Psathyrella atlantica (Agaricales: Basidiomycota), a new species from Brazil

ABSTRACT

Psathyrella atlantica is described based on material collected in an Atlantic Forest fragment in the state of Pernambuco, Northeast Brazil. It is characterized by slender, whitish and caespitose basidiomata; pileus with orange, small and floccose-squamulose veil remnants; presence of a persistent but fragile-membranous annulus; basidiospores 5-7 × 3-4 µm; and inconspicuous germ pore. A full description plus illustrations and comments on morphological and phylogenetic data are provided.

Keywords:
Agaricomycetes; Agaricomycetidae; Neotropics; Psathyrellaceae; taxonomy

Introduction

Psathyrella (Psathyrellaceae, Agaricales) is a large genus of dark-spored mushrooms, with 500 (Vašutová et al. 2008) to 600 (Kirk et al. 2008) known species. This genus is considered difficult to study (Nagy et al. 2013), due to its fragile basidiomata and because many known species possibly represent species complexes (Hoashi 2008). According to Vašutová et al. (2008), the known taxa are predominantly described from the Northern hemisphere and are frequently cited in the Southern hemisphere, demonstrating the importance of studying this genus for searching undescribed species in the tropics.

In recent years, molecular phylogenetic methods are being used in the studies of Psathyrella and satellite genera, based on nu-rDNA sequences (Larsson & Örstadius 2008; Padamsee et al. 2008; Vašutová et al. 2008; Nagy et al. 2013). This has resulted in considerable advances in the understanding of the relationships within these fungi and revealed that the current infrageneric classification does not reflect the phylogeny of Psathyrella (Vašutová et al. 2008). A recent study by Örstadius et al. (2015) changed the systematic of this group, placing all psathyrelloid fungi in Psathyrella sensu stricto, Coprinopsis, Cystoagaricus, Homophron, Kauffmania, Typhrasa and an unnamed clade called/cordisporus. However, only six among 116 samples analyzed in this study were collected from the tropics.

For Brazil, at least 23 names are reported: Psathyrella ampelina, P. annulosa, P. araguana, P. argillospora, P. atricastanea, P. atomata, P. candolleana, P. coprinoceps, P. euthygramma, P. hortulana, P. janauariensis, P. lignatilis, P. microcarpella, P. murrillii, P. obtusata, P. palmigena, P. piluliformis, P. plana, P. polycystidiosa, P. pygmae, P. roystoniae, P. typhae and P. varzeae (Viégas 1945; Singer 1961; 1973; 1989; Pegler 1983; 1997; Maia et al. 2002; Cortez & Coelho 2005; Meijer 2006; 2008; 2010; Drechsler-Santos et al. 2007; Bononi et al. 2008; Rosa & Capelari 2009; G.C. Alves et al. 2012; M.H. Alves et al. 2012; Lazarotto et al. 2014; Pereira et al. 2018; Wartchow & Gomes 2019).

Meijer (2006) cited 17 taxa only from Paraná State (South Brazil), out of which, only five were identified at the species level. In Northeast Brazil, where our current study was undertaken, this genus is poorly known, with only four reported species: P. ampelina, P. atomata, P. euthygramma, and P. obtusata, all from the State of Pernambuco (Maia et al. 2002; Wartchow & Gomes 2019). Furthermore, M.H. Alves et al. (2012) reported two additional unnamed Psathyrella from the State of Piauí and Pereira et al. (2018) reported another one from Bahia.

During a survey regarding agaricoid fungi in the Atlantic Rain Forest in Northeast Brazil, several macrofungi were collected, along with an undescribed psathyrelloid species. Thus, the aim of this study is to describe this new species of Psathyrella based on the morphological and phylogenetic data, as well as to provide comments on its systematic placement among psathyrelloid genera along with illustrations of the microstructures, and photographs of the basidiomata.

Materials and methods

Collection site

The basidiomata of were collected from the ‘Reserva Biológica de Saltinho’ (8°44′13″ and 8°43′ S, 35°10′ and 35°11′ W), a 475,21 ha Atlantic Forest remnant located in the municipalities of Tamandaré and Rio Formoso, Pernambuco State, Northeast Brazil (Andrade & Moura 2011). Its climate is tropical humid (As’) according to Köppen’s classification, with average temperature ranging from 22 ºC to 26 ºC. This reserve is dominated mainly by Lowland Ombrophilous Dense Forest in regeneration process (Teixeira et al. 2010).

Morphological study

The basidiomata were analyzed as described by Singer (1986) and Largent (1986) and basidiospore data terminology was according to Tulloss et al. (1992), slightly modified by Wartchow et al. (2012) and Wartchow (2012). Statistics are based on 20 basidiospores. The abbreviations for the biometrical values are L(W) = basidiospore length (width) average, Q = the length:width ratio range as determined from all measured basidiospores, and Qm = the Q value averaged from all the basidiospores measured.

Color names were according to Kornerup & Wanscher (1978). Drawings of the microstructures were done with the aid of a camera lucida and photographs of the fresh basidiomata were taken at the field. The exsiccatum was deposited at Herbarium URM, Departamento de Micologia, Universidade Federal de Pernambuco (Thiers 2019).

DNA study

Genomic DNA was extracted from frozen field basidiomata by using the CTAB method proposed by Góes-Neto et al. (2005). For the amplification of ITS and LSU rDNA regions, the following primer sets were used: ITS5/ITS4 for ITS region (White et al. 1990; Gardes & Bruns 1993); and LR0R/LR7 for LSU region (Vilgalys & Hester 1990). PCR products were purified using GeneJet Purification Kit (Thermo Fisher Scientific, USA), followed by sequencing using the primers ITS5, ITS4, LR0R and LR5 performed at ‘Centro de Pesquisas sobre o Genoma Humano e Células-Tronco, Universidade de São Paulo’ (São Paulo, Brazil).

Contig was prepared using Sequencher v. 4.1.4 (Gene Codes Corp.) and the obtained sequence was combined with previously published Psathyrella (Fr.) Quél. sequences (Tab. 1), including the closest matches from GenBank (Benson et al. 2007) and aligned in MEGA 5.0 (Tamura et al. 2011). Maximum likelihood (ML) analyses were conducted with 1,000 bootstrap replications and Bayesian analyses (BA) were conducted with 2.0 million replications both in TOPALi v2 (Milne et al. 2009) and the models of evolution GTR+I+G were used to ML and BA based on AIC value. Following Larsson & Örstadius (2008), we selected Agrocybe pusiola (Fr.) R. Heim, a member of Bolbitiaceae Singer, a closely related family to Psathyrellaceae Vilgalys, Moncalvo & Redhead, as outgroup. The obtained sequences have been deposited in GenBank database.

Table 1
Data of specimens used in the phylogenetic analysis

Species	Voucher	Country	GenBank		References
			nLSU	nITS
Agrocybe pusiola	LÖ304-05	Sweden	DQ389732	DQ389732	Larsson & Örstadius (2008)
Coprinellus silvaticus	LÖ172-08	Sweden	KC992943	KC992943	Örstadius et al. (2015)
Coprinellus christianopolitanus	LÖ141-08 type	Sweden	KC992944	KC992944	Örstadius et al. (2015)
Coprinopsis canoceps	LÖ148-95	Sweden	KC992964	KC992964	Örstadius et al. (2015)
Coprinopsis cineraria	CBM-FB-24142 type	Japan	KC992962	KC992962	Örstadius et al. (2015)
Coprinopsis cineraria	CBM-FB-32880	Japan	KC992963	KC992963	Örstadius et al. (2015)
Coprinopsis melanthina	WU19918	Portugal	KC992961	KC992961	Örstadius et al. (2015)
Coprinopsis submicrospora	AH27055 type/	Spain	KC992959	KC992959	Örstadius et al. (2015)
Coprinopsis udicola	AM1240 type	Germany	KC992967	KC992967	Örstadius et al. (2015)
Psathyrella atlantica	URM 84467 type	Brazil	KC348448	KC348454	This study
Psathyrella badhyzensis	79478 (TAA) type	Turkmenistan	KC992883	KC992883	Örstadius et al. (2015)
Psathyrella bivelata	MCVE29117	Italy	MF325962	MF325962	Genbank
Psathyrella candolleana	TNS-F-12192	Japan	AB306311	AB306311	Ogura-Tsujita & Yukawa (2008)
Psathyrella efflorescens	Pegler2133 (K)	Sri Lanka	KC992941	KC992941	Örstadius et al. (2015)
Psathyrella hymenocephala	2766	-	FJ168608	FJ168608	Slot et al. (2010)
Psathyrella hymenocephala	PBM2768	-	FJ168609	FJ168609	Slot et al. (2010)
Psathyrella leucotephra	MCVE28705	Spain	MF325979	MF325979	Genbank
Psathyrella leucotephra	LÖ138-01	-	KC992885	KC992885	Örstadius et al. (2015)
Psathyrella luteopallida	Sharp20863 (MICH) type	USA	KC992884	KC992884	Örstadius et al. (2015)
Psathyrella lutulenta	21379 (AH) type	Spain	KC992875	KC992875	Örstadius et al. (2015)
Psathyrella lyckebodensis	LÖ301-11 type	Sweden	KC992921	KC992921	Örstadius et al. (2015)
Psathyrella magnispora	24929 (AH) type	Spain	KC992863	KC992863	Örstadius et al. (2015)
Psathyrella magnispora	Barta, Spittelberg	Austria	KC992864	KC992864	Örstadius et al. (2015)
Psathyrella mesobromionis	Arnolds01-174 (L) type	Netherlands	KC992862	KC992862	Örstadius et al. (2015)
Psathyrella tuberculata	ADK4162 (BR)	Togo	KC992886	KC992886	Örstadius et al. (2015)
Psathyrella tuberculata	ADK3564	Benin	KC992934	KC992934	Örstadius et al. (2015)
Psathyrella trinitatensis	TL9035 (C)	Ecuador	KC992882	KC992882	Örstadius et al. (2015)

Results

Phylogenetic analyses

The final ITS+LSU rDNA alignment comprised 1,669 characters with gaps and included 27 specimens representing 22 species. The ML and BA analyses produced similar topologies, and the BA tree was chosen to represent the phylogenetic placement of P. atlantica (Fig. 1). The analyses revealed that P. atlantica has strong support (bp =100, pp = 1) in the phylogeny, clustering close to P. leucotephra.

Figure 1
Phylogenetic relationship of Psathyrella atlantica and related taxa, inferred from ITS+LSU rDNA. Sequences generated for this study are indicated in bold. The voucher number is given for each specimen. Support values (ML/BI) are given above the branches. Scale bar shows expected changes per site.

Psathyrella atlantica V. Coimbra & Wartchow, sp. nov. Figs. 2, 3

MycoBank: MB 834994

Figure 2
Psathyrella atlantica (holotype): A. basidiomata in situ. B. Detail of the hymenium C. Basidiospores in 3 % KOH. Bars: A-B = 20 mm, C = 10 µm.

Figure 3
Psathyrella atlantica (holotype): A. Basidiospores. B. Basidia. C. Cheilocystidia. Bar = 10 µm. Drawing by V. R. M. Coimbra.

Diagnosis - Psathyrella atlantica is characterized by the slender, whitish and caespitose basidiomata, pileus with small orange floccose-squamulose veil remnants, presence of persistent but fragile-membranous annulus, basidiospores measuring 5-7 × 3-4 µm, lacking pleurocystidia and presenting utriform to utriform-lageniform thin walled cheilocystidia.

Type - BRAZIL, Pernambuco, Tamandaré, Reserva Biológica de Saltinho, 8°43′47″ S, 35°10′37″ W, 52 m alt., 12 April 2012, V.R.M. Coimbra s/n (URM 84467- holotype).

Etymology - based on the biome of occurrence of this species, the Brazilian Atlantic Forest.

Gregariously caespitose in cluster of 11 small basidiomata. Pileus: 10-28 mm diam., convex-campanulate, sometimes shallowly umbonate; white (4A1), sometimes with brown shades (5F5) due to spore-print covering; margin slightly sulcate and edge regularly toothed; context fleshy, white (4A1); veil on pileus surface as small floccose-squamulose remnants, light orange (5A5), more abundant at the centre then turning more scarce toward margin. Lamellae: adnate, close, dark brown (6F5), edge entire; lamellulae abundant, with diverse lengths. Stipe: 40-110 × 1.5-4 mm, cylindrical, central, shiny white (4A1), surface appressed squamulose-fibrillose downwards; squamules minutely fibrillose, light orange (5A5); context hollow, whitish, unchanging; base strongly strigose, presenting droplets of yellowish exudates; annulus persistent even in mature basidiomata but fragile, membranous, blackish, apical. Odor: unnoted when fresh, as dried Boletus edulis Bull. when dried.

Basidiospores 5-7 × 3-4 µm (L = 5.7 µm; W = 3.4 µm; Q = 1.40-2.00; Qm = 1.70), phaseoliform in profile, ovate with slightly rectangular base in face view, constricted at middle in the adaxial side; brown in KOH (5E7, 5E8), inamyloid; germ pore inconspicuous; hilar appendix very small and inconspicuous; smooth, thin-walled. Basidia 14-18 × 5-7 µm, clavate, hyaline, thin-walled, 2-4 sterigmata. Lamellae edge sterile with crowded cheilocystidia. Cheilocystidia 25-36 × 7-10 µm, utriform to subutriform, hyaline, thin-walled. Pleurocystidia absent. Lamellar trama regular, made of 17 cylindrical hyphae of 6-24 (-32) μm diam., usually inflated, hyaline, thin-walled. Pileipellis cellular, made of clavate, ovoid to subglobose and inflated cells 20-52 × 12-27 µm in diam., colorless, thin-walled. Stipitipellis with abundant caulocystidia 30-49 × 11-17.5 µm, clavate, hyaline, thin walled, more frequent at apex. Elements of veil on pileus with cylindrical hyphae 3-6 µm diam., brownish orange intracellular pigment, thin-walled. Hyphae clamped in all tissues examined.

Known distribution - So far, known only from the type locality. It grows in the litter deposited on the soil, in an area of Lowland Ombrofilous Dense Forest sensuInstituto Brasileiro de Geografia e Estatística - IBGE (1992) in the Atlantic Rain Forest domain.

Notes - Psathyrella atlantica is a noteworthy species, mainly recognized by the slender, whitish, and caespitose basidiomata, pileus with small orange floccose-squamulose veil remnants, presence of persistent but fragile-membranous annulus, and basidiospores of 5-7 × 3-4 µm size. Based on the infrageneric classification of Psathyrella proposed by Kits van Waveren (1985), P. atlantica can be placed in subgenus Psathyra sect. Spintrigerae due to its small basidiospores (up to 10 µm diam.), clavate basidia with less than 10 µm diam. and absence of pleurocystidia. Smith’s (1972) circumscription included species only with annulate and species lacking pleurocystidia in the sect. Spintrigerae.

Discussion

Our results suggest the placement of P. atlantica among members of clade/candolleana sensuÖrstadius et al. (2015). They also corroborate the determination of this taxon as a new species of Psathyrella sensu stricto. Padamsee et al. (2008) already stated that the clade/candolleana is among the ones that form a monophyletic group that better represents the limits of Psathyrella sensu stricto. This clade is dominated by the members of subgen. Psathyra sect. Spintrigerae (according to the classification of Kits van Waveren 1985) or subgen. Pseudostropharia sect. Spintrigerae (according to the classification of Smith 1972). Later, Nagy et al. (2013), Moreno et al. (2015), Yan & Bau (2018) and Voto et al. (2019) demonstrated that this clade is well-supported, characterized by species with pale colored basidiomata with fibrillose veil, and lacking pleurocystidia

Among morphologically close species that fall in the same clade, the European P. leucotephra is the most similar species. It also grows caespitosely in large clusters of 10 basidiomata, presents utriform to utriform-lageniform cheilocystidia, small hilar appendix and inconspicuous germ pore on basidiospores, pale colored pileus, and whitish sericeous-fibrillose stipe. Differences are focused on more robust basidiomata, larger basidiospores (usually 7-10 × 5-7 μm), and lignicolous habit of P. leucotephra (Berkeley & Broome 1870; Orton 1960; Kits van Waveren 1985; Breitenbach & Kränzlin 1995).

The new species P. atlantica also clustered with the sequences from an African specimen named as P. tuberculata. The protologue from Guadeloupe by Patouillard (1899) and later revisions by Morgan (1908) and Smith (1972) reported scattered squamules slightly projecting on the lower portion of the stipe; however, it clearly differs in the greenish pileus with small obtuse tubercles on pileus surface.

The decorated stipe of P. atlantica can be compared with two other Neotropical species reported by Smith (1972): P. floccosa and P. vanhermanii, both from Cuba. Psathyrella floccosa differs from P. atlantica in its depressed, ochraceous-brown and densely lanose-squamulose pileus, densely villose stipe, and a whitish, well developed annulus. Psathyrella vanhermanii shares similarities with P. atlantica in the pallid pileus, but differs in the adnexed lamellae, white and thick annulus, more robust stipe (5-10 mm diam.) tapered at the base, and fusoid-ventricose cheilocystidia of 26-30 × 9-15 µm (Smith 1972).

Psathyrella incerta and P. hymenocephala, both morphologically similar to the new species and widely distributed in North-America, differ mainly in lacking annulus, having less slender stipes and larger cheilocystidia [32-46 × 9-14 μm and 32-46 (-50) × 10-18 μm respectively] (Smith 1972).

Psathyrella candolleana is considered as the most common and variable species in North America by Smith (1972). This cosmopolitan taxon differs from P. atlantica in the absence of annulus, pileal veil remnants flocculose and white to yellowish-ochraceous, mainly located on the peripheral half of pileus, ellipsoid basidiospores and very crowded lamellae (Kits van Waveren 1985; Breitenbach & Kränzlin 1995).

BLASTn analysis of our ITS sequence (KC348454) showed highest similarities with P. leucotephra (97.17 %, MCVE28705 - MF325979; 96.74 %, LÖ138-01 - KC992885), while LSU sequence (KC348448) showed highest similarities (98 %) with sequences of P. candolleana (AY207279, DQ389720, DQ110874, DQ986225, DQ986250, FN396165), P. leucotephra (FM160683, DQ986240), P. typhae (DQ389721, DQ986229), P. multipedata (AM712279, GQ249291), P. huronensis (DQ986270), P. incerta (DQ986246), P. calcarea (DQ389671), P. prona var. utriformis (FM160687), P. aff. vanhermanii (AF261487), P. floccosa (DQ986235) and P. spadiceogrisea (DQ389682).

Based on our morphological and phylogenetic analyses of the specimen found in the Brazilian Atlantic Rain Forest, it is possible to propose P. atlantica as a genuine member of Psathyrella sensu stricto as also a new taxon to science. Thus, future mycological studies in this threatened biome are strongly encouraged, as a way of aiding the scientific community to scavenge its hidden mycobiota. In addition, the future records of P. atlantica collections will specify a variability of its morphological characters and its ecology.

Acknowledgements

The authors thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the master’s scholarship of VRMC and CNPq and FACEPE (APQ-0444-2.03/08) for partially funding this research (PROTAX 562106/2010-3, SISBIOTA 563342/2010-2); Dr. Gladstone Silva for his valuable assistance on lab procedures and bioinformatics; and ICMBIO for the license for collection in the area of study and the REBIO Saltinho staff for the logistical support.

References

• Alves GC, Victoria FC, Albuquerque MP, Pereira AB. 2012. Primeiro relato de fungos Agaricales no município de São Gabriel, RS, Brasil. Caderno de Pesquisa: Série Biologia 24: 7-20.
• Alves MH, Nascimento CC, Andrades EO, Araújo LRC. 2012. Fungos da APA Delta do Parnaíba, Litoral Piauiense. In: Guzzi A. (ed.) Biodiversidade do Delta do Parnaíba, Litoral Piauiense. Teresina, EDUFPI. p. 35-62.
• Andrade EVE, Moura GJB. 2011. Proposta de manejo das rodovias da REBIO Saltinho para mitigação do impacto sobre a anurofauna de solo. Revista Ibero-Americana de Ciências Ambientais 2: 24-38.
• Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL. 2007. GenBank. Nucleic Acids Research 35: 21-25.
• Berkeley MJ, Broome CE. 1870. Notices of British Fungi (1182-1262) Annals and Magazine of Natural History, Zoology, Botany and Geology 6: 461-469.
• Bononi VLR, Oliveira AKM, Quevedo JR, Gugliotta AM. 2008. Fungos macroscópicos do Pantanal do Rio Negro, Mato Grosso do Sul, Brasil. Hoehnea 35: 489-511.
• Breitenbach J, Kränzlin F. 1995. Fungi from Switzerland. Agarics. 2nd part. Switzerland, Mykologia Lucerne.
• Cortez VG, Coelho G. 2005. Additions to the mycobiota (Agaricales, Basidiomycetes) of Rio Grande do Sul, Brazil. Iheringia, Série Botânica 60: 69-75.
• Drechsler-Santos ER, Pastorini LH, Putzke J. 2007. Primeiro relato de fungos Agaricales em fragmento de mata nativa em Frederico Westphalen - RS. Revista Brasileira de Biociências 5: 471-473.
• Gardes M, Bruns TD. 1993. ITS primers with enhanced specificity for Basidiomycetes: application to identification of mycorrhizae and rusts. Molecular Ecology 2: 113-118.
• Góes-Neto A, Loguercio-Leite C, Guerrero RT. 2005. DNA extraction from frozen field-collected and dehydrated herbarium fungal basidiomata: performance of SDS and CTAB-based methods. Biotemas 18: 19-32.
• Hoashi Y. 2008. Psathyrella turcosomarginata, a new species with cheilocystidia possessing mucoid deposits staining bluish green in ammonia solution. Mycoscience 49: 385-387.
• Instituto Brasileiro de Geografia e Estatística - IBGE. 1992. Manual Técnico da Vegetação Brasileira. Série Manuais Técnicos em Geociências, número 1. Rio de Janeiro, IBGE.
• Kirk PM, Cannon PF, Minter DW, Stalpers JA. 2008. Ainsworth & Bisby’s Dictionary of the Fungi. 10th edn. Wallingford, CAB International.
• Kits van Waveren E. 1985. The Dutch, French and British species of Psathyrella Persoonia Supplement 2: 1-300.
• Kornerup A, Wanscher JH. 1978. Methuen handbook of colour, 3rd edn. London, Eyre Methuen Ltd.
• Largent DL. 1986. How to identify mushrooms to genus I: Macroscopic Features. I. 2nd edn. California, Mad River Press, Eureka.
• Larsson E, Örstadius L. 2008. Fourteen coprophilous species of Psathyrella identified in the Nordic countries using morphology and nuclear rDNA sequence data. Mycological Research 112: 1165-1185.
• Lazarotto DC, Putzke J, Silva ER, et al 2014. Comunidade de fungos Agaricomycetes em diferentes sistemas florestais no noroeste do Estado do Rio Grande do Sul, Brasil: Floresta Estacional Decídua e monocultura de eucalipto. Hoehnea 41: 269-275.
• Maia LC, Yano-Melo AM, Cavalcanti MAQ. 2002. Diversidade de Fungos no Estado de Pernambuco. In: Tabarelli M, Silva JMC. (eds.) Diagnóstico da Biodiversidade de Pernambuco. Recife, Massangana. p. 15-50.
• Meijer AAR. 2006. Preliminary list of the macromycetes from the Brazilian State of Paraná. Boletim do Museu Botânico Municipal 68: 1-55.
• Meijer AAR. 2008. Notable Macrofungi from Brazil’s Paraná Pine Forest/Macrofungos Notáveis das Florestas de Pinheiro-do-Paraná Colombo, Embrapa Florestas.
• Meijer AAR. 2010. Preliminary list of the macromycetes from the Brazilian State of Paraná: corrections and updating. Boletim do Museu Botânico Municipal 72: 1-10.
• Milne I, Lindner D, Bayer M, et al 2009. TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multicore desktops. Bioinformatics 25:126-127.
• Moreno G, Heykoop M, Esqueda M, Olariaga I. 2015. Another lineages of secotioid fungi is discovered: Psathyrella secotioides sp. nov. from Mexico. Mycological Progress 14: 34. doi: 10.1007/s11557-015-1057-8
  » https://doi.org/10.1007/s11557-015-1057-8
• Morgan AP. 1908. North American species of Agaricaceae. The Journal of Mycology 14: 64-75.
• Nagy LG, Válgvölgyi C, Papp T. 2013. Morphological characterization of clades of the Psathyrellaceae (Agaricales) inferred from a multigene phylogeny. Mycological Progress 12: 505-517.
• Ogura-Tsujita Y, Yukawa T. 2008. Hight mycorrhizal specifity in an widespread mycoheterotrophic plant, Eulophia zollingeri (Orchidaceae). American Journal of Botany 95: 93-97.
• Örstadius L, Rygberg M, Larsson E. 2015. Molecular phylogenetics and taxonomy in Psathyrellaceae (Agaricales) with focus on psathyrelloid species: introduction of three new genera and 18 new species. Mycological Progress 14: 25. doi: 10.1007/s11557-015-1047-x
  » https://doi.org/10.1007/s11557-015-1047-x
• Orton PD. 1960. New check list of British agarics and boleti. Part III. Notes on genera and species in the list. Transactions of the British Mycological Society 43: 159-439.
• Padamsee M, Matheny PB, Dentinger BTM, McLaughlin DJ. 2008. The mushroom family Psathyrellaceae: Evidence for large-scale polyphyly of the genus Psathyrella Molecular Phylogenetics and Evolution 46: 415-429.
• Patouillard N. 1899. Champignons de la Guadeloupe. Bulletin de la Société Mycologique de France 15: 191-209.
• Pegler DN. 1983. Agaric flora of Lesser Antilles. Kew Bulletin Additional Series 9: 1-668.
• Pegler DN. 1997. The Agarics of São Paulo, Brazil. London, Kew, Royal Botanic Garden.
• Pereira JM, Duarte EAA, Oliveira TAS, Reis BMS, Bezerra JL, Soares ACF. 2018. Exploring the relationship between macrofungi (Agaricales) colonizing different natural substrates from Reconcavo of Bahia, Brazil. Asian Journal of Microbiology, Biotechnology & Environmental Sciences 20: 104-111.
• Rosa LH, Capelari M. 2009. Agaricales fungi from Atlantic rain Forest fragments in Minas Gerais, Brazil. Brazilian Journal of Microbiology 40: 846-851.
• Singer R. 1961. Fungi of Northern Brazil. Publicações do Instituto de Micologia da Universidade de Recife 304: 3-26.
• Singer R. 1973. Diagnoses fungorum novorum agaricalium. III. Beihefte zur Sydowia 7: 1-106.
• Singer R. 1986. The Agaricales in Modern Taxonomy. 4th edn. Koegnistein, Koeltz Scientific Books.
• Singer R. 1989. New taxa and new combinations in the Agaricales (Diagnoses Fungorum Novorum Agariclium IV). Fieldiana Botany 21: 1-133.
• Slot JC, Hallstrom KN, Matheny PB, et al 2010. Phylogenetic, structural and functional diversification of nitrate transporters in three ecologically diverse clade of mushroom-forming fungi. Fungal Ecology 3: 160-177.
• Smith AH. 1972. The North American species of Psathyrella Memoirs of the New York Botanical Garden 24: 1-633.
• Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution 10: 2731-2739.
• Teixeira LJ, Feliciano ALP, Galindo ICL, Martins CM, Alencar AL. 2010. Relações entre a florística arbórea e características do solo em um fragmento de Floresta Atlântica, Tamandaré - PE. Floresta 40: 625-634.
• Thiers B. 2019. Index Herbariorum: a global directory of public herbaria and associated staff; New York Garden’s Virtual Herbarium, Index Herbariorum: a global directory of public herbaria and associated staff; New York Garden’s Virtual Herbarium, http://sweetgum.nybg.org/ih .16 Dec. 2019.
  » http://sweetgum.nybg.org/ih
• Tulloss RE, Ovrebo CL, Halling RE. 1992. Studies on Amanita (Amanitaceae) from Andean Colombia. Memoirs of the New York Botanical Garden 66: 1-46.
• Vašutová M, Antonín V, Urban A. 2008. Phylogenetic studies in Psathyrella focusing on sections Pennatae and Spadiceae - new evidence for the paraphyly of the genus. Mycological Research 112: 1153-1164.
• Viégas AP. 1945. Uns poucos fungos do Brasil. Bragantia 9: 561-582.
• Vilgalys R, Hester M. 1990. Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238-4246.
• Voto P, Dovana F, Garbelotto M. 2019. A revision of the genus Psathyrella, with a focus on subsection Spadiceogriseae Fungal Systematics and Evolution 4: 97-170.
• Wartchow F. 2012. Clavulina incrustata, a new species from Pernambuco, Brasil. Cryptogamie, Mycologie 33: 105-113.
• Wartchow F, Gomes ARP. 2019. Psathyrella euthygramma (Agaricales, Basidiomycota), a new record from Brazil. Darwiniana, Nueva Serie 7: 187-190.
• Wartchow F, Buyck B, Maia LC. 2012. Cantharellus aurantioconspicuus (Cantharellales), a new species from Pernambuco, Brasil. Nova Hedwigia 94: 129-137.
• White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 18: 315-322.
• Yan JQ, Bau T. 2018. Northeast Chinese species of Psathyrella (Agaricales, Psathyrellaceae). MycoKeys 33: 85-102.

Publication Dates

• Publication in this collection
  03 Aug 2020
• Date of issue
  Apr-Jun 2020

History

• Received
  20 Dec 2019
• Accepted
  30 Mar 2020