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Acta botánica mexicana

versión On-line ISSN 2448-7589versión impresa ISSN 0187-7151

Act. Bot. Mex  no.128 Pátzcuaro  2021  Epub 13-Dic-2021

https://doi.org/10.21829/abm128.2021.1896 

Research articles

Melanogaster coccolobae sp. nov. (Paxillaceae, Boletales), a tropical hypogeous fungus from the urban areas of Quintana Roo, Mexico

Melanogaster coccolobae sp. nov. (Paxillaceae, Boletales), un hongo hipogeo tropical de las áreas urbanas de Quintana Roo, México

Javier Isaac de la Fuente1 
http://orcid.org/0000-0003-4667-1574

César Ramiro Martínez-González2 
http://orcid.org/0000-0002-0256-0840

Iván Oros-Ortega3 
http://orcid.org/0000-0002-7542-5391

Gonzalo Guevara1 
http://orcid.org/0000-0002-2707-4531

Víctor M. Bandala4 
http://orcid.org/0000-0001-7093-0623

Iván Córdova-Lara5 
http://orcid.org/0000-0002-4761-7265

Reyna Yazuly Vela-Hernández3 
http://orcid.org/0000-0002-1111-595X

Caribell Yuridia López6 
http://orcid.org/0000-0002-4604-9147

Jesús García Jiménez1  7 
http://orcid.org/0000-0001-9290-1460

1Tecnológico Nacional de México, Instituto Tecnológico de Ciudad Victoria, Boulevard Emilio Portes Gil 1301, 87010 Cd. Victoria, Tamaulipas, Mexico.

2Universidad Nacional Autónoma de México, Departamento de Biología, Facultad de Ciencias, Ciudad Universitaria, 04510 CdMx., Mexico.

3Tecnológico Nacional de México, Instituto Tecnológico de la Zona Maya, Carretera Chetumal-Escárcega, km 21.5, 77965 Juan Sarabia, Quintana Roo, Mexico.

4Instituto de Ecología A.C., Red Biodiversidad y Sistemática, 91000 Xalapa, Veracruz, Mexico.

5Centro de Investigación Científica de Yucatán (CICY), Unidad de Biotecnología, calle 43, Col. Chuburná de Hidalgo, 97025 Mérida, Yucatán, Mexico.

6Tecnológico Nacional de México, Instituto Tecnológico de Chetumal, Av. Insurgentes 330, Col. 17 de Octubre, 77013 Chetumal, Quintana Roo, Mexico.


Abstract:

Background and Aims:

The genus Melanogaster is characterized by its hypogeous to semi hypogeous habit, brownish basidiomata, gel-filled gleba locules, and globose to ellipsoid basidiospores. The genus is distributed in temperate zones, but sequences from Coccoloba root tips and a few basidiome collections have revealed its presence in the tropics. The aim of this article is to describe a new species of Melanogaster based on ecological, molecular, and morphological data.

Methods:

Specimens were collected in urban vegetation of Quintana Roo in the Yucatán Peninsula, Mexico. For morphological description, the classic protocols for sequestrate fungi were followed. The dried material was deposited in the mycological herbarium “José Castillo Tovar” of the Instituto Tecnológico de Ciudad Victoria (ITCV) and the herbarium of the Universidad Autónoma de Yucatán (UADY).

Key results:

Melanogaster coccolobae is presented as a new species from the urban gardens of Quintana Roo based on ecological, molecular, and morphological evidence. This species is characterized by its hypogeous to semi hypogeous basidioma, greyish orange, brown to reddish brown peridium composed of two layers, sweet smell, subglobose, ellipsoid or piriform basidiospores, and by its mycorrhizal association with Coccoloba spicata.

Conclusions:

Melanogaster coccolobae is the first species described from the Mexican Caribbean from urban gardens with Coccoloba spicata. More studies about the tropical sequestrate fungi are recommended.

Key words: Agaricomycetes; Basidiomycota; Polygonaceae symbionts; sequestrate fungi; tropical fungi

Resumen:

Antecedentes y Objetivos:

El género Melanogaster se caracteriza por su hábito hipogeo a semi hipogeo, basidiomas parduscos, gleba con lóculos llenos de gel y basidiosporas globosas a elipsoides. El género se distribuye en zonas templadas, pero secuencias de ectomicorrizas de Coccoloba y pocas colecciones de basidiomas han revelado su presencia en los trópicos. El objetivo de este artículo es describir una nueva especie de Melanogaster a partir de datos ecológicos, moleculares y morfológicos.

Métodos:

Los especímenes fueron recolectados en jardines urbanos de Quintana Roo en la Península de Yucatán, México. Para la descripción morfológica se siguieron los protocolos clásicos para hongos secuestrados. El material se depositó en el herbario micológico “José Castillo Tovar” del Instituto Tecnológico de Ciudad Victoria (ITCV) y en el herbario de la Universidad Autónoma de Yucatán (UADY).

Resultados clave:

Melanogaster coccolobae se presenta como una nueva especie de los jardines urbanos de Quintana Roo con base en evidencia morfológica, ecológica y molecular. Esta especie se caracteriza por sus basidiomas hipogeos a semi hipogeos, peridio naranja grisáceo, marrón o marrón rojizo, compuesto por dos capas, olor dulce, basidiosporas subglobosas, elipsoides o piriformes y por formar asociación micorrízica con Coccoloba spicata.

Conclusiones:

Melanogaster coccolobae es la primera especie descrita del Caribe mexicano en jardines urbanos con Coccoloba spicata. Se recomiendan más estudios sobre los hongos secuestrados tropicales.

Palabras clave: Agaricomycetes; Basidiomycota; hongos secuestrados; hongos tropicales; simbiontes de Polygonaceae

Introduction

The genus Melanogaster Corda (Paxillaceae, Boletales) comprises hypogeous to semi hypogeous species characterized by a brownish to yellowish peridium, sometimes with mycelial strands at the base or sides, sequestrate hymenophore composed of rounded to irregular locules filled with black basidiospores embedded in gel, separated by whitish to yellowish veins or walls; and dark brown, globose, ellipsoid, pyriform or citriform basidiospores. Most of the species have an odor ranging from sweet and pleasant to garlicky or nauseating (Castellano et al., 1986; Miller Jr. and Miller, 1988; Pegler et al., 1993; Montecchi and Sarasini, 2000; Cázares et al., 2008; Trappe et al., 2009). It differs from related sequestrate Paxillaceae such as Alpova C.W. Dodge, Neoalpova Vizzini, and Paralpova Cabero & P. Alvarado by the peridium structure (prostrated or interwoven hyphae in Melanogaster vs. pseudoparenchymatous with inflated hyphae in Alpova, Neoalpova, and Paralpova), and Rhizopogon Fr. (Rhizopogonaceae) by the locules without gel and basidiospore color (hyaline in Rhizopogon). The relationships between these have been widely discussed by Trappe (1975), Grubisha et al. (2001), Vizzini et al. (2010), Moreau et al. (2011; 2013), and Alvarado et al. (2021).

Melanogaster species are common in the Northern hemisphere, but also occur in the Southern one due to introduction of Quercus L. species (Trappe et al., 2009). They can develop from the sea level to high forests and form ectomycorrhizal association with conifers and hardwoods (Castellano et al., 1986; Rinaldi et al., 2008; Tedersoo et al., 2010). According to Binder and Hibbett (2006), the genus belongs to the clade Paxillinae along with Gyrodon Opat., Paxillus Fr., and Alpova. Moreau et al. (2011) provisionally separated the European species in three sections: section Melanogaster P.-A. Moreau (including the species with basidiospores with more than 10 µm long in average), section Variegati P.-A Moreau (including the species with basidiospores of 6-10 μm long on average, not associated with Alnus Mill.) and section Rivulares P.-A Moreau (including species with basidiospores of 5-6 μm long on average). Ten species are recognized from Europe (Moreau et al., 2011), 19 from North America (Zeller and Dodge, 1936), and only three are known from Mexico: Melanogaster umbriniglebus Trappe & Guzmán, M. variegatus (Vittad.) Tul. & C. Tul., and M. minisporus Cázares, G. Guevara, J. García & Trappe (Trappe and Guzmán, 1971; Cázares et al., 1992, 2008). All the species known from northern Mexico form mycorrhizal symbioses with Quercus species (Zeller and Dodge, 1936; Trappe and Guzmán, 1971; Cázares et al., 1992, 2008). Despite the fact that several species have been described from Asia, America and Europe, molecular information is only available for eight, mostly European ones (Vizzini et al., 2010; Moreau et al., 2011, 2013). Furthermore, several unnamed Melanogaster sequences available in public databases are waiting to be formally described or nested with previously known taxa (Alvarado et al., 2021).

The ectomycorrhizal fungi from the tropics are still poorly studied in comparison with those from the template zones. Although several studies have been carried out in the Antilles and Central America about ectomycorrhizal fungi associated to Polygonaceae species (Pegler and Fiard, 1979; Pegler, 1983; Singer et al., 1983; Miller Jr. et al., 2000; Hasselquist et al., 2011; Põlme et al., 2017; de la Fuente et al., 2018), the knowledge about the fungi associated to Coccoloba spicata Lundell is still scarce in Mexico. Furthermore, C. spicata is a common tree of the disturbed vegetation, backyards and urban gardens in Quintana Roo state (Yucatán Peninsula, Southern Mexico). In recent years, several hypogeous fungi have been collected growing under C. spicata from the urban gardens of some localities in Quintana Roo. The aim of this study is to describe Melanogaster coccolobae based on ecological, morphological, and molecular evidence.

Material and Methods

Sampling

The mycological explorations were carried out in the state of Quintana Roo, Mexico, in urban gardens from Chetumal and Felipe Carrillo Puerto (Fig. 1). The vegetation within the sampling zones is disturbed. Methods for collecting, sampling and describing sequestrate fungi were used following Castellano et al. (1986). Handcut sections were made from dried specimens mounted in KOH 5% and Meltzer reagent for microscopic description. Color terminology was according to the Methuen Handbook of Colour (Kornerup and Wanscher, 1978). At least 30 microscopic structures (basidiospores, basidia and peridium hyphae) were measured with an optical microscope (Motic ba310, San Antonio, USA). The Q range, average length (L) and average width (W) were obtained for basidiospores. The scanning electron microscope (JEOL JSM-6010PLUS, LA, Tokyo, Japan) of El Colegio de la Frontera Sur (ECOSUR, Chetumal, Mexico) was utilized to observe basidiospores. All the specimens were curated and deposited in the mycological herbarium “José Castillo Tovar” of the Instituto Tecnológico de Ciudad Victoria (ITCV, Ciudad Victoria, Mexico) and Universidad Autónoma de Yucatán (UADY, Mérida, Mexico).

Figure 1: Distribution of Melanogaster coccolobae de la Fuente, J. García & Guevara. 

Amplification and sequencing

Total DNA was extracted from dried herbarium specimens using a modification of the Murray and Thompson (1980) protocol. The PCR amplification, based on Mullis and Faloona (1987), included 35 cycles with an annealing temperature of 54 ºC, and was carried out with the ITS5 and ITS4 primers (White et al., 1990; Gardes and Bruns, 1993) for the ITS nrDNA region, the LR0R and LR5 primers (Vilgalys and Hester, 1990; Cubeta et al., 1991) for the 28S nrDNA region (LSU), and the primers bRPB2-6F2 (reverse of bRPB2-6R2), and bRPB2-7R2 for the second largest subunit of the RNA polymerase II gene (rpb2) (Matheny et al., 2007). The PCR products were verified by agarose gel electrophoresis. The gels were run for 1 h at 95 V cm⁻³ in 1.5% agarose and 1× TAE buffer (Tris Acetate-EDTA). The gel was stained with GelRed (Biotium, USA) and the bands were visualized in an Infinity 3000 transilluminator (Vilber Lourmat, Germany). The amplified products were purified with the ExoSAP Purification kit (Affymetrix, USA), following the manufacturer’s instructions. They were quantified and prepared for the sequence reaction using a BigDye Terminator v. 3.1 (Applied Biosystems, USA). These products were sequenced in both directions with an Applied Biosystem model 3730XL (Applied BioSystems, USA), at the Instituto de Biología of the Universidad Nacional Autónoma de México (UNAM). The sequences obtained were compared with the original chromatograms to detect and correct possible reading errors.

Phylogenetic analyses

To explore the phylogenetic relationships of the new species, an alignment was made based on the taxonomic sampling employed by Halász (2009), Moreau et al. (2011, 2013), Rochet et al. (2011), Vizzini et al. (2010), and Alvarado et al. (2021). The ITS dataset included sequences from 42 fungal specimens representing 35 taxa. The ITS region was aligned using the online version of MAFFT v. 7 (Katoh et al., 2002, 2017; Katoh and Standley, 2013). The alignment was revised in PhyDE v. 10.0 (Müller et al., 2005), followed by minor manual adjustments to ensure character homology between taxa. The matrix was composed of 42 individuals (700 characters) (Appendix). Phylogenetic inferences were estimated with maximum likelihood in Rax-ML v. 8.2.10 (Stamatakis, 2014) with a GTR + G model of nucleotide substitution. To assess branch support, 1000 rapid bootstrap replicates were run with the GTRCAT model. For Bayesian posterior probability, the best evolutionary model for alignment was sought using PartitionFinder v. 2 (Lanfear et al., 2014; 2017; Frandsen et al., 2015;), the best-fit model selected for these three partitions of ITS sequences was GTR+G for ITS1, JC for 5.8s, and HKY+G for ITS2. Phylogenetic analyses were performed using MrBayes v. 3.2.6 x64 (Huelsenbeck and Ronquist, 2001). The information block for the matrix included two simultaneous runs, four Montecarlo chains, temperature set to 0.2 and sampling 10 million generations (standard deviation ≤0.1) with trees sampled every 1000 generations. The first 25% of samples were discarded as burn-in, and stationarity was checked in Tracer v. 1.6 (Rambaut et al., 2014). Trees were visualized and optimized in FigTree v. 1.4.4 (Rambaut, 2014).

Results

Molecular analyses

The two simultaneous Bayesian runs continued until the convergence parameters were met, and the standard deviation fell below 0.002 after 4 million generations. No significant changes in tree topology trace or cumulative split frequencies of selected nodes were observed after about 0.25 million generations, which were discarded as 25% burn-in. In the present study, a new species based on morphological characters and phylogenetic analysis of ITS sequences is described (Fig. 2). Due to the lack of multilocus sequences from other species of the genus Melanogaster and the family Paxillaceae, we cannot construct a multilocus phylogenetic tree at this time. We have sequenced the ITS, 28S and rpb2 genes, hoping they will be useful for future studies. The analysis of ITS produced a phylogenetic tree where Melanogaster is shown as a monophyletic clade (1 Bayesian Posterior Probability (PP) and 100% bootstrap proportion (BP) for Maximum Likelihood). The new species is phylogenetically distant from the European and North American species and forms a well-supported clade (0.99 Bayesian PP and 98% BP for ML) near two unidentified Melanogaster sequences from Guadeloupe, in the Caribbean (0.98 Bayesian PP and 97% BP for ML) (Séne et al., 2015) (Fig. 2).

Figure 2: Bayesian inference phylogram of ITS sequences data. Posterior probability (left of slash) from Bayesian analysis and Bootstrap support (right of slash). The new species Melanogaster coccolobae de la Fuente, J. García & Guevara is shown in bold. Boldface names represent samples sequenced for this study.  

Taxonomy

Melanogaster coccolobae de la Fuente, J. García & Guevara sp. nov. Fig. 3.

Figure 3: Melanogaster coccolobae de la Fuente, J. García & Guevara. A. basidiomata, de la Fuente 375 (ITCV-Holotype); B. details of the hymenophore, de la Fuente 05 (ITCV); C. details of the pileus, showing the dark mycelial strands, de la Fuente 05 (ITCV); D. basidiospores; E. basidiospore under scanning electron microscope (SEM); F. basidia; G. hymenophoral trama; H. subcutis; I. epicutis. Scale bars: 10 mm (A,B,C); 2 µm (E); 10 µm (D,F,G,H,I). 

TYPE: MEXICO. Quintana Roo, municipality Othón Pompeyo Blanco, urban gardens of the Instituto Tecnológico de Chetumal under Coccoloba spicata, 18°31'12''N, 88°18'22''W, 10 m a.s.l., 16.XI.2017, de la Fuente 375 (holotype: ITCV; isotype: UADY). Mycobank: MB 839197.

Melanogaster coccolobae can be distinguished from all other Melanogaster species by the following combination of characters: greyish orange, brown to reddish brown peridium, hypogeous to semi hypogeous, basidiomata 19-59 × 10-17 mm, odor sweet, subglobose, basidiospores ellipsoid or piriform, 6.2-12 × 5.2-10 µm, and the association with Coccoloba spicata.

Basidiomata 19-59 × 10-17 mm, scattered, hypogeous or semi hypogeous, globose to subglobose, lobate, greyish orange (5B6), brown (7E7) to reddish brown (8E8), staining dark brown (7F8) when touched, dry, smooth or slightly velvety, sometimes exuding a bright yellow liquid, with mycelial strands attached in some parts or around the basidiomata, dark brown (7F8); hymenophore composed of locules covered by a thin layer of black basidiospores when young, filled with hyaline gel, blackened due to the basidiospores when mature, without color changes when injured, with pale orange intermixed veins (5A3); columella absent; odor pleasant, sweet to alcoholic; peridium 170-230 µm thick, composed of two layers; epicutis 48-96 µm thick, composed of interwoven hyphae with conspicuous erect hyphae, fusoid to cylindrical terminal cells, dark orange to slightly reddish brown, 2-5 µm in diameter, thick-walled, sometimes with incrusted dark brown pigments; subcutis 116-140 µm thick, composed of interwoven tubulose, globose to irregular hyphae, yellowish to hyaline near the hymenophore, 3.5-14 µm diameter, thin-walled; clamp connections present, hymenophoral trama 37-75 diameter, hyaline, irregular composed of strongly gelatinized and interwoven slender hyphae, 4-10 µm diameter, thin-walled; basidia 18.8-29.7 × 8.6-10.4 μm, clavate with a long and sinuous stalk, basidiospores 2-4 , hyaline, poorly reviving in KOH 5%, thin-walled, occurring randomly in the locules; basidiospores subglobose, ellipsoid or pyriform, 6.2-12 × 5.2-10 µm (Q=1.1-1.7, L= 9.9, W=7.5, N=30), hyaline when immature, becoming dark brown, smooth, with conspicuous hilar appendage, 0.5-1.5 × 1.4-2 µm, cylindrical and hollow, sometimes cracked, giving to the hilar appendage a spiny appearance in optical microscopy, thick-walled.

Habit and habitat: hypogeous to semi hypogeous under Coccoloba spicata in urban gardens (Fig. 4).

Figure 4: Type locality of Melanogaster coccolobae de la Fuente, J. García & Guevara, with Coccoloba spicata Lundell.  

Distribution: only known from Quintana Roo, Mexico.

Etymology: named coccolobae due to the putative micorrhizal association with Coccoloba spicata.

Additional material examined: MEXICO. Quintana Roo, Municipality Othón Pompeyo Blanco, gardens of the Instituto Tecnológico de Chetumal (ITCh), 05.II.2014, J. de la Fuente 05 (ITCV); loc. cit., 14.X.2018, J. de la Fuente et al. 436 (ITCV). Municipality Felipe Carrillo Puerto, Felipe Carrillo Puerto, in urban gardens, 17.XI.2017, A. Hernández-Cach and J. de la Fuente 378 (ITCV).

Notes: the most remarkable characteristic of this new species is its putative micorrhizal association with Coccoloba spicata. Furthermore, M. coccolobae has an interesting peridium structure, which is composed of two layers with different hyphal arrangement. Due to the size and shape of spore and basidiome size, it resembles M. tuberiformis Corda. Nevertheless, that species has a thinner peridium composed only by interwoven hyphae and is associated with Pinus L., Quercus and Erica L.

Discussion

Melanogaster coccolobae can be identified mainly by the subglobose, ellipsoid or piriform basidiospores, the two-layered peridium and the mycorrhizal association with Coccoloba spicata. It differs from other Mexican Melanogaster species, such as M. umbriniglebus, by the reddish reaction of the gleba when cut, and the larger (reaching up to 14 µm) and the light colored basidiospores (Trappe and Guzmán, 1971). Melanogaster variegatus, a common species in North America, has citriform to ellipsoid basidiospores shape and larger spores (reaching up to 17 µm long) and is associated with Quercus species (Zeller and Dodge, 1936; Trappe and Guzmán, 1971). Melanogaster minisporus differs by the yellowish pileus, the smaller spores and the ecological association with Quercus species (Cázares et al., 2008).

Close DNA sequences have been obtained from the Caribbean (KF472137 and KF472152), and also some basidiomatas have been collected and have been identified as Melanogaster sp. (Séne et al., 2015). According to our phylogenetic analyses, these sequences are nested near M. coccolobae. These sequences have been collected under Coccoloba uvifera (L.) L. in coastal vegetation (Séne et al., 2015). Although the authors have exhaustively studied the ectomycorrhizal fungi associated to Coccoloba P. Browne trees in different vegetations with different conservation degree in the Yucatán Peninsula, basidiomata of M. coccolobae have never been found elsewhere. This peculiar distribution has been observed before in the tropics by Singer and Morello (1960), who found greater diversity of ectomycorrhizal fungi in disturbed vegetation in comparison with well-conserved forest. This new species is common in urban gardens, sharing habitat with several ectomycorrhizal species such as Xerocomus coccolobae Pegler, Tremelloscypha gelatinosa (Murrill) Oberw. & K. Wells, Scleroderma bermudense Coker, Inocybe xerophytica Pegler, Amanita arenicola O.K. Mill. & Lodge, and Cantharellus coccolobae Buyck, P.-A. Moreau & Courtec. This fungal diversity has been partially studied by García-Jiménez and Garza-Ocañas (2001) and de la Fuente et al. (2018).

Conclusions

In this study, a new species of Melanogaster of Mexico based on morphological characters, ecological distribution and ITS phylogeny is described. Melanogaster coccolobae is the first species of the genus known from tropical vegetation in Mexico. The new species has a preference for disturbed vegetation or urban gardens. The discovery of this fungus from this unusual habitat shows that disturbed areas can harbor an interesting fungal diversity with several noteworthy species. More studies about the ectomycorrhizal fungi occurring in such areas are recommended.

Acknowledgements

The first author thanks Pablo Alvarado, León Ibarra, Anahí Hernández, Emilio Pérez, and Beni Arana for molecular and technical support. Martínez-González thanks Laura Márquez and Nelly López, Laboratorio Nacional de Biodiversidad (LaNaBio) of the Instituto de Biología, Universidad Nacional Autónoma de México for sequencing. To the Consejo Nacional de Ciencia y Tecnología (CONACYT) and El Colegio de la Frontera Sur (ECOSUR-Chetumal) for providing access to the scanning electron microscope.

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Author contributions

JIF, RYVH and CYL collected the material. JIF, JGJ and GGG described the species. CRMG, IOO, ICL and VMB made the molecular analysis. JIF, GGG, and JGJ wrote the manuscript. All authors contributed to the manuscript.

Funding

This project was supported by the Tecnológico Nacional de México-Instituto Tecnológico de Ciudad Victoria.

Appendix

Appendix: GenBank accession numbers corresponding to the sequences used in the phylogenetic analyses. In bold the accessions of the new species. 

Species name Isolate/Voucher/strain Locality GenBank Accessions
ITS nrLSU rpb2
Alpova alpestris P.-A. Moreau & F. Rich. PAM07082629 Holotype France HQ714696 --- ---
Alpova austroalnicola L.S. Domínguez LSD 2290 Argentina HQ714793 AY377574 ---
Alpova cinnamomeus C.W. Dodge HRL1384, 29 Canada MN594282 MN594298 MN594770
Alpova concolor J. Hayward 65696 (OSC) Holotype USA KF835994 --- ---
Alpova corsicus P.-A. Moreau & F. Rich. S284 France HQ714766 --- HQ714890
Alpova diplophloeus (Zeller & C.W. Dodge) Trappe & A.H. Sm. Hayward 1 USA KF835992 --- ---
Alpova komovianus B. Perić & P.-A. Moreau PAM10081201 Montenegro JQ436850 --- JQ436862
Alpova pseudostipitatus Calonge & Siquier 36826 Holotype Spain MN594285 --- ---
Gyrodon lividus (Bull.) Sacc. REG G11 Germany DQ534568 AF098378 GU187701
Gyrodon sp. 926 Mexico HQ271432 --- ---
Melanogaster ambiguus (Vittad.) Tul. & C. Tul. 1590 Hungary AJ555512 --- ---
Melanogaster broomeianus Berk. 124251 --- AJ555530 --- ---
Melanogaster broomeianus Berk. 2331 Hungary AJ555531 --- ---
Melanogaster broomeianus Berk. 2348 Hungary EU784370 --- ---
Melanogaster coccolobae de la Fuente, J. García & Guevara 375 ITCV Holotype Mexico MZ098622 MZ098618 MZ089614
Melanogaster coccolobae de la Fuente, J. García & Guevara 378 ITCV Mexico MZ098623 MZ098619 MZ089615
Melanogaster coccolobae de la Fuente, J. García & Guevara 05 ITCV Mexico MZ098624 MZ098620 MZ089616
Melanogaster intermedius (Berk.) Zeller & C.W. Dodge 130202 --- AJ555515 --- ---
Melanogaster intermedius (Berk.) Zeller & C.W. Dodge 1770 Hungary EU784372 --- ---
Melanogaster cf intermedius (Berk.) Zeller & C.W. Dodge 122480 --- EU784371 --- ---
Melanogaster luteus Zeller 328 France HQ714780 --- ---
Melanogaster luteus Zeller 407 Montenegro HQ714794 --- ---
Melanogaster macrosporus Velen. 94 Hungary AJ555526 --- ---
Melanogaster rivularis P.-A. Moreau & F. Rich. 190 Holotype France HQ714731 --- HQ714891
Melanogaster rivularis P.-A. Moreau & F. Rich. 08090514 France NR132848 --- ---
Melanogaster sp Ecu344 France KF472137 --- ---
Melanogaster sp Ecu313 France KF472152 --- ---
Melanogaster tuberiformis Corda 1295 Romania AJ555527 --- ---
Melanogaster cf tuberiformis Corda 48368 Hungary AJ555521 --- ---
Melanogaster variegatus (Vittad.) Tul. & C. Tul. 1688 Hungary AJ555523 --- ---
Melanogaster variegatus (Vittad.) Tul. & C. Tul. 1438 Hungary AJ555524 --- ---
Melanogaster vittadinii Soehner & Knapp 33090 Hungary AJ555525 --- ---
Neoalpova arenicola Cabero & P. Alvarado 49153 Holotype Spain MN594292 MN594304 MN594775
Neoalpova montecchii Cabero, P. Alvarado & Vizzini 51272 Holotype Spain MN594296 MN594306 MN594777
Neoalpova rubescens (Vittad.) Vizzini 3003022 Spain MT259304 --- ---
Paragyrodon sphaerosporus (Peck) Singer MB06-066 USA GU187540 GU187593 GU187803
Paxillus vernalis Watling AFTOL-715 China DQ647827 AY645059 ---
Paralpova artikutzensis Cabero, D. Moreno-Mateos & P. Alvarado 49154 Holotype Spain MN594297 --- MN594778
Paxillus adelphus J.-P. Chaumeton, Gryta, Jargeat & P.-A. Moreau Pf01 Germany EU084664 AF167680 ---
Paxillus involutus (Batsch) Fr. Bel10.4 France KF261366 --- JQ436854
Paxillus rubicundulus P.D. Orton 2905 U.K. KU163502 FM993114 ---
Paxillus vernalis Watling MB-062 Holotype China DQ647827 AY645059 ---

Received: May 10, 2021; Revised: June 08, 2021; Accepted: September 22, 2021; Published: September 29, 2021

7Author for correspondence: jgarjim@yahoo.com.mx

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