Микология и фитопатология, 2023, T. 57, № 1, стр. 25-32
Morganella Fimbriata (Lycoperdaceae, Agaricomycetes), a New Species from Cameroon
Yu. A. Rebriev *
Southern Scientific Centre of the Russian Academy of Sciences
344006 Rostov-on-Don, Russia
* E-mail: rebriev@yandex.ru
Поступила в редакцию 15.07.2022
После доработки 20.08.2022
Принята к публикации 4.11.2022
- EDN: HRXMAN
- DOI: 10.31857/S0026364823010117
Аннотация
Morganella fimbriata, a new puffball species, is described. The main diagnostic features are: cellular subgleba, exoperidium with spines which leave an areolate pattern on endoperidium after they fall off, and fimbriate stoma. Comparison with the morphologically closed species as well as ITS rDNA phylogenetic tree are presented.
INTRODUCTION
The genus Morganella was described by Zeller with the one species Morganella mexicana Zeller (1948). Later Morganella was amended by Kreisel and Dring (1967), with segregation several species from Lycoperdon Pers. The main distinguishing features are: small basidiomes with compact or chambered subgleba (perhaps lacking in some species), without a diaphragm; mature gleba without capillitium but with abundant paracapillitium; spores globose to broadly ovoid, verruculose to spinulose. The type species is M. mexicana, a synonym of Lycoperdon fuligineum Berk. et M.A. Curtis (Kreisel, Dring, 1967). Most of the species of Morganella are growing on dead wood, except Morganella stercoraria P. Ponce de León described as growing on cow dung and M. arenicola Alfredo et Baseia often found on sandy soil. The Morganella species are distributed mostly in tropical and subtropical regions. According to the Index Fungorum database (2022) there are approximately 20 species are known without synonyms.
Lycoperdon sulcatostomum (C.R. Alves et Cortez) Baseia, Alfredo et M.P. Martín described as Morganella sulcatostoma C.R. Alves et Cortez has strike features such as sulcate peristome, exoperidium detaching as large plates in maturity like in Lycoperdon marginatum Vittad. (Alves, Cortez, 2013). As pointed in Alfredo et al. (2017), the capillitium is present together with the paracapillitium. On the phylogenetic tree this species did not group in any of the subgenera of Lycoperdon s.l., described by Larsson and Jeppson (2008) and probably is a member of undescribed genus.
Using the morphological and molecular genetics methods new subgenus Apioperdon was described in Morganella (Krüger, Kreisel, 2003). L. pyriforme Schaeff. has been transferred from the genus Lycoperdon as a type species and new combination Morganella pyriformis (Schaeff.) Kreisel et D. Krüger was proposed. But this species is characterized by the presence of non-pitted capillitium along with paracapillitium and a number of other morphological features that distinguish it from Morganella. It was shown that Lycoperdon pyriforme has isolated position in Lycoperdon on Lycoperdaceae phylogenetic tree (Larsson, Jeppson, 2008; Bates et al., 2009). Based on this facts Apioperdon delimitated as independent genus (Vizzini, Ercole, 2017).
Phylogenetic analysis based on ITS and LSU nrDNA sequences showed that Morganella species are formed a weakly supported subclade in a Lycoperdon s.l. clade (Larsson, Jeppson, 2008; Bates et al., 2009; Alfredo et al., 2017). Taking a broad concept of the genus Lycoperdon, the Morganella (as well as Apioperdon, Bovistella, Vascellum) were accepted as subgenera in Lycoperdon s.l. (Larsson, Jeppson, 2008). According to modern views, it is possible to restore genus Morganella as independent genus (Wijayawardene et al., 2020).
In the course of the exchange of gasteroid basidiomycetes specimens between the Fungarium of the Royal Botanic Gardens Kew (K) and the Yu. Rebriev personal collection, several specimens were obtained. One of them was collected by P.J. Roberts in Korup National Park (Cameroon) and primarily labelled as L. fuligineum (cf.) Berk. et M.A. Curtis. On the basis of absence of the capillitium and lignicolous habitat this specimen was identified by me as Morganella sp. L. fuligineum is a synonym of Morganella fuliginea (Berk. et M.A. Curtis) Kreisel et Dring and characterized by very small or almost lacking compact subgleba and spinulose basidiospores (Kreisel, Dring, 1967) while our specimen has cellular subgleba and finely verruculose basidiospores. Using the phylogenetic analysis, it was shown that the ITS original sequence is quite far from those available in the GenBank database. The combination of morphological and molecular data made it possible to conclude that the studied specimen belongs to a new to science species.
MATERIALS AND METHODS
Morphology. The type material is deposited in the Komarov Botanical Institute of the Russian Academy of Sciences herbarium (LE). The examination of microstructures under the light microscope Mikmed-6 was made after boiling for a short time in lactophenol cotton blue. Scanning electronic microphotographs were taken using the Carl Zeiss EVO-40 XVP in the South Science Center of the Russian Academy of Sciences Center of Collective Use (no. 501994). Microscopic measurements were made by means of the specialized program Scandium 5.0. Light microphotographs as well as fruitbody photographs were taken using equipment of the Core Facility Center “Cell and Molecular Technologies in Plant Science” at the Komarov Botanical Institute of the Russian Academy of Sciences (BIN RAS).
Phylogenetic analysis. Genomic DNAs were isolated using CTAB method (Doyle, Doyle, 1987). ITS regions were PCR amplified and sequenced using primer pair ITS1F and ITS4 (White et al., 1990; Gardes, Bruns, 1993). The programs used for PCR amplifications are as following: pre-denaturation at 94°C for 5 min, then followed by 35 cycles of denaturation at 94°C for 30 s, annealing at 53°C for 50 s and elongation at 72°C for 50 s, followed by a final elongation at 72°C for 8 min. PCR products were cleaned and sequenced in the BIN RAS.
50 ITS sequences, including one newly generated from type specimen of Morganella fimbriata, were used (Table 1). Disciseda spp. were chosen as the outgroup taxa. All ITS sequences were aligned using the MAFFT on-line server, setting the Q-INS-i strategy (Katoh et al., 2019), and manually adjusted with MEGA 11 (Tamura et al., 2021). Phylogenetic differences were measured using BLAST (2022).
Table 1.
Taxon | ID (Specimen) | Country | GB no. ITS | Reference |
---|---|---|---|---|
Apioperdon pyriforme (Schaeff.) Vizzini | YuR1858 | Russia | MH628571 | GenBank |
Bovista aestivalis (Bonord.) Demoulin | YuR1600 | Russia | MH628569 | Rebriev et al. (2020) |
B. acuminata (Bosc) Kreisel | YuR0946 | “ ” | MH628567 | “ ” |
“ ” | YuR1993 | “ ” | MH628573 | “ ” |
B. furfuracea Pers. | MJ5435 | Sweden | DQ112622 | Larsson, Jeppson (2008) |
B. nigrescens Pers. | S&JJ980905 | “ ” | DQ112612 | “ ” |
B. plumbea Pers. | NYGD01 | Pakistan | JX183694 | Yousaf et al. (2013) |
Calvatia candida (Rostk.) Hollós | MJ3514 | Hungary | DQ112624 | Larsson, Jeppson (2008) |
Disciseda candida (Schwein.) Lloyd | STB304 | USA | EU833654 | Bates et al. (2009) |
D. hyalothrix (Cooke et Massee) Hollós | NSK1014099 | Russia | MN151399 | Vlasenko et al. (2020) |
Lycoperdon albostipitatum (Baseia et Alfredo) Baseia, Alfredo et M.P. Martín | UFRN-Fungos2249 | Brazil | KU958361 | Alfredo et al. (2017) |
L. albostipitatum* | INPA239563 | “ ” | KU958363 | “ ” |
L. arenicola (Alfredo et Baseia) Baseia, Alfredo et M.P. Martín* | UFRN-Fungos1006 | “ ” | KU958303 | “ ” |
“ ” | UFRN-Fungos655 | “ ” | KU958307 | “ ” |
L. echinatum Pers. | MJ6498 | Sweden | DQ112578 | Larsson, Jeppson (2008) |
L. fuligineum Berk. et M.A. Curtis | UFRN-Fungos371 | Brazil | KU958353 | Alfredo et al. (2017) |
“ ” | UFRN-Fungos1971 | “ ” | KU958321 | “ ” |
“ ” | UFRN-Fungos1972 | “ ” | KU958323 | “ ” |
“ ” | UFRN-Fungos2575 | “ ” | KU958325 | “ ” |
“ ” | UFRN-Fungos2562 | “ ” | KU958337 | “ ” |
L. molle Pers. | YuR2024 | Russia | MH628574 | Rebriev et al. (2020) |
L. nigrescens Pers. | MJ5376 | Sweden | DQ112577 | Larsson, Jeppson (2008) |
L. nudum (Alfredo et Baseia) Baseia, Alfredo et M.P. Martín | UFRN-Fungos1766 | Brazil | KU958315 | Alfredo et al. (2017) |
L. nudum* | UFRN-Fungos1765 | “ ” | KU958319 | “ ” |
L. oblongatum Accioly, Baseia et M.P. Martín * | UFRN-Fungos2570 | “ ” | KU958355 | “ ” |
L. perlatum Pers. | YuR597 | Russia | MH445551 | Crous et al. (2019) |
“ ” | MJ4684 | Sweden | DQ112630 | Larsson, Jeppson (2008) |
L. pratense Pers. | YuR0554 | Russia | MH445550 | Crous et al. (2019) |
“ ” | YuR1788 | “ ” | MH445554 | “ ” |
L. sulcatostomum (C.R. Alves et Cortez) Baseia, Alfredo et M.P. Martín | ICN177032 | Brazil | KU958373 | Alfredo et al. (2017) |
“ ” | ICN177033 | “ ” | KU958369 | “ ” |
Lycoperdon sp. 1 | CMU55-Ly1 | Thailand | KC414581 | GenBank |
Lycoperdon sp. 2 | HKAS 88251 | China | MH311863 | “ ” |
Morganella fimbriata* | LE 253894 | Cameroon | MT250089 | Сurrent study |
M. fuliginea (Berk. et M.A. Curtis) Kreisel et Dring | TFB11275 | Argentina | KY352656 | GenBank |
“ ” | TENN59070 | Paraguay | AF485065 | Krüger, Kreisel (2003) |
“ ” | AMP051 | Malaysia | KY777487 | GenBank |
M. puiggarii (Speg.) Kreisel et Dring | CMU-Mor3 | Thailand | KX064241 | Kumla et al. (2017) |
M. sosinii Rebriev et Bulakh* | YR-2013 | Russia | KC591769 | Rebriev, Bulakh (2015) |
“ ” | YuR3730 | “ ” | OP161223 | Current study |
“ ” | VLA19 09 97 | “ ” | OP161221 | “ ” |
M. subincarnata (Peck) Kreisel et Dring | 414 | Germany | AJ237626 | Krüger et al. (2001) |
“ ” | USA | MN964264 | GenBank | |
“ ” | TNS Kasuya B286 | Japan | KF551244 | Kasuya et al. (2013) |
“ ” | R-83 | Mexico | KR135347 | GenBank |
Morganella sp. | LE287320 | Vietnam | OP161220 | Current study |
“ ” | YuR3049 | “ ” | OP161222 | “ ” |
“ ” | YuR3054 | Russia | OP161224 | “ ” |
Vascellum curtisii (Berk.) Kreisel | HIP1 | USA | HQ235043 | Miller et al. (2011) |
V. intermedium A.H. Sm. | STB091 | “ ” | EU833667 | Bates et al. (2009) |
The ITS rDNA phylogenetic tree (Fig. 1) was obtained using MrBayes v. 3.2.1 (Ronquist et al., 2012) using the GTR + I + G model with 1.5 M. The best tree was visualized in FigTree v. 1.2.3 and edited in Adobe Illustrator CS5 (Fig. 1).
RESULTS
Our molecular data based on ITS sequences (Fig. 1) showed that the genus Morganella formed own clade (PP = 0.96). These data are inconsistent with previous phylogenetic reconstructions of the Lycoperdaceae (Larsson, Jeppson, 2008; Alfredo et al., 2017; Rebriev et al., 2020).
Taxonomy
Morganella fimbriata Rebriev sp. nov. (Fig. 2).
MycoBank no.: MB 844813
Diagnosis. Stoma dentate-fimbriate; exoperidium of slender spines up to 0.5–1.5 mm, clustered in stellate groups and leaving an inconspicuous reticulate pattern on the endoperidium when drop; subgleba cellular; basidiospores globose, 2.9–3.4 µm, punctate to almost smooth under the LM, often with a pedicel up to 5–7 µm.
Description. Basidiomes turbinate to pyriform, 10–15 mm high and 11–16 mm diam. Stoma wide, dentate-fimbriate, covered by a thin hyaline layer which can become detached in maturity. Exoperidium of dark-brown to cream-brown slender spines (up to 0.5–1.5 mm in upper part), clustering and joining at their tips forming stellate groups; finely granulose and echinulose in between; leaving at maturity an inconspicuous dark-brown reticulate pattern on the endoperidium when the spines drop. Endoperidium light greyish- to cream-brown. Gleba cream-brown. Subgleba white, prominent, cellular, occupying up to a third of the basidiome.
Basidiospores globose, pale brown, 2.9–3.4 µm, punctate to almost smooth under the LM and verruculose under the SEM, often with a pedicel up to 5–7 µm. Capillitium absent. Paracapillitium abundant, hyaline, incrusted, rarely bifurcated, 5–7 µm diam.
Holotype. Cameroon; South West Province, Korup National Park, trail from Mana Bridge to Transect P, N 5.20°, E 8.92°, on rotten wood, 05 04 1997, leg. P.J. Roberts (LE 253894; holotype). ITS sequence: GenBank MT250089.
Etymology. Name refers to the presence of a fimbriate stoma.
Habitat and distribution. The specimen was found on rotten wood in tropical forest, in a group of several basidiomes. Until now the known distribution is restricted to Central Africa, Cameroon.
DISCUSSION
On the basis of its small-size basidiomes, absence the capillitium and abundant the paracapillitium in combination with lignicolous habit the new species clearly refers to the genus Morganella.
Morphologically M. fimbriata is close to M. compacta (G. Cunn.) Kreisel et Dring, known from New Zealand (Cunningham, 1926), and M. costaricensis M.I. Morales, known from central and South America (Suárez, Wright, 1996), by showing a cellular subgleba and an areolate pattern on the endoperidium once the spines of the exoperidium have dropped in maturity. One else taxon from Africa named Lycoperdon fuligineum sensu Dring (Dring, Rayner, 1967) and described later as Morganella afra Kreisel et Dring (Kreisel, Dring, 1967) has minutely chambered subgleba, minutely granular exoperidium and minutely asperulate to short-spined basidiospores. However, M. fimbriata is distinct from all known species of Morganella in having a fimbriate stoma. The comparison of discussed species is presented in Table 2.
Table 2.
Species | Morganella fimbriata | M. afra | M. compacta | M. costaricensis |
---|---|---|---|---|
Basidiome size | 10–15 × 11–16 mm | 10–25 mm | up to 4 mm | up to 12 mm |
Stoma | dentate-fimbriate | torn | plane, torn, small | irregular |
Exoperidium | slender spines up to 0.5–1.5 mm, clustered in stellate groups; leaving an inconspicuous reticulate pattern on the endoperidium when drop | minutely granular | spines 3–4 mm, surrounded by a ring of minute brown granules; leaving an conspicuous reticulate pattern on the endoperidium when spines drop | simple pyramidal or groups of spines up to 1 mm long |
Basidiospores | globose, 2.9–3.4 µm diam., punctate to almost smooth, with pedicels up to 5–7 µm | globose, 3.5–4.5 µm, minutely asperulate to short-spined (to strongly echinulate in Dring, Rayner, 1967), with the stump of a pedicel | globose, 3.5–4.5 µm diam., asperulate, with caducous pedicels up to 5 µm | slightly ovate, 3.6–4.0 × × 3.2–3.6 µm, smooth, with pedicels 5.4–12.6 µm |
Paraсapillitium | rarely bifurcated | undescribed | sparsely branched or simple | distinctly branched |
Based on ITS nrDNA phylogenetic analyses, M. fimbriata is far from all sequenced taxa. The sequence of the new species differed from nearest M. puiggarii KX064241 by 11%, where 46 substitutions, four 1 bp incertions and 4 deletions (two 1bp, one 2bp and one 3bp).
Morganella clade has a good support in a Lycoperdon s.l. clade (PP = 0.96) (Fig. 1). This contradicts other publications, where Morganella has a weak support (Larsson, Jeppson, 2008; Bates et al., 2009; Alfredo et al., 2017). However, M. fimbriata take a separate position on the tree. If we consider this taxon as a sister group, then the rest of the Morganella clade has very weak support (PP = 0.64).
It is highly probably that there are several genera mentioned as Morganella s.l. on the basis of morphology. The Morganella s.l. is divided into the few groups (Fig. 1). The subclade A has high support (PP = 0.99) and consist of type species M. fuliginea as well as Lycoperdon nudum (Alfredo et Baseia) Baseia, Alfredo et M.P. Martín, L. albostipitatum (Baseia et Alfredo) Baseia, Alfredo et M.P. Martín and one non-identified sequence KR135347. All these species are characterised by compact subgleba and respond to the sect. Morganella Ponce de León (1971). Another species are distributed among weakly supported subclades B (PP = 0.88), C (PP = 0.65) and singletone with the new species Morganella fimbriata. All of them are characterised by chambered subgleba and respond to the sect. Subincarnata Ponce de León (1971). However Lycoperdon arenicola (Alfredo et Baseia) Baseia, Alfredo et M.P. Martín characterized by growing on soil basidiomes with the capillitium what does not correspond to the classical understanding of Morganella.
Subclade B has many unidentified sequences named as “Morganella sp.” or “Lycoperdon sp.”. Some of them are undescribed taxa probably.
It is notable that the sequences named as Morganella fuliginea are placed in two subclades of Morganella clade. In additional, type examination of M. puiggarii clearly establishes its synonymy with M. fuliginea (Suárez, Wright, 1996). Sequence KX064241 named M. puiggarii is grouped with unidentified sequences. The vouchers sequences of the M. fuliginea KY777487 and M. puiggarii KX064241 origin is Malaysia and Thailand respectively. M. fuliginea areal is in the tropics and subtropics of North and South America (Ponce de León, 1971). So it is highly probably that vouchers discussed was misidentified. This confirms the importance of molecular genetic studies in clarifying the identification of doubtful specimens (Brock et al., 2009).
The study was carried out within the frame of government assignments for the South Science Center RAS (project no. 122020100332-8). We are very grateful to Dr.A. Nazarenko for preparing SEM photo. Thanks to Begoña Aguirre-Hudson, the Curator – Mycologist of the Royal Botanic Gardens Kew (UK), for scientific discussions and observations on related material housed in the Kew Fungarium. We thank the two reviewers for their constructive criticism and suggestions to improve our work.
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