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Reclassication of Parapterulicium Corner (Pterulaceae, Agaricales)... 39
Reclassification of Parapterulicium Corner (Pterulaceae,
Agaricales), contributions to Lachnocladiaceae and
Peniophoraceae (Russulales) and introduction of
Baltazaria gen. nov.
Caio A. Leal-Dutra1,2,4, Maria Alice Neves1, Gareth W. Grith2, Mateus A. Reck1,
Lina A. Clasen2, Bryn T. M. Dentinger3
1 Micolab, Departamento de Botânica, Centro de Ciências Biológicas, Universidade Federal de Santa Ca-
tarina, Florianópolis, Santa Catarina, 88040-900, Brazil 2 Institute of Biological, Environmental and Ru-
ral Sciences, Aberystwyth University, Aberystwyth, Ceredigion SY23 3DD, UK 3 Natural History Museum
of Utah and School of Biological Sciences, University of Utah, Salt Lake City, UT, 84108 USA 4 CAPES
Foundation, Ministry of Education of Brazil, P.O. Box 250, Brasília – DF 70040-020, Brazil
Corresponding author: Gareth W. Grith (gwg@aber.ac.uk)
Academic editor: M.P. Martín | Received14 May 2018 | Accepted 12 July 2018| Published 31 July2018
Citation: Leal-Dutra CA, Neves MA, Grith GW, Reck MA, Clasen LA, Dentinger BTM (2018) Reclassication 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
Abstract
e genus Parapterulicium was rst introduced to accommodate two Brazilian species of coralloid fungi
with anities 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, dierentiate
this genus from Pterulaceae sensu stricto. Fieldwork in Brazil resulted in the rediscovery of two coralloid
fungi identiable as Parapterulicium, the rst veried 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 anities with the /peniophorales clade in the Russulales, rather than Pterulaceae. e
presence of distinctive hyphal elements, homologous to the dening features of /peniophorales, is consist-
ent 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 galacti-
num, S. neogalactinum and S. eurasiaticogalactinum also within /peniophorales.
Keywords
Molecular Phylogeny, Taxonomy, Russulales, /peniophorales, Corticioid fungi, Coralloid fungi
Copyright Caio A. Leal-Dutra et al. 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.
MycoKeys 37: 39–56 (2018)
doi: 10.3897/mycokeys.37.26303
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RESEARCH ARTICLE
Caio A. Leal-Dutra et al. / MycoKeys 37: 39–56 (2018)
40
Introduction
Pterulaceae Corner is a diverse but poorly known family of mostly tropical coralloid
fungi within order Agaricales Underw. (Dentinger and McLaughlin 2006), recognised
mainly by their coralloid/liform basidiomes with a dimitic hyphal structure (Corner
1952a, 1952b, 1957, 1970).
To date, only three of the ve Pterulaceae genera have been included in molecu-
lar phylogenetic analyses, viz. Pterula Fr., Deexula Corner and Pterulicium Corner
(Dentinger and McLaughlin 2006, Dentinger et al. 2009). e remaining genera,
Parapterulicium Corner and Allantula Corner, are known only from a few scant speci-
mens collected by Corner as the basis of his taxonomic proposal; these are poorly pre-
served and impractical for molecular studies. Allantula (meaning ‘sausage’ in ancient
Greek), characterised by decumbent, intercalary swellings resembling minute sausages,
is known only from the type specimen (Corner 1952a) and has not been recollected
despite several recent attempts at the type locality (Parque Nacional da Tijuca, Rio de
Janeiro, Brazil) by the present authors. Parapterulicium was described for two coralloid
species from Brazil that resembled Pterulaceae in their liform statues and dimitic hy-
phae, but diered in the presence of gloeocystidia and dichophyses.
Corner (1952a) suggested some similarity of Parapterulicium to Lachnocladium
Lév. based on the shared features of dichophyses and gloeocystidia combined with the
lack of clamps. However, due to the small liform basidiomes, branching pattern, col-
ourless dimitic hyphae and corticioid patch, Corner referred the genus to Pterulaceae
instead of Lachnocladiaceae. Corner’s emphasis of skeletal hyphae as a synapomorphy
for Pterulaceae has been shown previously to be incorrect with the reclassication of
Actinceps Berk. & Broome (=Dimorphocystis) (Dentinger and McLaughlin 2006), al-
though this feature remains a dening feature of Pterulaceae.
During recent eld expeditions in four Brazilian states, two coralloid fungi morpho-
logically assignable to Parapterulicium spp. were collected, providing fresh material for
molecular phylogenetic analysis. Here we present results that show Parapterulicium is para-
phyletic 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 Pteru-
laceae 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.
Methods
Collections and morphological observations
e new collections of Parapterulicium are deposited at FLOR, INPA and RB. Herbar-
ium acronyms follow Index Herbariorum (iers continuously updated). Macroscopic
analyses were conducted following the traditional methods of Largent (1986).
Reclassication of Parapterulicium Corner (Pterulaceae, Agaricales)... 41
Microscopic analyses were adapted from Largent et al. (1977) for pterulaceous
fungi, where, instead of sectioning the basidiomes with a razor, part of the fungus was
dissected with the aid of two small diameter needles. e dissections were mounted in
5% KOH, H2O, Melzer’s reagent, Congo red or 1% phloxine and then observed with
an Olympus CX21 (Olympus, Tokyo, Japan) light microscope equipped with 10x, 40x
and 100x objective lenses, the latter being used with immersion oil. Macro- and micro-
scopic illustrations were based on pictures taken in the eld with a Nikon D90 DSLR
camera (Nikon, Tokyo, Japan) and on photos taken during microscopic observations.
e colour codes follow the Munsell Soil Color Charts (Munsell 1975). Scanning
electron microscopy (SEM) images were obtained using a Hitachi S-4700 eld emis-
sion scanning electron microscope (Hitachi, Tokyo, Japan) and the air-dried specimens
were directly stuck on the carbon tab on the stubs without any treatment. e stubs
were coated with gold and platinum and examined and photographed at 5 kV.
DNA extraction, PCR amplification, cloning and sequencing
DNA was extracted from dried basidiomes by rst grinding with a mortar and pestle in
the presence of liquid nitrogen, followed by purication using the DNeasy Plant Mini
Kit (Qiagen) according to the manufacturer’s instructions. Partial sequences of the nu-
clear ribosomal internal transcribed spacers (nrITS) and nuclear ribosomal large subu-
nit (nrLSU) were amplied by PCR using the primer pairs ITS8F-ITS6R (Dentinger
et al. 2010) and LR0R-LR7 (Vilgalys and Hester 1990), respectively and following the
cycling conditions in the original publications. PCR products were puried using 2
units of Exonuclease I (ermo Fisher Scientics) and 1 U FastAP ermosensitive Al-
kaline Phosphatase (ermo Fisher Scientics) per 1 µl of PCR product, incubated at
37 °C for 15 min, followed by denaturing at 85 °C for 15 min. e samples were then
sent for Sanger sequencing at the IBERS Aberystwyth Translational Genomics Facility.
Sequences and chromatograms were checked, assembled and edited using GE-
NEIOUS 10.0.2 (Kearse et al. 2012). Samples presenting indels were cloned using
pGEM-T Easy Vector Systems (Promega) into Subcloning Eciency DH5α Competent
Cells (Invitrogen). Five clones from each PCR were then amplied and sequenced as
above. e sequences generated in this study have been submitted to GenBank (Table 1).
Phylogenetic analysis
Prior to the inclusion in the datasets, the clones were aligned to generate one or two consen-
sus sequences of each cloned species. Substitutions were replaced by the respective ambigu-
ous code and, in the cases where indels were found, two dierent sequences were generated.
To assess the global phylogenetic position of Parapterulicium within Agaricomy-
cetidae, a dataset containing the nrLSU sequences of 886 Agaricomycetidae taxa was
created by adding the sequences generated in this study to the dataset of Moncalvo
Caio A. Leal-Dutra et al. / MycoKeys 37: 39–56 (2018)
42
Table 1. 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 Larsson and Larsson (2003)
Asterostroma
macrosporum TMI 25697 Japan NR119394 –Suhara et al. (2010)
Asterostroma
muscicola TMI 25860 Japan AB439551 AB439551 Suhara et al. (2010)
Baltazaria
eurasiaticogalactina CBS 666.84 France –AY293211 Binder et al. (2005)
Baltazaria galactina NH4863 Sweden AF506466 AF506466 Larsson and Larsson (2003)
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 Larsson and Larsson (2003)
Dendrophora
albobadia TDeAB1029 USA AF119522 AF119522 Hsiau and Harrington
(2003)
Dichostereum durum FG1985 France AF506429 AF506429 Larsson and Larsson (2003)
Dichostereum
effuscatum GG930915 France AF506390 AF506390 Larsson and Larsson (2003)
Dichostereum
granulosum NH7137/696 Canada AF506391 AF506391 Larsson and Larsson (2003)
Dichostereum
pallescens NH7046/673 Canada AF506392 AF506392 Larsson and Larsson (2003)
Duportella lassa SP6129 Russia KJ509191 KJ509191 Spirin and Kout (2015)
Entomocorticium sp. FL_19 USA KJ620518 KJ620518 Bracewell and Six (2014)
Gloeocystidiopsis
flammea CBS 324.66 C. African Rep. AF506437 AF506437 Larsson and Larsson (2003)
Gloiothele lamellosa CBS404.83 Madagascar AF506487 AF506487 Larsson and Larsson (2003)
Gloiothele torrendii JB18615 France AF506455 AF506455 Larsson and Larsson (2003)
Lachnocladiaceae S1PMB7 Thailand AB365531 AB365531 Osono et al. (2009)
Lachnocladiaceae S335WS151 Thailand AB365532 AB365532 Osono et al. (2009)
Reclassication of Parapterulicium Corner (Pterulaceae, Agaricales)... 43
Taxa Sample no. Locality GenBank Accession no. Reference
nrITS nrLSU
Lachnocladium cf.
brasiliense
CALD
161213-1
Espírito Santo –
Brazil MH260037 MH260055 This study
Lachnocladium cf.
brasiliense KM 57848 Puerto Rico
MH260034 MH260052
This studyMH260035 MH260053
MH260036 MH260054
Lachnocladium
schweinfurthianum KM 49740 Cameroon MH260033 MH260051 This study
Lachnocladium sp. KHL10556 Jamaica AF506461 AF506461 Larsson and Larsson (2003)
Lachnocladium sp. BK171002-
23 Belize DQ154110 DQ154110 Unpublished
Metulodontia nivea NH13108 Russia AF506423 AF506423 Larsson and Larsson (2003)
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 Larsson and Larsson (2003)
Peniophora nuda FPL4756 – – AF287880 Hibbett et al. (2000)
Scytinostroma
alutum CBS 762.81 France –AF393075 Binder and Hibbett (2002)
Scytinostroma
caudisporum CBS 746.86 Gabon –AY293210 Binder et al. (2005)
Scytinostroma
portentosum EL11-99 Sweden AF506470 AF506470 Larsson and Larsson (2003)
Vararia insolita CBS 667.81 Ivory Coast –AF518665 Hibbett and Binder (2002)
Vararia investiens TAA161422 Norway AF506484 AF506484 Larsson and Larsson (2003)
Vesiculomyces citrinus EL53-97 Sweden AF506486 AF506486 Larsson and Larsson (2003)
etal. (2002), as adapted by Dentinger and McLaughlin (2006). e analyses of this
dataset demonstrated the placement of Parapterulicium within the Russulales. See
Suppl. material 1: Agaricomycetidae analysis, for details and results of these analyses.
A more focused dataset for higher resolution phylogenetic analysis was created by
removing duplicate species from the Russulales dataset of Chen et al. (2016) and add-
ing the new sequences generated in this study alongside 29 GenBank sequences and one
from CBS-KNAW database to represent all currently recognised families of Russulales, as
well as all the genera of Lachnocladiaceae and Peniophoraceae with sequences available.
Four sequences of Sistostrema Schumach. were used as outgroup. e Russulales data-
set contained 135 sequences and was divided in four partitions: ITS1, 5.8S, ITS2 and
nrLSU. A list of accession numbers of the sequences added to Chen et al. (2016) dataset
is presented in Table 1; the complete list can be found in Suppl. material 1: SuppTable 1
and in Dentinger and McLaughlin (2006) for the Agaricomycetidae dataset.
Caio A. Leal-Dutra et al. / MycoKeys 37: 39–56 (2018)
44
e ITS1 and ITS2 datasets were aligned using MAFFT v7.311 (Katoh and Stand-
ley 2013) using the E-INS-i algorithm and the 5.8S and nrLSU datasets were aligned
using the L-INS-i algorithm in MAFFT. e alignments were examined and adjusted
manually using MEGA 7 (Kumar et al. 2016) and trimmed to remove uneven ends.
e best-t evolutionary models were estimated for each partition separately using
JMODELTEST v2.1.3 (Darriba et al. 2012; Guindon and Gascuel 2003) following
the Bayesian Information Criterion (BIC). Bayesian Inference (BI) under the best-t
models was implemented using MRBAYES v3.2 (Ronquist et al. 2012) with two inde-
pendent runs, each one with four chains and starting from random trees. Chains were
run for 107 generations with tree sampling every 1000 generations. e burn-in was set
to 25% and the remaining trees were used to calculate a 50% majority consensus tree
and Bayesian Posterior Probability (BPP). e convergence of the runs was assessed on
TRACER v1.7 (Rambaut et al. 2018) to ensure the potential scale reduction factors
(PSRF) neared 1.0 and the eective sample size values (ESS) were suciently large.
Maximum-likelihood analysis was performed with IQTREE v1.6.3.b (Nguyen et
al. 2015). e best-t evolutionary models for this analysis were estimated by the built-
in ModelFinder (option -m MF+MERGE) allowing the partitions to share the same
set of branch lengths but with their own evolution rate (-spp option) (Chernomor et
al. 2016; Kalyaanamoorthy et al. 2017). Branch support was assessed with 1000 repli-
cates of ultrafast bootstrapping (Hoang et al. 2018).
Nodes with BPP ≥0.95 and/or BS ≥75 were considered strongly supported.
Alignments and phylogenetic trees are deposited in Treebase (ID: 22642).
Results
Phylogenetic analysis
A total of 37 sequences were generated in this study (19 nrITS and 18 nrLSU). e nal
alignment consisted of 135 sequences with 2295 characters. e BI analysis converged
all runs as indicated by the eective sample sizes (ESS) of all parameters above 2000
and the potential scale reduction factors (PSRF) equal 1.000 for all the parameters. e
two Parapterulicium species were placed with strong support into /peniophorales sensu
Larsson and Larsson (2003) as shown in the Russulales tree (Fig. 1).
e clade /peniophorales recovered in the Russulales tree and the genera which it
comprises are consistent with the neighbour-joining analyses of Larsson and Larsson
(2003). However, the ML tree presented here shows better resolution of the sub-clades.
Five main clades highlighted in Fig. 1 are /lachnocladiaceae (previously /asterostro-
mataceae), Baltazaria, /varariaceae, /peniophoraceae and /metulodontia.
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)
Reclassication of Parapterulicium Corner (Pterulaceae, Agaricales)... 45
Figure 1. Maximum likelihood tree of Russulales on the left with /peniophorales amplied 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. mate-
rial 1: SuppFigs 2, 3.
Caio A. Leal-Dutra et al. / MycoKeys 37: 39–56 (2018)
46
Donk, Scytinostroma ochroleucum Donk, Scytinostroma odoratum (Fr.) Donk and Bal-
tazaria gen. nov. (BS=99; BPP=1).
Baltazaria (BS=92; BPP=1)
is clade represents the newly proposed genus (see below). It contains the sequences of
P. octopodites, S. eurasiaticogalactinum, S. neogalactinum and S. galactinum. e presence
of P. octopodites here rendered Parapterulicium paraphyletic necessitating reclassication.
Clade /varariaceae (BS=75; BPP=0.98)
is clade includes Parapterulicium subarbusculum, Dichostereum Pilát and Vararia P.
Karst. e inclusion of Parapterulicium sequences enhanced support for this clade,
which was also recovered by Binder et al. (2005). e monophyly of Dichostereum
typied by D. durum (Bourdot & Galzin) Pilát is strongly supported (BS=98; BPP=1).
However, Vararia was rendered paraphyletic and will require a more thorough investi-
gation to resolve its classication.
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). e reclassication 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 ailand (Osono etal. 2009). Parapteru-
licium spp. are not known outside of South America, but this suggests this species may be
more widespread in subtropical and tropical regions than presently acknowledged.
Clade /peniophoraceae. (BS=100; BPP=1)
e clade /peniophoraceae includes Peniophora, Duportella Pat., Dendrophora (Parmas-
to) Chamuris and Entomocorticium H.S. Whitney, Bandoni & Oberw. ese genera
require special attention for detailed morphological and molecular studies to resolve
the paraphyly of Peniophora, by either proposing new genera or synonymising Den-
drophora and Entomocorticium. In all analyses performed in this study, there was no
clear resolution for this group.
Clade /metulodontia (BS=95; BPP=1)
e clade contains Metulodontia Parmasto and Confertobasidium Jülich. Following Larsson
and Larsson (2003), this well supported clade was recovered in all analyses performed.
Taxonomy
Parapterulicium subarbusculum Corner, Ann. Bot., 16: 288 (1952)
Fig. 2
Description. Basidiomes coralloid/liform, up to 35 mm high, branched, erect, mon-
oaxial with adventitious branches, yellow (10YR 8/6), solitary or gregarious. Stipe up
Reclassication of Parapterulicium Corner (Pterulaceae, Agaricales)... 47
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 liform 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, elon-
gate, subfusiform, apex obtuse, base acute with small apiculus (0.3 µm), thin-walled
and slightly amyloid, scarce in all the collected samples.
Specimens examined. 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 desig-
nated here: RB 639457, RB 639458, RB 639462, RB 639463, FLOR 56456, FLOR
56457, FLOR 56458, FLOR 0056459).
Distribution. Brazil. Rio de Janeiro: Rio de Janeiro (Corner 1952a, Type)
Notes. is species is recognised in the eld by its characteristic resupinate disc at
the base of the stipe (Fig. 2b, c). Corner (1952a) described P. subarbusculum from a single
specimen collected in November 1948 on Corcovado in Rio de Janeiro and, based on its
coralloid habit and dimitic hyphal system, placed the genus in Pterulaceae. e presence
of gloeocystidia, slightly amyloid spores and dextrinoid dichophyses corroborates its place-
ment in Russulales. It appears to be relatively common, though apparently overlooked.
Baltazaria C.A. Leal-Dutra, Dentinger & G.W. Gri. gen. nov.
Mycobank No: MB825233
Etymology. In honour of Dr. Juliano Marcon Baltazar, Brazilian mycologist and au-
thority on neotropical corticioid fungi.
Type species. Baltazaria galactina (Fr.) C.A. Leal-Dutra, Dentinger & G.W. Gri.
Diagnosis. Basidiomes corticioid, adherent to eused, 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.
Notes. e diagnosis of Boidin and Lanquetin (1987) for Scytinostroma eurasiati-
cogalactinum and S. neogalactinum describes both species with the same morphological
characters as S. galactinum (Fr.) Donk but with reproductive incompatibility between the
Caio A. Leal-Dutra et al. / MycoKeys 37: 39–56 (2018)
48
Figure 2. Parapterulicium subarbusculum: a–c basidiomes in the eld. e detail in c shows the developing
corticioid patch d basidiospores e dichophyses f gloeocystidia g, h SEM images of dichophyses; i. SEM im-
ages of basidiome surface with abundant dichophyses. Scale bars: a–c = 1 cm; d–f, i = 10 µm; g, h=5 µm.
Reclassication of Parapterulicium Corner (Pterulaceae, Agaricales)... 49
species and dierent distributions. In the discussion on the S. galactinum complex, the
authors mention the branched skeletal hyphae that starts with conspicuous 2–3 branched
short projections and then become longer, a feature resembling the Parapterulicium octo-
podites papillate skeletal hyphae (Fig. 3d–h). Moreover, the description of S. galactinum
by Lentz and Burdsall (1973) mentions the hymenium with conspicuous skeletodendro-
hyphidia. However, Bernicchia and Gorjón (2010) claimed the species does not present
dendrohyphae; instead, the authors describe the presence of skeletal-binding hyphae. It
is likely that the papillate skeletal hyphae described by Corner (1952a), the short and
branched projections described by Boidin and Lanquetin (1987) and the skeletodendro-
hyphidia described by Lentz and Burdsall (1973), are nothing more than early develop-
mental stages of the skeletal-binding hyphae described by Bernicchia and Gorjón (2010).
Baltazaria galactina (Fr.) C.A. Leal-Dutra, Dentinger & G.W. Gri., comb. nov.
Mycobank No: MB825235
Basionym. elephora galactina Fr., Nova Acta R. Soc. Scient. upsal., Ser. 3 1(1): 136
(1851) [1855]. ≡ Corticium galactinum (Fr.) Moatt, Bulletin of the Nat. Hist. Surv.
Chicago Acad. Sci. 7(1): 137 (1909). ≡ Scytinostroma galactinum (Fr.) Donk, Fungus,
Wageningen 26: 20 (1956).
= elephora 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 Lentz and Burdsall (1973).
Baltazaria eurasiaticogalactina (Boidin & Lanq.) C.A. Leal-Dutra, Dentinger &
G.W. Gri., comb. nov.
Mycobank No: MB825236
Basionym. Scytinostroma eurasiaticogalactinum Boidin & Lanq., Biblthca Mycol. 114:
57 (1987)
Description in Boidin and Lanquetin (1987).
Baltazaria neogalactina (Boidin & Lanq.) C.A. Leal-Dutra, Dentinger & G.W.
Gri., comb. nov.
Mycobank No: MB825237
Basionym. Scytinostroma neogalactinum Boidin & Lanq., Biblthca Mycol. 114: 59 (1987).
Description in Boidin and Lanquetin (1987).
Caio A. Leal-Dutra et al. / MycoKeys 37: 39–56 (2018)
50
Baltazaria octopodites (Corner) C.A. Leal-Dutra, Dentinger & G.W. Gri.,
comb. nov.
Mycobank No: MB825234
Fig. 3
Basionym. Parapterulicium octopodites Corner, Ann. Bot., 16: 286 (1952)
Description. Basidiomes resupinate (Fig. 3b), 0.1–0.5 mm thick, membrana-
ceous, covering leaves and twigs, hymenophore smooth, white (2.5Y 8/2) to pale
yellow (2.5Y 8/4), forming rhizomorph-like structures up to 7 cm high and scarcely
to profusely branched that may be confused with coralloid basidiomes (Fig. 3a, b).
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). Ter-
mini of hymenial skeletal hyphae papillate, presenting short protuberances 2–10 ×
1.5–2.5 µm, sometimes ramied 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 mul-
tiguttulate or with abundant granular contents. Present in all parts of the basidiomes,
including the corticioid form.
Basidiospores and basidia not observed.
Specimens examined. 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. Flo-
res 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).
Distribution. 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).
Notes. e dimitic hyphal system, the papillate surface at the ends of the skeletal
hyphae and the gloeocystidia agree perfectly with Corner’s original descriptions (Cor-
ner 1952a). Corner (1952a) described this species from a collection where no fertile
structures were observed; the new collections were also sterile. As no spores or fertile
basidia were found, the term putative hymenium is given to the region with abundant
basidiole-like structures. Furthermore, the lack of sexual characters observed in B. octo-
podites, combined with the undeveloped binding-skeletal hyphae, might indicate that
this species is only known by young basidiomes or non-reproductive growth forms
(i.e. explorative rhizomorphs). is is the rst record of B. octopodites from the States
of Amazonas, Paraná, Santa Catarina and São Paulo.
Reclassication of Parapterulicium Corner (Pterulaceae, Agaricales)... 51
Figure 3. Baltazaria octopodites: a, b basidiomes in the eld (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 inated in KOH (third from the right) and
generative hyphae (rst and second from the right) e–h SEM images of papillate skeletal hyphae. Scale
bars: a–b = 1 cm; c–d = 10 µm; e–h = 1 µm).
Caio A. Leal-Dutra et al. / MycoKeys 37: 39–56 (2018)
52
Discussion
e /lachnocladiaceae clade was named /asterostromataceae by Larsson and Larsson
(2003), who also proposed a deeper molecular study involving Lachnocladium to nd
the exact placement of the genus. In this study, Lachnocladium spp., typied by L.
brasiliense (Lév.) Pat., formed a strongly supported (BS=99; BPP=1) clade with the
previously called /asterostromataceae, which includes Scytinostroma, Vesiculomyces,
Gloiothele, Asterostroma, Vararia ocholeuca, Scytinostroma ochroleucum, Scytinostroma
odoratum and the new genus Baltazaria. us, we decided to name the clade /lach-
nocladiaceae to suggest the need for a thorough study on the morphology of these
genera to re-circumscribe Lachnocladiaceae. Binder et al. (2005) recovered this clade
but did not include Lachnocladium. Scytinostroma, typied by S. portentosum (Berk.
& M.A. Curtis) Donk, forms a clade with robust support with S. caudisporum Boi-
din, Lanq. & Gilles and S. alutum Lanq. (BS=99; BPP=1), meaning the other species
of Scytinostroma sampled in this study (S. ochroleucum, S. odoratum, S. eurasiaticoga-
lactinum) require reclassication. Monophyly of Asterostroma and Gloiothele is also
strongly supported (BS=100; BPP=1), including the type species A. apalum (Berk. &
Broome) Massee (= A. muscicola) and Gloiothele lamellosa (Henn.) Bres., respectively.
Future studies of Lachnocladiaceae may recommend Baltazaria be classied 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.
e 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 (Lentz and Burdsall 1973). Another
notable characteristic of this species is the hyphal swelling seen in KOH, which is also
found in some species of Peniophora Cooke, Dichostereum and Vararia (Stalpers 1996;
Stalpers and Buchanan 1991). In addition, the multigutullate gloeocystidia present
in P. subarbusculum and B. octopodites might have the same origin as those in Russula
Pers. and Auriscalpium Gray, which were shown by McLaughlin et al. (2008) to be a
likely synapomorphy of Russulales. Taken together, alongside the molecular evidence
presented in this study, these corroborating morphological features add strong support
to the reclassication of these fungi and suggest that aforementioned hyphal features
may be unifying characters for /peniophorales.
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 (Corner 1950, McLaughlin
and McLaughlin 1972), the function of the liform projections, believed to be coral-
loid basidiomes, may not be for sexual reproduction. Instead, they may function as
exploratory appendages, similar to mycelial cords and rhizomorphs in other fungi (e.g.
Crinipellis Pat./Marasmius Fr., Armillaria (Fr.) Staude etc.) or as a strategy for binding
substrate materials together (Cairney 1991; Hedger et al. 1993; Snaddon et al. 2011).
is characteristic, combined with the fact that no spores have been reported, raises
the possibility that an independent sexual form, similar to the resupinate basidiomes of
Reclassication of Parapterulicium Corner (Pterulaceae, Agaricales)... 53
Scytinostroma, may exist. Considering these assumptions, B. octopodites might be more
common than previously thought, since it is probably overlooked during eldwork,
mistakenly identied as a rhizomorph.
A third species of Parapterulicium, P. simplex, is still known only from type mate-
rial originally collected in Argentina (Corner 1957). It would be prudent to include
this species in a full revision of the genus, which would require targeted eldwork at
the type locality. We anticipate that, despite the rarity of their documentation, these
liform fungi are abundant and widespread.
Acknowledgements
CALD scholarship was provided by CAPES Foundation - Brazil, BEX 2145/15-4.
Funding was provided in part from a Systematics and Taxonomy (SynTax) grant (BB-
SRC, 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. is is publication 743 of the BDFFP - INPA/
STRI Technical Series (eld 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. e Institute of
Biological, Environmental, and Rural Sciences receives strategic funding from the BB-
SRC. We thank Felipe Ruppenthal for the line drawings.
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Supplementary material 1
Species used in the Russulales analyses and their GenBank accession numbers of
nrITS and nrLSU sequences
Authors: Caio A. Leal-Dutra, Maria Alice Neves, Gareth W. Grith, Mateus A. Reck,
Lina A. Clasen, Bryn T. M. Dentinger
Data type: species data
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/mycokeys.37.26303.suppl1
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