Two new Phragmidium species identified on Rosa plants native to China

Abstract

Two new Phragmidium species, Phragmidium zhouquensis and Ph. longissima, were identified on two native plants, Rosa omeiensis and R. lichiangensis respectively, during an investigation of the occurrence of rust fungi in western China. Phragmidium zhouquensis is mainly characterized by 3–9-celled teliospores bearing minute verrucae on the surface. Phragmidium longissima differs from other Phragmidium species in that it possesses echinulate urediniospores with a pore membrane at the germ pore. Phylogenetic analyses based on 28S rRNA partial gene sequences revealed that specimens of Ph. zhouquensis and Ph. longissima formed two distinct lineages. Phragmidium longissima is the first Phragmidium species to be identified on R. lichiangensis.

Full text

Phytotaxa 217 (2): 182–190
www.mapress.com/phytotaxa/
Copyright © 2015 Magnolia Press Article PHYTOTAXA
ISSN 1179-3155 (print edition)
ISSN 1179-3163 (online edition)
182 Accepted by Samantha Karunarathna: 3 Jun. 2015; published: 23 Jun. 2015
http://dx.doi.org/10.11646/phytotaxa.217.2.8
Licensed under a Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0
Two new Phragmidium species identified on Rosa plants native to China
TING YANG 1, WEI CHANG 1, BIN CAO 1, CHENG-MING TIAN 1, LONG ZHAO 2 & YING-MEI LIANG 3*
1 The Forestry Institute, Beijing Forestry University, Beijing 100083, China
2 Gansu Natural Forest Protection Center, Gansu 730000, China
3 Museum of Beijing Forestry University, Beijing 100083, China
* Correspondence author: liangym@bjfu.edu.cn
Abstract
Two new Phragmidium species, Phragmidium zhouquensis and Ph. longissima, were identified on two native plants, Rosa
omeiensis and R. lichiangensis respectively, during an investigation of the occurrence of rust fungi in western China. Phrag-
midium zhouquensis is mainly characterized by 3–9-celled teliospores bearing minute verrucae on the surface. Phragmidium
longissima differs from other Phragmidium species in that it possesses echinulate urediniospores with a pore membrane at
the germ pore. Phylogenetic analyses based on 28S rRNA partial gene sequences revealed that specimens of Ph. zhouquensis
and Ph. longissima formed two distinct lineages. Phragmidium longissima is the first Phragmidium species to be identified
on R. lichiangensis.
Key words: molecular phylogeny, Pucciniales, rose rusts, taxonomy
Introduction
The genus Rosa L. (Rosaceae) is of worldwide economic importance as the centre of a large ornamental shrub and cut
flower industry. Rosa species are widely distributed throughout the temperate and subtropical habitats of the northern
hemisphere (Matthews 1995). Rosa omeiensis Rolfe and R. lichiangensis T. T. Yu & T. C. Ku are two species native to
central and western China (Lu et al. 2003).
The genus
Phragmidium Link is a common rust fungus restricted to plants belonging to the family Rosaceae,
especially the genera Potentilla, Rosa and Rubus. Phragmidium is characterized by Caeoma-type aecia with catenulate
aeciospores, Uredo-type or Calodion-type uredinia with peripheral paraphyses and dark brown teliospores that are
typically festooned with several transverse septa along with 2–3 germ pores per teliospore cell (Cummins & Hiratsuka
2003, Yun et al. 2011). Most species within this genus produce subcuticular spermogonium, caeomatoid aecium,
uredinium and telium during the autoecious macrocyclic life cycle (Cummins & Hiratsuka 2003, Zhuang et al.
2012).
Approximately 60 to 65 species have been recognised as Phragmidium, and 30 of these have been reported to
infect wild Rosa species and ornamental Rosa cultivars (Cummins & Hiratsuka 2003). Wahyuno et al. (2001) described
seven Phragmidium species by analysing the morphological characteristics of a maximum of four spore stages from
ten previously recorded species. These authors determined that the length, width, degree of tapering toward both ends,
and apiculus length were sufficient to determine gross teliospore morphology, and these have been considered as
important taxonomic characters. The cell number, wall colour, surface rugosity, and hygroscopicity of the lower part
of the pedicel also have been used as taxonomic features at the telial stage. A total of 11 Phragmidium species have
been reported on Rosa in China, including Ph. butleri H. Sydow & P. Sydow, Ph. fusiforme J. Schröter, Ph. handelii
Petrak, Ph. hashiokai Hiratsuka f., Ph. kamtschatkae (F. W. Anderson) Arthur & Cummins, Ph. montivagum Arthur,
Ph. rosae-multiflorae Dietel., Ph. mucronatum (Persoon) Schlechtendal, Ph. robustum J. Y. Zhuang & S. X. Wei, Ph.
rosae-omeiensis S. X. Wei, and Ph. tuberculatum Jul. Müller. The latter four species have been described on Rosa
omeiensis (Tai 1979, Wei 1988, Hiratsuka et al. 1992, Cao & Li 1996, 1999, Zhuang & Wei 2003, Zhuang 2005,
Zhuang & Wang 2006, Zhuang et al. 2012, Xu 2013).
During an investigation of rust fungi in western China, two previously unknown Phragmidium species were

TWO NEW PHRAGMIDIUM SPECIES Phytotaxa 217 (2) © 2015 Magnolia Press • 183
found on Rosa omeiensis and R. lichiangensis. Phylogenetic analyses were performed to confirm that the isolates were
distinct species. Consequently, they were illustrated and described as the two novel species Phragmidium zhouquensis
and Ph. longissima.
TABLE 1. Sequence data analyzed in this study or obtained from GenBank (new species in bold).
Fungal taxon Host plant Specimen no Locality and date of collection GenBank accession no.
28S
Phragmidium zhouquensis Y.M. Liang & T. Yang
Rosa omeiensis BJFC-R01516 Gansu, China, Aug. 20, 2014 KP407637
BJFC-R01529 Gansu, China, Aug. 20, 2014 KP407638
Ph. longissima Y.M. Liang & T. Yang
Rosa lichiangensis BJFC-R00338 Yunnan China, Sep. 18, 2011 KP407633
BJFC-R00360 Yunnan China, Sep. 19, 2011 KP407634
Ph. biloculare
Potentilla flabellifolia BPI881121 USA JF907670a
Ph. fragariae
Potentilla sterilis — — JF907670a
Ph. fusiforme
Rosa hugonis BJFC-R00942 Gansu China, July. 18, 2013 KP407632
Rosa pendulina — Switzerland AJ715522a
Ph. handelii
Rosa webbiana BJFC-R01030 — KP407631
BJFC-R01421 Gansu, China, Aug. 15, 2014 KP407628
BJFC-R01437 Gansu, China, Aug. 15, 2014 KP407629
BJFC-R01458 Gansu, China, Aug. 17, 2014 KP407630
Ph. ivesiae
Potentilla gracilis BPI877968 USA JF907673a
BPI863637 USA JF907672a
Ph. mexicanum
Potentilla hebiichigo BPI881108 South Korea JF907671a
P. indica BPI877884 USA JF907664a
Ph. montivagum
Rosa cf. woodsii FO47828 — AF426213a
Ph. mucronatum
Rosa corymbifera — Germany AJ715520a
R. rubiginosa — Germany AJ715521a
Ph. potentillae-canadensis
Potentilla canadensis BPI877885 USA JF907668a
Ph. rubi-idaei
Rubus idaeus — — AF426215a
Ph. sanguisorbae
Sanguisorba minor — — AF426216a
Ph. tormentillae
Potentilla simplex BPI877888 USA JF907669a
Ph. tuberculatum
Rosa rugosa BJFC-R00936 Gansu, China, July. 18, 2013 KP407635
BJFC-R00959 Qinghai, China, July. 22, 2013 KP407636
Rosa sp. BPI877980 USA KJ841922a
Rosa floribunda BPI877977 USA KJ841923a
Ph. violaceum
Rubus fruticosus — — AF426214a
Puccinia tanaceti
Artemisia brevifolia IBA5340 Japan AB190908ab
a stands for sequences from GenBank.
b stands for sequences used as outgroup.

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184 • Phytotaxa 217 (2) © 2015 Magnolia Press
Materials and methods
Materials
Fresh specimens used in this study were collected in western China during 2011–2014 and deposited at the Mycological
Herbarium, Museum of Beijing Forestry University (BJFC), Beijing, China. This study also included dried specimens
on Rosa, which were loaned from the Herbarium Mycologicum Academiae Sinicae, Beijing (HMAS) (Tables 1 and
2).
TABLE 2. Comparison of telial characteristics of Phragmidium species on Rosa omeiensis in China used in this study (new species in bold).
Species
Telia Teliospores
Color Location on
hosts
Number of
cells
Size
(μm ×μm)
Papillae
(μm)
Length of
Pedicels
(μm)
Ph. zhouquensis dark brown hypophyllous (3–)6–8(–9) 67–103 × 32–39 3.5–6 80–160
Ph. mucronatum black hypophyllous (4–)6–8(–9) 55–104 × 29–36 5–17 62–184
Ph. robustum dark brown hypophyllous 3–7 50–106 × 35–45(–48) 2–8 75–190
Ph. rosae-omeiensis black stem (4–)7–9(–10) (67–)80–126 (–160) × 27–34 2–7(–10) up to 400
Ph. tuberculatum black hypophyllous (3–)4–6(–7) 52–101(–126) × 29–36 up to 20 up to 110
Microscopic analysis
For light microscopy (LM) observation, spores and leaf sections were mounted in a drop of lactophenol or lactophenol-
cotton blue. For each specimen, approximately 30 spores were randomly selected and measured using a LEICA DM2500
upright microscope (Leica, Germany). To prepare samples for surface structure examination using scanning electron
microscopy (SEM), urediniospores and leaf sections with uredinia were adhered onto aluminium stubs covered with
double-adhesive tape, coated with gold using the Hitachi SCD-005 Sputter Coater, and then observed with a Hitachi
S-3400N scanning electron microscope (Hitachi, Tokyo, Japan) operated at 5 kV.
DNA extraction and sequencing
DNA extraction and amplification of 28S rRNA were modified from the method of Tian et al. (2004) using the primers
NL1 (5-GCATATCAATAAGCGGAGGAAAAG-3) and NL4 (5-GGTCCGT GTTTCAAGACGG-3) (O’Donnell
1993). The methods for PCR analysis were according to the method of Yang et al. (2014). PCR products were examined
by electrophoresis on 1% (w/v) agarose gels stained with ethidium bromide in 1×TAE buffer. The sequences were
deposited in the GenBank database (Table 1).
Phylogenetic analysis
Sequences were aligned using ClustalX 1.83 (Thompson et al. 1997) and MEGA 6.0. Partitioned and combined
data matrices were analysed by maximum parsimony (MP) and Bayesian analyses (BA) using the Puccinia tanaceti
(AB190908) sequence obtained from GenBank as the out-group. Sequence alignments were deposited at TreeBase
(http://www.treebase.org/) under accession number 16998. Parsimony analyses were performed in PAUP* 4.0b10
(Swofford 2002), with all dataset characters treated as equally weighted and gaps treated as missing data. Trees
were inferred using the heuristic search option with tree bisection and reconnection (TBR) branch swapping and
1,000 random sequence additions. Clade stability was assessed using a bootstrap (BT) analysis with 1,000 replicates
(Felsenstein 1985). The BA was performed using MrBayes 3.1 (Ronquist et al. 2005) with Markov chain Monte Carlo
(MCMC) and Bayesian posterior probabilities (Larget & Simon 1999). Default parameters were selected, and the

TWO NEW PHRAGMIDIUM SPECIES Phytotaxa 217 (2) © 2015 Magnolia Press • 185
evolutionary model was set to the GTR model with gamma-distributed rate variation across sites and a proportion of
invariable sites (Ronquist et al. 2005). The simultaneous Markov chains were run with 1,000,000 generations, and the
tree were sampled every 100th generation.
Results
Morphology
Based on the characteristics of multiple-celled teliospores borne singly on hygroscopic pedicels and 23 germ pores
in each spore cell, the present two species identified on Rosa were assigned to Phragmidium and illustrated as Ph.
zhouquensis and Ph. longissima in the taxonomy section (Figs. 1, 2).
Molecular phylogeny
The 28S phylogenetic trees included the 30 samples listed in Table 1. Following alignment, the final dataset contained
620 total characters, with 461 constant characters and 54 parsimony-uninformative variable characters. MP analysis
with the remaining 105 parsimony-informative characters resulted in eight equally parsimonious trees with the
following parameters: tree length (TL) = 256; consistency index (CI) = 0.742; retention index (RI) = 0.912; and
rescaled consistency index (RC) = 0.677. The average standard deviation of split frequencies calculated by BA was
0.008781.
MP and BA gives the same topology that the two new species formed two distinct lineages with a BT value and
Bayesian posterior probability of 96/0.97 and 100/1.00, respectively (Fig. 3).
Taxonomy
Phragmidium zhouquensis Y. M. Liang & T. Yang, sp. nov. (Fig. 1)
MycoBank no.:—MB811453
Etymology:—Zhouquensis, referring to the location of the collection of this species.
Diagnosis:—Telia hypophyllous, dark brown, teliospores 67–103 × 32–39 m, (3–)6–8(–9)-celled, yellowish
brown, apical papilla 3.5–6 m, verrucose, 2–3 germ pores in each cell, pedicels 80–160 × 14–24 m.
Type :—CHINA, Gansu Province, Zhouqu County, on Rosa omeiensis Rolfe (Rosaceae), 20 August 2014, coll. Y.
M. Liang & B. Cao (Holotype: BJFC-R01516; Paratype: BJFC-R01529).
Spermogonia, aecia, and uredinia unknown.
Telia produced on the abaxial leaf, scattered or loosely grouped, minute, 0.5–2.5 mm, pulverulent, dark brown,
leaf colour turns rose-red to aubergine at the position of the sorus (Figs 1A, 1B); teliospores ellipsoid-oblong to
cylindrical, 67–103 × 32–39 m, 3–9-celled, mostly 6–8-celled, the uppermost cell longer than the others, rounded at
both ends, often somewhat attenuate at the apex, wall 2–5 m thick, yellowish brown (Figs 1E, 1F), with coarse and
nearly hyaline verrucae on the spore surface (Figs 1C, 1D), apical papilla conical, pale-coloured or hyaline with dense
tubercles, 3.5–6 m long, not constricted at the septa, with 2–3 germ pores in each cell (Fig. 1E); pedicels 80–160 m
long, persistent, upper part colourless or pale brown, lower part with coarse surface and yellowish content, slightly
swollen, gradually become lanceolate, approximately 14–24 wide at the broadest diameter (Figs 1D, 1E).
Notes:—Phragmidium primarily parasitise Potentilla, Rubus, and Rosa, and rust species do not overlap among
these three host genera. Of the 11 Phragmidium species reported on Rosa in China, four species colonise Rosa omeiensis,
including Ph. mucronatum, Ph. robustum, Ph. rosae-omeiensis, and Ph. tuberculatum (Table 2). Phragmidium
zhouquensis differed from Ph. mucronatum primarily by the dark brown telia (Figs 1A, 1B) and short papilla with
lengths up to 6 m (Figs 1D, E), whereas Ph. mucronatum telia were black and teliospores with papillae at the top
had lengths up to 17 m (Wei 1988, Zhuang et al. 2012). Phragmidium robustum was characterized by wider and
more robust teliospores (50–106 × 35–48 m), mostly 5–6-celled, with longer pedicels of 70–190 m (Zhuang & Wei
2009, Zhuang et al. 2012); these features can be used to distinguish it from the present species. The new species Ph.
zhouquensis could be distinguished from Ph. rosae-omeiensis by its verrucose teliospores (Fig. 1D); by contrast, the
surface of Ph. rosae-omeiensis teliospores was smooth. The common species, Ph. tuberculatum, can be distinguished

YANG ET AL.
186 • Phytotaxa 217 (2) © 2015 Magnolia Press
from Ph. zhouquensis according to its 1–8-celled (mostly 6-celled) teliospores bearing long papillae (7–23 m) at the
spore apices; the papillae of Ph. zhouquensis were 3.5–6 m long (Figs 1D, 1E) (Wei 1988, Zhuang et al. 2012).
Phragmidium zhouquensis
can be distinguished from other morphologically closely-related Rosa species as
follows. Phragmidium fusiforme is one of the most widespread Phragmidium species in the northern hemisphere; it
is characterized by multiple-celled (mostly greater than 10-celled) and fusiform teliospore with long papilla up to 15
m at the spore apex, which is obviously different from that of the present species (Wei 1988, Hiratsuka et al. 1992,
Wahyuno 2001, Zhuang et al. 2012). Phragmidium zhouquensis also differed from Ph. montivagum by the dark brown
telia (Figs 1A, 1B) with ellipsoid-oblong to cylindrical teliospores and lanceolate pedicels (Figs 1D, 1E), whereas
the latter species had black telia aggregated by fusiform or subclavate teliospores with hygroscopic and bulbous
pedicels.
FIGURE 1. Phragmidium zhouquensis (BJFC-R01516, holotype). A. Gross features of infected leaves. B and C. Surface view of telium.
D. Teliospores with verrucose surface. E. Teliospores with yellow content and hyaline verrucae, 2–3 germ pores in each cell. F. Vertical
section of telium. Scale bars: A = 1 cm; B = 500 m; C and F = 200 m; D and E = 50 m.
Phragmidium longissima Y. M. Liang & T. Yang, sp. nov. (Fig. 2)
MycoBank no.:—MB811452
Etymology:—Longissima, referring to the characteristically long teliospores of this species.
Diagnosis:—Urediniospores uniformly echinulate, with pore membrane at the germ pore, telia black, teliospores
(8–)9–11(–12)-celled, 85–122 × 21–30 m, wall dark brown, verrucose, papilla 2.5–5.5 m, verrucose, pedicel length
0.51 times the spore length.
Holotype:—CHINA, Yunnan Province, Lanping County, Mt. Changyan, on Rosa lichiangensis T. T. Yu & T. C .
Ku, 18 September 2011, coll. T. Yang, Exsiccate BJFC-R00338.

TWO NEW PHRAGMIDIUM SPECIES Phytotaxa 217 (2) © 2015 Magnolia Press • 187
FIGURE 2. Phragmidium longissima (BJFC-R00338, holotype). A. Vertical section of paraphyses in uredinium. B. Urediniospore with
echinulate surface. C. Globose or sub-globose urediniospores with pore membrane at the germ pore (arrow indicates the position of the
pore membrane). D. Teliospore with two germ pores in each cell. E. Black telium on the abaxial leaf. F. Vertical section of telium. G.
Surface view of telium. H and I. Teliospores with verrucose surface and smooth pedicel. Scale bars: A and C = 20 m; B = 10 m; C and
I = 20 m; D and H = 50 m; E = 200 m; F and G = 100 m.
Paratype:—CHINA, Yunnan Province, Lanping County, Mt. Luoguqing, on Rosa lichiangensis T. T. Yu & T. C.
Ku, 19 September 2011, coll. T. Yang, Exsiccate BJFC-R00360.
Spermogonia and aecia unknown.
Uredinia hypophyllous, scattered or loosely grouped, minute, rounded, 0.05–0.2 mm across, pale yellow;
paraphyses numerous, clavate or broadly clavate, 42–75 × 16–30 m, sub-erect or incurved, located around the sorus,
wall smooth, colourless (Fig. 2A); urediniospores globose or sub-globose, 20–26 × 18–21 m, wall approximately 1
m thick, uniformly echinulate, colourless, wall at germ pore conspicuously intruding in the spore lumen to form a
pore membrane (Figs 2B, 2C). Telia produced on the abaxial leaf, scattered or grouped, minute, irregular in shape, 0.1–
0.3 mm across, early naked, pulverulent, black (Fig. 2E); teliospores cylindrical, 8–12-celled, generally 9–11-celled,
85–122 × 21–30 m, round at both ends, not constricted at the septum, apical papillae obtuse, approximately 2.5–5.5
m long, brownish-yellow, densely verrucose, usually two germ pores in each cell, wall approximately 2–5 m thick,
dark brown, densely and minutely verrucose, with colourless tubercles (Figs 2D, 2F–2I); pedicles persistent, 65–111
m long, average length 0.51 times the spore length, swelling broadly clavate at the lower half, approximately 11–17
m at the broadest diameter, brownish-yellow in the upper half, nearly colourless in the lower half, smooth (Figs 2C,
2H).
Notes:—Phragmidium longissima differed from Ph. rosae-multiflorae in that it had uniformly echinulate
urediniospores (Fig. 2B) and generally 9–11-celled teliospores (Figs 2D, 2F), whereas the latter was characterized
by verrucose urediniospores and mostly 7–8-celled teliospores. Phragmidium. rosae-multiflorae pedicels were

YANG ET AL.
188 • Phytotaxa 217 (2) © 2015 Magnolia Press
obviously wider (up to 30 m) than those of Ph. longissima (Wei 1988, Hiratsuka et al. 1992, Zhuang et al. 2012).
Phragmidium americanum was similar to Ph. longissima with respect to teliospore size and cell number, but was
distinct in that teliospores were sometimes slightly narrowed above and the pedicel length averaged 11.5 times the
spore length (Cummins 1931, Wahyuno 2001). Phragmidium longissima resembled Ph. rosae-californicae in the size
of teliospores and pedicels, but was distinguished by the rounded cells at both teliospore ends (Fig. 2D). Phragmidium
rosae-californicae was characterized by teliospores strikingly acuminate above and with a typically longer apical
cell, which graded directly into the apiculus (Cummins 1931). Phragmidium americanum and Ph. rosae-californicae
are distributed primarily in North America and have never been recorded in China (Cummins 1931). Phragmidium
longissima was the first Phragmidium species reported on Rosa lichiangensis, which obviously differed from all the
previously described Phragmidium species by the uredinial and telial host range (Wei 1988, Hiratsuka et al. 1992,
Wahyuno 2001, Tykhonenko 2007, Zhuang & Wei 2009, Zhuang et al. 2012).
FIGURE 3. Phylogram constructed by maximum parsimony and Bayesian analyses based on 28S sequences. Bootstrap values were
calculated from 1,000 replications. Parsimony bootstrap (before the slash marks) and Bayesian posterior probabilities (after the slash
marks) greater than 50% are shown. Bars: 10 nucleotide substitutions. New species are shown in bold.

TWO NEW PHRAGMIDIUM SPECIES Phytotaxa 217 (2) © 2015 Magnolia Press • 189
Discussion
The new species Ph. zhouquensis was characterized by dark brown telia and 3–9-celled teliospores (Fig. 1E) with
minute verrucae on the surface and a 3.5–6 m long papilla at the spore apex (Fig. 1D). The other new species, Ph.
Longissima, was characterized by echinulate urediniospores (Fig. 2B), with a pore membrane at the germ pore (Fig.
2C), 9–11-celled teliospores with typically two germ pores per cell, and hygroscopic pedicels of about 0.51 times the
spore length (Fig. 2D).
The phylogenetic results indicate that Ph. zhouquensis and Ph. longissima are two distinct lineages with high BT and
Bayesian posterior probability (96/0.97 and 100/1.00, respectively) (Fig. 3). The two new species are phylogenetically
distinct from other Phragmidium species. Phragmidium zhouquensis is more closely related to Ph. fragariae, which
is parasitic to Potentilla plants; however, they are clearly different in terms of telial characteristics. The telia of Ph.
fragariae are often present on the petioles of Potentilla, while the telia of Ph. zhouquensis are only found on the leaf
surfaces of Rosa. Except for the difference of host range and infect different portions of the plants. Ph. zhouquensis
is characterized by larger teliospores (67–103 × 32–39 m) with mostly 6–8-celled and conical papillae at the top of
spores, while Ph. fragariae has 2–5-celled teliospores (46.5–77.5 × 24–34.5 m) without papillae. Furthermore, Ph.
fragariae also differs from Ph. zhouquensis in that it has shorter pedicels (24.5–57 m in length vs. about 80–160 m
in length) (Petrova & Denchev, 2004). The high supported cluster formed by two Ph. longissima specimens is treated
as a sister clade of Ph. mucronatum, which is also found on Rosa plants. However, they are morphologically different
in many respects. Phragmidium longissima is characterized by long, mostly 9–11-celled teliospores (85–122 × 21–30
m), while the teliospores of Ph. mucronatum are commonly 5–9-celled and 67.5–103.5 m long. In addition, Ph.
mucronatum has papilla at the top of the teliospore (up to 13.5 m long), which are clearly longer than those of Ph.
longissima (Wei 1988, Hiratsuka et al. 1992, Wahyuno 2001, Zhuang et al. 2012).
According to the consensus results of morphological and phylogenetic analyses, Ph. zhouquensis and Ph. longissima,
which were collected from two native Rosa species (R. omeiensis and R. lichiangensis, respectively), are two distinct
taxa.
Acknowledgements
This research was supported by the National Natural Science Foundation of China (no. 31470646). We wish to thank
the Herbarium Mycologicum Academiae Sinicae, Beijing, China (HMAS), for providing herbarium specimens.
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