless, hyaline, smooth, inamyloid. Basidia 22–65 × 9–12 μm, fusiform to ventricose-fusiform, hyaline; sterigmata 4–5 μm long; Cystidia absent. Subhymenium 8–20 μm thick, composed of 4–7 μm wide filamentous hyphal segments. Lamellar trama regular, composed of colorless, thin-walled hyphae 4–17 μm in diam, branching, sometimes anastomosing. Pileipellis a cutis with transition to a trichoderm at regular intervals, composed of loosely and more or less radially arranged, thin-walled hyphae 90–200 (–370) × 5–20 μm, and upper part of pileipellis often with fine brownish granular incrustations and yellowish to brownish filamentous hyphae, constricted at septa; Mycocecidia composed of abundant ovoid to subglobose inflated cells, and filamentous hyphae similar to those on the pileus; chlamydospores not observed. Clamp connections present.

Additional specimen examined:—CHINA. Jiangxi Province: Jian, Jinggangshan City, Jinggangshan scenic spots, 800–900 m elev. 19. July. 2019, Chunlei Pan JGS001 (HKAS 107309A, GenBank Acc. No.: 28S = xxxx, ITS = xxxxxx, rpb2= xxxxxx, 18S= xxxxxx).

Habit and habitat:—Parasitic on Amanita kitamagotake growing on soil under trees of Fagaceae and Pinaceae.

Distribution:—Currently known from Yunnan and Jiangxi Province, southwestern and central China.

In this study, molecular evidence confirms that the hosts of S. mira and the two collections of Amanita in the nearby area within two kilometer´s range of S. mira are A. kitamagotake (Figs. 4, 6).

Morphologically, S. mira highly resembles the informally published S. tropica (“nom. prov.”), because both of them are parasitic on basidiomes of Amanita and form a volva-like structure at the base of the stipe. Furthermore, they share abundant tawny squamules on the pileus surface, serrate-dentate or subundulate lamellae edges, irregular ring analogues on the upper part of the stipe and ellipsoid to subreniform basidiospores. However, S. mira differs from S. tropica in its subconical to convex pileus with a distinct umbo. The material of S. tropica is lost (Bas 1965).

Squamanita mira is also similar to S. schreieri and species of the “S. umbonata” complex. However, S. mira can be distinguished from the aforementioned taxa by its mycocecidia with a limbate volva-like structure and absence of cystidia. Phylogenetically, they are grouped, however, in different clades (Figs. 2–3).

Squamanita orientalis J. W. Liu & Zhu L. Yang, sp. nov. Figs. 8–10

MycoBank MB 836585.

Etymology:—orientalis (Lat.): from the East

Diagnosis: S. orientalis differs from other species by its irregular fibrillose annular zone on the upper part of the stipe and ciliate squamules on the pileal margin, larger cystidia (90–105 × 17–27 μm), and subglobose mycocecidia.

Type:—CHINA. Yunnan Province: Laowopo dunk, Chongren, Nujiang, 1700–1800 m elev., in forest dominated by Fagaceae and Rhododendron, 7 Aug. 2011, Gang Wu 548 (HKAS 574862A, GenBank Acc. No.: 28S = xxxxxxx, ITS = xxxxxx, rpb2= xxxxxx, 18S= xxxxxx).

Pileus ca. 40 mm in diam, subconical to convex; surface dry, covered with yellowish brown (6C6–7), light brown (6D4–5) to dark brown (6E5) or dark grey (6E1–3), more or less radially arranged, repent, fibrillose squamules; margin with ciliate squamules derived from breaking up of the veil, and the color is slightly lighter than surface of pileus; volval remnants of host present on the disc, grey. Lamellae white (1A1), adnexed to adnate, moderately crowded, denticulate. Stipe 30 × 6–10 mm, nearly cylindric, usually tapering upward; surface densely covered by squamules arranged in irregular fibrillose annular zone at the upper part of the stipe, extreme apex white (1A1) and nearly smooth, the part below the ring is covered with orange (6A6–7), tawny yellow (6C7) or yellowish brown (6D7–8) appressed or erect, obliquely lacerate scales. Mycocecidium subglobose 35 × 20–30 mm, nearly smooth, and whitish or grey spots on external surface. The transitional zone between stem and mycocecidium with some irregular rings of tawny-ochraceous (6B7–8) or dingy brown (6E5) color, fibrillose, appressed, or with erect, obliquely upward-pointing scales or lacerate scales.

Basidiospores [50/1/1] (5–) 5.5–6 (–6.5) × 4–5 (–6) μm [Q = (1.2–) 1.5–1.65, Q = 1.43±0.10], broadly ellipsoid, ellipsoid to elongate, sometimes subreniform in side view. Basidia 20–35 × 5–10 μm, subclavate, 4-spored, fusiform to ventricose-fusiform, hyaline; sterigmata 3–4 μm long; basal septa often with clamps. Cystidia numerous, 90–105 × 17–27 μm, fusiform to ventricose-fusiform, with obtuse to acute apex, upper part slightly to moderately thick-walled (up to 1 μm diam.), sometimes with refractive incrustations, hyaline. Lamellar trama regular, composed of colorless, thin-walled hyphae 4–15 μm in diam, branching, sometimes anastomosing; clamps present and common. Subhymenium 10–15 μm thick, composed of 4–6 μm wide filamentous hyphal segments; volval remnants of host on pileus composed of ± irregularly arranged elements: inflated cells very abundant (to locally dominant), subglobose (30–50 × 30–50 μm) or ovoid to broadly clavate (30–60 × 20–30 μm), solitary and terminal, or in chains of 2–3 and then terminal, inflated cells sometimes external upset (up to 1 μm thick), usually colorless and hyaline, occasionally with brownish vacuolar pigments, and the majority of hyphae without clamp connection; inner part of volval remnants near pileus surface composed of ± irregularly arranged elements: inflated cells usually brownish to fawn colored, two types of filamentous hyphae in the tissues: either with filamentous hyphae usually colorless and hyaline, 2–6 μm wide, without clamp connection; or with hyphae similar to lotus root, 60–150 × 4–15 μm, swollen in the middle but constricted at septa, with clamp connection. Mycocecidium composed of abundant ovoid to subglobose inflated cells (45–110 × 24–65 μm) and filamentous hyphae colorless and hyaline, 2–6 μm wide, with clamp connection similar to those on the pileus; chlamydospores not observed.

Habit and habitat:—Parasitic on Amanita sepiacea growing on soil under trees of Fagaceae and Rhododendron.

Distribution:—Currently known from Yunnan Province, southwestern China.

Our morphological data and molecular phylogenetic evidences confirm that the host of S. orientalis and the collection of Amanita in the nearby area within two kilometers’ range of S. orientalis are A. sepiacea (Fig. 5, Fig. 10). Interestingly, some volval remnants of A. sepiacea are found on the center of the pileal surface of S. orientalis (Fig. 8), and its anatomical features are those of A. sepiacea (Yang 2005) (Fig. 10), and the filamentous hyphae with clamp connection belong to S. orientalis (Fig. 10).

Squamanita orientalis is similar to S. schreieri. However, the latter species has no cystidia. Furthermore, the former is a parasite on A. sepiacea, while S. schreieri is possibly associated with A. strobiliformis (Paulet ex Vittad.) Bertillon or A. echinocephala (Vittad.) Quél. (Bas 1965).

Squamanita orientalis is also similar to S. sororcula and S. umbonata. However, S. orientalis differs from S. sororcula by its irregular fibrillose annular zone on the upper part of the stipe and ciliate squamules on the pileal margin, and larger cystidia (90–105 × 17–27 μm). In addition, there are ca. 50 and ca. 40 base differences in ITS and 28S segments between the two species respectively, and even their hosts are A. sepiacea, but there also have ca. 25 different bases in the ITS segment. Squamanitaumbonata differs from S. orientalis by its umbonate pileus, and narrower cystidia (60–95 × 9–20 μm), cylindrical to clavate fusiform mycocecidia.

Squamanita sororcula J. W. Liu & Zhu L. Yang, sp. nov. Figs. 11–12

MycoBank MB 836586.

Etymology:—sororcula (Lat.): little sister, indicating a close relation with S. orientalis.

Diagnosis: S. sororcula differs from other species by without irregular fibrillose annular zone on the upper part of the stipe, with subglobose mycocecidia.

Holotype:—CHINA. Yunnan Province: Laojun Mountain, Jianchuan City, Dali, 26°38'51.792"N, 99°49'10.43E, 2756 m elev., in a forest dominated by plants of Pinus yunnanensisFranch., 10 Aug. 2019, Fa Li 237 (HKAS 107306A!, GenBank Acc. No. : 28S = xxxx, ITS = xxxxxx, rpb2= xxxxxx, 18S= xxxxxx).

Pileus medium-sized, ca. 45 mm in diam, at first globose, then hemispheric, plano-convex with slightly incurved margin, thick-fleshed; surface buff (6B7–8), viscid when wet, covered with buff (6B7–8) floccose-fibrillose or slightly fibrillose squamules; pileal margin strongly appendiculate, with irregularly and densely corniform and fibrillose squamules derived from breaking up of the veil. Lamellae white (1A1), adnexed to adnate, moderately crowded, denticulate, rather thin, 6–7 mm wide. Stipe 50 × 10–19 mm, nearly cylindric, usually tapering upward; surface covered with buff (6B7–8) floccose-fibrillose or slightly fibrillose scaly zones, but not forming an irregular fibrillose annular zone at the upper part of the stipe, extreme apex white and nearly smooth. Mycocecidia subglobose 35 × 25 mm, white (1A1) with brownish (6A4–5) to rusty (6B7–8) spots. The transitional zone between stem and mycocecidia with some irregular rings of tawny-ochraceous (6B7–8) or dingy brown (6E5), fibrillose, appressed, or erect, obliquely upward-pointing or lacerate scales. Context white (1A1), rather firm. Smell rather strongly musty when crushed.

Basidiospores [40/1/1] 5.5–7.5 (–9) × (3.5–) 4–5 (–5.5) μm [Q = (1.2–) 1.3–1.8 (–2), Q = 1.6 ± 0.8], broadly ellipsoid, ellipsoid to elongate, sometimes subreniform in side view. Basidia 20–35 × 8–10 μm, subclavate, 4-spored, fusiform to ventricose-fusiform, hyaline; sterigmata 4–5 μm long; basal septa often with clamps. Pleurocystidia and cheilocystidia numerous, 60–90 × 13–17 μm, fusiform to ventricose-fusiform, with obtuse to acute apex, nearly all upper part of cystidia are slightly thick-walled (up to 1.5 μm), sometimes with refractive incrustations, hyaline. Lamellar trama regular, composed of colorless, thin-walled hyphae 5–10 μm in diam, branching, sometimes anastomosing; clamps present and common. Subhymenium consisting of 4–6 μm wide filamentous hyphal segments, narrow. Pileipellis a cutis with transition to a trichoderm at regular intervals, composed of loosely and more or less radially arranged, thin-walled hyphae 60–120 × 5–20 μm, and at the upper of the pileipellis often with fine brownish granular incrustations on the yellowish to brownish filamentous hyphae, clamps present and common, occasionally with brown vacuolar pigments, 2–5 μm wide; Mycocecidia composed of abundant subglobose to broadly clavate inflated cells (20–55 × 20–40 μm), and colorless and hyaline clampless filamentous hyphae, 2–6 μm wide, and clamped filamentous hyphae nearly 5–15 μm wide similar to those on the pileus; chlamydospores not observed.

Habit and habitat: Parastic on Amanita sepiacea growing on soil in forest dominated by Pinus yunnanensis.

Distribution:—Currently known from Yunnan and Hunan Provinces, southwestern and central China.

Additional specimens examined:—CHINA. Hunan Province: Fulin, Changsha City, 12. VI. 2001, Z. L. Yang 3049 (HKAS 38127); Mangshan, Yazishi, Yizhang County, 1500 m elev., 17. VI. 2001, Z. L. Yang 3071 (HKAS 38149), growing on soil in forest dominated by Pinus kwangtungensis Chun ex Tsiang and LithocarpusBlume sp.

Squamanita sororcula is similar to S. mira, S. orientalis, S. schreieri, S. umbonata, and other unidentified “S. umbonata”. The differences between the first two and S. sororcula have been discussed above. Besides, S. sororcula differs from S. schreieri by the presence of cystidia but differs from S. umbonata by its subglobose mycocecidia.

Wang and Yang (2004) treated two collections (HKAS 38127 and 38149) as “S. umbonata”. However, the two collections are without an annular zone, and should be close to S. sororcula rather than S. orientalis. Accordingly, we treat them as S. sororcula.

Squamanita umbonata (Sumst.) Bas, Persoonia 6: 335, 1965. Figs. 13–14.

Basionym: Vaginata umbonata Sumst., Mycologia 6: 35, pl. 117/fig. 1, 1914

≡Armillaria umbonata (Sumst.) Murrill, North Amer. Fl. 10: 38, 1914

Pileus 55–65 mm broad, convex with prominent broad obtuse umbo, background off-white (1B2), densely covered with coarse persisting, golden, yellowish brown, grayish orange (6B3-6B6) to brownish orange (6C3-6C8), strongly fibrillose attached or suberect scales and squamules, dry. Lamellae adnexed to adnate, up to 50 reaching stipe, emarginate with short decurrent tooth, white (1A1), with concolorous entire to eroded lamellar edges. Stipe 50–55 mm long, almost cylindrical, 1 cm broad at apex, white (1A1) to grayish orange (6B3-6B6) at apex, with coarse brownish orange (6C3-6C8) squamules formed from veil and sheathing stipe. Mycocecidia cylindrical to clavate fusiform, 80 mm long, 10–25 mm broad, from swollen bulb gradually tapering or rooting towards base, white (1A1), upper part of mycocecidia densely covered with coarse persisting grayish orange (6B3-6B6) fibrillose bands and squamules, lower part of mycocecidia subpileate, white (1A1), dry, solid, white, unchanging on exposure, solitary. The transitional zone between stem and mycocecidia with some irregular rings of tawny-ochraceous (6B7–8) or dingy brown (6E5), fibrillose, appressed, or erect, obliquely upward-pointing scales or lacerate scales. Odor weakly aromatic-acidulous. Taste mild. Spore print white.

Basidiospores [40/1/1] (6–) 6.5–8.5 (–9.5) × (3.5–) 4–4.5 (–5) μm [Q = (1.5–) 1.6–2.1 (2.3), Q = (1.5) 1.6 ± 2.1 (2.3)], ovoid, ellipsoid to elongate ellipsoid, sometimes subreniform, thin-walled, colourless, smooth, with small apiculus, thin-walled, inamyloid. Basidia 25–38 × 6–9 μm, 4-spored, with clamp at base. Cystidia scattered on sides of lamellae, (50–)60–95(–100) × (10.5)14–20 μm, slender fusiform to ventricose-fusiform, sometimes sublageniform, with obtuse to acute apex, thin walled (occasionally wall < 1 µm), colourless, sometimes with refringent both plasmatic and encrusting pigment, especially at apex. Trama of regular, made up of hyphae, 4–6 μm wide just below subhymenium, but to 40 (–60) μm wide in the middle; subhymenium densely ramose, very narrow. Squamules on pileus consisting of radially arranged hyphae 70–120 (220) × (6) 15–24 μm wide, with constricted at septa and yellow-brown walls. Pileipellis a cutis with transition to a trichoderm at regular intervals, composed of loosely and more or less radially arranged, thin-walled hyphae 70–220 × 6–24 μm, and at the upper of the pileipellis often with fine brownish granular incrustations and yellowish to brownish filamentous hyphae, constricted at septa, clamps present and common; Mycocecidia composed of abundant ellipsoid inflated cells without clamps, and filamentous hyphae similar to those on the pileus with clamps; chlamydospores not observed.

Specimens examined: —Costa Rica. Alajuela: Grecia, Bosque del Niño. In the forests consisting of plants of Quercus seemannii Liebm. and Quercus L. sp. 10°9′4″N, 84°14′42″W, 1900 m elev. 15 June 1996, R. E. Halling 7691 (GenBank Acc. No.: 28S = xxxx, ITS = xxxxxx, 18S=XXX ); —USA. North Carolina: Highlands, Ellicott Rock Trail, Bull Pen Road. In mixed broadleaf-conifer forest. 853 m elev. 21 Jul. 1987, E. Horak ZT 3989.

Habit and habitat:—Fungal hosts unknown.

Distribution:—Northeastern U.S.A.: Pennsylvania, North Carolina, and Costa Rica: Alajuela.

Characteristics of the collections, R. E. Halling 7691 and E. Horak ZT 3989 match well with the original description of S. umbonata. The most typical features of this species are the umbonate pileus, irregular rings of scales on the transitional zone between the orange brown squamulose stem and the cylindrical to clavate fusiform mycocecidia, thin-walled cystidia sometimes covered with refractive incrustations.

Vizzini and Girlanda (1997) reported four collections of “Squamanita umbonata” from Italy, and the hosts were supposed to be Inocybe oblectabilis (Britzelm.) Sacc. Our data indicated that collections of “S. umbonata” from Europe might differ from those of the North American S. umbonata.

TABLE 1. GenBank accession numbers of newly generated sequences in this study.

					SSU
Taxon	Voucher	Location	ITS	LSU	PNS1/NS41	NS51/NS8
Squamanita mira	HKAS 100826A	China	XXXXX	XXXXX	XXXXX	XXXXX
S. orientilis	HKAS 74862A	China	XXXXX	XXXXX	XXXXX	XXXXX
S. sororcula	HKAS 107306A	Italy	XXXXX	XXXXX	XXXXX	XXXXX
S. schreieri	ZTMyc 2185	Germany	XXXXX	XXXXX	XXXXX	XXXXX
S. umbonata	R.E.Halling 7691	Costa Rica	XXXXX	XXXXX	XXXXX	XXXXX
"S. umbonata"	H.E.Bigelow 17431	USA	XXXXX	XXXXX	XXXXX	XXXXX
"S. umbonata"	C.BAS 3808	USA	XXXXX	XXXXX	XXXXX	XXXXX
"S. umbonata"	HKAS 107325A	Italy	XXXXX	XXXXX	XXXXX	XXXXX
Cystoderma amianthinum	HKAS 106238	China	XXXXX	XXXXX	XXXXX	XXXXX
C. amianthinum	HKAS 105568	China	XXXXX	XXXXX	XXXXX	XXXXX
C. amianthinum	HKAS 57757	China	XXXXX	XXXXX	XXXXX	XXXXX
C. amianthinum	HKAS 107328	China	XXXXX	XXXXX	XXXXX	XXXXX
C. amianthinum	HKAS 107326	China	XXXXX	XXXXX	XXXXX	XXXXX
C. amianthinum	HKAS 107327	China	XXXXX	XXXXX	XXXXX	XXXXX
C. amianthinum	HKAS 80211	China	XXXXX	XXXXX	XXXXX	XXXXX
C. carcharias var. fallax	HKAS 107329	China	XXXXX	XXXXX	XXXXX	XXXXX
Phaeolepiota aurea	HKAS 93945	China	XXXXX	XXXXX	XXXXX	XXXXX
Amanita excelsa	HKAS 107325B	Italy	XXXXX	XXXXX	XXXXX	XXXXX
A. kitamagotake	HKAS 100824	China	XXXXX	XXXXX	XXXXX	XXXXX
A. kitamagotake	HKAS 100825	China	XXXXX	XXXXX	XXXXX	XXXXX
A. kitamagotake	HKAS 100826B	China	XXXXX	XXXXX	XXXXX	XXXXX
A. sepiacea	HKAS 574861	China	XXXXX	XXXXX	XXXXX	XXXXX
A. sepiacea	HKAS 74862B	China	XXXXX	XXXXX	XXXXX	XXXXX
A. sepiacea	HKAS 107306B	China	XXXXX	XXXXX	XXXXX	XXXXX

Systematic position of Cystodermateae sensu Singer

Singer (1986) included in Cystodermateae the following seven genera, viz. Cystoderma, Dissoderma (A. H. Sm. & Singer) Singer (current name: Squamanita), Horakia Oberw. (current name: Verrucospora E. Horak), Phaeolepiota, Pseudobaeospora Singer, Ripartitella Singer and Squamanita. Based on the phylogenetic analyses of Matheny and Griffith (2010), Matheny et al. (2015), Vizzini et al. (2019) and our present studies, three genera viz. Cystoderma, Phaeolepiota, and Squamanita can be assigned to the family Squamanitaceae within the Agaricineae (agaricoid clade). Phylogenetic placements of Pseudobaeospora, Ripartitella, and Cystodermella Harmaja, separated from Cystoderma by Harmaja (2002), are unclear yet, although previous research based on nLSU, rpb1 and ITS molecular sequences indicated that Ripartitella and Cystodermella are near Cercopemyces (Baroni et al. 2014). Recently, in multigene phylogenetic analyses (Sánchez-García and Matheny 2017; He et al. 2019), Pseudobaeospora was recognized as a member of the Tricholomataceae s. stricto within the Tricholomatineae (tricholomatoid clade).

Diversity of “S. umbonata” species complex

Our study indicated that S. umbonata and its allies are a complex of species (Fig. 4). Taken all morphological characteristics and molecular phylogenetic analysis data into consideration, the collections R. E. Halling 7691 and E. Horak ZT 3989 are considered to represent S. umbonata in this study (Fig. 13), because of their umbonate pileus, cylindrical to clavate fusiform mycocecidia and thin-walled cystidia (Bas 1965). TENN 57939 from North Carolina may also be S. umbonata. Although it seems that these specimens are separated by the genetic distance between TENN 57939 and R. E. Halling 7691 from Costa Rica as indicated in the phylogenetic tree, such sequence differences may well be caused by sequencing errors or quality of material.

The collection H. E. Bigelow 17431 (Fig. 15) has a subglobose mycocecidium, slightly smaller basidiospores (5–7 × 3.5–5 μm) and cystidia (45–65 × 12–18 μm) in comparison with those of S. umbonata, the mycocecidium is composed of abundant inflated cells, indicating the possibility of Amanita as host. The material may represent a new species.

Bas 3808 (Fig. 15) was published under the name of S. umbonata by Bas (1965). However, Cotés-Pérez et al. (2014) showed that the upper parts of the cystidia of C. Bas 3808 were slightly to moderately thick-walled, being consistent with our observations of the collection. Phylogenetically C. Bas 3808 forms a distinct branch (Fig. 3), differing from S. umbonata and other species of “S. umbonata”. DAOM 199323 [AF261508], submitted by Moncalvo et al. (2002), may well be conspecific with C. Bas 3808. A collection (HKAS 107306A) from Italy is sister to the above two collections (Fig. 15), and its hosts belong to the species complex of A. excelsa (NCBI accession number XXXXX). “Squamanita umbonata” was also reported from Japan (Ikeda 1996), Italy (Vizzini and Girlanda 1997), and Mexico (Cortés-Pérez et al. 2014). Whether this species actually occurs in East Asia and Europe or not, needs to be evaluated further.

Host preference or specificity of Squamanita species

It is interesting to notice that the species of Squamanita are clustered in four clades (Fig. 3): clades I and II possess no cystidia, while clades III and IV have cystidia, with DAOM 199323 and H. E. Bigelow 17431 not examined by us. In addition, S. paradoxa and S. pearsonii in clade I are strictly parasitic on Cystoderma, S. schreieri and S. mira in clade II are parasitic on Amanita. In clade IV, the known hosts of Squamanita are species of A. sect. Validae (Fig. 3).

Our study reveals that the basidiomes of S. mira are composed of its own hyphae, while its mycocecidia include both hyphae of the host and its own, which is consistent with the observation on S. paradoxa by Mondiet et al. (2007) and Griffith et al. (2019). Interestingly, host hyphae are found in the volval remnants that are attached to the pileal surface of the host S. orientalis (Fig. 5, 10). This character may provide an additional help for the host identification of Squamanita. Although sometimes the basidiomes of Squamanita may macromorphologically deform the hosts, most of the time the shapes of infected hosts (mycocecidia) still largely maintain consistent morphological characteristics with nearby uninfected homogeneous species. Our study showed that S. orientalis, S. sororcula and a “S. umbonata” (HKAS 107306A) from Italy with subglobose mycocecidium are parasitic on A. sect. Validae, S. mira with sheathing volva arising from margin of bulb is parasitic on A. kitamagotake, the shapes and identities of mycocecidia of known Squamanita are same with nearby hosts. Therefore, the shape and the size of the mycocecidia could be a reliable morphological character at species level.

28S: The large nuclear ribosomal RNA subunit; ITS: The internal transcribed spacers 1 and 2 with the 5.8S rDNA; 5.8S: 5.8S gene; 18S: the small subunit region; 18SF: The former segments of 18S amplified with primer pairs PNS1/NS41; 18SL: The later segments of 18S amplified with primer pairs NS51/NS8; tef1-α: Translation elongation factor 1-α; CTAB: Cetyltrimethyl ammonium bromide; HKAS: Herbarium of Cryptogams, Kunming Institute of Botany of the Chinese Academy of Sciences; ML: Maximum likelihood.

Acknowledgements

The authors are very grateful to the herbaria of New York Botanical Garden, Eidgenössische Technische Hochschule Zürich; and Gang Wu, Lihong Han, Fa Li, R. Berndt, Fabrizio Boccardo for providing specimens and images for this study, Shannon Asencio for providing helpful locality informations of DAOM 199323 and DAOM 225481; Gang Wu, Xiaobin Liu, YanLiang Wang for revising early manuscript.

Adherence to national and international regulations

Not applicable.

Authors’ contributions

Zhu L. Yang and Jianwei Liu designed the research. Jianwei Liu performed experiments, analyzed data and wrote the manu-script. Zhu L. Yang, Zai-Wei Ge, Egon Horak, Alfredo Vizzini, Roy. E. Halling revised the manuscript. Egon Horak, Alfredo Vizzini, Roy. E. Halling and Chun-Lei Pan also provided some specimens, The authors read and approved the final manuscript.

Funding

This work was supported by the Second Tibetan Plateau Scientific Expedition and Research Program (2019QZKK0503) and the Biodiversity Investigation, Observation and Assessment Program (2019-2023) of the Ministry of Ecology and Environment of China, and the International (Regional) Cooperation and Exchange Projects of the National Natural Science Foundation of China (No. 31961143010).

Availability of data and materials

All data generated or analyzed during this study are included in this published article.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Author details

¹Yunnan Key Laboratory for Fungal Diversity and Green Development, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China. ²CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, Yunnan, China. ³CAS Germplasm Bank of Wild Species in Southwestern China, Kunming Institute of Botany, Chinese Academy of Sciences, 132 Lanhei Road, Kunming, Yunnan 650201, China. ⁴Schlossfeld 17, AT-6020 Innsbruck, Austria. ⁵Department of Life Sciences and Systems Biology, University of Torino, Italy. ⁶Institute of Systematic Botany, New York Botanical Garden, 2900 Southern Blvd., Bronx, NY 10458-5126, USA. ⁷Mudanjiang Branch of Heilongjiang Academy of Agricultural Sciences, Mudanjiang, Heilongjiang 157041, China.

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Squamanitaceae and Three New Species of Squamanita Parasitic on Amanita Basidiomes

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