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Phytotaxa 609 (3): 195–208
https://www.mapress.com/pt/
Copyright © 2023 Magnolia Press Article PHYTOTAXA
ISSN 1179-3155 (print edition)
ISSN 1179-3163 (online edition)
Accepted by Genevieve Gates: 11 Aug. 2023; published: 24 Aug. 2023
https://doi.org/10.11646/phytotaxa.609.3.3
195
A new species of Russula subgenus Russula (Russulaceae, Russulales) from
Yanshan Mountains, North China
HAO ZHOU1, XIAO-YE SHEN2,* & CHENG-LIN HOU3
College of Life Science, Capital Normal University, Beijing, 100048, China
1
�
hadrian_zhou@126.com; https://orcid.org/0000-0002-4869-2187
2
�
shenxiaoye2009@cnu.edu.cn; https://orcid.org/0000-0003-0789-6850
3
�
chenglin-hou@cnu.edu.cn; https://orcid.org/0000-0001-8162-5560
*Correspondence author
Abstract
A new species of Russula subgenus Russula, Russula pseudosinoparva, is described from the Yanshan Mountains in northern
China based on morphology and phylogenetic analysis of the nrITS and nrLSU-rpb2-mtSSU-tef1α gene regions. Russula
pseudosinoparva is characterized macroscopically by small basidiomata with a dark red to dark pink pileus; lamellae usually
forked near the stipe, with a small number of lamellulae; and microscopically by a suprapellis made up of loose and upright
hyphae. Phylogenetic and morphological analyses placed the new species in the lineages of subsect. Puellarinae. As well as
an illustrated description we provide a key to the species of Russula subgenus Russula distributed in China.
Key words: Ectomycorrhizal fungi, taxonomy, phylogenetic analysis
Introduction
Russula Pers. (1796: 100) (Russulaceae, Russulales, Agaricomycetes, Basidiomycota) was described by the Dutch
mycologist, Persoon. Russula species are widely distributed globally (Looney et al. 2016), and include at least 2000
species (Buyck et al. 2018, 2020; Adamčík et al. 2019; Wijayawardene et al. 2020). Russula is a large genus of
ectomycorrhizal (ECM) fungi that are found in all common ecosystems (Agerer 2001; Looney et al. 2016; Chen et al.
2022; Song et al. 2022; Zhou et al. 2022c). Furthermore, some members of Russula not only play an important role
in ecology by being symbiotic with a variety of plants but also serve as a food source for many animals, including
humans (Wang 2020).
According to traditional taxonomy, the genus is mainly characterized by a pale-colored or multi-colored pileus,
amyloid ornamented basidiospores, heteromerous trama with abundant sphaerocytes in the pileipellis, an absence of
latex, and hyphae that lack clamp connections (Romagnesi 1967; Singer 1986; Sarnari 1998). With the development
of molecular systematics, the classification of Russula has changed dramatically. Miller and Buyck (2002) used a
phylogenetic analysis of the ITS1, 5.8S, and ITS2 regions of 87 European species of Russula resulting in the species
being contained within six clades with high support. Buyck et al. (2018, 2020) demonstrated that Russula was one
of four monophyletic groups in non-corticioid Russulaceae and was divided into eight subgenera by two multi-
locus phylogenetic studies. The subgenus Russula Pers. (1976: 100) is a species-rich subgenus of Russula that is
morphologically characterized mainly by a large variation in basidiocarp size with a thick to extremely thin-fleshed
pileus and spores with amyloid suprahilar spots. Phylogenetically, this subgenus is divided into two parts: a core and
a crown clade (Looney et al. 2016; Buyck et al. 2018; Adamčík et al. 2019). So far, 27 species belong to the subgenus
Russula in China (Chen et al. 2021b, Li et al. 2018, 2020, 2023, Wang 2020, Zhou et al. 2022c).
The Yanshan Mountains (115°–119°47’ E, 39°40’–41°20’ N), located in North China, have a warm temperate
continental monsoon climate. This region is known for its high plant diversity, with the main forest types being
deciduous broad-leaved forest and mixed coniferous and broad-leaved forest. Dominant ectomycorrhizal trees in this
region include Quercus mongolica Fisch. ex Ledeb., Betula platyphylla Suk., Abies nephrolepis (Trautv.) Maxim.,
Populus tomentosa Carrière and Pinus tabuliformis Carr. (Wang et al. 2021, Zhou et al. 2022b). This region has an
ZHOU ET AL.
196 • Phytotaxa 609 (3) © 2023 Magnolia Press
annual precipitation of approximately 350–700 mm, and the altitude ranges from 200 to 2200 m (Zhou et al. 2022
a,b,c).
In this study, we describe a new species of Russula subgenus Russula from Yanshan Mountains based on
morphological and molecular phylogenetic analyses. Detailed macro- and micromorphological descriptions and
illustrations are provided. A phylogenetic tree based on nrITS and nrLSU-rpb2-mtSSU- tef1α datasets was also
constructed. Furthermore, we provide a key to the species of Russula subgenus Russula distributed in China.
Materials and methods
Sampling and Morphological analyses
Specimens were collected during 2019 to 2022. The fresh specimens were photographed in the field, and characters
such as color, odor, and viscosity were noted. Color codes are from the reference website colourhexa (https://www.
colourhexa.com). Specimens were dried using a Dorrex dryer at 50 °C and deposited in the Herbarium of the College
of Life Science, Capital Normal University, Beijing, China (BJTC).
Microscopic characters were observed from thin sections of dried material mounted in 3 % KOH or sterilized water.
1 % Congo Red was used to make the structures more visible. Melzer’s reagent was used to test the amyloid reaction
of the spore ornamentation. All tissues were examined in Cresyl Blue to verify the presence of ortho- or metachromatic
reactions as explained in Buyck (1989). Cystidia were observed in sulfovanillin (SV) solution (Caboň et al. 2017). The
shape and size of microscopic structures were observed and measured from the dried material mounted in 3 % KOH
using a light microscope (Olympus DP71, Tokyo, Japan), digital cameras (Olympus U-TV0.5XC-3, Tokyo, Japan) and
measuring software (Image Pro Plus 6.0). The basidiospores were further observed under a field emission scanning
electron microscope (SEM, Hitachi S-4800, Tokyo, Japan). Basidiospore measurements without ornamentation are
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 (Adamčík
et al. 2019), statistics for most of the microscopic characteristics are based on 30 measurements per specimen. The
descriptive terms and description standards follow Adamčík et al. (2019).
DNA extraction PCR amplification and sequencing
DNA extraction was achieved via the M5 Plant Genomic DNA Kit (Mei5 Biotechnology, Co., Ltd, 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 S1000TM Thermal Cycler (Bio-Rad Laboratories, Inc, USA). The following primer sets
were used for amplification: nrITS 1f/ nrITS 4 for the nrITS region (White et al. 1990), LR0R /LR5 for the nrLSU
region (Vilgalys & Hester 1990), MS1/MS2 for the ribosomal mitochondrial small subunit (mtSSU) region (White et
al. 1990), RBP2-6f/RBP2-7r for the second largest subunit of RNA polymerase II (rpb2) region (Matheny 2005) and
tef1F/tef1R for the second largest subunit of transcription elongation factor 1-alpha (tef1α) region (Morehouse et al.
2003). The PCR volume was 25 μL and consisted of 2 μL of DNA template, 1 μL of each primer (10 μM), 8.5 μL sterile
ddH2O, 12.5 μL 2× Master Mix (Mei5 Biotechnology, Co., Ltd, China) (Zhou et al. 2022b). PCR conditions for nrITS
and nrLSU followed Li et al. (2020), for mtSSU and rpb2 followed Song et al. (2022), for tef1α followed Morehouse et
al. (2003). Samples were sequenced by Sangon Biotechnology (Shanghai), Co., Ltd, China. Newly obtained sequences
in this study were submitted to NCBI GenBank database (https://submit.ncbi.nlm.nih.gov/). Accession numbers of
sequences used for phylogenetic analyses are provided in Figure 1 and Table 1.
Molecular data analyses
DNA chromatograms were edited using SeqMan v.7.1.0 (DNASTAR Inc., Madison, WI, USA). All sequences were
analysed using MAFFT v.6 and manually trimmed using MEGA 6 (Tamura et al. 2013). All reference sequences of
subgenus Russula were selected for phylogenetic analyses based on previous studies and the GenBank database in
NCBI.
The nrLSU- rpb2- tef1α-mtSSU multi-locus phylogenetic analysis used to analyse the phylogenetic position of
our specimens in the genus Russula included 89 ingroup samples. The nrITS phylogenetic analysis used to analyse
the relationships among our collections and other species in the subgenus Russula included 127 ingroup samples, All
reference sequences of subgenus Russula of dataset were chosen for phylogenetic analyses based on previous studies
and GenBank database in NCBI (Accession number on Table 1 and Figure 1). Multifurca aurantiophylla (Bills &
A NEW SPECIES OF RUSSULA SUBGENUS RUSSULA Phytotaxa 609 (3) © 2023 Magnolia Press • 197
O.K. Mill.) (2008: 37) Buyck & V. Hofst. (644/BB 09.119), Multifurca ochricompacta (Bills & O.K. Mill.) Buyck &
V. Hofst. (BB02.107) (2008: 37), M. ochricompacta (580/BB 07.010), and Multifurca zonaria (Buyck & Desjardin)
Buyck & V. Hofst. (DED7442) (2008: 37), Multifurca were the outgroup taxa following Buyck et al. (2018).
The Maximum Likelihood (ML) gene trees were estimated using the RAxML 7.4.2 Black Box software (Stamatakis
2016; Stamatakis et al. 2008; Zhou et al. 2019, 2021, 2022a). Bayesian Inference (BI) phylogenetic analysis was
performed using MrBayes v.3.1.2 (Ronquis & Huelsenbeck 2003). Branch supports were calculated using a bootstrapping
(BS) method with 1000 replicates (Hillis & Bull 1993). ML analysis used a GTR locus substitution model by running
1000 bootstrap replicates with all default settings parameters (Guindon et al. 2010). Bayesian Inference (BI) analysis
was performed by the Markov chain Monte Carlo (MCMC) algorithm (Rannala & Yang 1996). MrModeltest v. 2.3 was
used to estimate the best model for BI (GTR+I+G for nrITS, nrLSU, rpb2, and mtSSU; SYM+I+G for tef1α) (Ronquis
& Huelsenbeck 2003). 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
(Posada & Crandall 1998). ML bootstrap support (BS) ≥ 50% and Bayesian Posterior Probability (PP) ≥ 0.95 are
shown on the nodes in Figures 1 and 2.
TABLE 1. Sequence data used in the nrLSU- rpb2-mtSSU- tef1α phylogenetic analysis in this study. The new species
is in bold. ‘-’ means no sequence.
Taxa Voucher Location
GenBank accession numbers
References
nrLSU mtSSU rpb2 tef1α
Multifurca aurantiophylla 644/BB 09.119 New Caledonia KU237581 KU237429 KU237867 KU238008 Buyck et al. 2018
Multifurca ochricompacta 580/BB 07.010 USA KU237565 KU237413 KU237851 KU237994 Buyck et al. 2018
Russula abbottabadensis LAH 310071 Pakistan MN518356 MG386719 MG386737 MZ364137 Caboň et al. 2019
Russula abbottabadensis FH 00304558 Pakistan MN518355 MG386721 MG386738 MZ364138 Caboň et al. 2019
Russula acrifolia 543/BB 08.662 Italy KU237535 KU237381 KU237821 KU237965 Buyck et al. 2018
Russula adusta 223/BB 06.562 Canada KU237476 KU237320 KU237762 KU237907 Buyck et al. 2018
Russula amethystina 529/BB 07.314 Slovakia KU237521 KU237367 KU237807 KU237951 Buyck et al. 2018
Russula archaeosuberis 1118/BB 12.085 Italy KU237593 KU237441 KU237878 KU238019 Buyck et al. 2018
Russula ayubiana LAH 35438 Pakistan MZ358816 MZ364121 MZ364131 MZ364139 Kiran et al. 2021
Russula ayubiana LAH 35439 Pakistan MZ358817 MZ364122 MZ364132 MZ364140 Kiran et al. 2021
Russula azurea 537/BB 08.668 Italy KU237529 KU237375 KU237815 KU237959 Buyck et al. 2018
Russula aff. betularum 225/BB 06.463 Mexico KU237478 KU237322 KU237764 KU237909 Buyck et al. 2018
Russula aff. bicolor 224/BB 06.565 Canada KU237477 KU237321 KU237763 KU237908 Buyck et al. 2018
Russula brevipes 226/BB 06.508 Mexico KU237479 KU237323 KU237765 - Buyck et al. 2018
Russula burlinghamiae 548/BB 05.108 USA KU237540 KU237386 KU237826 KU237970 Buyck et al. 2018
Russula carpini 551/BB 07.262 Slovakia KU237543 KU237389 KU237829 KU237973 Buyck et al. 2018
Russula chloroides 572/BB 07.209 Slovakia KU237559 KU237407 KU237845 KU237990 Buyck et al. 2018
Russula compacta 228/BB 06.295 USA KU237480 KU237324 KU237766 - Buyck et al. 2018
Russula corallina- 229/BB 06.324 USA KU237481 KU237325 KU237767 KU237910 Buyck et al. 2018
Russula aff. crustosa 31/BB 06.616 Canada KU237461 KU237305 KU237747 KU237896 Buyck et al. 2018
Russula cuprea 565/BB 07.233 Slovakia KU237555 KU237401 KU237841 KU237984 Buyck et al. 2018
Russula decolorans 549/BB 07.322 Slovakia KU237541 KU237387 KU237827 KU237971 Buyck et al. 2018
Russula emetica 635/JMT39-08092228 France KU237578 KU237426 KU237864 - Buyck et al. 2018
Russula exalbicans 584/BB 07.786 France KU237568 KU237416 KU237854 KU237996 Buyck et al. 2018
Russula farinipes 576/BB 08.632 Italy KU237561 KU237409 KU237847 KU237992 Buyck et al. 2018
......continued on the next page
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198 • Phytotaxa 609 (3) © 2023 Magnolia Press
TABLE 1 (Continued)
Taxa Voucher Location
GenBank accession numbers
References
nrLSU mtSSU rpb2 tef1α
Russula fattoensis Buyck 02.227 USA MN315514 MN315537 MN326797 MN326800 Buyck et al. 2020
Russula fragilis 443/BB 07.791 France KU237506 KU237351 KU237792 - Buyck et al. 2018
Russula glutinosa Roody WRWV 04.1154 USA MN315511 MN315532 MN326798 MN326799 Buyck et al. 2020
Russula gracillima 441/BB 07.785 France KU237504 KU237349 KU237790 KU237934 Buyck et al. 2018
Russula aff.griseobrunnea 741/BB 09.344 New Caledonia KU237592 KU237440 KU237877 KU238018 Buyck et al. 2018
Russula herrerae 239/BB 06.532 Mexico KU237486 KU237330 KU237772 KU237915 Buyck et al. 2018
Russula integra 518/BB 07.198 Slovakia KU237513 KU237359 KU237799 KU237943 Buyck et al. 2018
Russula laeta 519/BB 07.267 Slovakia KU237514 KU237360 KU237800 KU237944 Buyck et al. 2018
Russula laricina 575/BB 08.681 Italy KU237560 KU237408 KU237846 KU237991 Buyck et al. 2018
Russula leucomarginata RITF3133 China MW309327 MW309338 MW310568 - Chen et al. 2022
Russula leucomarginata RITF3123 China MW309328 MW309339 MW310569 - Chen et al. 2022
Russula lilacea 435/BB 07.213 Slovakia KU237498 KU237343 KU237784 KU237928 Buyck et al. 2018
Russula mansehraensis HUP SUR 180 Pakistan MG944280 MG944266 MG944255 - Crous et al. 2018
Russula mansehraensis HUP SUR 803 Pakistan - MG944267 MG944256 - Crous et al. 2018
Russula minutula 539/BB 08.636 Italy KU237531 KU237377 KU237817 KU237961 Buyck et al. 2018
Russula miyunensis BJTC Z1357 China - OP135984 OP156826 OP156837 Zhou et al. 2022c
Russula miyunensis BJTC Z1355 China OP133232 OP135985 OP156827 - Zhou et al. 2022c
Russula mustelina 1176/SA 09.88 Slovakia KU237596 KU237444 KU237881 KU238022 Buyck et al. 2018
Russula nauseosa 588/BB 07.285 Italy KU237572 KU237420 KU237858 KU238000 Buyck et al. 2018
Russula nigricans 429/BB 07.342 Slovakia KU237495 KU237339 KU237781 KU237924 Buyck et al. 2018
Russula nothofagineae 723/BB 09.044 New Caledonia KU237583 KU237431 - KU238010 Buyck et al. 2018
Russula nothofagineae 726/BB 09.069 New Caledonia KU237585 KU237433 KU237870 KU238012 Buyck et al. 2018
Russula cf.odorata 525/BB 07.219 Slovakia KU237517 KU237363 KU237803 KU237947 Buyck et al. 2018
Russula odorata 526/BB 07.186 Slovakia KU237518 KU237364 KU237804 KU237948 Buyck et al. 2018
Russula olivascens 530/BB 08.663 Italia KU237522 KU237368 KU237808 KU237952 Buyck et al. 2018
Russula cf.olivobrunnea 240/BB 06.505 Mexico KU237487 KU237331 KU237773 KU237916 Buyck et al. 2018
Russula plana BJTC Z1398 China OP133233 OP135986 OP156828 OP156838 Zhou et al. 2022c
Russula plana BJTC T2101 China OP265903 OP265901 OP267556 OP267558 Zhou et al. 2022c
Russula pseudoaurantiophylla 740/BB 09.219 New Caledonia KU237591 KU237439 KU237876 KU238017 Buyck et al. 2018
Russula pseudosinoparva BJTC L131 China OR056322 OR066239 OR073884 OR073885 this study
Russula pseudosinoparva BJTC C381 China OR056323 OR066240 - - this study
Russula puellaris 523/BB 07.311 Slovakia KU237515 KU237361 KU237801 KU237945 Buyck et al. 2018
Russula purpureoverrucosa GDGM32902 China MG214699 - MT085652 MT085623 Zhou et al. 2020
Russula quercus-floribundae LAH 36219 Pakistan MN513043 MN053397 MN053389 MZ364152 Crous et al. 2019
Russula quercus-floribundae LAH 36220 Pakistan MN513043 MN053396 MN053390 MZ364153 Crous et al. 2019
Russula raoultii 561/BB 08.674 Italy KU237551 KU237397 KU237837 KU237980 Buyck et al. 2018
Russula rosea 430/BB 07.780 France KU237496 KU237340 KU237782 KU237925 Buyck et al. 2018
Russula roseola RITF3418 China MW309319 MW309330 MW310560 - Chen et al. 2022
Russula roseola RITF3428 China MW309320 MW309331 MW310561 - Chen et al. 2022
Russula sinoparva BJTC C540 China OP133234 OP135987 OP156829 OP156839 Zhou et al. 2022c
Russula sinoparva BJTC Z441 China OP133235 OP135988 - OP156840 Zhou et al. 2022c
......continued on the next page
A NEW SPECIES OF RUSSULA SUBGENUS RUSSULA Phytotaxa 609 (3) © 2023 Magnolia Press • 199
TABLE 1 (Continued)
Taxa Voucher Location
GenBank accession numbers
References
nrLSU mtSSU rpb2 tef1α
Russula sinorobusta BJTC Z050 China OP133236 OP135989 OP156830 OP156841 Zhou et al. 2022c
Russula sinorobusta BJTC Z052 China - OP135990 - OP156842 Zhou et al. 2022c
Russula sinorobusta BJTC Z662 China OP133237 OP135991 OP156831 OP156843 Zhou et al. 2022c
Russula sichuanensis ZRL20162017 China MG786572 MG792323 - MG812160 Li et al. 2018
Russula solaris 559/BB 07.282 Slovakia KU237549 KU237395 KU237835 KU237978 Buyck et al. 2018
Russula sp. 735/BB 09.172 New Caledonia KU237588 KU237436 KU237873 KU238015 Buyck et al. 2018
Russula aff.subdensifolia 552/BB 07.158 USA KU237544 KU237390 KU237830 KU237974 Buyck et al. 2018
Russula subsanguinaria RITF2236 China MW309322 MW309333 MW310563 - Chen et al. 2022
Russula subsanguinaria RITF2208 China MW309323 MW309334 MW310564 - Chen et al. 2022
Russula subtilis 536/BB 05.107 USA KU237528 KU237374 KU237814 KU237958 Buyck et al. 2018
Russula subversatilis BJTC C653 China OP133238 OP135992 OP156832 OP156844 Zhou et al. 2022c
Russula subversatilis BJTC T2001 China OP265904 OP265902 OP267557 OP267559 Zhou et al. 2022c
Russula aff. turci 433/BB 07.325 Slovakia KU237497 KU237342 KU237783 KU237927 Buyck et al. 2018
Russula turci 528/BB 07.328 Slovakia KU237520 KU237366 KU237806 KU237950 Buyck et al. 2018
Russula versicolor 589/BB 07.288 Slovakia KU237573 KU237421 KU237859 KU238001 Buyck et al. 2018
Russula vinosobrunneola HMAS 281138 China MG786569 MG792320 - MG812157 Li et al. 2018
Russula vinosobrunneola HMAS 278885 China MG786570 MG792321 - MG812158 Li et al. 2018
Russula yanshanensis BJTC C561 China OP133239 OP135993 - OP156845 Zhou et al. 2022c
Russula yanshanensis BJTC Z1448 China OP133240 OP135994 OP156833 - Zhou et al. 2022c
Russula yanshanensis BJTC Z421 China OP133241 OP135995 - OP156846 Zhou et al. 2022c
Russula yanshanensis BJTC Z1385 China OP133242 OP135996 - OP156847 Zhou et al. 2022c
Russula yanshanensis BJTC Z1305 China OP133243 OP135997 OP156834 OP156848 Zhou et al. 2022c
Russula yanshanensis BJTC Z1390 China OP133244 OP135998 OP156835 OP156849 Zhou et al. 2022c
Russula yanshanensis BJTC L349 China OP133245 OP135999 OP156836 OP156850 Zhou et al. 2022c
Russula zvarae 538/BB 08.639 Italy KU237530 KU237376 KU237816 KU237960 Buyck et al. 2018
Results
Phylogenetic analyses
The nrLSU- rpb2-mtSSU- tef1α and nrITS phylogenetic analyses revealed that the subgenera proposed by Buyck et
al. (2018) were well-supported with significant Bayesian Posterior Probability (PP) values and Maximum Likelihood
Bootstrap (MLB).
The nrLSU-rpb2-mtSSU-tef1α multi-loci dataset contains 2626 characters including alignment gaps. The
phylogenetic topologies generated from ML and BI analyses are nearly identical, and the Bayesian tree is shown in
Figure 1. Phylogenetic analysis showed that sequences of two specimens (BJTC C381 and BJTC L131) clustered
together, forming a strongly supported clade (pp = 1.00, MLB = 99 %). This clade clustered with Russula sinoparva
C.L. Hou, Hao Zhou & G.Q. Cheng (2022: 18) and formed a supported group, which nested in the subgenus Russula.
The dataset of the nrITS loci comprised 454 characters including the alignment gaps, a best Bayesian tree is
shown in Figure 2, ML tree proves that the topology of the tree obtained by Maximum Likelihood is consistent with
Bayesian analysis. Sequences of two specimens (BJTC C381 and BJTC L131) clustered together, forming a highly
supported clade (pp = 0.99, MLB = 98 %) identified as Russula sp. nov.
ZHOU ET AL.
200 • Phytotaxa 609 (3) © 2023 Magnolia Press
FIGURE 1. The nrLSU-rpb2-mtSSU-tef1α multi-locus phylogenetic tree obtained from Bayesian analysis. Numbers above branches
represent strong support (pp≥0.95 or MLB≥50 %). Numbers above branches are Bayesian Posterior Probability (PP) values and Maximum
Likelihood Bootstrap (MLB). The red font indicates the position of the new sequences. See Table 1 for sequence data. Asterisks (*) denotes
branches with PP = 1.00, MLB = 100 %.
A NEW SPECIES OF RUSSULA SUBGENUS RUSSULA Phytotaxa 609 (3) © 2023 Magnolia Press • 201
FIGURE 2. The nrITS phylogenetic tree obtained from the Bayesian analysis. Numbers above branches represent strong 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 the new sequences. Sequence data are indicated on the Figure. Asterisks (*) denote branches with
PP = 1.00, MLB = 100 %.
ZHOU ET AL.
202 • Phytotaxa 609 (3) © 2023 Magnolia Press
Taxonomy
Russula pseudosinoparva sp. nov. H. Zhou & C. L. Hou (Figs. 3, 4, 5)
MycoBank: MB 847567
Diagnosis:—Russula pseudosinoparva is characterised macroscopically by small basidiomata with a dark red to dark
pink pileus; lamellae usually forked near the stipe, with a small number of lamellulae; and microscopically by a
suprapellis made up of loose and upright hyphae. Morphologically, R. pseudosinoparva is easily confused with Russula
puellaris Fr. (1983: 362). Russula pseudosinoparva differs from R. puellaris by having usually forked lamellae and
bigger basidia.
Etymology:—The epithet “pseudosinoparva” refers to its related phylogenetic position to Russula sinoparva.
Holotype:—CHINA. Hebei Province, Xinglong County, Wulingshan Mountains National Nature Reserve,
40.272411 N, 117.13521 E, elev. 222 m, 19 August 2019, coll. C.L. Hou, J.Q. Li and G.Q. Cheng (BJTC L131).
FIGURE 3. Russula pseudosinoparva (BJTC L131). A–B. Basidiomes. C–D. SEM of basidiospores. Scale bar: A=1 cm, B=1 cm, C–D
=1 μm. Photos by: Hao Zhou.
Description:—Basidiomata small size. Pileus 10–25 mm diam., initially hemispherical when young, flattened
when mature, slightly concave at the center, dry at the edge, slightly viscid in the center, smooth when young, striate
when old, cracking near the margin with age, smooth, peeling to 1/3 of the radius, pure red (#e60039) to dark red
(#9a0026), central dark pink (#810041) to very dark pink. (#680034). Lamellae white (#ffffff) when young, white
(#ffffff) to very pale cream (#ffffd4) when mature, with 9–11 gills per cm of cap circumference, brittle, unequal,
usually forked near the margin. Stipe 31–55 × 5–12 mm, white (#ffffff), subcylindrical, smooth, dry, non-brittle,
gradually broadening towards base. Pileus context 2–6 mm thick, white (#ffffff) without color change when bruised.
Spore print not observed. Taste and smell not observed.
Basidiospores (5.8–)6.8–7.2–7.9(–8.8) × (5.5–)5.9–6.3–6.9(–7.2) μm, [Q = (1.02–)1.06–1.11–1.25(–1.35)],
subglobose to broadly ellipsoid, ornamentation consisting of small, moderately distant [(4–)5–7(–8) in a 3 μm diameter
circle] amyloid warts, 0.4–1.2 μm 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–)1–2 in the circle], suprahilar
spot large, inamyloid. Basidia (33–)36–39–45(–52) × (11–)13–14–15 (–17) μm, 2–4-spored, clavate, with particles
A NEW SPECIES OF RUSSULA SUBGENUS RUSSULA Phytotaxa 609 (3) © 2023 Magnolia Press • 203
and oil droplets, basidioles clavate or subcylindrical, ca. 7–16 μm wide. Hymenial cystidia on lamellae faces (39–
)48–51–63(–70) × (8.1–)8.9–10–12(–14) μm, clavate or fusiform, apically often obtuse or mucronate, sometimes with
2–6-μm-long appendage, contents with refracted inclusions, or some-times with granulose or crystalline, turning ash
black (#0d0d0d) in SV. Hymenial cystidia on lamellae edges smaller and narrower to hymenial cystidia on lamellae
sides, (23–)27–33–39(–46) × (4.4–)5.4–6.8–10(–12) μm, clavate or subcylindrical, apically often obtuse, sometimes
with 2–4 μm long appendage, contents granulose. Pileipellis orthochromatic in Cresyl Blue, sharply delimited from
the underlying context, 90–150 μm deep, two-layered. Suprapellis 40–70 μm deep, with strongly gelatinized loose
and upright hyphae. Subpellis 50–90 μm deep, composed of horizontally oriented, relatively dense, intricate, 3–8 μm
diam hyphae. Hyphal terminations near the pileus margin occasionally branched, sometimes flexuous, thin-walled;
terminal cells (10.4–)11–13–19(–22) × (2.8–)3.2–3.8–5.6(–7.1) μm, subcylindrical or clavate, apically mainly obtuse,
occasionally attenuated, subterminal cells often wider, ca. 3–6 μm diam, always unbranched. Hyphal terminations
near the pileus center similar to those near the pileus margin; terminal cells (14–)15–24(–28) × (2.9–)3.5–6.1(–7.2)
μm, subcylindrical or clavate, occasionally ellipsoid, apically obtuse, constricted or attenuated; subterminal cells
often wider, ca. 3–8 μm diam, always unbranched. Pileocystidia near the pileus margin mostly 2–4-celled, a few
one-celled, terminal cells (10.2–)13–31–44(–75) × (3.8–)4.6–5.9–6.4(–7.1) μm, thin-walled, mainly cylindrical or
subcylindrical, occasionally clavate, apically usually obtuse, contents with heteromorphous granulose, turning light
ash black (#0d0d0d) in SV. Pileocystidia near the pileus center often smaller, 2–5-celled, thin-walled, terminal cells
(13–)17–27–47(–70) × (4.0–)4.5–5.7–6.6(–7.9) μm, mainly clavate or cylindrical, contents granulose or occasionally
crystalline. Cystidioid hyphae in subpellis and context with heteromorphous granulose contents, oleiferous hyphae in
the subpellis close to the context.
FIGURE 4. Microscopic features of Russula pseudosinoparva (BJTC L131). A. Basidia. B. Basidioles. C. Marginal cells. D. Hymenial
cystidia on lamellae sides. E. Hymenial cystidia on lamellae edges. Scale bar: 10 μm. Drawings by: Hao Zhou.
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204 • Phytotaxa 609 (3) © 2023 Magnolia Press
FIGURE 5. Microscopic features of Russula pseudosinoparva (BJTC L131). 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. Drawings by: Hao Zhou.
Habitat and distribution:—Solitary and scattered in coniferous forests and mixed coniferous and broad-leaved
forests of Pinus tabuliformis Carr. and Juglans mandshurica Maxim, in a warm temperate region of North China
(Beijing and Hebei).
Additional specimens examined:—CHINA. Beijing, Pinggu District, Sizuolou Nature Reserve, 40.272411 N,
117.13521 E, elev. 222 m, 19 August 2020, coll. C.L. Hou, G.Q. Cheng and R.T. Zhang (BJTC C381).
Discussion
Morphologically, R. pseudosinoparva differs from R. sinoparva in pileus color, i.e., the pileus of R. sinoparva is
light pink to pink, while that of R. pseudosinoparva is dark red to dark pink. Moreover, R. pseudosinoparva and R.
sinoparva are also different in the structure of the lamellae and suprapellis. The lamellae of R. sinoparva are not forked
and there are no lamellulae; furthermore, the suprapellis of R. sinoparva is made up of ascending to erect, and slight
interlaced hyphae (Zhou et al. 2022c). Russula pseudosinoparva is easily confused with R. puellaris. Morphologically,
R. puellaris differs from our new species by having non forked lamellae, and smaller basidia (28–43 × 9–12 µm) (Fries
1838).
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In this study, R. pseudosinoparva belongs to subsection Puellarinae Singer (1932: 237) of subgenus Russula.
Subsect. Puellarinae was established by Singer (1932). Singer had studied American and tropical Russula prior to
proposing his classification. This study also made an important supplement to the species diversity of Russula subgenus
Russula in Yanshan Mountains.
Key to Russula subgenus Russula from China
1. Pileipellis with primordial hypha, the surface of pileus is mainly purple tone ................................................ R. purpureoverrucosa
1. Pileipellis without primordial hypha ..................................................................................................................................................2
2. Spore print cream, ochre yellow to yellow .........................................................................................................................................3
2. Spore print white to cream .................................................................................................................................................................4
3. Basidiomata medium-sized .......................................................................................................................................... R. rubiginosus
3. Basidiocarps small to medium-sized ................................................................................................................... R. heilongjiangensis
4. Stipe with brownish tone ...............................................................................................................................................R. subversatili
4. Stipe with red, rose red, purple tone ...................................................................................................................................................5
4. Stipe with yellow tone ........................................................................................................................................................................7
4. Stipe white ........................................................................................................................................................................................14
5. Lamellulae not observed ..................................................................................................................................................... R. begonia
5. Lamellulae present .........................................................................................................................................................R. rhodochroa
5. Lamellulae rare ...................................................................................................................................................................................6
6. Lamellae adnate, white ....................................................................................................................................................... R. photinia
6. Lamellae adnate to adnexed, white to cream .............................................................................................................................R. rufa
7. Pileus with red tone ...................................................................................................................................................... R. sinorobusta
7. Pileus with brown tone .......................................................................................................................................................................8
7. Pileus with pink tone ..........................................................................................................................................................................9
8. Context slowly and partly turning ocherous color after bruising ............................................................................... R. khinganensis
8. Context unchanging after bruising ....................................................................................................................... R. vinosobrunneola
9. Central dark red to deep red pileus ...................................................................................................................................................10
9. Central light yellow to yellowish-brown pileus ......................................................................................................... R. yanshanensis
10. Lamellae hardly forked .................................................................................................................................................... R. sinoparva
10. Lamellae usually forked .......................................................................................................................................R. pseudosinoparva
11. Very little red tone on the pileus .......................................................................................................................................................12
11. Pileus with red tone ..........................................................................................................................................................................14
11. Pileus with pink tone ........................................................................................................................................................................19
11. Pileus with yellow tone ................................................................................................................................................. R. miyunensis
11. Pileus white ...........................................................................................................................................................................R. nivalis
12. Stipe spongy to hollow ...............................................................................................................................................R. zhejiangensis
12. Stipe hollow ......................................................................................................................................................................................13
13. Lamellulae present .............................................................................................................................................................R. jilinensis
13. Lamellulae absent ........................................................................................................................................................R. sichuanensis
14. Flesh of the pileus organisms turns slightly yellow after injury.............................................................................................. R. chiui
14. Flesh of the pileus organisms no color change after injury ..............................................................................................................15
15. Slightly pungent to moderately pungent flavor ................................................................................................................................16
15. Soft flavor .........................................................................................................................................................................................17
16. Lamellulae absent .............................................................................................................................................................. R. quercina
16. Lamellulae present ................................................................................................................................................. R. brunneovinacea
17. Stipe hollow ......................................................................................................................................................................................18
17. Stipe firm ................................................................................................................................................................................ R. plana
17. Stipe spongy .........................................................................................................................................................................R. fanjing
18. Yellowish red to reddish brown pileus center.........................................................................................................R. leucomarginata
18. Reddish white to ruby red in the pileus center ....................................................................................................................R. roseola
18. Reddish brown to dark brown pileus center ........................................................................................................... R. subsanguinaria
19. Lamellae intervenose ...................................................................................................................................................R. coronaspora
19. Lamellae adnate ......................................................................................................................................................................R. minor
Acknowledgements
This study was financed by the National Natural Science Foundation of China (No. 32270012) and the Biodiversity
Survey and Assessment Project of the Ministry of Ecology and Environment, China (2019HJ2096001006). We also
thank the anonymous reviewers for their constructive criticism and suggestions to improve our work.
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206 • Phytotaxa 609 (3) © 2023 Magnolia Press
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