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Citation: Zhou, H.; Cheng, G.-Q.;
Wang, Q.-T.; Guo, M.-J.; Zhuo, L.;
Yan, H.-F.; Li, G.-J.; Hou, C.-L.
Morphological Characteristics and
Phylogeny Reveal Six New Species in
Russula Subgenus Russula
(Russulaceae, Russulales) from
Yanshan Mountains, North China. J.
Fungi 2022,8, 1283. https://doi.org/
10.3390/jof8121283
Academic Editor: Ruilin Zhao
Received: 11 November 2022
Accepted: 5 December 2022
Published: 7 December 2022
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4.0/).
Fungi
Journal of
Article
Morphological Characteristics and Phylogeny Reveal Six New
Species in Russula Subgenus Russula (Russulaceae, Russulales)
from Yanshan Mountains, North China
Hao Zhou 1, Gui-Qiang Cheng 1, Qiu-Tong Wang 1, Mei-Jun Guo 1, Lan Zhuo 1, Hui-Fang Yan 1, Guo-Jie Li 2,3
and Cheng-Lin Hou 1, *
1College of Life Science, Capital Normal University, Xisanhuan Beilu 105, Beijing 100048, China
2College of Horticulture, Hebei Agricultural University, Baoding 071001, China
3Key Laboratory of Vegetable Germplasm Innovation and Utilization of Hebei, Collaborative Innovation
Center of Vegetable Industry in Hebei, Baoding 071001, China
*Correspondence: chenglin-hou@cnu.edu.cn
Abstract:
Species of the genus Russula are key components of ectomycorrhizal ecosystems world-
wide, some of which are famous edible fungi. Although many new species have been described in
China, their diversity in North China is still poorly known. Based on the morphology observation of
specimens and molecular phylogenetic analyses, combined with the current classification frame of
Russula, six new species of Russula subgenus Russula are proposed from the Yanshan Mountains in
northern Beijing and northern Hebei Province of China in this study: viz.
Russula miyunensis
(sub-
section Chamaeleontinae), R.plana (subsection Chamaeleontinae),
R. sinoparva
(subsection
Puellarinae
),
R. sinorobusta
(subsection
Puellarinae
),
R. subversatilis
(subsection
Roseinae
), and
R. yanshanensis
(sub-
section
Puellarinae
). This is the first report of the species of Russula subgenus Russula from the Yanshan
Mountains. This study enriches the species diversity of Russula in North China and provides new
data support for the systematic study of Russula in subsequent research, including research and
development on edibility.
Keywords: Russulaceae; new taxa; edible fungi; taxonomy
1. Introduction
Russula Pers. (Russulaceae,Russulales,Agaricomycetes, and Basidiomycota) was estab-
lished in 1796, which is one of the most abundant genera, including at least 2000 species [
1
,
2
].
This genus is mainly characterized by colorless to multi-colored pileus, amyloid warty
basidiospores, abundant spherocytes in a heteromerous trama, an absence of latex, and
hyphae without clamp connections [
3
–
5
]. Russula is a large genus of ectomycorrhizal (ECM)
fungi that are found in all common ecosystems, such as broad-leaved forest, coniferous
forest, mixed coniferous, broad-leaved forest, or scrubland [
6
–
8
]. Furthermore, some mem-
bers of Russula not only play an important role in ecology by symbiotic with a variety of
plants but also serve as a food source for many animals, including humans. Some species
of Russula, e.g., Russula delica Fr., Russula griseocarnosa X.H. Wang, Zhu L. Yang, & Knudsen,
Russula nigricans Fr. et al., are famous edible fungi and important commercial trade goods
in the world [
7
,
9
–
12
]. According to recent statistics on the diversity of Chinese edible
macrofungi resources, there are about 70 edible species in China [12].
The previous classification system for Russula was based on morphology, e.g., pileus
color, spore print, and spore. Miller and Buyck et al. first used phylogenetic analysis of
nrITS loci to compare with the previous classification system of Russula in Europe, resulting
in 78 Russula species forming six clades with higher supported values on the phylogenetic
tree [
13
]. Buyck et al. [
1
,
2
] demonstrated that Russula was one of four monophyletic
groups in non-corticoid Russulaceae and was divided into eight subgenera by multi-locus
phylogenetic studies [1,14].
J. Fungi 2022,8, 1283. https://doi.org/10.3390/jof8121283 https://www.mdpi.com/journal/jof
J. Fungi 2022,8, 1283 2 of 33
The subgenus Russula Pers. is a species-rich subgenus of Russula, which is morphologi-
cally characterized mainly by a great variation of basidiocarp size, pileus thick to extremely
thin fleshed; stipe abnormally annulate gills unusually equal or lamellulae; spore print
white to yellow; spores with amyloid suprahilar spot. Phylogenetically, this subgenus is
divided into two parts: a core and a crown clade [1,2].
The first record of Russula in China is Russula alutacea (Fr.) Fr. from Tibet and Sichuan
Province [
15
]. So far, about 190 species have been recorded in China [
6
,
8
,
16
–
31
], and nearly
20 species belong to the subgenus Russula [
18
,
23
,
26
,
32
–
37
]. As a subgenus with the most
species in the genus Russula, its members are also widely distributed all over the world.
The Yanshan Mountains (115
◦
–119
◦
47
0
E, 39
◦
40
0
–41
◦
20
0
N) are located in North China
and have a warm temperate continental monsoon climate. This region is known for its high
plant diversity. The main forest types of this region are deciduous broad-leaved forest and
mixed coniferous and broad-leaved forest. Dominant ectomycorrhizal trees in this region
include Pinus tabuliformis Carr, Betula spp., Quercus spp. and Abies (Mill.) spp. The Yanshan
Mountains have an annual precipitation of approximately 350–700 mm, and their altitude
ranges from 200 to 2200 m [
37
,
38
]. Until the present study, records about the Russula species
in this area were very few [39].
In this study, six new species of the subgenus Russula crown clade from the Yanshan
Mountains were described based on multi-locus phylogenetic analyses and detailed macro-
and micromorphological data. The aims of this study are to identify the taxonomic status
and phylogenetic position of new species, to establish a comprehensive database on the
diversity of macrofungal in North China, especially the status of Russula in the Yanshan
Mountains, and to use this as a basis for promoting research on macrofungal diversity and
edible Russula species in this region.
2. Materials and Methods
2.1. Sampling and Morphological Observations
Specimens were collected from 2017 to 2021. Fresh specimens were photographed
in the field, and characteristics such as color, odor, and viscosity were noted. Specimens
were dried with a Dorrex dryer at 45
◦
C and deposited in the Herbarium of the College of
Life Science, Capital Normal University, Beijing, China (BJTC). Macroscopic characteristics
were recorded from fresh specimens. Microscopic characteristics were observed from
thin sections of dried material mounted in 3% KOH or sterilized water. Congo Red
(1%) was used to make the structures more visible. Melzer’s reagent was used to test
the amyloid reaction of the spores [
40
]. All tissues were also examined in cresyl blue
to verify the presence of ortho- or metachromatic reactions, as explained in Buyck [
1
].
Cystidia contents were examined in sulfovanillin (SV) solution [
40
]. Microscopic structures
(e.g., basidiospores, basidia, cystidia) were observed and measured using a light microscope
(Olympus DP71, Tokyo, Japan) and Image Pro Plus 6.0. The basidiospore structures were
further observed under a field emission scanning electron microscope (SEM, Hitachi S-4800,
Tokyo, Japan), digital cameras (Olympus U-TV0.5XC-3, Tokyo, Japan), and measuring
software (Image Pro Plus 6.0). Basidiospore measurements were presented as (Min–) AV-
SD–AV–AV + SD (–Max), where Min is the minimum value, Max is the maximum value, AV
is the average value, SD is the standard deviation, and Q represents the length/width ratio
of the basidiospores [
8
]. Statistics for the microscopic characteristics (e.g., basidiospores
and basidia) were based on 30 measurements per specimen. The descriptive terms follow
Adamˇcík et al. [
2
]. In this study, color codes were used from the reference website colorhexa
(https://www.colorhexa.com (accessed on 8 September 2022)).
2.2. DNA Extraction and Sequencing
DNA extraction was achieved via the M5 Plant Genomic DNA Kit (Mei5 Biotechnology,
Co., Ltd., Beijing, China). The DNA obtained was dissolved in 1
×
TE buffer/sterile water
and stored at
−
20
◦
C for later use. The PCR amplifications were performed in a Bio-Rad
S1000
TM
Thermal Cycler (Bio-Rad Laboratories, Inc, Hercules, CA, USA). The primer set
J. Fungi 2022,8, 1283 3 of 33
nrITS 1f/nrITS 4 was used to amplify for rDNA ITS region [
41
], T LR0R/LR5 for the large
subunit nuclear ribosomal DNA (nuLSU rDNA) region [
42
], MS1/MS2 for the ribosomal
mitochondrial small subunit (mtSSU) region [
41
], RBP2-6f/RBP2-7r for the second largest
subunit of RNA polymerase II (rpb2) region [
43
] and tef1F/tef1R for the second largest
subunit of transcription elongation factor 1-alpha (tef-1
α
) region [
44
], respectively. The
PCR volume was 25
µ
L, and the detailed composition was described by Zhou et al. [
39
].
PCR amplification conditions for nrITS and nrLSU refer to Li et al. [
25
]. PCR amplification
conditions for mtSSU and rpb2 refer to Song et al. [
8
]. PCR amplification conditions for
tef-1
α
refer to Morehouse et al. [
44
]. DNA sequences were sequenced by Zhongkexilin
Biotechnology, Co., Ltd., Beijing, China. Newly obtained sequences in this study were
submitted to the NCBI GenBank database (https://submit.ncbi.nlm.nih.gov/ (accessed
on 20 July 2022)). Accession numbers of sequences used for phylogenetic analyses are
provided in Figure 1and Table 1.
2.3. Molecular Phylogenetic Analyses
Raw reads of the generated DNA sequences were used to obtain consensus sequences
using SeqMan v.7.1.0 (DNASTAR Inc., Madison, WI, USA). All sequences (nrITS, nrLSU,
rpb2,tef-1
α
and mtSSU) were analyzed using MAFFT v.6 and manually trimmed using
MEGA 6 [
45
]. All reference sequences of subgenus Russula of dataset were chosen for
phylogenetic analyses based on previous studies and GenBank database in NCBI.
The nrLSU-rpb2-tef-1
α
-mtSSU multi-locus phylogenetic analysis included 83 ingroup
samples, which were used to analyze the phylogenetic position of our specimens in the
genus Russula. Moreover, the nrITS phylogenetic analysis included 129 ingroup samples,
which were used to analyze the relationships among our collections and other species in the
subgenus Russula. All reference sequences of subgenus Russula of the dataset were chosen
for phylogenetic analyses based on previous studies and the GenBank database in NCBI
and UNITE (accession number in Table 1and Figure 2). Multifurca aurantiophylla (Bills &
O.K. Mill.) Buyck and V. Hofst. (644/BB 09.119), Multifurca ochricompacta (Bills & O.K. Mill.)
Buyck & V. Hofst. (BB02.107), M. ochricompacta (580/BB 07.010),
Multifurca zonaria
(Buyck &
Desjardin) Buyck & V. Hofst. (DED7442), and Multifurca were outgroup taxa referring to
Buyck et al. [1].
The maximum likelihood (ML) gene trees were estimated using the RAxML 7.4.2 Black
Box software [
38
,
46
–
49
]. ML analysis used a GTR locus substitution model by running
1000 bootstrap replicates with all default settings parameters [
50
]. Bayesian inference (BI)
phylogenetic analysis was performed using MrBayes v.3.1.2 [
51
]. Branch supports were
calculated using a bootstrapping (BS) method with 1000 replicates [
52
]. Bayesian inference
(BI) analysis was performed by the Markov chain Monte Carlo (MCMC) algorithm [
53
].
MrModeltest v. 2.3 was used to estimate the best model for Bayesian inference (
GTR+I+G
for nrITS, nrLSU, rpb2, and mtSSU; SYM + I + G for tef-1
α
) [
51
]. Two MCMC chains were
run from the random trees for 10,000,000 generations and stopped when the mean standard
deviation of split frequencies fell below 0.01. Trees were saved once every 1000 generations
by the default settings. The first 25% of trees were discarded as the burn-in phase of each
analysis. In the remaining trees, branches with significant Bayesian posterior probabilities
were estimated, it has relatively stable topologies, and clades with high Bayesian posterior
probability (pp) values can also illustrate relative relationships between species [
54
]. ML
bootstrap support (BS)
≥
50% and Bayesian posterior probability (PP)
≥
0.95 were shown
on the nodes in Figures 1and 2.
J. Fungi 2022,8, 1283 4 of 33
Table 1. Sequences information used in the nrLSU-rpb2-tef-1α-mtSSU phylogenetic analysis in this study.
Taxa Voucher Location GenBank Accession Numbers
nrLSU mtSSU rpb2 tef-1α
Multifurca aurantiophylla 644/BB 09.119 New Caledonia KU237581 KU237429 KU237867 KU238008
Multifurca ochricompacta 580/BB 07.010 USA KU237565 KU237413 KU237851 KU237994
Russula abbottabadensis LAH 310071 Pakistan MN518356 MG386719 MG386737 MZ364137
Russula abbottabadensis FH 00304558 Pakistan MN518355 MG386721 MG386738 MZ364138
Russula acrifolia 543/BB 08.662 Italy KU237535 KU237381 KU237821 KU237965
Russula adusta 223/BB 06.562 Canada KU237476 KU237320 KU237762 KU237907
Russula amethystina 529/BB 07.314 Slovakia KU237521 KU237367 KU237807 KU237951
Russula archaeosuberis 1118/BB 12.085 Italy KU237593 KU237441 KU237878 KU238019
Russula ayubiana LAH 35438 Pakistan MZ358816 MZ364121 MZ364131 MZ364139
Russula ayubiana LAH 35439 Pakistan MZ358817 MZ364122 MZ364132 MZ364140
Russula azurea 537/BB 08.668 Italy KU237529 KU237375 KU237815 KU237959
Russula betularum BPL269 USA KT933829 KT933969 KT933900 -
Russula bicolor HMJAU 32180 China KX095080 KX095031 - -
Russula brevipes 226/BB 06.508 Mexico KU237479 KU237323 KU237765 -
Russula burlinghamiae 548/BB 05.108 USA KU237540 KU237386 KU237826 KU237970
Russula carpini 551/BB 07.262 Slovakia KU237543 KU237389 KU237829 KU237973
Russula chloroides 572/BB 07.209 Slovakia KU237559 KU237407 KU237845 KU237990
Russula compacta 228/BB 06.295 USA KU237480 KU237324 KU237766 -
Russula corallina- 229/BB 06.324 USA KU237481 KU237325 KU237767 KU237910
Russula crustosa BPL265 USA KT933826 - KT933898 -
Russula cuprea 565/BB 07.233 Slovakia KU237555 KU237401 KU237841 KU237984
Russula decolorans 549/BB 07.322 Slovakia KU237541 KU237387 KU237827 KU237971
Russula emetica 635/JMT39-08092228 France KU237578 KU237426 KU237864 -
Russula exalbicans 584/BB 07.786 France KU237568 KU237416 KU237854 KU237996
Russula farinipes 576/BB 08.632 Italy KU237561 KU237409 KU237847 KU237992
Russula fattoensis Buyck 02.227 USA MN315514 MN315537 MN326797 MN326800
Russula fragilis 443/BB 07.791 France KU237506 KU237351 KU237792 -
Russula glutinosa Roody WRWV 04.1154 USA MN315511 MN315532 MN326798 MN326799
Russula gracillima 441/BB 07.785 France KU237504 KU237349 KU237790 KU237934
Russula griseobrunnea JAC11227 New Zealand MW683630
Russula herrerae 239/BB 06.532 Mexico KU237486 KU237330 KU237772 KU237915
Russula integra 518/BB 07.198 Slovakia KU237513 KU237359 KU237799 KU237943
Russula laeta 519/BB 07.267 Slovakia KU237514 KU237360 KU237800 KU237944
Russula laricina 575/BB 08.681 Italy KU237560 KU237408 KU237846 KU237991
J. Fungi 2022,8, 1283 5 of 33
Table 1. Cont.
Taxa Voucher Location GenBank Accession Numbers
nrLSU mtSSU rpb2 tef-1α
Russula leucomarginata RITF3133 China MW309327 MW309338 MW310568 -
Russula leucomarginata RITF3123 China MW309328 MW309339 MW310569 -
Russula lilacea 435/BB 07.213 Slovakia KU237498 KU237343 KU237784 KU237928
Russula mansehraensis HUP SUR 180 Pakistan MG944280 MG944266 MG944255 -
Russula mansehraensis HUP SUR 803 Pakistan - MG944267 MG944256 -
Russula minutula 539/BB 08.636 Italy KU237531 KU237377 KU237817 KU237961
Russula miyunensis BJTC Z1357 China -OP135984 OP156826 OP156837
Russula miyunensis BJTC Z1355 China OP133232 OP135985 OP156827 -
Russula mustelina 1176/SA 09.88 Slovakia KU237596 KU237444 KU237881 KU238022
Russula nauseosa 588/BB 07.285 Italy KU237572 KU237420 KU237858 KU238000
Russula nigricans 429/BB 07.342 Slovakia KU237495 KU237339 KU237781 KU237924
Russula nothofagineae 723/BB 09.044 New Caledonia KU237583 KU237431 - KU238010
Russula nothofagineae 726/BB 09.069 New Caledonia KU237585 KU237433 KU237870 KU238012
Russula odorata 526/BB 07.186 Slovakia KU237518 KU237364 KU237804 KU237948
Russula olivascens 530/BB 08.663 Italia KU237522 KU237368 KU237808 KU237952
Russula olivobrunnea JV28388 Finland - MW633232 - -
Russula plana BJTC Z1398 China OP133233 OP135986 OP156828 OP156838
Russula plana BJTC T2101 China OP265903 OP265901 OP267556 OP267558
Russula pseudoaurantiophylla 740/BB 09.219 New Caledonia KU237591 KU237439 KU237876 KU238017
Russula puellaris 523/BB 07.311 Slovakia KU237515 KU237361 KU237801 KU237945
Russula purpureoverrucosa GDGM32902 China MG214699 - MT085652 MT085623
Russula quercus-floribundae LAH 36219 Pakistan MN513043 MN053397 MN053389 MZ364152
Russula quercus-floribundae LAH 36220 Pakistan MN513043 MN053396 MN053390 MZ364153
Russula raoultii 561/BB 08.674 Italy KU237551 KU237397 KU237837 KU237980
Russula rosea 430/BB 07.780 France KU237496 KU237340 KU237782 KU237925
Russula roseola RITF3418 China MW309319 MW309330 MW310560 -
Russula roseola RITF3428 China MW309320 MW309331 MW310561 -
Russula sinoparva BJTC C540 China OP133234 OP135987 OP156829 OP156839
Russula sinoparva BJTC Z441 China OP133235 OP135988 -OP156840
Russula sinorobusta BJTC Z050 China OP133236 OP135989 OP156830 OP156841
Russula sinorobusta BJTC Z052 China -OP135990 -OP156842
Russula sinorobusta BJTC Z662 China OP133237 OP135991 OP156831 OP156843
Russula sichuanensis ZRL20162017 China MG786572 MG792323 - MG812160
Russula solaris 559/BB 07.282 Slovakia KU237549 KU237395 KU237835 KU237978
J. Fungi 2022,8, 1283 6 of 33
Table 1. Cont.
Taxa Voucher Location GenBank Accession Numbers
nrLSU mtSSU rpb2 tef-1α
Russula sp. 735/BB 09.172 New Caledonia KU237588 KU237436 KU237873 KU238015
Russula subsanguinaria RITF2236 China MW309322 MW309333 MW310563 -
Russula subsanguinaria RITF2208 China MW309323 MW309334 MW310564 -
Russula subtilis 536/BB 05.107 USA KU237528 KU237374 KU237814 KU237958
Russula subversatilis BJTC C653 China OP133238 OP135992 OP156832 OP156844
Russula subversatilis BJTC T2001 China OP265904 OP265902 OP267557 OP267559
Russula turci 528/BB 07.328 Slovakia KU237520 KU237366 KU237806 KU237950
Russula versicolor 589/BB 07.288 Slovakia KU237573 KU237421 KU237859 KU238001
Russula vinosobrunneola HMAS 281138 China MG786569 MG792320 - MG812157
Russula vinosobrunneola HMAS 278885 China MG786570 MG792321 - MG812158
Russula yanshanensis BJTC C561 China OP133239 OP135993 -OP156845
Russula yanshanensis BJTC Z1448 China OP133240 OP135994 OP156833 -
Russula yanshanensis BJTC Z421 China OP133241 OP135995 -OP156846
Russula yanshanensis BJTC Z1385 China OP133242 OP135996 -OP156847
Russula yanshanensis BJTC Z1305 China OP133243 OP135997 OP156834 OP156848
Russula yanshanensis BJTC Z1390 China OP133244 OP135998 OP156835 OP156849
Russula yanshanensis BJTC L349 China OP133245 OP135999 OP156836 OP156850
Russula zvarae 538/BB 08.639 Italy KU237530 KU237376 KU237816 KU237960
Remarks: The new generated sequences are emphasized in bold, “-” show no sequence. Database.
J. Fungi 2022,8, 1283 7 of 33
Figure 1.
The nrITS phylogenetic tree obtained from the Bayesian analysis. Numbers above branches
represent strongly and moderately support (pp
≥
0.95 and/or MLB
≥
50%). Numbers above branches
are Bayesian posterior probability (pp) values and maximum likelihood bootstrap (MLB). The red
font indicates the position of newly obtained sequences. Accession numbers of sequences information
used are indicated on the figure. Asterisks (*) denote branches with pp = 1.00, MLb = 100%.
J. Fungi 2022,8, 1283 8 of 33
Figure 2.
The nrLSU-rpb2-tef-1
α
-mtSSU multi-locus phylogenetic tree obtained from the Bayesian
analysis. Numbers above branches represent strongly and moderately support (pp
≥
0.95 and/or
MLB
≥
50%). Numbers above branches are Bayesian posterior probability (pp) values and maximum
likelihood bootstrap (MLB). The red font indicates the position of newly obtained sequences. Acces-
sion numbers of sequences information used are indicated in Table 1. Asterisks (*) denote branches
with pp = 1.00, MLb = 100%.
J. Fungi 2022,8, 1283 9 of 33
3. Results
3.1. Phylogenetic Analyses
The nrITS phylogenetic analysis included 129 ingroup samples, M. zonaria (DED7442)
and M. ochricompacta (BB02.107) were used as the outgroups. The dataset of nrITS loci
comprised 611 characters including alignment gaps. The best Bayesian tree is shown
in Figure 1. The nrLSU-rpb2-tef-1
α
-mtSSU multi-locus phylogenetic analysis included
83 ingroup samples, M. ochricompacta (580/BB 07.010) and M. aurantiophylla (644/BB 09.119)
were used as the outgroups. The dataset of multi-locus comprised 2511 characters including
alignment gaps. The nrLSU-rpb2-tef-1
α
-mtSSU dataset was analyzed by ML analysis and
BI analysis. Phylogenetic analysis generated topologies from ML analysis and BI analysis
were almost identical, and the Bayesian tree are shown in Figure 2.
The nrLSU-rpb2-tef-1
α
-mtSSU and nrITS phylogenetic analyses revealed that the sub-
genera proposed by Buyck et al. [
1
] were well-supported with significant Bayesian pos-
terior probability (PP) values and maximum likelihood bootstrap (MLB). Sequences of
our collections all fell into the Russula subgenus Russula crown clade and formed six
new lineages (marked in red and bolded in Figures 1and 2) with significant support.
Thus, they were considered as six distinct clades and described as new species in this
paper, i.e.,
Russula miyunensis
,R. plana,
R. sinoparva
,
R. sinorobusta
,
R. subversatilis
, and
R. yanshanensis.
The nrLSU-rpb2-tef-1
α
-mtSSU multi-locus phylogenetic analysis showed that two se-
quences of the new species Russula sinoparva (BJTC C540, BJTC Z441) were supported as one
clade (pp = 1.00, MLB = 100%) and clustered with Russula odorata Romagn.
Russula subversatilis
(BJTC C653, BJTC T2001) formed one clade (pp = 0.99, MLB = 99%) together with
Russula solaris
Ferd. & Winge. Sequences of seven specimens of Russula yanshanensis (BJTC C561, BJTC
Z421, BJTC Z1385, BJTC Z1305, BJTC L349, BJTC Z1448, and BJTC Z1390) were clustered
together, forming a completely supported clade (pp = 1.00, MLB = 100%),
R. yanshanensis
clustered with Russula puellaris Fr. and formed a sister clade in the phylogenetic tree. Two
new clades of
Russula miyunensis
(BJTC Z1355, BJTC Z1357) and Russula plana (BJTC Z1398,
BJTC T2101) clustered with Russula olivascens Fr. formed a group (pp = 0.98, MLB = 99%).
Sequences of three specimens of
Russula sinorobusta
(BJTC Z052, BJTC Z050, and BJTC Z662)
clustered into a branch, with high support values (pp = 1.00, MLbs = 100%), and the branch
further clustered a clade with Russula minutula Velen.,
Russula rosea
Pers. and Russula sp.
(735/BB 09.172) with moderate support.
The nrITS phylogenetic analysis showed similar topologies to that of multi-locus phy-
logenetic tree, and sequences of our collections also formed six strong support end branches.
Notebly,
R. subversatilis
and
R. sinoparva
were clustered together with
R. khinganensis
G.J. Li &
R.L. Zhao.
Russula miyunensis
and R. plana formed a well-supported clade.
Russula sinorobusta
formed a clade clustered with Russula lepidicolor Romagn. and Russula intermedia P. Karst.
but without support values.
3.2. Taxonomy
Based on phylogenetic analyses and morphology, six new species of Russula subgenus
Russula from the Yanshan Mountains were recognized and described in this study.
Russula miyunensis C. L. Hou, H. Zhou, &G. Q. Cheng, sp. nov.
Figures 3–6.
MycoBank: MB 845047
Diagnosis: Russula miyunensis
is diagnosed by small to big-sized basidiomata, light
pink or grayish-yellow, central deep red to deep brown pileus, basidiospores ornamented
with amyloid warts, and more or less chain-like, suprahilar spot obvious, longer ba-
sidia, shorter terminal cells near the pileus margin, pileocystidia without color change
in sulfovanillin. Morphologically, R. miyunensis is similar to Russula olivascens Fr. and
Russula clavatohyphata
R.P. Bhatt, A. Ghosh, Buyck, & K. Das,but pileus of R. miyunensis
has severely cracked when mature.
J. Fungi 2022,8, 1283 10 of 33
Figure 3. Russula miyunensis
(BJTC Z1355). (
A
–
D
) Basidiomata. (
E
,
F
) Basidiospores. Scale bar:
(A–D) = 10 mm, (E,F)=1µm.
Figure 4.
Microscopic features of
Russula miyunensis
(BJTC Z1355). (
A
) Basidia. (
B
) Basidiola.
(
C
) Marginal cells. (
D
) Hymenial cystidia on lamellae sides. (
E
) Hymenial cystidia on lamellae edges.
Scale bar: 10 µm.
J. Fungi 2022,8, 1283 11 of 33
Figure 5.
Microscopic features of
Russula miyunensis
(BJTC Z1355). (
A
) Primordial hyphae near the
pileus margin. (
B
) Hyphal terminations near the pileus margin. (
C
) Primordial hyphae near the
pileus center. (D) Hyphal terminations near the pileus center. Scale bar: 10 µm.
Figure 6.
Microscopic features of
Russula miyunensis
(BJTC Z1355). (
A
) Basidiospores. (
B
) Hyphal
terminations near the pileus margin. (
C
) Hyphal terminations near the pileus center. Scale bar:
(A)=5µm; (B,C) = 10 µm.
Holotype:
CHINA, Beijing, Miyun District, Heilongtan, 40
◦
33
0
42” N, 116
◦
46
0
20” E, alt.
381 m, 29 August 2021, coll. C.-L.H., H.Z. and G.-Q.C. (BJTC Z1355).
Etymology:
The epithet “miyunensis” referred to the locality “Miyun District” where
the type specimen was collected.
J. Fungi 2022,8, 1283 12 of 33
Basidiomata:
small to big size, pileus 32–135 mm in diameter, initially hemispherical
when young, applanate with depressed in the center when mature, large pieces crack near
the margin in age, smooth, peeling to 1/3 of the radius, margin light pink (#d69188) or
grayish-yellow (#cec7a7), sometimes light yellow (#d59a6f), central deep red (#af4d43) to
deep brown (#623f2d).
Lamellae:
white (#ffffff) to light yellow-brown (#ffffed), adnate,
lamellulae absent, hardly forked.
Stipe:
52–89
×
25–34 mm, white (#ffffff), sometimes
with brownish (#a52a2a) on the base, cylindrical, inflated toward base, hollow, smooth.
Context:
8–34 mm thick in half of the pileus radius, white (#ffffff), without color change
when bruised. Spore print: not observed.
Basidiospores:
(6.7–)6.9–7.4–7.9(–8.5)
×
(5.7–)6.1–6.4–6.7(–7)
µ
m, [Q = (1.03–)1.09–
1.17–1.23(–1.31)], globose to broadly ellipsoid, ornamentation of relatively small, dense
[(5–)6–9(–10)] in a 3
µ
m diameter circle] amyloid warts, 0.3–0.7
µ
m high, occasionally with
isolated warts, occasionally fused in pairs or triplets chains [0–2 in the circle], occasionally
to frequently connected by short, fine line connections [1–3(–4) in the circle], suprahilar
spot obvious, amyloid.
Basidia:
(35–)36.2–38.5–40.8(–43)
×
(10–)10.4–11.9–13.4(–15)
µ
m,
2–4-spored, clavate, with particles and oil droplets, basidiola clavate or subcylindrical,
ca. 7–12
µ
m wide.
Hymenial cystidia:
dispersed, ca. 400–600/mm
2
.
Hymenial cys-
tidia on lamellae sides:
(45–)50.3–59.7–69.1(73–)
×
(10–)9.7–11–12.3(–13)
µ
m, thin-walled,
clavate, subfusiform or lanceolate, apically mainly obtuse, sometimes mucronate, often
with
2–5 µ
m long appendage; contents with heteromorphous and granulose, turning
light brown (#a52a2a) in SV.
Hymenial cystidia on lamellae edges:
smaller to hymenial
cystidia on lamellae sides, (42–)44.4–50.2–56(–60)
×
(6.3–)7.4–8.5–9.6(–10)
µ
m, clavate or
subfusiform, apically often obtuse, sometimes with 2–3
µ
m long appendage, refracted
inclusions, contents with heteromorphous-granulose, distribute mainly in the middle,
relatively less, turning light brown (#a52a2a) in SV.
Marginal cells:
(15–)17.5–20.9–24.3
(–27) ×(3.0–)3.2–4.3–5.3(–6.4) µm, subcylindrical, occasionally flexible.
Pileipellis:
orthochromatic in cresyl blue, sharply delimited from the underlying
context, 35–60
µ
m deep, single-layered, weakly gelatinized, composed of relatively dense,
intricate, horizontally oriented near the context, 2–7-
µ
m-wide hyphae. Acid-resistant
incrustations are present but mainly distinct only on subterminal cells of primordial hy-
phae, occasionally on terminal cells. Hyphal terminations near the pileus margin occa-
sionally branched, sometimes flexuous, thin-walled; terminal cells (10.4–)12.9–18.7–24.5(–
32.2)
×
(4.0–)4.8–5.7–6.6(–7.1)
µ
m, mainly cylindrical, clavate, subfusiform or irregular
shape, apically obtuse, occasionally attenuated, constricted or inflated, a few forked, sub-
terminal cells often wider, ca. 2–8
µ
m wide, sometimes branched; hyphal terminations
near the pileus center similar to those near the pileus margin; terminal cells (13–)15.8–
19.7–23.6(–25)
×
(3.2–)3.7–4.8–5.9(–7.1)
µ
m, cylindrical, clavate, subfusiform or irregular
shape, apically obtuse, occasionally constricted or inflated, a few forked; subterminal
cells often wider, sometimes branched, ca. 2–6
µ
m wide. Primordial hyphae near the
pileus margin are always 2–3-celled, sometimes one-celled, thin-walled, terminal cells
(20–)
23.8–37.7–51.5(–71)
×
(4.0–)4.7–5.5–6.3(–7.2)
µ
m, cylindrical or fusiform, apically usu-
ally obtuse, sometimes constricted; contents with heteromorphous-crystalline or banded,
no color change in SV. Primordial hyphae near the pileus center are often smaller, always
2–3-celled, thin-walled, terminal cells (14–)23.2–33.1–43 (–48)
×
(3.4–)4.2–5.1–6(–8.1)
µ
m,
cylindrical or subfusiform, apically typically obtuse or occasionally attenuated, contents
with heteromorphous-crystalline or banded.
Cystidioid hyphae or oleiferous hyphae:
not observed.
Habit and habitat: Scattered in broad-leaved forests of Carpinus turczaninowii Hance.
Additional specimens examined:
CHINA, Beijing, Miyun District, Heilongtan,
40
◦
33
0
42” N, 116
◦
46
0
20” E, alt. 384 m, 29 August 2021, coll. C.-L.H., H.Z. and G.-Q.C.
(BJTC Z1357).
Notes: Russula miyunensis
belongs to subsection Chamaeleontinae Singer. On the phylo-
genetic tree, R. miyunensis is closely related to
R. olivascens
and R. plana (Figure 1). Morpho-
logically,
R. olivascens
has light green-yellow pileus and bigger basidia (39–52
×
12–15
µ
m)
J. Fungi 2022,8, 1283 13 of 33
than R. miyunensis; Russula plana has a small size, brick-red to deep red pileus, stipe with a
pink tone, shorter basidia (23.4–33.2 ×12.1–15.9 µm), hymenial cystidia on lamellae sides
turning light brown in SV. Moreover, the similarity of nrITS sequences with R. plana is
91.19% (coverage 99%) [
55
].
Russula miyunensis
is similar to
R. uttarakhandia
A. Ghosh & K.
Das, without molecular data, but
R. uttarakhandia
has a yellow to grayish-yellow color in
the pileus middle, smaller basidia (28.5–37
×
12–15.6
µ
m), hymenial cystidia on lamellae
edges without color change in SV, two-layered pileipellis, the absence of hymenial cystidia
on lamellae edges, longer terminal cells of near the pileus margin (25–37 ×4–6 µm) [56].
Russula plana C. L. Hou, H. Zhou, &G. Q. Cheng, sp. nov.
Figures 7–10.
Figure 7.
Russula plana (BJTC Z1398). (
A
,
B
) Basidiomata. (
C
,
D
) Basidiospores. Scale bar:
(A,B) = 10 mm, (C,D)=1µm.
MycoBank: MB 845049
Diagnosis:
Russula plana is diagnosed by small-sized basidiomata, brick-red to deep
red pileus, large basidiospores ornamented with amyloid warts or spines, suprahilar spot
large, smaller basidia, longer terminal cells near the pileus margin, pileocystidia without
color change in sulfovanillin. Russula plana and Russula clavatohyphata P. Bhatt, A. Ghosh,
Buyck, and K. Das have similar morphological characteristics, but R. plana has brick-red to
deep red pileus and small basidia and bigger basidiospores.
Holotype: CHINA, Beijing, Miyun District, Sileng Mountain, 40◦28022” N, 117◦6017” E,
alt. 722 m, 30 August 2021, coll. C.-L.H., H.Z. and G.-Q.C. (BJTC Z1398).
J. Fungi 2022,8, 1283 14 of 33
Figure 8.
Microscopic features of Russula plana (BJTC Z1398). (
A
) Basidia. (
B
) Basidiola. (
C
) Marginal
cells. (
D
) Hymenial cystidia on lamellae sides. (
E
) Hymenial cystidia on lamellae edges. Scale bar:
10 µm.
Figure 9.
Microscopic features of Russula plana (BJTC Z1398). (
A
) Primordial hyphae near the pileus
margin. (
B
) Hyphal terminations near the pileus margin. (
C
) Primordial hyphae near the pileus
center. (D) Hyphal terminations near the pileus center. Scale bar: 10 µm.
Etymology:
The epithet “plana” refers to the flat pileus of the basidiomata after
maturity
.
Basidiomata:
small size, pileus 19–43 mm in diameter, initially hemispherical when
young, applanate with depressed in the center when mature, recurved in age, smooth, sticky
when wet, peeling to 1/5 of the radius. brick-red (#c62d42) to deep red (#622f30), sometimes
red (#ff1a1a), margin light pink (#d69188).
Lamellae:
cream (#ffffff), yellow (#ffffed) in
age, adnate to adnexed, lamellulae absent, hardly forked.
Stipe: 23–41 ×6–13 mm
, white
(#ffffff), cylindrical, smooth, firm.
Context:
5–10 mm thick in half of the pileus radius, white
(#ffffff), without color change when bruised. Spore print: not observed.
J. Fungi 2022,8, 1283 15 of 33
Figure 10.
Microscopic features of Russula plana (BJTC Z1398). (
A
) Basidiospores. (
B
) Hyphal
terminations near the pileus margin. (
C
) Hyphal terminations near the pileus center. Scale bar:
(A)=5µm; (B,C) = 10 µm.
Basidiospores:
(6.8–)7.2–7.9–8.6(–9.9)
×
(5.8–)6.1–6.7–7.3(–8.3)
µ
m, [Q = (1.02–)1.09–
1.18–1.27(–1.44)], subglobose to broadly ellipsoid, ornamentation of relatively of small,
dense [(5–)7–9(–10)] in a 3
µ
m diameter circle] amyloid warts or spines, 0.3–0.8
µ
m high,
occasionally with isolated verrucous, occasionally to frequently fused in pairs or short
chains [(0–)1–3(–4) in the circle], occasionally to frequently connected by short, fine line
connections [(0–)1–3(–4) in the circle], suprahilar spot large, amyloid.
Basidia:
(22–)23.4–
28.3–33.2(–38)
×
(10–)12.1–14–15.9(–18)
µ
m, 2–4-spored, mainly clavate, sometimes broadly
ellipsoid, with particles and oil droplets, basidiola broadly ellipsoid, clavate or subcylin-
drical, ca. 8–15
µ
m wide.
Hymenial cystidia:
dispersed, ca. 500–650/mm
2
.
Hymenial
cystidia on lamellae sides:
(42–)48.2–57.1–66(–70)
×
(8.1–)9–10.4–11.8(–13)
µ
m, clavate or
subfusiform, apically mainly obtuse, often with 3–5
µ
m long appendage, thin-walled; con-
tents with heteromorphous or granulose, turning grayish-red (#8b0000) in SV.
Hymenial
cystidia on lamellae edges:
smaller to hymenial cystidia on lamellae sides, (36–)39.2–43.3–
47.4(–50)
×
(6.5–)7.3–8.4–9.5(–10)
µ
m, clavate or subfusiform, sometimes subulate, apically
often obtuse or constricted, sometimes with 2–5
µ
m long appendage, refracted inclusions,
contents with heteromorphous or granulose, turning ash black (#080808) in SV.
Marginal cells:
(15–)20.2–25.5–30.8(–33)
×
(3.8–)3.1–4.8–5.7(–6.4)
µ
m, subfusiform or
irregular shape, sometimes flexible.
Pileipellis:
orthochromatic in cresyl blue, sharply
delimited from the underlying context, 80–120
µ
m deep, single-layered, weakly gelatinized,
relatively dense, intricate, horizontally oriented near the context, 4–9
µ
m wide hyphae.
Acid-resistant incrustations present, distinct on the terminal or subterminal cells of primor-
dial hyphae, occasionally on terminal cells. Hyphal terminations near the pileus margin
occasionally branched, sometimes flexuous, thin-walled; terminal cells (13–)13.4–17.5–
21.6(–26)
×
(3.8–)4.2–5.2–6.2(–7.8)
µ
m, cylindrical, clavate, subfusiform or irregular shape,
apically mainly obtuse, sometimes constricted or inflated, less forked, subterminal cells ca.
3–5
µ
m wide, occasionally branched; hyphal terminations near the pileus center similar
to those near the pileus margin; terminal cells (8.4–)12–18–24(–35)
×
(3.0–)3.7–4.3–4.9
µ
m,
cylindrical, clavate, subfusiform, subulate or irregular shape, apically obtuse, sometimes
constricted or inflated; subterminal cells often wider, occasionally branched, ca. 3–6
µ
m
wide. Primordial hyphae near the pileus margin are always single-celled, sometimes
2–3
celled, terminal cells (11–)14.9–21.4–27.9(–40)
×
(3.0–)3.7–4.3–4.9(–5.4)
µ
m, thin-walled,
mainly cylindrical, apically usually obtuse, sometimes attenuated; contents with less
heteromorphous-granulose, no color change in SV. Primordial hyphae near the pileus center
are often smaller, always single-celled, thin-walled, (15–)16.4–21.7–27(–32)
×(3.0–)
3.4–3.9–
J. Fungi 2022,8, 1283 16 of 33
4.4(–5.2)
µ
m, clavate, apically typically obtuse or occasionally attenuated, contents with
heteromorphous-granulose. Cystidioid hyphae or oleiferous hyphae: not observed.
Habit and habitat:
Individual or scattered in broad-leaved forests such as B. costata
and P. davidiana trees.
Additional specimens examined:
CHINA, Hebei Province, Chengde City, Xinglong
County, Baboziling, 40
◦
18
0
36” N, 117
◦
35
0
6” E, alt. 880 m, 20 August 2021, coll. C.-L.H.,
R.-T.Z. and G.-Q.C. (BJTC T2101).
Notes:
Russula plana belongs to subsection Chamaeleontinae. Phylogenetic analy-
ses showed that R. plana,
R. olivascens
and R. miyunensis are closely related (Figure 1).
Morphologically, R. miyunensis has light yellow to grayish-yellow, dark red and dark
brown color in the pileus middle, colorless on the stipe, larger basidia (36.2–40.8
×
10.4–13.4 µ
m) than
R. plana
, hymenial cystidia on lamellae sides turning light brown in
SV.
Russula olivascens
has light green-yellow pileus, bigger basidia (39–52
×
12–15
µ
m)
than R. plana [
57
].
Russula plana
is similar to
R. clavatohyphata
, which without molecular
data, but
R. clavatohyphata
has short warty striate on the edge of the pileus, forked lamellae
near the stipe, bigger basidia (22–54
×
9–13
µ
m) and smaller basidiospores (6.34–7.63
×
5.53–6.7 µm), hymenial cystidia on lamellae edges without color change in SV [30].
Russula sinoparva C. L. Hou, H. Zhou, &G. Q. Cheng, sp. nov.
Figures 11–14.
Figure 11.
Russula sinoparva (BJTC ZH441). (
A
,
B
) Basidiomata. (
C
,
D
) Basidiospores. Scale bar:
(A,B) = 10 mm, (C,D)=5µm.
J. Fungi 2022,8, 1283 17 of 33
Figure 12.
Microscopic features of Russula sinoparva (BJTC ZH441). (
A
) Basidia. (
B
) Basidiola.
(C) Marginal cells. (D) Hymenial cystidia on lamellae sides. Scale bar: 10 µm.
Figure 13.
Microscopic features of Russula sinoparva (BJTC ZH441). (
A
) Pileocystidia near the pileus
margin. (
B
) Hyphal terminations near the pileus margin. (
C
) Pileocystidia near the pileus center.
(D) Hyphal terminations near the pileus center. Scale bar: 10 µm.
MycoBank: MB 845048
Diagnosis:
Russula sinoparva is diagnosed by small basidiomata, light pink to pink
pileus, subglobose to broadly ellipsoid basidiospores ornamented with small amyloid
warts, the absence of hymenial cystidia on lamellae edges, bigger hymenialcystida on
lamellae sides. Russula sinoparva and Russula cessans A. Pearson have similar morphological
characteristics, but
R. sinoparva
has light pink to pink pileus and smaller basidiospore, and
bigger hymenial cystidia on lamellae sides.
J. Fungi 2022,8, 1283 18 of 33
Figure 14.
Microscopic features of Russula sinoparva (BJTC ZH441). (
A
) Basidiospores. (
B
) Hyphal
terminations near the pileus margin. (
C
) Hyphal terminations near the pileus center. Scale bar:
(A)=5µm; (B,C) = 10 µm.
Holotype:
CHINA, Beijing, Huairou District, Erdaogou Village, 40
◦
52
0
23.8” N,
116◦31022.4” E, alt. 758 m, 20 August 2019, coll. X.-Y.S., H.Z. and R.-T.Z. (BJTC Z441).
Etymology:
The epithet “sinoparva“ refers to this Chinese species that has smaller
basidiomata resembling the Russula parva Carteret & Reumaux.
Basidiomata:
small size, pileus 18–30 mm in diameter, initially convex lenticular
when young, flattened when mature, margin striations with small verrucas, sharp, cracked
margin not obvious, light pink (#ffb6c1) to pink (#ffc0cb), central dark red (#ff0000) to
strong deep red (#985144).
Lamellae:
white (#ffffff) to light yellow-brown (#ffffed), with
7–10 gills per cm at the edges, brittle, unequal, hardly forked.
Stipe:
28–54
×
8–15 mm,
white (#ffffff), sometimes brownish (#a52a2a), subcylindrical, smooth, firm, dilate gradually
at the base.
Context:
4–8 mm thick in half of the pileus radius, white (#ffffff) without color
change when bruised. Spore print: not observed.
Basidiospores:
(5.6–)6.5–7.0–7.6(–8.4)
×
(5.4–)5.8–6.3–6.7(–7.2)
µ
m, [Q = (1.01–)1.04–
1.13–1.21(–1.35)], subglobose to broadly ellipsoid, starchy ornamented, ornamentation of
relatively small, moderately distant [(4–)5–7(–8) in a 3
µ
m diameter circle] amyloid warts,
0.3–1.0
µ
m high, occasionally to frequently fused in pairs or triplets, short-branched chains
[(0–)1–3 (–4) in the circle], frequently connected by short or long, fine line connections
[(0–)1–3 in the circle], suprahilar spot small.
Basidia:
(28–)29.6–34.5–39.4(–45)
×
(9–)10.5–
11.8–13.1(–14)
µ
m, 2–4-spored, clavate or fusiform, with particles and oil droplets, basidiola
clavate or subcylindrical, ca. 5–15
µ
m wide.
Hymenial cystidia:
widely dispersed, ca.
200–300/mm
2
.
Hymenial cystidia on lamellae sides:
(30–)40.2–49.6–59.1(–67)
×
(7.2–)8.5–
10–11.6(–13)
µ
m, clavate or fusiform, apically often obtuse or mucronate, sometimes with
3–5-
µ
m-long appendage, contents with refracted inclusions, or sometimes with granulose
or crystalline, turning ash black (#0d0d0d) in SV.
Hymenial cystidia on lamellae edges:
not observed.
Pileipellis:
orthochromatic in cresyl blue, sharply delimited from the underlying con-
text, 70–100
µ
m deep, two-layered. Suprapellis 30–60
µ
m deep, strongly gelatinized, made
up of ascending to erect, and slight interlaced hyphae. Subpellis 50–70
µ
m deep, composed
of horizontally oriented, relatively dense, intricate, 3–6-
µ
m-wide hyphae. Hyphal termi-
nations near the pileus margin occasionally branched, sometimes flexuous, thin-walled;
terminal cells (7.5–)14.7–23.5–32.4(–44)
×
(2.1–)2.6–3.4–4.1(–5.0)
µ
m, mainly subcylindrical
or clavate, apically mainly obtuse, occasionally attenuated, subterminal cells often wider,
ca. 2–6
µ
m wide, always unbranched; hyphal terminations near the pileus center similar
to those near the pileus margin; terminal cells (9–)16.7–31.9(–38)
×
(2.8–)3.1–4.3(–5.2)
µ
m,
mainly subcylindrical, occasionally ellipsoid, apically obtuse, constricted or attenuated;
J. Fungi 2022,8, 1283 19 of 33
subterminal cells often wider, ca. 3–6
µ
m, always unbranched. Pileocystidia near the pileus
margin are always 2–5-celled, a few one-celled, terminal cells (12–)18.1–32.6–47.2(–61)
×
(3.7–)4.7–5.9–7.2(–8.1)
µ
m, thin-walled, mainly cylindrical or subcylindrical, occasionally
clavate, apically usually obtuse, contents with granulose-heteromorphous, turning light
ash black (#0d0d0d) in SV. Pileocystidia near the pileus center are often smaller, always
2–6-celled, thin-walled, terminal cells (12–)21.4–29.6–37.8(–45)
×
(4.8–)5.0–5.6–6.2(–7.2)
µ
m,
clavate or cylindrical, apically typically obtuse or occasionally attenuated, contents with
granulose or occasionally crystalline.
Cystidioid hyphae:
in subpellis and context with
heteromorphous-granulose contents, oleiferous hyphae in the subpellis close to the context.
Habit and habitat:
Individual or scattered in coniferous forests and mixed coniferous
and broad-leaved forests of Pinus tabuliformis Carr. and Juglans mandshurica Maxim.
Additional specimens examined:
CHINA, Beijing, Huairou District, Sunzhazi Village,
40
◦
56
0
39.1” N, 116
◦
30
0
23.4” E, alt. 780 m, 25 August 2020, coll. C.-L.H., R.-T.Z. and G.-Q.C.
(BJTC C540).
Notes:
Russula sinoparva belongs to the subsection Puellarinae Singer. Phylogenetic
analyses revealed that
R. sinoparva
is related to R. odorata,R. khinganensis, and
R. subversatilis
(new species in this paper) (Figures 1and 2). Morphologically, they are somewhat similar
in pileus shape and basidia size. However,
R. sinoparva
is diagnosed by the light pink
to pink, central dark red to deep red pileus, strongly gelatinized suprapellis, 1–3-celled
pileocystidia near the pileus margin; R. odorata is distinguished from
R. sinoparva
by the
central brown or olive pileus and irregularly bifurcated lamellae.
R. khinganensis
by the
livid brown or deep livid brown to russet vinaceous pileus and thicker pileipellis [
24
], and
R. subversatilis
by the light gray-red to deep red, central yellowish-brown to dark red pileus,
bigger basidia and hymenial cystidia on lamellae sides. Russula cessans, which is without
molecular data, is similar to
R. sinoparva
in lamellae color and density, but it has a pileus of
black color in the middle and smooth, unstriped edges, bigger spores (8–9
×
7–8
µ
m) and
smaller hymenial cystidia on lamellae sides (7–9 µm) [58].
Russula sinorobusta C. L. Hou, H. Zhou, &G. Q. Cheng, sp. nov.
Figures 15–18.
MycoBank: MB 845050
Diagnosis: Russula sinorobusta
is diagnosed by small to medium-sized basidiomata,
gray-red to rose red, central deep red pileus, basidiospores ornamented with small amy-
loid warts, suprahilar spot small, longer basidia, shorter hymenial cystidia on lamellae
sides, pileocystidia absent. Morphologically,
R. sinorobusta
is similar to R. intermedia and
Russula vinosa
Lindblad., but
R. sinorobusta
has gray-red to rose red, central deep red pileus,
and smaller basidiospore.
Holotype:
CHINA, Beijing, Changping District, Yanshou Temple, 40
◦
22
0
23.3” N,
116◦19022.3” E, alt. 270 m, 14 August 2019, coll. J.-Q.L. and H.Z. (BJTC Z052).
Etymology
: The epithet “sinorobusta” refers to the stipe of this Chinese species that is
relatively sturdy, resembling the Russula robusta R. Heim.
Basidiomata
: small to medium size, pileus 51–82 mm in diameter, initially hemispher-
ical when young, applanate with depressed in the center when mature, sometimes convex,
slightly curved in edges, smooth when young, wrinkle in age, sticky when wet, peeling to
1/5 of the radius. gray-red (#8e6f70) to rose red (#b57281), sometimes deep red (#3b1f1f) in
the center.
Lamellae:
white (#ffffff) to light yellow-brown (#ffffed), with 9–11 gills per cm
at the edges, adnate, equal, lamellulae absent, hardly forked.
Stipe:
60–102
×
19–34 mm,
white (#ffffff), cylindrical, becoming hollow when mature, slightly inflated near the base,
longitudinally striate.
Context:
13–21 mm thick in half of the pileus radius, white (#ffffff),
without color change when bruised. Spore print: not observed.
Basidiospores:
(5.7–)6.2–6.6–7(–7.4)
×
(5.3–)5.5–5.9–6.3(–7.3)
µ
m, [Q = (1.01–)1.06–
1.12–1.18(–1.22)], subglobose to broadly ellipsoid, ornamentation of relatively of small, mod-
erately distant to dense [(4–)5–8(–10)] in a 3
µ
m diameter circle] amyloid warts,
0.2–0.7 µ
m
high, with abundant isolated verrucous, occasionally fused in pairs, triplets or short chains
[0–2(–3) in the circle], occasionally connected by short, fine line connections [0–2(–3) in
J. Fungi 2022,8, 1283 20 of 33
the circle], suprahilar spot small, weakly amyloid.
Basidia:
(35–)41.1–46–50.9(–57)
×
(11–)11.4–12.5–13.6(–14)
µ
m, 2–4-spored, clavate or broadly ellipsoid, with particles and
oil droplets, basidiola clavate or subcylindrical, ca. 6–10
µ
m wide.
Hymenial cystidia:
moderately numerous, ca. 720–900/mm
2
.
Hymenial cystidia on lamellae sides:
(60–)70.9–
80.3–89.7(–94)
×
(10–)10.4–11.1–11.8(–12)
µ
m, thin-walled, clavate or fusiform, apically
mainly obtuse, occasionally mucronate or constricted, with 3–7-
µ
m-long appendage; con-
tents with granulose or banded, turning gray (#808080) to grayish purple in SV.
Hymenial
cystidia on lamellae edges:
smaller and narrower to hymenial cystidia on lamellae sides,
(40–)43.1–50–56.9(–63)
×
(6.0–)6.4–7.5–8.6(–10)
µ
m, clavate or subcylindrical, apically often
obtuse, sometimes with 2–4 µm long appendage, contents with granulose or banded.
Figure 15. Russula sinorobusta
(BJTC Z052). (
A
–
D
) Basidiomata. (
E
,
F
) Basidiospores. Scale bar:
(A–D) = 10 mm, (E,F)=1µm.
Marginal cells:
(14–)14.9–20.6–26.3(–33)
×
5.8–6.5–7.2(–8.1)
µ
m, cylindrical orclavate.
Pileipellis:
orthochromatic in cresyl blue, sharply delimited from the underlying context,
100–190
µ
m deep, two-layered. Suprapellis 50–100
µ
m deep, weakly gelatinized, composed
of ascending to erect hyphae, trichoderm. Subpellis 45–90
µ
m deep, strongly gelatinized,
composed of horizontally oriented, relatively dense, intricate, 3–9-
µ
m wide hyphae. Hyphal
terminations near the pileus margin occasionally branched, sometimes flexuous, thin-
walled; terminal cells (14–)14.3–57.6(–62)
×
2–4
µ
m, mainly cylindrical or subcylindrical,
apically obtuse, subterminal cells often wider, ca. 2–3
µ
m wide, always unbranched;
Hyphal terminations near the pileus center similar to those near the pileus margin; terminal
cells (15–)15.6–45.3(–47.8)
×
(2–)3–5
µ
m, cylindrical, apically obtuse; subterminal cells
J. Fungi 2022,8, 1283 21 of 33
often wider, always unbranched, ca. 2–3
µ
m wide. Pileocystidia not observed.
Cystidioid
hyphae or oleiferous hyphae: not observed.
Figure 16.
Microscopic features of
Russula sinorobusta
(BJTC Z052). (
A
) Basidia. (
B
) Basidiola.
(
C
) Marginal cells. (
D
). Hymenial cystidia on lamellae sides. (
E
) Hymenial cystidia on lamellae edges.
Scale bar: 10 µm.
Figure 17.
Microscopic features of
Russula sinorobusta
(BJTC Z052). (
A
) Hyphal terminations near the
pileus margin. (B) Hyphal terminations near the pileus center. Scale bar: 10 µm.
J. Fungi 2022,8, 1283 22 of 33
Figure 18.
Microscopic features of
Russula sinorobusta
(BJTC Z052). (
A
) Basidiospores. (
B
) Hyphal
terminations near the pileus margin. (
C
) Hyphal terminations near the pileus center. Scale bar:
(A)=5µm; (B,C) = 10 µm.
Habit and habitat:
Individual or scattered in broad-leaved forests of
Castanea mollissima
Blume.
Additional specimens examined:
CHINA, Beijing, Changping District, Yanshou Tem-
ple, 40
◦
22
0
23.3” N, 116
◦
19
0
22.5” E, alt. 270 m, 14 August 2019, coll. J.-Q.L. and H.Z. (BJTC
Z050); CHINA, Beijing, Changping District, Yanshou Temple, 40
◦
22
0
7.4” N, 116
◦
19
0
21.7” E,
alt. 223 m, 26 July 2019, coll. G.-Q.C. and H.Z. (BJTC Z662).
Notes: Russula sinorobusta
belongs to subsection Roseinae Singer ex Sarnari. Multi-loci
phylogenetic analysis showed that
R. sinorobusta
,R. minutula and R. rosea are closely re-
lated (Figure 1). Russula sinorobusta may be related to Russula lepidicolor Romagn. and
Russula intermedia
P. Karst., but not have supported value in ITS tree (Figure 2). Morpho-
logically,
R. sinorobusta
is similar to R. intermedia and R. vinosa, but R. vinosa has a short
and fuzzy striate on the edge of the pileus, the pileus middle color is copper, ochre, or
brown, and the lamellae is close to the stipe forked, stipe hollow, larger basidiospores
(8–11.5
×
6.5–8.5
µ
m) and hymenial cystidia on lamellae sides (85–120
×
10–13
µ
m)
than
R. sinorobusta
[
55
]. Russula intermedia has wider hymenial cystidia on lamellae edges
(
9–11 µ
m) than
R. sinorobusta
, the width of pileocystidia is 4–11
µ
m, and with lilac color in
SV [39].
Russula subversatilis C. L. Hou, H. Zhou, &G. Q. Cheng, sp. nov.
Figures 19–22.
MycoBank: MB 845051
Diagnosis: Russula subversatilis
is diagnosed by light gray-red to deep red, central
yellowish-brown to dark red pileus, basidiospores ornamented with amyloid warts or
spines, and more or less reticulate or chain-like, bigger basidia and hymenial cystidia on
lamellae sides, light red pileocystidia in sulfovanillin.
Russula subversatilis
and R. versatilis
Romagn have similar morphological characteristics, but
R. subversatilis
has light gray-
red to deep red, central yellowish-brown to dark red pileus, shorter basidiospore, and
narrower pileocystidia.
Holotype:
CHINA, Beijing, Miyun District, Heilongtan, 40
◦
33
0
38.1” N, 116
◦
46
0
55.8” E,
alt. 255 m, 27 August 2020, coll. C.-L.H. and G.-Q.C. (BJTC C653).
J. Fungi 2022,8, 1283 23 of 33
Figure 19. Russula subversatilis
(BJTC C653). (
A
,
B
) Basidiomata. (
C
,
D
) Basidiospores. Scale bar:
(A,B) = 10 mm, (C,D)=1µm.
Figure 20.
Microscopic features of
Russula subversatilis
(BJTC C653). (
A
) Basidia. (
B
) Basidiola.
(
C
) Marginal cells. (
D
) Hymenial cystidia on lamellae sides. (
E
) Hymenial cystidia on lamellae edges.
Scale bar: 10 µm.
J. Fungi 2022,8, 1283 24 of 33
Figure 21.
Microscopic features of
Russula subversatilis
(BJTC C653). (
A
) Pileocystidia near the pileus
margin. (
B
) Hyphal terminations near the pileus margin. (
C
) Pileocystidia near the pileus center.
(D) Hyphal terminations near the pileus center. Scale bar: 10 µm.
Figure 22.
Microscopic features of
Russula subversatilis
(BJTC C653). (
A
) Basidiospores. (
B
) Hyphal
terminations near the pileus margin. (
C
) Hyphal terminations near the pileus center. Scale bar:
(A)=5µm; (B,C) = 10 µm.
Etymology:
The epithet “subversatilis” refers to its morphological similarity to
Russula versatilis Romagn.
Basidiomata:
small to medium size, pileus 32–55 mm in diameter, initially hemispher-
ical when young, flattened when mature, slightly concave in the middle, slightly curved in
the margin, sticky when wet, with inconspicuous striations, margin light gray-red (#b09a95)
to deep red (#985144), central yellowish-brown (#aa8d6f) to dark red (#481c1c).
Lamellae:
white (#ffffff) to light yellow-brown (#ffffed), with 5–7 gills per cm at the edges, free, brittle,
lamellulae absent, hardly forked.
Stipe:
35–65
×
15–20 mm, white (#ffffff), sometimes
with brownish (#a52a2a) on the base, cylindrical, smooth, firm.
Context:
8–14 mm thick in
half of the pileus radius, white (#ffffff), without color change when bruised. Spore print:
not observed.
Basidiospores:
(6.1–)6.6–7.1–7.6(–8.2)
×
(5.3–)5.7–6.1–6.6(–7.3)
µ
m, [Q = (1.02–)1.09–
1.17–1.25(–1.32)], subglobose to broadly ellipsoid, ornamentation of relatively small, mod-
erately distant to dense [(5–)6–9(–10) in a 3
µ
m diameter circle] amyloid warts or spines,
J. Fungi 2022,8, 1283 25 of 33
0.4–0.9
µ
m high, occasionally formed reticulate, occasionally to frequently fused in short or
long branched chains [(0–)1–3 (–5) in the circle], occasionally connected by short or long,
fine line connections [(0–)1–2(–3) in the circle], suprahilar spot small, amyloid.
Basidia:
33.5–37–40.5(–45.2)
×
(11.8–)12.6–13.6–14.5(–15.2)
µ
m, 2–4-spored, clavate, with particles
and oil droplets, basidiola clavate or subcylindrical, ca. 9–14
µ
m wide.
Hymenial cystidia:
moderately numerous, ca. 950/mm
2
.
Hymenial cystidia on lamellae sides:
(47.6–)53.2–
58.7–64.2 (–65.3)
×
(9.2–)10.5–11.9–13.3(–14.1)
µ
m, clavate or subfusiform, apically mainly
obtuse, often with 5–7-
µ
m-long appendage, thin-walled; contents with heteromorphous-
crystalline or granulose, mainly in the middle and upper part, turning purple (#800080)
in SV.
Hymenial cystidia on lamellae edges:
similar to hymenial cystidia on lamellae
sides, (36.5–)42.7–49.5–56.3(–64.4)
×
(6.9–)7.4–8.5–9.6(–10.1)
µ
m, clavate or subfusiform,
apically often obtuse, sometimes with 2–6-
µ
m-long appendage, contents with granulose or
crystalline, turning purple (#800080) in SV.
Marginal cells:
(14.2–)15.6–17.8–20(–21.5)
×
(7.8–)8.4–9.2–10.1(–11.4)
µ
m, usually
broadly clavate and shorter than basidiola.
Pileipellis:
orthochromatic in cresyl blue,
sharply delimited from the underlying context, 90–140
µ
m deep, two-layered. Suprapellis
40–60
µ
m deep, less gelatinized, composed of relatively loose, ascending to erect hyphae.
Subpellis 60–100
µ
m deep, strongly gelatinized, composed of relatively dense, intricate, hor-
izontally oriented near context, 2–7
µ
m wide hyphae. Hyphal terminations near the pileus
margin occasionally branched, sometimes flexuous, thin-walled; terminal cells
(12.4–)
16.1–
21.9–27.7(–32.4)
×
(2.0–)2.5–3.3–4.1(–5.1)
µ
m, mainly cylindrical, sometimes clavate or
fusiform, apically obtuse or constricted, subterminal cells often wider, ca. 2–4
µ
m wide,
occasionally branched; hyphal terminations near the pileus center similar to those near the
pileus margin; terminal cells (10.2–)12.9–23.5(–28.7)
×
(2.0–)2.3–4.1(–4.9)
µ
m, cylindrical or
subfusiform, apically obtuse, sometimes attenuated or constricted; subterminal cells often
wider, occasionally branched, ca. 2–5
µ
m wide. Pileocystidia near the pileus margin are
always 2–3 celled, sometimes one-celled, thin-walled, terminal cells (30.2–)35–67.8(–88.4)
×
(3.0–)3.5–5.3(–6.1)
µ
m, cylindrical, subclavate or subfusiform, apically usually obtuse, some-
times attenuated, contents with abundant, heteromorphous, granulose or occasionally
crystalline, turning light ash black (#0d0d0d) to light red (#ff4d4d) in SV. Pileocystidia
near the pileus center are often smaller, always 2–3-celled, thin-walled, (21.4–)25.5–60.7(–
78.1)
×
(3.8–)4.1–5.7(–6.0)
µ
m, cylindrical or subclavate, apically obtuse, contents with
heteromorphous, granulose. Cystidioid and oleiferous hyphae: not observed.
Habit and habitat: Individual in broad-leaved forests of Carpinus turczaninowii.
Additional specimens examined:
CHINA, Beijing, Miyun District, Heilongtan,
40
◦
33
0
38.2” N, 116
◦
46
0
56.2” E, alt. 265 m, 27 August 2020, coll. C.-L.H. and G.-Q.C.
(BJTC T2001).
Notes: Russula subversatilis
belongs to the subsection Puellarinae. The phylogenetic
trees (Figures 1and 2) show that
R. subversatilis
is closely related to Russula carpini R.
Girard & Heinem, Russula khinganensis G.J. Li & R.L. Zhao, and
Russula solaris
Ferd. &
Winge, but R. carpini has light brownish purple or yellow pileus, bigger basidiospores
(
7–10 ×6.5–8 µ
m) [
57
],
R. khinganensis
has thinner basidia (35–43
×
10–11
µ
m), and hy-
menial cystidia on lamellae sides (51–65
×
6–9
µ
m), no hymenial cystidia on lamellae edges [
24
],
R. solaris has pale orange to tinged yellowish pileus, bigger basidia (
40–52 ×12–14 µm
) and
basidiospores (7.5–9
×
6.5–7.5
µ
m) [
59
]. Morphologically, R. versatilis, which is without
molecular data, is similar to
R. subversatilis
in light gray-red pileus, light yellow-brown
lamellae, and basidiospores with isolated warts or spines. However, R. versatilis has a pink
or cream color in the middle pileus, longer basidiospores (7–8.5
×
5–6
µ
m), and wider
pileocystidia (6–8 µm) [60].
Russula yanshanensis C. L. Hou, H. Zhou, &G. Q. Cheng, sp. nov.
Figures 23–26.
J. Fungi 2022,8, 1283 26 of 33
Figure 23.
Russula yanshanensis (BJTC C561). (
A
,
B
) Basidiomata. (
C
,
D
) Basidiospores. Scale bar:
(A,B) = 10 mm, (C,D)=1µm.
MycoBank: MB 845052
Diagnosis: Russula yanshanensis diagnosed by light pink to pink, central light yellow
to yellowish-brown pileus, smaller basidiospores ornamented with amyloid warts, and
frequently chain-like, shorter hymenial cystidia on lamellae sides and hymenial cystidia on
lamellae edges. Russula yanshanensis and Russula cremeirosea Murrill have similar morpho-
logical characteristics,but
R. yanshanensis
has pink, central light yellow to yellowish-brown
pileus, shorter basidiospore, shorter hymenial cystidia on lamellae sides and hymenial
cystidia on lamellae edges.
Holotype:
CHINA, Beijing, Huairou District, Sunzhazi Village, 40
◦
56
0
35” N, 116
◦
30
0
26” E,
alt. 763 m, 20 August 2019, coll. C.-L.H., J.-Q.L. and G.-Q.C. (BJTC C561).
Etymology:
The epithet “yanshanensis” refers to the locality where the type specimen
was collected.
Basidiomata:
small to medium size, pileus 21–53 mm in diameter, initially hemi-
spherical to convex when young, applanate with slightly depressed in the center when
mature, not obvious striations or no striations in the margin, sticky when wet, peeling to
1/3 of the radius, margin light pink (#ffb6c1) to pink (#ffc0cb), sometimes red (#ff1a1a),
central light yellow (#ffffed) to yellowish-brown (#aa8d6f).
Lamellae:
white (#ffffff) to light
yellow-brown (#ffffed), with 6–9 gills per cm at the edges, free, brittle, unequal, lamellulae
absent, hardly forked.
Stipe:
31–60
×
10–20 mm, white (#ffffff), sometimes with brownish
J. Fungi 2022,8, 1283 27 of 33
(#a52a2a) on the base, cylindrical, inflated toward the base, hollow, longitudinally striate.
Context:
5–11 mm thick in half of the pileus radius, white (#ffffff), without color change
when bruised. Spore print: not observed.
Figure 24.
Microscopic features of Russula yanshanensis (BJTC C561). (
A
) Basidia. (
B
) Basidiola.
(
C
) Marginal cells. (
D
) Hymenial cystidia on lamellae sides. (
E
) Hymenial cystidia on lamellae edges.
Scale bar: 10 µm.
Figure 25.
Microscopic features of Russula yanshanensis (BJTC C561). (
A
) Pileocystidia near the pileus
margin. (
B
) Hyphal terminations near the pileus margin. (
C
) Pileocystidia near the pileus center.
(D) Hyphal terminations near the pileus center. Scale bar: 10 µm.
Basidiospores:
(5.6–)6.1–6.6–7.1(–7.5)
×
(5.1–)5.5–5.8–6.1(–6.4)
µ
m, [Q = (1.03–)1.07–
1.14–1.21(–1.29)], subglobose to broadly ellipsoid, ornamentation of relatively small, dense
[7–10(–11)] in a 3
µ
m diameter circle] amyloid warts, 0.2–0.6
µ
m high, occasionally with
isolated warts, occasionally to frequently fused in short or long branched chains [(0–)1–3(–4)
in the circle], frequently connected by short or long fine line connections [(0–)1–4(–5) in the
circle], suprahilar spot not obvious, amyloid or weakly amyloid.
Basidia:
(34–)34.6–37.7–
40.8(–47)
×
(11–)11.4–12.5–13.6(–15)
µ
m, 2–4-spored, clavate, with particles and oil droplets,
J. Fungi 2022,8, 1283 28 of 33
basidiola clavate or subcylindrical, ca. 8–13
µ
m wide.
Hymenial cystidia:
disperse, ca.
550/mm
2
.
Hymenial cystidia on lamellae sides:
(36–)37.5–50–62.5(–68)
×
(6.4–)7.1–8.3–
9.5(–11)
µ
m, thin-walled, clavate, subcylindricalor subfusiform, apically mainly obtuse,
often with 2–4
µ
m long appendage; contents with heteromorphous-granulose or banded
turning reddish brown (#a52a2a) in SV.
Hymenial cystidia on lamellae edges:
smaller
to hymenial cystidia on lamellae sides, (30–)32.7–37.3–41.9(–45)
×
(7.0–)7.1–8–8.9(–9)
µ
m,
subclavate or fusiform, apically occasionally mucronate, sometimes with 2–7
µ
m long
appendage, contents with heteromorphous-granulose or a few refractive, turning reddish
brown (#a52a2a) in SV.
Figure 26.
Microscopic features of Russula yanshanensis (BJTC C561). (
A
) Basidiospores. (
B
) Hyphal
terminations near the pileus margin. (
C
) Hyphal terminations near the pileus center. Scale bar:
(A)=5µm; (B,C) = 10 µm.
Marginal cells:
(13.7–)14.6–17.3–19.9(–22.3)
×
(4.9–)5.7–6.5–7.2(–8.1)
µ
m, cylindrical
or ellipsoid.
Pileipellis:
orthochromatic in cresyl blue, sharply delimited from the un-
derlying context, 50–80
µ
m deep, two-layered, less gelatinized. Suprapellis 40–60
µ
m
deep, composed of ascending hyphae. Subpellis 20–35
µ
m deep, composed of horizontally
oriented, intricate, 2–10
µ
m wide hyphae. Hyphal terminations near the pileus margin
rarely branched, sometimes flexuous, thin-walled; terminal cells (13–)15.5–28.7–41.9(–52)
×
(2.0–)2.5–3.2–3.9(–4.1)
µ
m, cylindrical, subfusiform, less lageniform, occasionally flexible,
apically obtuse, sometimes attenuated or constricted, subterminal cells often wider, ca.
2–4
µ
m wide, always unbranched; hyphal terminations near the pileus center similar to
those near the pileus margin; terminal cells (9.2–)10.4–19.4–28.4(–33.6)
×
(2.0–)2.2–3–3.8(–
4.1)
µ
m, mainly subcylindrical, less lageniform, apically obtuse; sometimes attenuated or
constricted, subterminal cells often wider, always unbranched, ca. 2–4
µ
m wide. Pileo-
cystidia near the pileus margin are always 2–3-celled, sometimes one-celled, thin-walled,
sometimes subpellis extends to suprapellis, terminal cells (23.8–)25.6–39.4–53.2(–65.2)
×
(5.0–)5.4–7.6–8(–9.1)
µ
m, cylindrical or clavate, apically usually obtuse; contents with abun-
dant granulose or heteromorphous-crystalline, have weakly reaction turning light ash
black (#0d0d0d) to light red (#ff4d4d) in SV. Pileocystidia near the pileus center simiar to
the pileus margin, usually 2–3-celled, thin-walled, (20.2–)18.6–25.1–31.6(–39.8)
×
6–6.7–
9
µ
m, clavate, apically obtuse, contents with granulose or crystalline.
Cystidioid hyphae:
in subpellis and context with granulose or crystalline contents. Oleiferous hyphae in
the subpellis.
Habit and habitat:
Individual or scattered in coniferous or broad-leaved forests such
as P. tabuliformis Carr., Betula costata Trautv. And Populus davidiana Dode trees.
Additional specimens examined:
CHINA, Beijing, Huairou District, Sunzhazi Village,
40
◦
56
0
40.5” N, 116
◦
30
0
25.2” E, alt. 763 m, 20 August 2019, coll. C.-L.H., J.-Q.L. and
G.-Q.C. (BJTC L349); CHINA, Beijing, Miyun District, Sileng Mountain, 40
◦
28
0
23” N,
117
◦
6
0
17” E, alt. 709 m, 30 August 2021, coll. C.-L.H., H.Z. and G.-Q.C. (BJTC Z1390);
CHINA, Beijing, Miyun District, Sileng Mountain, 40
◦
28
0
24” N, 117
◦
6
0
32” E, alt. 663 m,
30 August 2021, coll. C.-L.H., H.Z. and G.-Q.C. (BJTC Z1385); CHINA, Beijing, Huairou
District, Xiaozhuanghu Village, 40
◦
52
0
35.6” N, 116
◦
31
0
16.6” E, alt. 804 m, 20 August 2019,
J. Fungi 2022,8, 1283 29 of 33
coll. H.Z. and X.-Y.S. (BJTC Z421); CHINA, Beijing, Huairou District, Sunzhazi Village,
40
◦
56
0
35.6” N, 116
◦
30
0
26.0” E, alt. 779 m, 25 August 2020, coll. C.-L.H., H.Z. and G.-Q.C.
(BJTC C561); CHINA, Beijing, Yanqing District, Sijihuahai, 40
◦
33
0
26” N, 116
◦
20
0
28” E, alt.
733 m, 4 August 2021, coll. H.Z. and G.-Q.C. (BJTC Z1305); CHINA, Beijing, Yanqing
District, Yudu Mountain, 40
◦
33
0
5” N, 115
◦
52
0
15” E, alt. 978 m, 31 August 2021, coll. C.-L.H.,
H.Z. and G.-Q.C. (BJTC Z1448).
Notes:
Russula yanshanensis belongs to the subsection Puellarinae. Specimens of
R. yanshanensis
were placed in a high-support branch on the phylogenetic tree and prob-
ably related to R. puellaris (Figures 1and 2). Russula puellaris can be distinguished from
R. puellaris by its thinner basidiospores (28–43
×
9–12
µ
m), larger hymenial cystidia on
lamellae sides (40–85
×
8–12), and turning gray in SV [
55
]. Morphologically, compare
with similar species without molecular data. Russula yanshanensis is easy to be confused
with
R. cremeirosea
in the appearance of basidiomata, but
R. cremeirosea
has bigger basid-
iospores (8–11
×
7.5–10
µ
m), longer hymenial cystidia on lamellae sides (50–76
×
3–10
µ
m),
hymenial cystidia on lamellae edges (42–48 ×7–9 µm) and without pileocystidia [61].
4. Discussion
The topological structure of the two trees of the nrITS phylogenetic analysis (Figure 1)
and the nrLSU-rpb2-tef-1
α
-mtSSU phylogenetic analysis (Figure 2) are basically similar, but
the Bayesian posterior probability values and maximum likelihood bootstrap were higher
in the nrLSU-rpb2-tef-1
α
-mtSSU analysis. In recent studies, many new species of Russula
have been described only by nrITS loci phylogenetic analysis [
14
,
25
,
62
], which also results
in the lack of other gene sequences and may cause some difficulties when performing
multi-gene phylogenetic analysis. Therefore, it is crucial to discover better-differentiated
DNA barcodes within the subgenus Russula in subsequent studies.
Through the current investigation, most species of the Russula were found in broad-
leaved forests and associated with Carpinus turczaninowii, Castanea mollissima,J. mandshurica,
B. costata, and P. davidiana trees, few species of the Russula occurred in coniferous forests,
such as P. tabuliformis. The distributing characteristics may be related to the large area of
broad-leaved forest in the Yanshan Mountains.
Russula Subgenus Russula has a very high species richness worldwide. At least
50 novel species have been described based on both morphological characters and molec-
ular data since 2006, of which at least 30 species were reported from Asia [
35
]. In
previous research, 16 species of Russula subgenus Russula are reported from southern
China.
[9,18,23,32–35,63,64]
. Moreover, six species are from Northeast China [
18
,
24
,
65
,
66
].
Regarding the provincial distribution in China, more species of subgenus Russula are found
in Guangdong Province and Heilongjiang Province. The reason for this phenomenon may
be that these two provinces are actively investigated by mycologists.
In this study, six new species belonged to three subsections under the subgenus Rus-
sula, namely subsection Chamaeleontinae (R. miyunensis and R. plana), subsection Puellarinae
(
R. sinoparva
,
R. sinorobusta
,and
R. yanshanensis
) and subsection Roseinae (
R. subversatilis
).
Subsection Chamaeleontinae belongs to species of normally small size. The cap is not much
fleshy, the cuticle is detachable, and the margin is smooth or just grooved, especially when
ripe; the stem is white, frail, and meaty, then hollow. Two new species, R. miyunensis and
R. plana
, described in this study, also fit these characteristics. Referring to Sarnari’s classifi-
cation system, subsection Chamaeleontinae belongs to section Amethystinae Romagn. [
5
], and
the position of this group in the systematic tree is also relatively stable. No Chinese Russula
species belonging to subsection Chamaeleontinae have been identified in previous studies.
Subsection Puellarinae was established by Singer in 1932 [
67
]. Singer had studied American
and tropical Russulas prior to proposing his classification. Subsections Chamaeleontina
Singer, Subcompactinae Singer, and Puellarinae were separated out within section Constantes
Singer [
68
]. Russula khinganensis, described by Li et al., is also a member of subsection
Puellarinae [
24
]. Subsection Roseinae was recognized by Sarnari in 1998 [
5
]. Morphologically,
members of the subsection Roseinae provide a persistent bright red-colored reaction in
J. Fungi 2022,8, 1283 30 of 33
dried fruit bodies with sulfovanilin. No species of subsection Roseinae were reported before
among Russula species in China.
Russula contains a number of wild edible fungi in the world, and there are also a
certain number of poisonous fungi. The classification of Russula is a difficult point in
the classification of macrofungi [
11
]. Therefore, a classification study of the Russula is
also essential to promote the study of edible species within the genus. According to
incomplete statistics, 128 species of Russula are used as edible mushrooms in 28 coun-
tries worldwide [
69
]. Moreover, 78 edible species of Russula in China were recorded by
Wu et al. [
12
], e.g.,
Russula delica
Fr., Russula densifolia Secr. ex Gillet, Russula griseocarnosa
X.H. Wang, Zhu L. Yang, & Knudsen.
Through literature review, all three subsections in which the six new species of this
study are located have edible species distributed in China [
70
]. In subsection Chamaeleon-
tinae,Russula turci Bres. and Russula roseipes Secr. ex Bres. are representative species. In
subsection Puellarinae,Russula puellaris Fr. is a representative species and is more widely
distributed in China. In subsection Roseinae, there are more edible mushrooms known
in this subsection, including Russula pseudointegra Arnould & Goris,
Russula rosea
Pers.,
Russula lepidicolor Romagn., and all the above species are also distributed in China. There-
fore, the six new species discovered this time should also contain edible species that worth
to be studied.
This study is the first report of the species of Russula subgenus Russula from the
Yanshan Mountains in northern Beijing and northern Hebei Province. Considering the
large area of China and its diverse forest types, it is reasonable to infer that many more
species of the genus Russula are expected to be found in the following studies. On the
premise of determining the number of Russula species, relevant studies on edible species
can be further deepened.
Author Contributions:
C.-L.H. and H.Z. conceived and designed the study; H.Z., G.-Q.C. and G.-J.L.
wrote the manuscript; G.-Q.C., H.Z. and Q.-T.W. conducted phylogenetic analysis and morphological
observations; G.-Q.C., M.-J.G., H.-F.Y. and L.Z. conducted the experiments. All authors have read
and agreed to the published version of the manuscript.
Funding:
This research was funded by The Biodiversity Survey and Assessment Project of the
Ministry of Ecology and Environment, China (2019HJ2096001006) and the National Natural Science
Foundation of China (No. 31870629).
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement:
All sequence data are available in NCBI GenBank following the acces-
sion numbers in the manuscript.
Acknowledgments:
Thanks to Li Fan, Capital Normal University, for providing experimental guid-
ance and assistance with the writing of the manuscript. We thank the two anonymous reviewers for
their constructive criticism and suggestions to improve our work.
Conflicts of Interest: The authors declare no conflict of interest.
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