Research Article |
Corresponding author: Gareth W. Griffith ( gwg@aber.ac.uk ) Academic editor: María P. Martín
© 2018 Caio A. Leal-Dutra, Maria Alice Neves, Gareth W. Griffith, Mateus A. Reck, Lina A. Clasen, Bryn T. M. Dentinger.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Leal-Dutra CA, Neves MA, Griffith GW, Reck MA, Clasen LA, Dentinger BTM (2018) Reclassification of Parapterulicium Corner (Pterulaceae, Agaricales), contributions to Lachnocladiaceae and Peniophoraceae (Russulales) and introduction of Baltazaria gen. nov. MycoKeys 37: 39-56. https://doi.org/10.3897/mycokeys.37.26303
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The genus Parapterulicium was first introduced to accommodate two Brazilian species of coralloid fungi with affinities to Pterulaceae (Agaricales). Despite the coralloid habit and the presence of skeletal hyphae, other features, notably the presence of gloeocystidia, dichophyses and papillate hyphal ends, differentiate this genus from Pterulaceaesensu stricto. Fieldwork in Brazil resulted in the rediscovery of two coralloid fungi identifiable as Parapterulicium, the first verified collections of this genus since Corner’s original work in the 1950s. Molecular phylogenetic analyses of nrITS and nrLSU sequences from these modern specimens revealed affinities with the /peniophorales clade in the Russulales, rather than Pterulaceae. The presence of distinctive hyphal elements, homologous to the defining features of /peniophorales, is consistent with the phylogenetic evidence and thus clearly distinguished Parapterulicium and its type species P. subarbusculum from Pterulaceae, placing this genus within /peniophorales. Parapterulicium was also found to be polyphyletic so Baltazaria gen. nov. is proposed to accommodate P. octopodites, Scytinostroma galactinum, S. neogalactinum and S. eurasiaticogalactinum also within /peniophorales.
Molecular Phylogeny, Taxonomy, Russulales , /peniophorales, Corticioid fungi, Coralloid fungi
Pterulaceae Corner is a diverse but poorly known family of mostly tropical coralloid fungi within order Agaricales Underw. (
To date, only three of the five Pterulaceae genera have been included in molecular phylogenetic analyses, viz. Pterula Fr., Deflexula Corner and Pterulicium Corner (
During recent field expeditions in four Brazilian states, two coralloid fungi morphologically assignable to Parapterulicium spp. were collected, providing fresh material for molecular phylogenetic analysis. Here we present results that show Parapterulicium is paraphyletic and evolutionarily related to Peniophoraceae Lotsy and Lachnocladiaceae D.A. Reid in the Russulales Kreisel ex P.M. Kirk, P.F. Cannon & J.C. David, rather than Pterulaceae in the Agaricales. We propose taxonomic changes precipitated by these results and provide a re-evaluation of distinctive morphological features, such as variations in skeletal hyphae that may be considered phylogenetically informative in light of this discovery.
The new collections of Parapterulicium are deposited at FLOR, INPA and RB. Herbarium acronyms follow Index Herbariorum (Thiers continuously updated). Macroscopic analyses were conducted following the traditional methods of
Microscopic analyses were adapted from
DNA was extracted from dried basidiomes by first grinding with a mortar and pestle in the presence of liquid nitrogen, followed by purification using the DNeasy Plant Mini Kit (Qiagen) according to the manufacturer’s instructions. Partial sequences of the nuclear ribosomal internal transcribed spacers (nrITS) and nuclear ribosomal large subunit (nrLSU) were amplified by PCR using the primer pairs ITS8F-ITS6R (
Sequences and chromatograms were checked, assembled and edited using GENEIOUS 10.0.2 (
Prior to the inclusion in the datasets, the clones were aligned to generate one or two consensus sequences of each cloned species. Substitutions were replaced by the respective ambiguous code and, in the cases where indels were found, two different sequences were generated.
To assess the global phylogenetic position of Parapterulicium within Agaricomycetidae, a dataset containing the nrLSU sequences of 886 Agaricomycetidae taxa was created by adding the sequences generated in this study to the dataset of
A more focused dataset for higher resolution phylogenetic analysis was created by removing duplicate species from the Russulales dataset of
The ITS1 and ITS2 datasets were aligned using MAFFT v7.311 (
The best-fit evolutionary models were estimated for each partition separately using JMODELTEST v2.1.3 (
Maximum-likelihood analysis was performed with IQTREE v1.6.3.b (
Nodes with BPP ≥0.95 and/or BS ≥75 were considered strongly supported.
Alignments and phylogenetic trees are deposited in Treebase (ID: 22642).
Species from clade /peniophorales and their GenBank accession numbers of ITS and nrLSU sequences. Newly generated sequences are shown in bold.
Taxa | Sample no. | Locality | GenBank Accession no. | Reference | |
---|---|---|---|---|---|
nrITS | nrLSU | ||||
Asterostroma cervicolor | KHL9239 | Puerto Rico | AF506408 | AF506408 |
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Asterostroma macrosporum | TMI 25697 | Japan | NR119394 | – |
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Asterostroma muscicola | TMI 25860 | Japan | AB439551 | AB439551 |
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Baltazaria eurasiaticogalactina | CBS 666.84 | France | – | AY293211 |
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Baltazaria galactina | NH4863 | Sweden | AF506466 | AF506466 |
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Baltazaria neogalactina | CBS 758.86 | France | – | – | Unpublished |
Baltazaria octopodites | FLOR 56442 | São Paulo – Brazil | MH260024 | MH260043 | This study |
MH260044 | |||||
MH260045 | |||||
MH260046 | |||||
Baltazaria octopodites | FLOR 56449 | São Paulo – Brazil | MH260025 | MH260047 | This study |
Baltazaria octopodites | FLOR 56460 | Santa Catarina – Brazil | MH260032 | MH260050 | This study |
Baltazaria octopodites | FLOR 63715 | Paraná – Brazil | MH260042 | MH260060 | This study |
Baltazaria octopodites | INPA 280140 | Amazonas – Brazil | MH260038 | MH260056 | This study |
MH260039 | MH260057 | ||||
MH260040 | MH260058 | ||||
MH260041 | MH260059 | ||||
Confertobasidium olivaceoalbum | FP90196 | USA | AF511648 | AF511648 |
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Dendrophora albobadia | TDeAB1029 | USA | AF119522 | AF119522 |
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Dichostereum durum | FG1985 | France | AF506429 | AF506429 |
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Dichostereum effuscatum | GG930915 | France | AF506390 | AF506390 |
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Dichostereum granulosum | NH7137/696 | Canada | AF506391 | AF506391 |
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Dichostereum pallescens | NH7046/673 | Canada | AF506392 | AF506392 |
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Duportella lassa | SP6129 | Russia | KJ509191 | KJ509191 |
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Entomocorticium sp. | FL_19 | USA | KJ620518 | KJ620518 |
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Gloeocystidiopsis flammea | CBS 324.66 | C. African Rep. | AF506437 | AF506437 |
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Gloiothele lamellosa | CBS404.83 | Madagascar | AF506487 | AF506487 |
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Gloiothele torrendii | JB18615 | France | AF506455 | AF506455 |
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Lachnocladiaceae | S1PMB7 | Thailand | AB365531 | AB365531 |
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Lachnocladiaceae | S335WS151 | Thailand | AB365532 | AB365532 |
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Lachnocladium cf. brasiliense | CALD 161213-1 | Espírito Santo – Brazil | MH260037 | MH260055 | This study |
Lachnocladium cf. brasiliense | KM 57848 | Puerto Rico | MH260034 | MH260052 | This study |
MH260035 | MH260053 | ||||
MH260036 | MH260054 | ||||
Lachnocladium schweinfurthianum | KM 49740 | Cameroon | MH260033 | MH260051 | This study |
Lachnocladium sp. | KHL10556 | Jamaica | AF506461 | AF506461 |
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Lachnocladium sp. | BK171002-23 | Belize | DQ154110 | DQ154110 | Unpublished |
Metulodontia nivea | NH13108 | Russia | AF506423 | AF506423 |
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Parapterulicium subarbusculum | FLOR 56456 | Rio de Janeiro – Brazil | MH260026 | MH260048 | This study |
Parapterulicium subarbusculum | FLOR 56459 | Rio de Janeiro – Brazil | MH260027 | MH260049 | This study |
MH260028 | |||||
MH260029 | |||||
MH260030 | |||||
MH260031 | |||||
Peniophora incarnata | NH10271 | Denmark | AF506425 | AF506425 |
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Peniophora nuda | FPL4756 | – | – | AF287880 |
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Scytinostroma alutum | CBS 762.81 | France | – | AF393075 |
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Scytinostroma caudisporum | CBS 746.86 | Gabon | – | AY293210 |
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Scytinostroma portentosum | EL11-99 | Sweden | AF506470 | AF506470 |
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Vararia insolita | CBS 667.81 | Ivory Coast | – | AF518665 |
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Vararia investiens | TAA161422 | Norway | AF506484 | AF506484 |
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Vesiculomyces citrinus | EL53-97 | Sweden | AF506486 | AF506486 |
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A total of 37 sequences were generated in this study (19 nrITS and 18 nrLSU). The final alignment consisted of 135 sequences with 2295 characters. The BI analysis converged all runs as indicated by the effective sample sizes (ESS) of all parameters above 2000 and the potential scale reduction factors (PSRF) equal 1.000 for all the parameters. The two Parapterulicium species were placed with strong support into /peniophorales sensu
The clade /peniophorales recovered in the Russulales tree and the genera which it comprises are consistent with the neighbour-joining analyses of
Five main clades highlighted in Fig.
Maximum likelihood tree of Russulales on the left with /peniophorales amplified on the right. Support values on the branches are BS (>65) / BPP (>0.95), names in bold represent the newly generated sequences for this study and bold lines show the new genus. Details for the complete tree can be found in Suppl. material
Clade /lachnocladiaceae (BS=99; BPP=1)
Lachnocladium formed a well-supported clade with Scytinostroma, Vesiculomyces E. Hagstr., Gloiothele Bres., Asterostroma Massee, Vararia ocholeuca (Bourdot & Galzin) Donk, Scytinostroma ochroleucum Donk, Scytinostroma odoratum (Fr.) Donk and Baltazaria gen. nov. (BS=99; BPP=1).
Baltazaria (BS=92; BPP=1)
This clade represents the newly proposed genus (see below). It contains the sequences of P. octopodites, S. eurasiaticogalactinum, S. neogalactinum and S. galactinum. The presence of P. octopodites here rendered Parapterulicium paraphyletic necessitating reclassification.
Clade /varariaceae (BS=75; BPP=0.98)
This clade includes Parapterulicium subarbusculum, Dichostereum Pilát and Vararia P. Karst. The inclusion of Parapterulicium sequences enhanced support for this clade, which was also recovered by
Parapterulicium subarbusculum, the type species of the genus, was nested within a strongly supported clade, which also contains Vararia insolita Boidin & Lanq. (BS=98; BPP=0.99). The reclassification of Vararia insolita may be warranted if future data support its placement here. Parapterulicium subarbusculum is also clustered with environmental sequences derived from subtropical leaf litter in Thailand (
Clade /peniophoraceae. (BS=100; BPP=1)
The clade /peniophoraceae includes Peniophora, Duportella Pat., Dendrophora (Parmasto) Chamuris and Entomocorticium H.S. Whitney, Bandoni & Oberw. These genera require special attention for detailed morphological and molecular studies to resolve the paraphyly of Peniophora, by either proposing new genera or synonymising Dendrophora and Entomocorticium. In all analyses performed in this study, there was no clear resolution for this group.
Clade /metulodontia (BS=95; BPP=1)
The clade contains Metulodontia Parmasto and Confertobasidium Jülich. Following
Basidiomes coralloid/filiform, up to 35 mm high, branched, erect, monoaxial with adventitious branches, yellow (10YR 8/6), solitary or gregarious. Stipe up to 13 × 0.3–0.7 mm, glabrous, concolorous with the rest of the basidiomes, attached to a small resupinate base up to 3 mm wide. Branches up to 1.3 × 0.2 mm, tapering upwards, rarely with branchlets.
Habitat: On dead twigs, petioles, leaves or seeds in the forest.
Hyphal system dimitic. Generative hyphae up to 7 μm wide thin-walled, without clamps. Skeletal hyphae 2–7 μm wide, thick-walled (up to 1.3 μm), rarely branched. Abundant dextrinoid dichophyses, up to 30 μm wide, slightly thick-walled (0.5–1 μm), branching with filiform ends, tips less than 0.5 μm wide.
Resupinate patch not well-developed in the studied material but with abundant dichophyses.
Basidia not observed.
Gloeocystidia up to 65 μm long, clavate to lanceolate/subulate, thin-walled, with numerous internal droplets, IKI-.
Basidiospores (12–)13.4–16.8(–17) × 3–3.5 μm (n = 19), hyaline, smooth, elongate, subfusiform, apex obtuse, base acute with small apiculus (0.3 μm), thin-walled and slightly amyloid, scarce in all the collected samples.
Brazil. Rio de Janeiro: Rio de Janeiro, Parque Nacional da Tijuca, close to Casa do Pesquisador, growing on the ground in rainforest litter, 24-25 Nov 2014, C.A. Leal-Dutra 108, 109, 117,118, 119, 120, 121, 122 (topotypes designated here: RB 639457, RB 639458, RB 639462, RB 639463, FLOR 56456, FLOR 56457, FLOR 56458, FLOR 0056459).
Brazil. Rio de Janeiro: Rio de Janeiro (
This species is recognised in the field by its characteristic resupinate disc at the base of the stipe (Fig.
Parapterulicium subarbusculum: a–c basidiomes in the field. The detail in c shows the developing corticioid patch d basidiospores e dichophyses f gloeocystidia g, hSEM images of dichophyses; i. SEM images of basidiome surface with abundant dichophyses. Scale bars: a–c = 1 cm; d–f, i = 10 μm; g, h = 5 μm.
In honour of Dr. Juliano Marcon Baltazar, Brazilian mycologist and authority on neotropical corticioid fungi.
Baltazaria galactina (Fr.) C.A. Leal-Dutra, Dentinger & G.W. Griff.
Basidiomes corticioid, adherent to effused, coriaceous/membranaceous when fresh, hard when dry, usually white, cream or pale ochraceous. Context densely homogeneous with thick-walled and dextrinoid skeletal-binding hyphae, sometimes bearing rows of short papillae or skeletodendrohyphidia. Global distribution.
The diagnosis of
Thelephora galactina Fr., Nova Acta R. Soc. Scient. upsal., Ser. 3 1(1): 136 (1851) [1855]. ≡ Corticium galactinum (Fr.) Moffatt, Bulletin of the Nat. Hist. Surv. Chicago Acad. Sci. 7(1): 137 (1909). ≡ Scytinostroma galactinum (Fr.) Donk, Fungus, Wageningen 26: 20 (1956).
= Thelephora suaveolens Moug. ex Fr., Elench. fung. (Greifswald) 1: 208 (1828).
= Stereum suaveolens (Moug. ex Fr.) Fr., Epicr. syst. mycol. (Upsaliae): 553 (1838) [1836-1838].
= Xerocarpus suaveolens (Moug. ex Fr.) P. Karst., Bidr. Känn. Finl. Nat. Folk 37: 137 (1882).
Description in
Scytinostroma eurasiaticogalactinum Boidin & Lanq., Biblthca Mycol. 114: 57 (1987)
Description in
Scytinostroma neogalactinum Boidin & Lanq., Biblthca Mycol. 114: 59 (1987).
Description in
Parapterulicium octopodites Corner, Ann. Bot., 16: 286 (1952)
Basidiomes resupinate (Fig.
Substrate: On dead twigs and leaves.
Hyphal system dimitic, profusely interwoven. Generative hyphae 2–5 μm wide, thin-walled, without clamps. Skeletal hyphae 2–6 μm (up to 10 μm in KOH) wide, walls dextrinoid, up to 1.5 μm thick, strongly swelling in KOH (up to 4.5 μm). Termini of hymenial skeletal hyphae papillate, presenting short protuberances 2–10 × 1.5–2.5 μm, sometimes ramified resembling skeletodendrohyphidia.
Putative hymenium with abundant basidioles up to 25 × 6 μm, clavate, growing immersed in the papillate hyphae.
Gloeocystidia up to 80 × 8–14 μm, clavate to lanceolate, thin-walled, densely multiguttulate or with abundant granular contents. Present in all parts of the basidiomes, including the corticioid form.
Basidiospores and basidia not observed.
Brazil. Rio Grande do Sul: no date, J. Rick (holotype: BPI 333063). São Paulo: Apiaí, Parque Estadual Turístico do Alto Ribeira, growing on the ground in rainforest litter, 14-15 Dec. 2014, M.A. Reck 1003/14, 1069/14 (FLOR 56442, FLOR 56449). Santa Catarina: Florianópolis, UCAD, 9 Jan. 2015, G. Flores 14 (FLOR 56460). Paraná: Foz do Iguaçú, Parque Nacional do Iguaçú, Trilha da torre, 22 Jan. 2017, C.A.T. Oliveira 160 (FLOR 63715). Amazonas: Rio Preto da Eva, ARIE-PDBFF - Reserva do Km 41, 17 Mar. 2017, C.A. Leal-Dutra, L.A. Clasen, Q.V. Montoya, O. Pereira 170309-26 (INPA 280140).
Brazil. Rio Grande do Sul: São Leopoldo (Corner, 1952a; Type). São Paulo: Apiaí. Santa Catarina: Florianópolis. Paraná: Foz do Iguaçu. Amazonas: Rio Preto da Eva (this study).
The dimitic hyphal system, the papillate surface at the ends of the skeletal hyphae and the gloeocystidia agree perfectly with Corner’s original descriptions (
Baltazaria octopodites: a, b basidiomes in the field (INPA280140 and FLOR56460), the detail in a shows the anchorage point in the leaf, the whitish resupinate area in b shows the corticioid portion of the fungus c gloeocystidia d skeletal hyphae, skeletal hyphae inflated in KOH (third from the right) and generative hyphae (first and second from the right) e–hSEM images of papillate skeletal hyphae. Scale bars: a–b = 1 cm; c–d = 10 μm; e–h = 1 μm).
The /lachnocladiaceae clade was named /asterostromataceae by
Future studies of Lachnocladiaceae may recommend Baltazaria be classified in its own family. However, we view our study as incomplete and it would therefore be premature to erect a new family at this time.
The most distinctive feature of B. octopodites is the papillate skeletal hyphae that form one or two rows of short, round and sometimes branched projections, similar to some skeletodendrohyphidia of B. galactinum (
All collections of B. octopodites made to date are sterile with no spores or basidia observed. Although the hymenium might have been missed due to developmental idiosyncrasies, such as ephemeral nocturnal production (
A third species of Parapterulicium, P. simplex, is still known only from type material originally collected in Argentina (
CALD scholarship was provided by CAPES Foundation - Brazil, BEX 2145/15-4. Funding was provided in part from a Systematics and Taxonomy (SynTax) grant (BBSRC, NERC) to BTMD. Parque Nacional da Tijuca (ICMBio), for logistic support and collection permits. Biological Dynamics of Forest Fragmentation Project (BDFFP) for providing logistical and field support. This is publication 743 of the BDFFP - INPA/STRI Technical Series (field reserve; location of specimen used here). We are grateful to Alan Cookson, IBERS, for assistance with Scanning electron microscopy and also to IBERS HPC and Supercomputing Wales for computing support. The Institute of Biological, Environmental, and Rural Sciences receives strategic funding from the BBSRC. We thank Felipe Ruppenthal for the line drawings.
Species used in the Russulales analyses and their GenBank accession numbers of nrITS and nrLSU sequences