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Blum versus Romagnesi: testing possible synonymies of some European russulas (Russulaceae, Basidiomycota)

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  • Institute of Botany, Plant Science and Biodiversity Centre, Slovak Academy of Sciences

Abstract and Figures

Among 45 Russula species and infraspecific taxa described by J. Blum, only few are currently accepted. Here we present a case study on R. formosa nom. illeg. (homotypic synonym of R. blumiana), R. decipiens var. ochrospora nom. inval. and R. roseobrunnea. The study is based on sequences and morphological observations of authentic herbarium material determined by J. Blum. The sequence data demonstrate that R. decipiens var. ochrospora is probably identical with the type variety and R. roseobrunnea is probably conspecific with R. rutila. Russula blumiana is recognised and described in detail as a good species related to R. badia.
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1 23
Plant Systematics and Evolution
ISSN 0378-2697
Plant Syst Evol
DOI 10.1007/s00606-018-1506-3
Blum versus Romagnesi: testing possible
synonymies of some European russulas
(Russulaceae, Basidiomycota)
Miroslav Caboň, Soňa Jančovičová, Jean
M.Trendel, Pierre-Arthur Moreau, Felix
Hampe, Miroslav Kolařík, Annemieke
Verbeken, et al.
1 23
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Vol.:(0123456789)
1 3
Plant Systematics and Evolution
https://doi.org/10.1007/s00606-018-1506-3
ORIGINAL ARTICLE
Blum versusRomagnesi: testing possible synonymies ofsome
European russulas (Russulaceae, Basidiomycota)
MiroslavCaboň1 · SoňaJančovičová2· JeanM.Trendel3· Pierre‑ArthurMoreau4 · FelixHampe5·
MiroslavKolařík6 · AnnemiekeVerbeken5 · SlavomírAdamčík1
Received: 2 August 2017 / Accepted: 5 March 2018
© Springer-Verlag GmbH Austria, part of Springer Nature 2018
Abstract
Among 45 Russula species and infraspecific taxa described by J. Blum, only few are currently accepted. Here we present a
case study on R. formosa nom. illeg. (homotypic synonym of R. blumiana), R. decipiens var. ochrospora nom. inval. and R.
roseobrunnea. The study is based on sequences and morphological observations of authentic herbarium material determined
by J. Blum. The sequence data demonstrate that R. decipiens var. ochrospora is probably identical with the type variety and
R. roseobrunnea is probably conspecific with R. rutila. Russula blumiana is recognised and described in detail as a good
species related to R. badia.
Keywords Multi-locus phylogeny· Russula blumiana· Russula decipiens var. ochrospora· Russula roseobrunnea· Type
studies
Introduction
Jean Blum was a French mycologist who published 101 new
names of agarics and bolets, among them 45 species and
infraspecific names in the genus Russula Pers. published
between 1951 and 1968 (http://www.mycob ank.org). A
large part of his Russula names (29) are invalid, mainly
because he did not provide Latin diagnosis (Bon 1986)
(Table1). His work on Russula resulted in the monographic
publication “Les Russules” (Blum 1962), but its influence
and use were subdued by the raise of a more comprehen-
sive and innovative monograph “Les Russules d’Europe
et d’Afrique du Nord” by Henri Romagnesi (1967). There
is a parallel in the mycological careers of the two French
mycologists. A substantial part of Romagnesi’s publica-
tions is also about the genus Russula, and among 524 of his
validly published names of species and infraspecific taxa
Handling editor: Wilhelm de Beer.
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s0060 6-018-1506-3) contains
supplementary material, which is available to authorized users.
* Miroslav Caboň
miroslav.cabon@savba.sk
Soňa Jančovičová
jancovicova@fns.uniba.sk
Pierre-Arthur Moreau
pierre-arthur.moreau@univ-lille2.fr
Felix Hampe
felix.hampe@email.de
Miroslav Kolařík
miroslavkolarik@seznam.cz
Annemieke Verbeken
mieke.verbeken@UGent.be
Slavomír Adamčík
slavomir.adamcik@savba.sk
1 Plant Science andBiodiversity Centre SAS, Institute
ofBotany, Dúbravská cesta 9, 84523Bratislava, SA,
Slovakia
2 Department ofBotany, Faculty ofNatural Sciences,
Comenius University inBratislava, Révová 39,
81102Bratislava, Slovakia
3 Haguenau, France
4 Faculte des Sciences Pharmaceutiques et Biologiques,
Laboratoire IMPECS, Université de Lille, 59000Lille,
France
5 Ghent University, K.L. Ledeganckstraat 35, 9000Ghent,
Belgium
6 Institute ofMicrobiology, Czech Academy ofSciences,
Vídeňská 1083, 14220Prague4, CzechRepublic
Author's personal copy
M. Caboň etal.
1 3
of agarics and bolets, are 78 of Russula published between
1937 and 1997 (http://www.mycob ank.org). It was Romag-
nesi’s influential monograph (Romagnesi 1967) that had a
negative impact on accepting of Blum’s russulas in the cur-
rent literature. Among 43 of Blum’s species and lower-rank
names already described at that time, Romagnesi (1967)
Table 1 List of all species and infraspecific Russula names described by J. Blum arranged chronologically
BSMF Bulletin trimestriel de la Société mycologique de France, L Latin diagnosis in the protologue, T type specimen designated in the proto-
logue
Blum’s names Status Validations
R. fuscorubra var. olivovirens J.Blum, BSMF 67: 166. 1951 Valid (L)
R. amoena var. intermedia J.Blum, BSMF 68: 255. 1952 Invalid
R. caeruleomalva J.Blum, BSMF 68: 238. 1952 Valid (L)
R. grisea var. leucospora J.Blum, BSMF 68: 257. 1952 Invalid R. leucospora Bon, Cryptog. Mycol. 7: 301. 1986
R. lilacinicolor J.Blum, BSMF 68: 253. 1952 Valid (L)
R. maculata var. globispora J.Blum, BSMF 68: 232. 1952 Valid (L)
R. roseicolor J.Blum, BSMF 68: 224. 1952 Valid (L)
R. adulterina f. frondosae J.Blum, BSMF 69: 70. 1953 Invalid R. frondosae Reumaux, Russules rares ou méconnues: 284. 1996
R. formosa J.Blum, BSMF 69: 60. 1953 Illeg. (L) R. blumiana Bon, Cryptog. Mycol. 7: 299. 1986
R. roseobrunnea J.Blum, BSMF 69: 64. 1953 Valid (L)
R. carminipes J.Blum, BSMF 69: 449. 1953 Valid (L)
R. cupreoviolacea J.Blum, BSMF 69: 440. 1953 Valid (L)
R. lepida subsp. flavescens J.Blum, BSMF 69: 435.1953 Invalid
R. pseudolilacea J.Blum, BSMF 69: 434. 1953 Valid (L)
R. pseudorosea J.Blum, BSMF 69: 436. 1953 Valid (L)
R. robertii J.Blum, BSMF 69: 443. 1953 Valid (L)
R. variecolor J.Blum, BSMF 69: 445. 1953 Illeg. (L) R. blumii Bon, Cryptog. Mycol. 7: 309. 1986
R. xerampelina var. abietum J.Blum, BSMF 69: 429. 1953 Valid (L)
R. fulva J.Blum, BSMF 70: 406. 1955 Invalid R. mustelina var. fulva Bon, Cryptog. Mycol. 7: 299. 1986
R. fuscorosea J.Blum, BSMF 70: 406. 1955 Invalid R. fuscorosea Bon, Cryptog. Mycol. 7: 300. 1986
R. integra f. fulvidula J.Blum, BSMF 70: 394. 1955 Invalid
R. pseudoromellii J.Blum, BSMF 70: 399. 1955 Invalid R. pseudoromellii Bon, Cryptog. Mycol. 7: 305. 1986
R. subintegra J.Blum, BSMF 70: 395. 1955 Invalid R. subintegra Bon, Cryptog. Mycol. 7: 307. 1986
R. tinctipes J.Blum, BSMF 70: 401. 1955 Invalid R. tinctipes Bon, Cryptog. Mycol. 7: 308. 1986
R. crawshayriana J.Blum, BSMF 72:152. 1956 Invalid R. joannis Bon, Cryptog. Mycol. 7: 297. 1986
R. luteotacta var. semitalis J.Blum, BSMF 72: 143. 1956 Invalid R. luteotacta var. semitalis Bon, Cryptog. Mycol. 7: 303. 1986
R. luteotacta var. serrulata J.Blum, BSMF 72: 142. 1956 Invalid
R. persicina var. montana J.Blum, BSMF 73:268. 1957 Invalid
R. pyrenaica J.Blum, BSMF 73: 257. 1957 Invalid R. pyrenaica Singer, Collect. Bot. (Barcelona) 13: 687. 1982
R. speciosa J.Blum, BSMF 73: 264. 1957 Invalid R. speciosa Bon, Cryptog. Mycol. 7: 307. 1986
R. flavocitrina J.Blum, BSMF 76: 267. 1960 Invalid R. flavocitrina Bon, Cryptog. Mycol. 7: 298. 1986
R. multicolor J.Blum, BSMF 76: 266. 1960 Invalid R. multicolor Bon, Cryptog. Mycol. 7: 304. 1986
R. vesca f. montana J.Blum, BSMF 76: 253. 1960 Invalid
R. xerampelina var. ochracea J.Blum, BSMF 77: 162. 1961 Invalid
R. decipiens var. ochrospora J.Blum, Les Russules: 175. 1962 Invalid
R. brunneoviolacea var. cristatispora J.Blum, Les Russules: 94. 1962 Invalid R. brunneoviolacea var. cristatispora Bon, Cryptog. Mycol. 7: 297. 1986
R. delica var. glutinosa J.Blum, Les Russules: 207. 1962 Invalid R. chloroides var. glutinosa Bon, Cryptog. Mycol. 7: 300. 1986
R. maximispora J.Blum, Les Russules: 113. 1962 Invalid R. maximispora Bon, Cryptog. Mycol. 7: 303. 1986
R. pseudodelica var. flavispora J.Blum, Les Russules: 208. 1962 Invalid R. flavispora Romagn., Russules d’Europe Afr. Nord: 233. 1967
R. pseudodelica var. pallidospora J.Blum, Les Russules: 208. 1962 Invalid R. pallidospora Romagn. Russules d’Europe Afr. Nord: 233. 1967
R. pseudomelitodes J.Blum, Les Russules: 132. 1962 Invalid R. pseudomelitodes Bon, Cryptog. Mycol. 7: 305. 1986
R. sabulosa Heim & J.Blum,, Les Russules: 204. 1962 Invalid R. adusta var. sabulosa Bon, Cryptog. Mycol. 7: 306. 1986
R. werneri var. europae J.Blum, Les Russules: 128. 1962 Invalid R. europae Romagn., Russules d’Europe Afr. Nord: 834. 1967
R. delicatoides J.Blum, Rev. Mycol. (Paris) 33 (1): 113. 1968 Valid (L, T)
R. straminea var. battouenii J.Blum, Rev. Mycol. (Paris) 33 (1): 111.
1968
Valid (L, T)
Author's personal copy
Blum versus Romagnesi: checking possible Russula synonymies
1 3
adopted, re-described and accepted only few without any
hesitation: R. carminipes J.Blum, R. pseudoromellii J.Blum
ex Bon, R. tinctipes J.Blum ex Bon, R. pallidospora J.Blum
ex Romagn. and R. flavispora J.Blum ex Romagn. In most
cases, Romagnesi was not aware of the invalid or illegitimate
status of Blum’s names, and he was probably rather unable
to assign Blum’s names to particular species he recognised.
Bon (1986) validated 15 of Blum’s names and proposed
three more species names that replace Blum’s illegitimate
names. He provided all validly published names with Latin
diagnoses, type designations and his microscopic obser-
vations on Blum’s authentic collections (from which he
selected the types). The validation of Blum’s Russula names
has only little impact on their treatment in the current lit-
erature, e.g. Sarnari (1998, 2005) and Marxmüller (2014)
accepted only R. blumiana Bon, R. pseudomelitodes J.Blum
ex Bon and R. pseudoromellii among russulas re-described
by Bon. The majority of Blum’s Russula names are currently
treated as ambiguous or unknown. In this study, we seek
to check possible synonymies of Blum’s names with other
widely used Russula names based on a case study on three
taxa described by Blum: R. formosa J.Blum nom. illeg. (Art.
53,McNeill etal. 2012; homotypic synonym of R. blumi-
ana), R. decipiens var. ochrospora J.Blum nom. inval. (Art.
39 of the Code; missing Latin diagnosis) and R. roseobrun-
nea J.Blum.
All three studied taxa are defined by acrid taste, yellow
spore prints and red pilei, and wereplaced by Blum in one
“Section O” (Blum 1962), but their concept and nomencla-
ture were treated variably in the literature. None of these
names is applied for a common and widely accepted spe-
cies and was not recognised as a good species in any ofthe
important Russula monographs (Romagnesi 1967; Sarnari
1998). The most frequently accepted and described is R.
blumiana (Bon 1986; Reumaux etal. 1996; Sarnari 2001;
Tassi 2003; Marxmüller 2014), but Bon (1988), contrary to
all other authors, observed incrustations on pileocystidia,
which allow different opinions about its relationships and
classification. Russula roseobrunnea was validly published
by Blum (1953) and soon was considered to be a synonym
of R. pseudoemetica Singer (Singer 1962). The latter is cur-
rently treated as another species with dubious concept and
affinity to R. vinosopurpurea Jul.Schäff. (Romagnesi 1967;
Sarnari 1998). This opinion was adopted by themajority of
authors, except for Bon (1979, 1988) who described it as
a good species similar to R. blumiana. Russula decipiens
var. ochrospora, nom. inval. is an abandoned name that is
even not listed in the nomenclatural databases (http://www.
mycob ank.org, http://www.index fungo rum.org, http://
www2.muse.it/russu lales -news). Romagnesi (1967) reported
and described his personal collection that was similar to
the Blum’s description, but he was not certain about its
placement, status and relationships. Reumaux etal. (1996)
presented the only later description and record of Blum’s
variety, but they attributed it the species rank and proposed
a new name Russula ochrosperma Moënne-Locc. with a new
type (collected by these authors, not by J. Blum).
Materials andmethods
Sampling
This study is based on specimens from Blum’s herbarium
deposited in PC representing the authentic material of three
selected taxa: R. formosa nom. illeg., R. decipiens var.
ochrospora nom. inval. and R. roseobrunnea. Only for R.
blumiana, the type specimen designated by Bon (1986) was
studied. To identify phylogenetic relationships of sequences
retrieved from Blum’s material, we used sampling froma
previous study (Caboň etal. 2017) and sequences with 97%
similarity and higher retrieved by BLAST search from Gen-
Bank (https ://www.ncbi.nlm.nih.gov/genba nk) and UNITE
(Kõljalg etal. 2013) databases and our dataset. To assess
phylogenetic placement of the studied species in the higher-
rank taxa of the genus Russula, the final dataset was supple-
mented by sequences of the Crown clade, the phylogenetic
group defined by Looney etal. (2016) retrieved from Caboň
etal. (2017). Three samples of R. subgenus Russula were
used as the outgroup. All specimens and sequences are listed
in Supplementary Tab. 1. Herbarium material collected by
the authors is deposited in the herbaria: SAV and LIP.
Molecular analysis
Total genomic DNA was extracted from dried material using
the methods previously described by Adamčík etal. (2016).
Three molecular markers were amplified: (1) the internal
transcribed spacer regions of the ribosomal DNA (ITS),
(2) partial mitochondrial small subunit ribosomal DNA
(mtSSU), (3) the region between domains six and seven
of the nuclear gene encoding the second largest subunit of
RNA polymerase II (rpb2). The ITS region was amplified
using the primers ITS1F—ITS4 or alternatively ITS1F—
ITS2 and ITS3—ITS4 (White etal. 1990; Gardes and Bruns
1993). The mtSSU region was amplified using the primer
pair MS1—MS2 (White etal. 1990). Both molecular mark-
ers were amplified with polymerase PerfectTAQ (5 PRIME,
Hilden, Germany) or Hot Start Firepol Polymerase (Solis
BioDyne, Tartu, Estonia) in accordance with the manufac-
turer’s recommendation using the same cycling protocol
followed of Eberhardt (2012) or Knebelsberger and Stöger
(2012) with longer denaturation and annealing times of up to
1min instead of 30s. For the amplification of rpb2, we used
a forward primer A-Russ-F (Caboň etal. 2017) and a reverse
primer frpb2-7CR (Matheny 2005). The rpb2 was amplified
Author's personal copy
M. Caboň etal.
1 3
with Hot Start Firepol Polymerase, following cycling proto-
col of Caboň etal. (2017).
The PCR products were purified using the QIAquick
PCR Purification Kit (Qiagen, Hilden, Germany) or Exo-
Sap enzymes (Thermo Fisher Scientific, Wilmington, Dela-
ware, USA). Samples were sequenced directly with BigDye
3.1 technology (Applied Biosystems, now Thermo Fisher
Scientific, Wilmington, USA), sent to Macrogen Europe
(Amsterdam, the Netherlands) or to SEQme (Dobříš, Czech
Republic), respectively.
Raw sequences were edited in the BioEdit Sequence
Alignment Editor version 7.2.5 (Hall 2013), Geneious ver-
sion R10 (Kearse etal. 2012) or Sequencher version 4.8
(Gene Codes Corporation, Ann Arbor, USA). Intraindividual
polymorphic sites having more than one signal were marked
with NC-IUPAC ambiguity codes.
Phylogenetic analysis
Final datasets were aligned by MAFFT version 7 using the
strategy E-INS-i (Katoh and Standley 2013) and manually
improved in Geneious version R10 (Kearse etal. 2012). All
three single-locus datasets were concatenated into one data-
set using SeaView version 4.5.1 (Gouy etal. 2010). The con-
catenated final alignment has been deposited in TreeBASE
(21097). The multi-locus dataset was analysed using two
different methods: Bayesian inference (BI) and the maxi-
mum likelihood method (ML). Maximum likelihood was
computed in PhyML using SeaView (Gouy etal. 2010) using
GTR + GAMMA substitution model with six rate classes and
1000 bootstrap replications. For BI, the dataset was divided
into six partitions: ITS, mtSSU, intronic region 7 of rpb2,
and the 1st, 2nd and 3rd codon positions of rpb2. The best
substitution model for each partition was computed jointly
in MEGA version 6 (Tamura etal. 2013). The BI was com-
puted independently twice in MrBayes version 3.2.6 (Ron-
quist etal. 2012) with four MCMC chains for 10,000,000
iterations until the standard deviation of split frequencies
reached below the 0.01 threshold. The convergence of runs
was visually assessed using Trace function in Tracer version
1.6 (Rambaut etal. 2013).
Morphological observations
Micromorphological characteristics were observed using
Olympus CX-41 with oil-immersion lens at a magnification
of 1000×. All drawings of microscopic structures, with the
exception of spores, were made with a “camera lucida” using
an Olympus U-DA drawing attachment at a projection scale
of 2000×. The contents of hymenial cystidia and pileocyst-
idia were illustrated as observed in Congo red preparations
from dried material, with the exception of some pileocyst-
idia for which the contents are indicated schematically (by
plus signs). Spores were observed on the lamellae with
Melzer’s reagent. All other microscopic observations were
made in ammoniacal Congo red, after a short treatment in
warm, aqueous KOH solution to dissolve the gelatinous
matrix and improve tissue dissociation. All tissues were also
examined in Cresyl blue to verify the presence of ortho-
or metachromatic reactions as explained in Buyck (1989).
Trama and cystidia were examined in a sulfovanillin solu-
tion. Acidoresistant incrustations of the primordial hyphae
were stained with carbolfuchsin and observed in distilled
water after incubation for a few seconds in a 10% solution
of HCl (cf. Romagnesi 1967). Spores were scanned with
an ART RAY Artcam 300MI camera and measured by the
Quick Micro Photo version 2.1 software with an accuracy
of 0.1μm. Spore measurements excluded ornamentation,
and their line drawings were made using enlarged, scanned
pictures. The Q value indicates the length/width ratio of the
spores. The spore ornamentation density was estimated fol-
lowing Adamčík and Marhold (2000). The cystidia density
estimates follow Buyck (1991). Statistics for the measure-
ments of microscopic characteristics were based on 30 meas-
urements per specimen and are based on all examined mate-
rials of the described species. The range of measured values
is expressed as mean ± standard deviation; in the parenthesis
are 5 and 95 percentiles.
Results
Three specimens from Blum’s herbarium representing the
authentic material of R. formosa (PC0084516, J. Blum
1617), R. decipiens var. ochrospora (PC0084509, J. Blum
1933) and R. roseobrunnea (PC0084512, J. Blum 1395)
were successfully sequenced. The final dataset was com-
posed of 18 specimens with a high sequence similarity to
these three samples, 41 samples of 38 different species of
the Crown clade and three of the outgroup. In summary, 62
specimens were included in the analysis. Of these speci-
mens, majority (38) encompassed three genetic markers, 18
encompassed two markers, and only six had one marker (five
with only ITS and one with mtSSU). The final topologies
of the ML and BI analyses show generally similar results
as in our previous study (Caboň etal. 2017): they were not
congruent and there were few clusters with a good support
across the backbone of the Crown clade (Fig.1).
We confirmed moderate statistical support for the Inte-
grae clade (70/1), which contain two of Blum’s specimens:
R. formosa and R. roseobrunnea. Blum’s specimen of R. for-
mosa is clustered with another four specimens of R. blumi-
ana from France and an unidentified specimen from USA in
strongly supported (95/1) clade, nested in newly recognised
and strongly supported (99/1) Badia clade. Blum’s specimen
identified as R. roseobrunnea is placed in the species clade
Author's personal copy
Blum versus Romagnesi: checking possible Russula synonymies
1 3
Fig. 1 Maximum likelihood phylogeny inferred from three loci (ITS,
mtSSU and rpb2) with three target species-level clades highlighted.
Supported superclades comprising the target species are indicated
by arrows. Basidiomata samples are labelled by herbarium code, and
collections number in parenthesis, sequences of environmental sam-
ples are labelled with GenBank accession numbers in italics. Coun-
tries of origin are provided for the target speciesif available. Boot-
strap values followed by Bayesian posterior probabilities are indicated
above nodes
Author's personal copy
M. Caboň etal.
1 3
of R. rutila Romagn. in the Rubrinae clade. Blum’s speci-
men identified as R. decipiens var. ochrospora is clustered
in the strongly supported (97/1) clade together with other
specimens identified as typical variety of the species (includ-
ing the type specimen). The species clade of R. decipiens
(Singer) Svrček shows arelatively isolated position out of
the Integrae clade.
Discussion
Two ofBlums names are probable synonyms
Two sequenced collections from Blum’s herbarium suggest
that two studied collections are probably conspecific with
another currently accepted species. The collection of R.
roseobrunnea is conspecific with the current concept of R.
rutila (Caboň etal. 2017), and the collection of R. decipiens
var. ochrospora is identical with the type of the typical vari-
ety of R. decipiens (Fig.1). Our results are against opinions
of mycologists who dealt with these names ofBlum.
Blum (1962) recognised and described R. rutila and R.
roseobrunnea as two separate species. Singer (1962) treated
R. roseobrunnea as synonym of R. pseudoemetica, a spe-
cies related to or identical with R. vinosopurpurea, but the
latter species has multi-septate pileocystidia (Adamčík and
Jančovičová 2013) contrary to pileocystidia of R. roseob-
runnea described as “vaguement septées en général” in the
protologue (Blum 1953). Our morphological observation
on the Blum’s specimen of R. roseobrunnea confirmed the
presence of incrustations typical for R. rutila (Caboň etal.
2017), but this is contrary to Bon’s interpretation (Bon 1988)
who recognised Blum’s species from R. rutila based on the
absence of the incrustations.
In our knowledge, R. decipiens var. ochrospora was only
accepted and re-described by Reumaux etal. (1996) as a
new species, R. ochrosperma. The new species is typified by
material collected by authors of the name, and the pileocyst-
idia are described as having 0–1 septum. Our morphological
revision of the Blum’s studied specimen did not confirm the
presence of septa on pileocystidia, and this is in agreement
with the type study of R. decipiens var. decipiens (Adamčík
and Jančovičová 2012) that shows exclusively not septate
(one-celled) pileocystidia. In our opinion, R. ochrosperma
inthe sense of Reumaux etal. (1996) represents a species
different from R. decipiens.
Circumscription ofRussula blumiana
This study does not demonstrate synonymy coincidence of
R. formosa J.Blum = R. blumiana with any other name. We
did not sequence successfully the type specimen of R. blu-
miana designated by Bon (1986), but we got the sequence
from another Blum’s specimen (J. Blum 1617, PC0084516)
as well as our recent collection (LIP PAM 97090701) origi-
nated from the same site as the type collection (Rambouillet,
Etang d’Or, 40km from Paris). The morphology of the type
collection agrees well with our recent collection from the
type locality and other sequenced material, too. The output
of this study confirms theimportance of material from type
collecting areas for the interpretation of concept of poorly
known species (Holec etal. 2017). We did not confirm the
presence of the incrustations on the pileocystidia reported
by Bon (1986) in his type study, and such incrustations are
absent also in descriptions by Sarnari (2001, 2005), Tassi
(2003) and Marxmüller (2014).
Russula blumiana belongs to the strongly supported
Badia clade together with R. badia Quél. and R. quercilicis
Sarnari. These three species are traditionally classified in
two morphologically defined groups based on the presence
of incrustations on pileocystidia: R. quercilicis with incrus-
tations in R. subsect. Rubrinae (Melzer & Zvára) Singer
and other two species without incrustations in R. subsect.
Urentes Maire (Sarnari 1998, 2005). The Badia clade is
another example of disagreement between traditional mor-
phological concepts and lineages recognised by phylogenetic
studies (Adamčík etal. 2016; Caboň etal. 2017). All three
species of Badia clade are characterised by acrid taste, yel-
low spore print and contents of pileocystidia turning grey to
black in sulfovanillin. However, this combination of charac-
ters is present in several other unrelated groups of the Crown
clade. The Badia clade differs from the Rubrinae clade by
the absence of pink incrustation on pileocystidia in sulfo-
vanillin (Caboň etal. 2017) and from the Maculatinae clade
by the absence of yellow-brownish spots on the surfaces
of basidiomata. Russula decipiens differs by exclusively
one-celled pileocystidia (Adamčík and Jančovičo2012).
Russula intermedia P. Karst. has smaller (up to 8μm long)
spores (Ruotsalainen and Vauras 1994) and R. adulterina
Fr. larger (longer than 10μm) spores (Sarnari 1998). Rus-
sula cuprea Krombh., R. vinosopurpurea, R. gigasperma
Romagn., R cupreola Sarnari, R. cupreoaffinis Sarnari and
R. aurantioflammans Ruots., Sarnari & Vauras have all more
densely septate (with often more than 2 cells) pileocystidia
with frequent diverticules (Sarnari 1998).
Our observations suggest that a possible combination of
characters distinguishing the Badia clade from other mem-
bers of Maculatinae sensu lato might be relatively dense
spore ornamentation (6–10 elements in the 3-μm circle
on the spore surface) and one- to two-celled pileocystidia
(0–1-septate). Russula blumiana differs from R. badia by
very flexuous and usually apically obtuse hyphal termina-
tions in pileipellis near the pileus margin and from R. querci-
licis by narrower and not incrusted pileocystidia. Asequence
ofa North American (USA) origin very similar to European
Author's personal copy
Blum versus Romagnesi: checking possible Russula synonymies
1 3
collections of R. blumiana possibly represents a closely
related species (Fig.1).
Conclusions
Our study suggests that some taxa described by J. Blum
are possible synonyms of other widely used Russula names.
Among three studied taxa, only R. blumiana is confirmed to
be a good species. This study also suggests a high probabil-
ity to obtain sequences of ribosomal DNA from authentic
material collected by J. Blum that may help to interpret the
concept of his taxa. Specimens determined by J. Blum are
available in his herbarium (http://cobay e.mnhn.fr/insti tutio
n/mnhn/colle ction /pc/).
Taxonomic treatment
Russula blumiana Bon, Cryptog. Mycol. 7(4): 299.
1986. ≡ Russula formosa J.Blum, Bull. Soc. Mycol. France
69: 60. 1953, nom.illeg. (Art. 53: later homonym of R. for-
mosa Kučera)—HOLOTYPE: France: Rambouillet, Étang
d’Ór, s.d., s.col., J. Blum 6529 (PC).
Description: Field aspect (Fig.2). Basidiomata of inter-
mediate size. Pileus 5–7cm in diam., relatively fleshy, at
first hemispherical, then plano-convex, when mature with
broad, but not very deep central depression, margin usu-
ally deflexed, sometimes when old also inflexed, not or only
shortly striated; cuticle relatively matt, slightly rugulose,
at first lemon-yellow, soon developing to bright-yellow
and orange, finally brick-red, often near the margin darker
(orange or bright red), then with a paler zone near the cen-
tre or between the margin and the centre, often variegated
with darker small dots or bumps on the paler background.
Stipe 3–4.5 × 1–1.3(–1.8)cm, cylindrical, often wider near
the lamellae, with obtuse base, surface more or less longi-
tudinally striated, white, hardly changing colour but some-
times with a pink to red shade or a pink flush. Lamellae
moderately distant, slightly ventricose, up to 7mm wide,
towards the cap margin obtuse, adnate-emarginated, cream
to pale yellow, edges sometimes red near the pileus margin.
Context firm, odour indistinct, taste acrid, reaction to guaiac
negative. Spore print yellow, IVa according to the scale of
Romagnesi (1967).
Microscopic characters (Figs.3, 4). Spores broadly
ellipsoid, (7.6–)8.3–8.8–9.3(–9.9) × (6.2–)6.8–7.2–7.6
(–8.3) μm, Q = (1.11–)1.19–1.22–1.25(–1.34);
Fig. 2 Field appearance of Russula blumiana. ab JMT 14072513 (SAV), photograph by J.M. Trendel. cd PAM 97090701 (LIP), photograph
by P.-A. Moreau
Author's personal copy
M. Caboň etal.
1 3
ornamentation composed of small, dense [(5–)6–9(–10)
spines in a 3-μm diam. circle] amyloid spines, 0.5–0.8(–1)
μm high; connected with occasional, fine, short line con-
nections [0–2(–3) in the circle], often fused in pairs or short
chains (1–6 fusions in the circle), isolated spines frequent;
suprahilar plage amyloid, large. Basidia (33–)40.2–46.5
52.8(–59) × (10–)10.6–11.6–12.5(–14.5) μm, 4-spored,
clavate, pedicellate; basidioles first cylindrical or ellipsoid,
then clavate, ca. 5–10µm wide (some equally wide as basidia,
but shorter). Subhymenium pseudoparenchymatic. Lamellar
trama mainly composed of large sphaerocytes. Pleurocys-
tidia dispersed, ca. 500–900/mm2, measuring (74–)83.7–
100.8–117.9(–145) × (9.5–)10.5–11.7–12.9(–17) μm, clavate
or fusiform, pedicellate, apically mainly acute, mucronate
and with 3–13(−20)-µm-long appendage, thin-walled, with
heteromorphous (mainly granular or crystalline) contents,
slowly turn grey in sulfovanillin. Cheilocystidia clavate,
measuring (45–)61.9–73.2–84.5(–101) × (7–)9–10.4
11.8(–14) µm, with obtuse or acute tips, usually without an
appendage, with heteromorphous (granular or sometimes
also banded) contents. Marginal cells in shape similar to
basidioles but smaller and narrower, narrowly clavate to sub-
cylindrical, measuring (8–)15.9–20.9–25.8(–31) × (3–)3.6–
4.3–5.1(–7) µm, apically obtuse. Pileipellis orthochromatic
in Cresyl blue, not sharply delimited from the underlying
sphaerocytes of the context, strongly gelatinised through-
out, 120–190μm deep; vaguely divided into 50–90-μm-deep
suprapellis of slender, intricate, ascending and up to
5-μm-wide hyphae; and ca. 70–110-μm-deep subpellis of
mainly parallel, filamentous but frequently inflated, up to
8-μm-wide hyphae. Acidoresistant incrustations absent.
Terminal cells of hyphae in pileipellis near the cap margin
measuring (18–)23–32–41(–65) × (3–)3.1–3.6–4.2(–5) µm,
cylindrical, strongly moniliform-flexuous, apically mainly
obtuse, occasionally with slightly constricted tips; subter-
minal cells equally wide and usually also equally long, often
Fig. 3 Hymenial elements of Russula blumiana, J. Blum 1617
(PC0084516, as R. formosa). a Cheilocystidia. b Pleurocystidia. c
Basidioles. d Basidia. e Marginal cells. f Spores in Melzer’s reagent.
Contents of cystidia are shown as observed in Congo red for some
elements only; the plus sign indicates the contents of the others sche-
matically. Scale bar equals 10μm, but only 5μm for spores. Draw-
ings by: S. Jančovičová
Fig. 4 Pileipellis of Russula blumiana. a Pileocystidia near the pileus
centre, JMT 14072513C (SAV). b Pileocystidia near the pileus mar-
gin, J. Blum 1617 (PC0084516, as R. formosa). c Hyphal termina-
tions near the pileus centre, JMT 14072513C(SAV). d Hyphal ter-
minations near the pileus margin, J. Blum 1617 (PC0084516, as R.
formosa). Contents of cystidia are shown as observed in Congo
red for some elements only; the plus sign indicates the contents of
the others schematically. Scale bar equals 10 μm. Drawings by: S.
Jančovičová
Author's personal copy
Blum versus Romagnesi: checking possible Russula synonymies
1 3
with lateral nodules or branches, intricate. Terminal cells of
hyphae in pileipellis near the cap centre shorter, cylindri-
cal, measuring (17–)20.6–26.3–32(–42) × (2.5)3–3.5–3.9
(–4.5) µm, frequently nodulose; subterminal cells shorter
than those near the cap margin. Pileocystidia narrowly
clavate or subcylindrical, mainly one-celled, occasionally
or rarely of two or three cells, originating deep in suprapellis
or in subpellis, terminal cells near the cap margin measuring
(30–)58.3–74.7–91(–140) × (5–)6.5–7.3–8(–9.5) µm, api-
cally obtuse, towards the basal part often strongly narrowed
(3.5–5µm), thin-walled, in Congo red with heteromorphous
(mostly granular) contents, hardly reacting to sulfovanillin;
pileocystidia near the cap centre more frequently septate,
with shorter terminal cells measuring (22–)44–64.3–84.6
(–111) × (6.5–)6.8–7.5–8.2(–9.5) µm. Pileus trama without
cystidioid hyphae. Clamp connections absent in all parts.
Additional specimens examined: France, Rambouillet:
Étang d’Ór, s.d., s.col., J. Blum 6529 (PC); ibid., s.d., s.col.,
J. Blum 1617 (PC0084516); ibid., 7 Sep 1997, R. Chalange
PAM 97090701 (LIP); France, Bas-Rhin, Gunstett: Forêt de
Gunstett, 25 Jul 2014, J.M. Trendel JMT 14072513 (SAV).
Acknowledgements Curator and staff of the herbarium PC are
acknowledged for the loan of the material from Blum’s herbarium; H.
Marxmüller is acknowledged for the collection of R. badia. The stud-
ies of S. Adamčík, M. Caboň and S. Jančovičová were funded by the
Slovak Research and Development Agency APVV-15-0210. The stud-
ies of M. Caboň and M. Kolařík were supported by bilateral scientific
mobility project SAV-AV ČR 16-06 and Intra-Visegrad scholarship
No. 51400484.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Information onElectronic supplementary
materials
Online Resource 1. List of all sequences used in this study with associ-
ated data.
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Author's personal copy
Blum versus Romagnesi: testing possible synonymies of some European russulas (Russulaceae, Basidiomycota)
Miroslav Caboň, Soňa Jančovičová, Jean Michel Trendel, Pierre-Arthur Moreau, Felix Hampe, Miroslav Kolařík, Annemieke Verbeken,
Slavomír Adamčík
Online resource 1 List of sequences used in this study with associated data. Sequences with accession numbers starting with UDB are retrieved from the
UNITE database, all other are from GenBank. EcM – ectomycorrhizal isolates.
Species (orig.
identification) Herb. acronym
(collection number) Country: Collecting area Host or habitat Collector Date Sequences source ITS mtSSU RPB2
R. aurea SAV F-4196 Slovakia: W Carpathians, Štiavnické vrchy Mts.,
Kráľovec Krnišov Carpinus
S. Adamčík
14 Jul
2010 Caboň et al. 2017 KY582718 KY471610
R. badia SAV F-3903 Slovakia: Panonia, Záhorská nížina lowland,
Šajdíkove Humence – Horáreň Kalaštov Pinus silvestris
M. Caboň
5 Nov
2012 Adamčík et al.
2016, Caboň et al.
2017
KU928168 KY471607
R. badia M (HM R-0866) France: Rhône-Alpes – Gigors le Savel Castanea sativa,
Pinus H.
Marxmüller 6 Sep
2008 This study MF138072 MF138083
R. blumiana GENT (HM R-
1366) France: Seine et Marne Forêt
d’Armainvilliers Quercus robur,
Populus tremula
10 Oct
2013 Marxmüller 2014 UDB031140
R. blumiana LIP (PAM 97090701) France: Rambouillet Étang d´Ór Quercus
R. Chalange
7 Sep
1997 This study MF138084
R. blumiana SAV (JMT
14072513D) France: Grand Est, Bas-Rhin, Gunstett – Forêt de
Gunstett Carpinus
J.M. Trendel
25 Jul
2014 This study MF138073 MF138085
R. blumiana SAV (JMT
14072513C) France: Grand Est, Bas-Rhin, Gunstett – Forêt de
Gunstett Carpinus
J.M. Trendel
25 Jul
2014 This study MF138074 MF138086
R. betularum SAV F-20026 Romania: Apuseni Mts., Vladeasa Mts., Poiana
Horea – S of the village Betula, Picea
M. Caboň
6 Oct
2014 Caboň et al. 2017 KY582694 KY471585 KY616687
R. caerulea SAV F-3900 Slovakia: Panonia, Záhorská nížina lowland,
Studienka – Tŕnie Quercus, Pinus
silvestris
M. Caboň
1 Nov
2012 Caboň et al. 2017 KY582713 KY471606 KY616706
R. claroflava GENT (FH-12-212) Germany: Niedersachsen, Hildesheim
F. Hampe
18 Aug
2012 Looney et al. 2016 KT933997 KT933929
R.
cremeoavellanea SAV F-2125 Estonia: Saarema, Põlluküla – Viidumäe Natural
Reserve Betula
S. Adamčík
21 Sep
2008 Caboň et al. 2017 KY582695 KY471586 KY616688
R. cuprea SAV (HK12050) Sweden: Gotland, Hangvar – Elingshems
oderkyrka Quercus
H. Kaufmann
17 Aug
2012 Adamčík et al.
2016, Caboň et al.
2017
KU886591 KY471620 KY616721
R. decipiens SAV F-1022 Slovakia: W Carpathians, Štiavnické vrchy Mts.,
Nová Dedina – Sovia dolina Quercus
S. Adamčík
28. Jul
2005 Caboň et al. 2017 KY582683 KY471572 KY616679
Species (orig.
identification) Herb. acronym
(collection number) Country: Collecting area Host or habitat Collector Date Sequences source ITS mtSSU RPB2
R. decipiens SAV F-991 Slovakia: W Carpathians, Tríbeč Mts., Súľovce
Betlehem Quercus
S. Adamčík
29 Jul
2005 This study MF138075 MF138087
R. decipiens SAV F-1346 Slovakia: W Carpathians, Pohronský Inovec Mts.,
elár Quercus
S. Adamčík
7 Sep
2006 This study MF138076 MF138088
R. decipiens SAV F-1567 Slovakia: W Carpathians, Štiavnické vrchy Mts.,
Nová Dedina – Sovia dolina Quercus
S. Adamčík
4 Sep
2007 This study MF138077 MF138089 MF139291
R. decipiens SAV F-3241 Spain: Comunitat Valenciana, Castellón, Morella –
Barranco de los Corrales Quercus ilex
S. Adamčík
19 Oct
2010 This study MF138078 MF138090
R. decipiens
(neotype) PC 0084523 France: Oise – Forêt de Coye beech forest
H. Romagnesi
22 Aug
1943 This study MF138079
R. decipiens var.
ochrospora PC 0084509 (J. Blum
1933) This study MF138080 MF138091
R. decolorans SAV F-3131 Slovakia: W Carpathians, Vysoké Tatry Mts., Ždiar
– Trojrohé pleso Pinus mugo
S. Adamčík
16 Sep
2009 Caboň et al. 2017 KY582705 KY471597 KY616698
R. dryadicola TURA 151632 Finland: Lapland, Kilpisjärvi – Saana birch forest J.
Ruotsalainen 16 Aug
1990 Adamčík et al.
2016, Caboň et al.
2017
KU928141 KY471623 KY616724
R. favrei SAV F-4234 Poland: W Carpathians, Západné Tatry Mts., Kiry
Koscielicka potok Picea
S. Adamčík
27 Aug
2014 Caboň et al. 2017 KY582721 KY471614 KY616715
R. firmula GENT (2010 BT85) Germany: Thuringia, Troistedt
F. Hampe
24 Aug
2010 Adamčík et al.
2016, Caboň et al.
2017
KU928142 KY471568 KY616675
R. formosa PC 0084516 (J. Blum
1617) France: Rambouillet This study MF138081 MF138092
R. globispora GENT (2007 BT111) Germany: Thuringia, Gügleben – Werningslebener
Wald
F. Hampe
8 Sep
2007 Adamčík et al.
2016, Caboň et al.
2017
KU928144 KY471564 KY616671
R. integra SAV F-20023 Poland: W Carpathians, Západné Tatry Mts.,
Zakopane – Droga pod Reglami Picea
M. Caboň
25 Aug
2014 Caboň et al. 2017 KY582682 KY471582 KY616685
R. juniperina GENT
(RUS11121210) Spain: Mallorca, Valdemossa – Plateau Plan de
Pouet Quercus ilex F. Hampe, J.
Kleine 12 Dec
2011 Caboň et al. 2017 KU886596 KY471571 KY616676
R. laeta SAV F-3949 Slovakia: W Carpathians, Pohronský Inovec Mts.,
Hostie Quercus,
Carpinus
P. Marstad
16 Sep
2013 Caboň et al. 2017 KY582708 KY471600 KY616709
R. lepida UPS (HJB9990) Belgium: Hainaut, Soignes Broadleaf
woodland
H.J. Beker
24 Jul
2004 GenBank, Caboň
et al. 2017 DQ422013 KY471624 DQ421954
R. maculata GENT (2009 BT05) Germany: Thuringia, Arnstadt – Gustav-Freytag-
Weg, Schlossleite
J. Girwert
1 Jun
2009 Adamčík et al.
2016, Caboň et al.
2017
KU928155 KY471566
R. melliolens SAV F-4201 Slovakia: W Carpathians, Štiavnické vrchy Mts.,
Sebechleby – Stará hora Quercus,
Carpinus
S. Adamčík
13 Jul
2010 Caboň et al. 2017 KY582719 KY471611 KY616712
Species (orig.
identification) Herb. acronym
(collection number) Country: Collecting area Host or habitat Collector Date Sequences source ITS mtSSU RPB2
R. nauseosa SAV F-20022 Poland: W Carpathians, Západné Tatry Mts., Kiry –
Koscielicka potok Picea
S. Adamčík
27 Aug
2014 Caboň et al. 2017 KY582691 KY471581 KY616684
R. nitida SAV F-2924 Slovakia: W Carpathians, Volovské vrchy Mts.,
Predná Hora – recreation area Betula I.
Kautmanová 8 Jul
2009 Caboň et al. 2017 KY582702 KY471594 KY616696
R. odorata SAV F-3174 Slovakia: W Carpathians, Tríbeč Mts., Jelenec – N
of the autocamp Quercus,
Carpinus
S. Adamčík
12 Jul
2010 Caboň et al. 2017 KY582706 KY471598 KY616699
R. olivacea SAV F-3943 Slovakia: W Carpathians, Tríbeč Mts., Zlatno –
Veľký Tríbeč
Fagus,Quercus,
Carpinus
S.
Adamčík
19 Jul
2013 Caboň et al. 2017 KY582715 KY471608 KY616708
R. paludosa SAV F-20025 Poland: W Carpathians, Západné Tatry Mts.,
Zakopane – Mala Polanka under Grzybowec Picea
S. Adamčík
25 Aug
2014 Caboň et al. 2017 KY582693 KY471584 KY616686
R. persicina SAV F-3971 Slovakia: W Carpathians, Pohronský Inovec Mts.,
Hostie Carpinus, Fagus,
Quercus cerris
S. Adamčík
16 Sep
2013 Caboň et al. 2017 KY582717 KY471609 KY616711
R. puellaris SAV F-4224 Slovakia: W Carpathians, Spišská Magura Mts.,
Vojňany – Dlhá hora Abies
S. Adamčík
26 Aug
2014 Caboň et al. 2017 KY582720 KY471613 KY616714
R. puellula SAV F-3107 Slovakia: W Carpathians, Muránska planina
National Park, Muráň – Hrdzavá dolina Fagus, Carpinus
V. Kautman
6 Jul
2009 Caboň et al. 2017 KY582704 KY471596 KY616697
R. quercilicis SAV F-4889 Italy: Tuscany, Marsiliana, Riserva Statale Quercus suber,
Quercus ilex
L. Michelin
8 Nov
2016 Caboň et al. 2017 KY613998 KY582728 KY616725
R. quercilicis GENT (RUS
11121209) Spain: Mallorca, Valdemossa – Plateau Plan de
Pouet Quercus ilex
F. Hampe
12 Dec
2011 Caboň et al. 2017 KY613996 MF138094
R. risigallina UPS
(UE03.07.2003-08) Sweden: Östagötland, Linköping in direction to
Björkby-Sälja, Ekäng Quercus, Betula,
Picea
U. Eberhardt
3 Jul
2003 GenBank DQ422022 DQ421961
R. romellii SAV F-3355 Slovakia: W Carpathians, Malé Karpaty Mts.,
Kuchyňa – Vývrať, Bučková Fagus, Quercus
S. Adamčík
6 Jul
2011 Caboň et al. 2017 KY582710 KY471602 KY616702
R. roseobrunnea PC 0084517 (J. Blum
1395) This study MF138082 MF138093
R. rubra SAV (HK04078) Sweden: Bohuslän, Tossene – Hogsams Fagus
H. Kaufmann
15 Sep
2004 Adamčík et al.
2016, Caboň et al.
2017
KU928161 KY471619 KY616720
R. rubroalba SAV F-3349 Slovakia: W Carpathians, Štiavnické vrchy Mts.,
Prenčov – Sitno Carpinus,
Quercus
S. Adamčík
5 Jul
2011 Caboň et al. 2017 KY582709 KY471601 KY616701
R. rutila GENT (2007 BT122) Germany: Thuringia, Gügleben – Werningslebener
Wald
J. Girwert
26 Aug
2007 Adamčík et al.
2016, Caboň et al.
2017
KU928163 KY471565
R. rutila GENT (2010 BT31) Germany: Thuringia, Nohra
J. Girwert
19 Aug
2010 Caboň et al. 2017 KY582674 KY471567 KY616674
R. rutila SAV F-1497 Slovakia: W Carpathians, Štiavnické vrchy Mts.,
Jabloňovce – Bohunický Roháč
Quercus, Pinus
silvestris,
Carpinus
S. Adamčík
8 Sep
2006 Caboň et al. 2017 KY582686 KY471577 KY616678
R. rutila SAV F-2296 Slovakia: W Carpathians, Štiavnické vrchy Mts.,
Nová Dedina – Sovia dolina. Quercus
(Carpinus)
S. Adamčík
21 Jul
2008 Caboň et al. 2017 KY582697 KY471588 KY616690
Species (orig.
identification) Herb. acronym
(collection number) Country: Collecting area Host or habitat Collector Date Sequences source ITS mtSSU RPB2
R. rutila SAV (HK14028) Sweden: Västergötland, Kina Quercus
H. Kaufmann
30 Aug
2014 Caboň et al. 2017 KY582724 KY471621 KY616722
R. rutila
(holotype) PC 0723457 (n°12-IX-
45) France: Val-d’Oise, Asniéres sur Oise Quercus
H. Romagnesi
12 Sep
1945 Caboň et al. 2017 KY582681
R. sardonia SAV F-3914 Slovakia: W Carpathians, Záhorská nížina lowland,
Malacky - Pekyna Quercus, Pinus
silvestris
M. Caboň
1 Nov
2011 Caboň et al. 2017 KY582714 KY582727 KY616707
R. tinctipes SAV F-2494 Slovakia: W Carpathians, Tríbeč Mts., Súľovce
Betlehem Quercus,
Carpinus
S. Adamčík
23 Jul
2008 Caboň et al. 2017 KY582698 KY471590 KY616692
R. turci SAV F-3075 Norway: Nord-Trøndelag, Steinkjer – Noem Picea
S. Adamčík
2 Sep
2009 Caboň et al. 2017 KY582703 KY471595
R. velenovskyi SAV F-2921 Slovakia: W Carpathians, Volovské vrchy Mts.,
Predná Hora – recreation area Betula
V. Kautman
8 Jul
2009 Caboň et al. 2017 KY582701 KY471593 KY616695
R. velutipes SAV F-3428 Slovakia: E Carpathians, Bukovské vrchy Mts.,
Nová Sedlica – Stužica Natural Reserve Fagus, Abies
S. Adamčík
26 Sep
2011 Caboň et al. 2017 KY582711 KY471604 KY616704
R. versicolor SAV F-2919 Slovakia: W Carpathians, Volovské vrchy Mts.,
Predná Hora – recreation area Betula
P. Marstad
8 Jul
2009 Caboň et al. 2017 KY582700 KY471592 KY616694
R. veternosa SAV F-1401 Slovakia: W Carpathians, Pohronský Inovec Mts.,
Malá Lehota – Dudkov vrch Quercus, Fagus
S. Adamčík
6 Sep
2006 Adamčík et al.
2016, Caboň et al.
2017
KU928164 KY471574 KY616680
R. vinosa SAV F-20024 Poland: W Carpathians, Západné Tatry Mts.,
Zakopane – Mala Polanka under Grzybowec Picea
M. Caboň
25 Aug
2014 Caboň et al. 2017 KY582692 KY471583
R. zvarae GENT (FH-12-175) Germany: Thuringia, Erfurt – Aspenbusch
F. Hampe
1 Aug
2012 KT933986 KT933918
Russula sp.
(EcM) (TRFLP 153) USA: Indiana, Porter County – Dunes National
Lakeshore oak forest Avis et al. 2008 EU375714
References
Adamčík S, Caboň M, Eberhardt U, Saba M, Hampe F, Slovák M, Kleine J, Marxmüller H, Jančovičová S, Pfister DH, Khalid AN, Kolařík M, Marhold K, Verbeken A (2016) A molecular
analysis reveals hidden species diversity within the current concept of Russula maculata (Russulaceae, Basidiomycota). Phytotaxa 270: 71–88. doi: 10.11646/phytotaxa.270.2.1
Avis PG, Mueller GM, Lussenhop J (2008) Ectomycorrhizal fungal communities in two North American oak forests respond to nitrogen addition. New Phytol 179: 472–483. doi: 10.1111/jM
469-8137.2008.02491.x
Caboň M, Eberhardt U, Looney B, Hampe F, Kolařík M, Jančovičová S, Verbeken A, Adamčík S (2017) New insights in Russula subsect. Rubrinae: phylogeny and the quest for synapomorphic
characters. Mycol Prog 16: 877–892. doi: 10.1007/s11557-017-1322-0
Looney BP, Ryberg M, Hampe F, Sánchez-García M, Matheny PB (2016) Into and out of the tropics: global diversification patterns in a hyper-diverse clade of ectomycorrhizal fungi. Mol Ecol
25: 630–647. doi: 10.1111/mec.13506
Marxmüller H (2014) Russularum Icones, Vol. 2. Anatis Verlag, München
... New collections from Pakistan with 97.75% similarity to closest published sequence in GenBank (MK966687 labelled as R. dryadicola originated from China) suggest that they may represent fifth Maculatinae species from this area. Recent studies have detected the highest number of known Maculatinae members in Europe with six species confirmed molecularly, from which four are agaric and two sequestrate species [16,17]. Southwest Himalayas in Pakistan seem to be the diversity hotspot of the group. ...
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Russula subsect. Maculatinae is morphologically and phylogenetically well-defined lineage of ectomycorrhizal fungi associated with arctic, boreal, temperate and Mediterranean habitats of Northern Hemisphere. Based on phylogenetic distance among species, it seems that this group diversified relatively recently. Russula ayubiana sp. nov., described in this study, is the fifth in the group known from relatively small area of northern Pakistan situated in southwestern Himalayas. This is the highest known number of agaric lineage members from a single area in the world. This study uses available data about phylogeny, ecology, and climate to trace phylogenetic origin and ecological preferences of Maculatinae in southwestern Himalayas. Our results suggest that the area has been recently colonised by Maculatinae members migrating from various geographical areas and adapting to local conditions. We also discuss the perspectives and obstacles in research of biogeography and ecology, and we propose improvements that would facilitate the integration of ecological and biogeographical metadata from the future taxonomic studies of fungi in the region.
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Three new species of Russula subsect. Lactarioideae, Russula byssina, R. cremicolor and R. leucocarpa collected from Guizhou Province grown under coniferous forest are described and illustrated based on morphological observation and ITS phylogenetic analyses. A key to these new species and closely related taxa in subsect. Lactarioideae and subsect. Pallidosporinae is provided. Phylogenic topologies show that R. cremicolor has a close relationship with Brevipes-Delica clade; R. byssina and R. leucocarpa are members of two independent clades.
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Russula is one of the most speciose genera of mushroom-forming fungi, but phylogenetic relationships among species and subgeneric groupings are poorly understood. Our multi-locus phylogenetic reconstruction places R. firmula, R. rubra, R. rutila and R. veternosa in a well-supported Rubrinae clade, belonging to the Integrae clade of the Crown clade of the genus Russula. Traditional morphology-based classifications placed these four species in two different subsections based on the presence or absence of incrustations on pileocystidia. The Integrae clade also contains R. integra and related species that are traditionally placed in other groups based on their mild taste. Ancestral state reconstruction suggests that the common ancestor of the Crown clade and the Integrae clade probably did not have any incrustations in the pileipellis, had a mild taste, yellow spore print and were associated with angiosperms. All four species of the Rubrinae clade are defined by a darker yellow or ochre spore print, acrid taste and incrustations on pileocystidia. This last character contradicts the former splitting of the group because incrustations were apparently overlooked in R. firmula and R. veternosa. Incrustation type is now highlighted as being important for the delimitation of species and groups within the Crown clade. Pink or red staining of the incrustations in sulphovanillin is present in all species of the Rubrinae clade and a majority of the analysed species of the Integrae clade. The delimitation of the Rubrinae clade and its species circumscriptions are summarised here in a new diagnostic key.
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The holotype of Galerina saxicola Svrček, a never revised species described from the Czech Republic in 1994, was studied in detail. Due to its poor state and the impossibility to obtain DNA data, we fixed its taxonomic position by designating an epitype using recent material from the type locality. The species proved to be conspecific with Norwegian and Czech collections of Galerina stordalii A.H.Sm., both morphologically and molecularly. Full synonymy and diagnostic characters of G. stordalii are provided, its morphological and ecological variability is discussed, and information on type specimens is corrected. Our collections document that G. stordalii has a broader ecological amplitude than thought before, living not only on Sphagnum and peat in boreal and arctic-alpine habitats like bogs and snow beds, but also among mosses in boggy spruce forests, on decaying conifer trunks in old-growth forests and on moist sandstone rocks in a river canyon under the influence of climatic inversion.
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The current generally accepted concept of Russula maculata defines the species by yellow-brownish spots on the basidi-omata, an acrid taste, a yellow spore print and a red pileus. This concept was tested using collections originating from various geographical areas mainly in Europe. Analyses of the ITS region suggested that there were three species within this broad concept. One of them, R. maculata, was identified based on the sequence from the epitype. Two other species, R. nympharum and R. sp., are described here as newly identified species. The European species R. maculata and R. nympharum grow in deciduous forests, are similar in their field aspect and are distinctly different in micro-morphological characteristics of spores, pleurocystidia and pileipellis. An Asian species, R. sp., is associated with pine and has smaller basidiomata and spores. These three species form the R. maculata complex and represent the sister clade to the R. globispora complex. This clade consists of species also characterized by a yellow-brownish context discolouration but with a different type of spore ornamentation. All of the other tested species had an acrid taste and yellow spore print but did not have a conspicuous yellow-brownish context discolouration and were placed in various unrelated clades.
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Ectomycorrhizal (ECM) fungi, symbiotic mutualists of many dominant tree and shrub species, exhibit a biogeographic pattern counter to the established latitudinal diversity gradient of most macroflora and fauna. However, an evolutionary basis for this pattern has not been explicitly tested in a diverse lineage. In this study, we reconstructed a mega-phylogeny of a cosmopolitan and hyper-diverse genus of ECM fungi, Russula, sampling from annotated collections and utilizing publically available sequences deposited in GenBank. Metadata from molecular operational taxonomic unit cluster sets were examined to infer the distribution and plant association of the genus. This allowed us to test for differences in patterns of diversification between tropical and extratropical taxa, as well as how their associations with different plant lineages may be a driver of diversification. Results show that Russula is most species-rich at temperate latitudes and ancestral state reconstruction shows that the genus initially diversified in temperate areas. Migration into and out of the tropics characterizes the early evolution of the genus, and these transitions have been frequent since this time. We propose the 'generalized diversification rate' hypothesis to explain the reversed latitudinal diversity gradient pattern in Russula as we detect a higher net diversification rate in extratropical lineages. Patterns of diversification with plant associates support host switching and host expansion as driving diversification, with a higher diversification rate in lineages associated with Pinaceae and frequent transitions to association with angiosperms. This article is protected by copyright. All rights reserved.