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菌物学报
jwxt@im.ac.cn 15 July 2015, 34(4): 589‐603
Http://journals.im.ac.cn Mycosystema ISSN1672‐6472 CN11‐5180/Q © 2015 IMCAS, all rights reserved.
研究论文 Research paper DOI: 10.13346/j.mycosystema.150080
Supported by the National Basic Research Program of China (973 Program, 2014CB138305) and the National Natural Science
Foundation of China (31270074).
*Corresponding author. E‐mail: zaiweige@gmail.com, fungi@mail.kib.ac.cn
Received: 23‐03‐2015, accepted: 09‐04‐2015
Species diversity of Flammulina in China: new varieties and a new record
GE Zai‐Wei1* LIU Xiao‐Bin1, 2 ZHAO Kuan1, 2 YANG Zhu‐Liang1*
1Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences,
Kunming, Yunnan 650201, China
2University of Chinese Academy of Sciences, Beijing 100039, China
Abstract: Species within the genus Flammulina are among the most important economically cultivated mushrooms in East Asia.
Based on examinations of the morphological characters and molecular phylogeny reconstructed from the internal transcribed
spacer (ITS) sequences, F. velutipes var. filiformis and F. velutipes var. himalayana are proposed as new varieties, and F.
populicola is reported as a new record for China. Detailed descriptions and illustrations of macroscopic and microscopic
characters are provided for the taxa known from China, and a key to the taxa is included.
Key words: Flammulina, Physalacriaceae, Flammulina velutipes
冬菇属的新变种和中国新记录种
葛再伟 1* 刘晓斌 1, 2 赵宽 1, 2 杨祝良 1*
1中国科学院昆明植物研究所东亚植物多样性与生物地理学院重点实验室 云南 昆明 650201
2中国科学院大学 北京 100039
摘 要：冬菇属 Flammulina 真菌是重要的食用菌，在东亚广为栽培。基于形态特征及内转录间隔区（ITS）序列分析，报
道了该属真菌的两个新变种——冬菇丝盖变种 F. velutipes var. filiformis 和冬菇喜玛拉雅变种 F. velutipes var. himalayana，以
及中国的一个新记录种——杨树冬菇 F. populicola。提供了中国冬菇属已知物种和变种的形态描述、生境照片及检索表。
关键词：冬菇属，膨瑚菌科，金针菇
INTRODUCTION
The genus Flammulina P. Karst. is a member of
the family Physalacriaceae (Agaricales), and contains
14 species, including the well‐known edible
mushroom F. velutipes (Curtis) Singer and allies.
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Species within Flammulina are mainly distributed in
the Northern Hemisphere, although F. velutipes can
also be found in Australasia and South America,
which probably due to recent introduction (Methven
et al. 2000; Yokoyama 1991). Flammulina can be
easily recognized based on characters such as
glabrous pileus which is viscid when wet, yellowish
lamellae often adnately to adnexedly attached,
inamyloid spores and suprapellis of a hymeniform or
palisadic layer over gelatinized hypodermium
interspersed with pilocystidia. However, species
within this genus look quite similar to each other in
the field and microscopical characters must be
applied to delimit the taxa. Suprapellis structure,
spore shape and size, and to a lesser extent,
cheilocystidia are the most useful characters for
identification in this genus.
Since Arnolds (1977) revealed that Flammulina
is not a monotypic genus by separating F. ononidis
from F. velutipes, and Bas (1983) later on
demonstrated that there are several different taxa
distributed in Western Europe, there has been a
revival of interest in detailed investigation on the so
called F. velutipes from different geographical
regions, and a few new species have been described
then (Redhead & Petersen 1999; Redhead et al.
1998, 2000; Perez‐Butron & Fernández‐Vicente 2007;
Ge et al. 2008). Most of the morphological species
were confirmed by mating studies (Petersen et al.
1999), restriction fragment length polymorphism
(RFLP) patterns (Methven et al. 2000), and
phylogeny reconstructed from the internal
transcribed spacer (ITS) sequences (Hughes et al.
1999).
In Europe and North America, more than ten
species have been reported (Methven et al. 2000),
and Europe has been suggested as a center of
diversity where F. populicola, F. velutipes, F. elastica,
F. rossica and F. ononidis are distributed (Hughes et
al. 1999). In a recent study focusing on the species
diversity of Flammulina in China (Fig. 1),
southwestern China has been suggested as another
center for Flammulina species and F. rossica has
been suggested as a Holarctic element (Ge et al.
2008).
Among the species distributed in China, F.
velutipes and F. rossica are the most common ones.
However, only F. yunnanensis (Fig. 1F) has been
provided with detailed descriptions and illustrations
in that study. After examination of additional
specimens collected in the following years, this
study presents some findings resulted in the
investigations based on the morphological
examinations and ITS sequences analyses. The
objectives of the present study are: (i) to
characterize species occurred in China on the basis
of morphology and molecular data; (ii) to provide
detailed description and illustrations of macro‐ and
micro‐morphology for the Chinese species of
Flammulina.
1 MATERIALS AND METHODS
Specimens examined in this study have been
deposited in Herbarium of Cryptogams, Kunming
Institute of Botany, Chinese Academy of Sciences
(HKAS), Jilin Agricultural University (HMJAU), or
Farlow Herbarium (FH). Methods for morphological
examinations were described in Ge et al. (2008).
DNA was ex t rac ted us ing a modi f ied
cetyltrimethylammonium bromide (CTAB) extraction
protocol (Doyle & Doyle 1987). ITS region was PCR
amplified using the primer pair ITS1F/ITS4 (White et
al. 1990; Gardes & Bruns 1993). PCR products were
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Fig. 1 Basidiomata of Flammulina species in China. A: F. populicola (HKAS 81094); B: F. rossica (HKAS 84307); C: F. velutipes var.
filiformis (HKAS 85819); D: F. velutipes var. himalayana (HKAS 80829); E: F. sp. (HKAS 51191); F: F. yunnanensis (HKAS 41344).
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sent to commercial company (Shanghai Sangon
Biological Engineering Technology and Service Co.,
Ltd.) for sequencing. Sequences generated from this
study (GenBank numbers KP867921–KP867934,
Table 1) and additional representative sequences
from GenBank were aligned with those used in Fig. 1
of Ge et al. (2008). Alignment, maximium likelihood
(ML) analysis were the same with those used in Ge
et al. (2014), and maximium parsimony (MP)
analysis was the same as that used in Ge et al.
(2008), except the gaps were treated as missing data.
Flammulina stratosa was used to root the tree as
performed by previous studies (Hughes et al. 1999;
Ge et al. 2008).
2 TAXONOMIC DESCRIPTIONS
Flammulina populicola Redhead & R.H. Petersen,
Mycotaxon 71: 288, 1999. Fig. 2
Basidiomata (Fig. 1A, Fig. 2a) in clusters. Pileus
6–7.5cm in diam., stout, convex to broadly convex;
surface smooth, shining, greasy, some with brownish
patches, center golden brown, elsewhere bright
ochraceous brown, hygrophanous, subviscid to
viscid when wet, margin (3–5mm) transparently
sulcate, waved. Lamellae emarginately adnate,
crowded, yellowish cream, edge even; lamellulae
3–4 tires. Stipe central, 5–7 × 1–1.5cm,
subcylindrical, subequal to slightly attenuate upward,
apical part concolorous with pileus, elsewhere
brownish, flat, tough, with pseudorrhiza. Context
whitish, unchanging when bruised, tough; taste
mild.
Basidiospores (Fig. 2b) [40/2/1] 5–6.5(7.5) ×
(3)3.5–4µm (x = 5.64 ± 0.60 × 3.61 ± 0.31µm), Q =
1.43–1.71(2.0), (Q = 1.56 ± 0.13), ellipsoid,
sometimes obvoid or lacrymoid, smooth, hyaline,
thin‐walled, non‐amyloid, with an apiculus 1–1.3µm
long. Basidia (Fig. 2c) 23–30 × 4–5µm, narrowly
clavate, hyaline, thin‐walled, 4‐spored, occasionally
2‐spored; sterigmata up to 3µm long. Pleurocystidia
(Fig. 2c) lageniform to ventricose, abundant to
scattered, projecting up to 35–40µm beyond the
surface of the hymenium, 52–96 × 8–12µm, hyaline
to yellowish, slightly thick‐walled. Cheilocystidia (Fig.
2d) similar to pleurocystidia both in size and form.
Lamellar trama regular to somewhat interwoven,
composed of colorless filamentous hyphae 6–15µm
in width. Suprapellis (Fig. 2e) a hymeniform layer
composed of broadly clavate to pedundiculate cells
(14–20 × 7–10µm) and irregularly subclavate to
clavate cells measuring of 2.5–6µm in width,
interspersed with typical brownish to reddish brown,
lageniform to ventricose pileocystidia (70–85 ×
7–10µm).
Habitat: Clustered on the ground at the base of
Populus sp. in a forest dominated by Pinus
tabulaeformis Carr.
Material examined: China, Inner Mongolia:
Alxa Zuoqi, Helan Mountains, Beisi, 29 September
2009, X.‐H. Wang 2342 (HKAS 81094), alt. 2 000m.
Notes: Flammulina polulicola is a record new to
China. Macromorphology of the Chinese collection is
in accordance with the descriptions of typical F.
populicola, which is originally described from
California and Alaska (Redhead & Petersen 1999),
and later on also found in Sweden (Hughes et al.
1999). The presence of this species in Inner
Mongolia extends its distribution range to northern
China. Microscopically, this species is characterized
by the combination of a hymeniform suprapellis with
typical pileocystidia, short, ellipsoid basidiospores.
Flammulina populicola seems to prefer Populus spp.
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Fig. 2 Flammulina populicola (HKAS 81094). a: Basidiomata; b:
Basidiospores; c: Basidia and pleurocystidia; d: Cheilocystidia;
e: Elements of suprapellis.
The Chinese collection was found growing at the
base of Populus sp., and similar substrates were
recorded for American collections (Redhead &
Petersen 1999). The basidiospores are smaller than
those reported from North America (6.3–7.4 ×
3.7–4.5µm) by Redhead & Petersen (1999), and
there are not many basidiospores can be observed in
the Chinese collection probably because that the
basidiomata were premature when they were
collected. As discussed in Ge et al. (2008), F.
yunnanensis is very similar to F. populicola in
producing a hymeniform suprapellis and small
basidiospores. However, F. yunnanensis occurs on
rotten trunks of fagaceous plants and other
broad‐leaved trees in warm regions in southwestern
China, whereas F. populicola most frequently fruits
on the ground at the base of Populus trees in
temperate regions (Redhead & Petersen 1999). The
ITS sequence of F. populicola generated from the
Chinese collection is closely related to that
generated from the Alaska collection (Fig. 3).
However, the phylogenetic position of species is
unsettled, as it clustered with F. mexicana Redhead,
Estrada & R.H. Petersen.
Flammulina rossica Redhead & R.H. Petersen,
Mycotaxon 71: 290, 1999. Fig. 4
Basidiomata (Fig. 1B, Fig. 4a) in clusters. Pileus
1.5–7cm in diam., convex to almost applanate;
surface smooth, disc area ochraceous brown,
elsewhere ochraceous, dull yellow to cream,
subviscid to viscid when wet, hygrophanous, margin
paler, transparently striate (3–5mm), waved.
Lamellae emarginately adnate, crowded, white,
cream to yellowish, edge even, with 3–4 tires of
lamellulae. Stipe central, 2–7 × 0.2–0.7cm, hollow,
subcylindric, slightly attenuate upward, apical part
concolorous with pileus, elsewhere blackish, densely
covered with brown to dark brown velvety hairs.
Context whitish, unchanging; taste mild.
Basidiospores (Fig. 4b) [111/5/3] (7.5) 8.5–10
(11) × (3.5) 4–5µm (x = 9.22 ± 0.55 × 4.25 ± 0.32µm),
Q = (1.88) 2–2.38 (2.5), (Q = 2.17 ± 0.13), ellipsoid to
oblong ellipsoid, smooth, hyaline, thin‐walled,
non‐amyloid, with an apiculus up to 1.5µm. Basidia
(Fig. 4c) 23–35 × 5–8µm, narrowly clavate, hyaline,
thin‐walled, 4‐spored; sterigmata up to 3.5µm long.
Pleurocystidia (Fig. 4c) lageniform to ventricose,
scattered, projecting up to 30µm beyond the surface
of the hymenium, 10–15µm in width, yellowish,
slightly thick‐walled. Cheilocystidia abundant,
ventricose to fusiform, similar to pleurocystidia both
in shape and size. Lamellar trama regular to
somewhat interwoven, composed of colorless
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Fig. 3 One of the 267 most parsimonious trees based on ITS sequences (tree length = 300, CI = 0.690, RC = 0.595). Clade with ML
Bootstrap support values greater than 50% are indicated with thick branches. MP bootstrap support values greater than 50% are
indicated above the branch.
filamentous hyphae. Suprapellis (Fig. 4d) a
hymeniform layer composed of clavate to subclavate
(12–40 × 8–16µm) cells with moniliform hyphal tips
or protruding branched hyphae (2–4µm in width),
pale brown to yellow brown, occasionally
interspersed with typical elongate‐fusiform to
lanceolate pileocystidia (50–75 × 12–15µm) which is
brownish, brown to yellow tawny, slightly
thick‐walled. Medipellis nearly not gelatinized.
Habitat: Mostly clustered on substrates of Salix
spp. and Betula spp., occasionally on Picea spp.
Material examined: China: Jilin, Baihe, 15
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Fig. 4 Flammulina rossica (HKAS 32155). a: Basidiomata; b: Basidiospores; c: Basidia and pleurocystidia; d: Elements of
suprapellis.
August 2009, L.F. Zhang 506 (HKAS 7930), in Betula
sp. forest; Jilin, Zuojia, 16 September 2000, 1209
(HMJAU 20588); Sichuan, Daocheng, 4 July 1998, on
Picea sp., Zhu. L. Yang 1993 (HKAS 32155); Sichuan,
Xiangcheng, 16 July 1998, on rotten wood of Salix,
Zhu. L. Yang 2353 (HKAS 32154); Tibet, Riwoqe, 8
August 2004, on Salix sp., Zhu. L. Yang 4320 (HKAS
43699); Tibet, Qamdo, 27 July 2004, on Salix sp., Z.
W. Ge 190 (HKAS 45970); ibidem, 7 August 2004, on
Salix sp., Z.W. Ge 296 (HKAS 46076); ibidem, 7
August 2013, on Salix sp., Z.W. Ge 3469 (HKAS
84307).
Note: Flammulina rossica is characterized by its
paler basidiomata, a somewhat hymeniform
suprapellis with typical pileocystidia, and elongated
ellipsoid basidiospores (Redhead & Petersen 1999).
Suprapellis structure of this species is intermediate
between those of F. velutipes and F. populicola, thus,
makes the identification difficult in some cases if
only morphological characters are used. The
elements of suprapellis of the Chinese collections
exhibit a wide range variation, from composed of
mostly moniliform hyphal tips (HKAS 32155) to
almost by clavate to narrowly clavate elements
(HKAS 7930). However, the ITS sequences of these
collections have little differences, and the phylogeny
based on ITS sequences clearly shows they are
conspecific (Fig. 3).
Flammulina velutipes (Curtis) Singer, Lilloa 22: 307,
1951 (1949).
The identity of F. velutipes was murky before its
lectotype and epitype were designated respectively
by Bas (1983) and Redhead & Petersen (1999). Even
after the segregation of two species (F. ononidis
Arnolds and F. fennae Bas) from it, the remaining F.
velutipes is still a highly variable species (Badalyan &
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Hughes 2004; Bas 1983; Nishizawa et al. 2003;
Psurtseva & Mnoukhin 1998), and recombination or
gene conversion were detected in the ribosomal ITS
region (Hughes & Petersen 2001). Bas (1983)
proposed F. velutips var. lactea for those having
white to cream basidiomata; and F. velutips var.
lupinicola was proposed for another variety with
larger spores (7–14.8 × 3.7–6.5µm) and so far only
known from California on Lupinus arboreus
(Redhead & Petersen 1999).
According to ITS phylogeny, sequences from
Chinese F. velutipes were clustered with those from
North America and Europe (Fig. 3, shaded in grey).
The sequence from the Northwestern Yunnan
collection and a sequence from India clustered
together (clade A); strains from the Europe and
United States were jointly grouped together and
form another clade (clade B); collections from China,
South Korea and Canada jointly formed the third
clade (clade C).
Several Chinese collections examined displayed
morphological characters that are diagnostic for
identifying F. velutipes: suprapellis composed by an
ixotrichodermium of ramifying filamentous to
strangulate hyphal tips with interspersed
fusoid‐lanceolate pileocystidia (Bas 1983; Redhead
& 1999). ITS sequences of Chinese collections were
grouped with sequences generated from collections
from other regions of the world, but detailed
microscopic examinations revealed that there are
subtle differences among collections of these three
subclades. Considering their differences in the
phylogeny and distribution areas, as well as the
subtle differences in morphology, we propose two
varieties for F. velutipes herein.
Flammulina velutipes var. filiformis Z.W. Ge, X.B. Liu
& Zhu L. Yang, var. nov. Fig. 1C, Fig. 5
Fungal Name Number: FN570170
Holotypus: China: Yunnan, Kunming, Kunming
Botanical Garden, 28 August 2014, Zhu. L. Yang 5810
(HKAS 83890).
Etymology: filiformis refers to the suprapellis of
this taxon dominantly formed by slender hyphae.
Basidiomata (Fig. 1C) in clusters. Pileus
1.5–4.5cm in diam., convex to applanate; surface
smooth, shining, greasy, center brown to yellowish
brown, elsewhere ochraceous brown or brownish,
yellowish, cream to nearly white, hygrophanous,
subviscid to viscid when wet, margin (2–3mm)
transparently sulcate. Lamellae emarginately adnate,
crowded, yellowish or cream, edge even; lamellulae
2–3 tires. Stipe central, 1.5–8 × 0.2–0.6cm,
subcylindrical, subequal to slightly attenuate upward,
whitish near the apex, becoming brown to dark
brown downward, densely covered with brown
velvety hairs. Context whitish; taste mild.
Basidiospores (Fig. 5a) [52/3/3] 5.5–7.5(8) ×
2.5–3.5µm (x = 6.63 ± 0.74 × 3.02 ± 0.27µm), Q =
(1.83) 1.86–2.4(2.6) (Q = 2.20 ± 0.22), ellipsoid to
oblong ellipsoid, smooth, hyaline, thin‐walled, with
an apiculus 0.4–0.5µm. Basidia (Fig. 5b) 22–27 ×
4–5.5µm, narrowly clavate, hyaline, thin‐walled,
4‐spored; sterigmata up to 4µm long. Pleurocystidia
(F ig. 5d) lageniform to ventricose, scattered,
projecting about 30µm beyond the surface of the
hymenium, 45–70 × 10–20(25)µm, hyaline to
yellowish, slightly thick‐walled. Cheilocystidia (Fig.
5c) rare to abundant, vase‐form, ventricose to
fusiform, similar to pleurocystidia, 30–60 × 9–13µm.
Lamellar trama regular to somewhat interwoven,
composed of colorless fi lamentous hyphae.
Suprapellis (Fig. 5e) composed by an ixotrichodermium
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Fig. 5 Flammulina velutipes var. filiformis (HKAS 83890). a:
Basidiospores; b: Basidia at different stages of development;
c: Cheilocystidia; d: Pleurocystidia; e: Elements of suprapellis.
of rarely branching filamentous hyphae (1.5–5µm in
width), interspersed with fusoid‐lanceolate
pileocystidia (50–160 × 6–15µm) which is brownish,
brown to yellow tawny, slightly thick‐walled. Clamp
connections common in all tissue.
Habitat: substrates of Betula platyphylla,
Broussonetia papyrifera, Dipentodon sinicus,
Neolitsea sp., Salix spp., and other broad‐leaved
trees.
Additional material examined: China: Hubei,
Wuhan, 20 November 2006, H.Y. Zhang s.n. (HKAS
51962); Hunan, Changsha, 24 July 2004, P. Zhang 273
(HKAS 47767); Jilin, Changbai Mt., 27 October 2006,
B. Wang 2 (HKAS 51988); Sichuan, Gongga Mt., 17
August 1997, DH97‐080 (FH DSH97‐080); Yunnan,
Kunming, 9 July 2004, Z.W. Ge 401 (HKAS 49485);
ibidem, 23 August 2014, Zhu L. Yang 5808 (HKAS
83888); ibidem, 28 August 2014, Zhu L. Yang 5810
(HKAS 83890); Yunnan, Longling, 21 June 2014, X. B.
Liu 355 (HKAS 85819); 11 August 2014, X.B. Liu 610
(HKAS85820); ibidem, 21 August 2014, X.B. Liu 681
(HKAS85821), ibidem, 21 August 2014, X.B. Liu 682
(HKAS85822); China Center for Mushroom Spawn
Standards and Control, strain CCMSSC04549,
CCMSSC04550, CCMSSC04551, CCMSSC04553,
CCMSSC04554, CCMSSC04555.
Note: Flammulina velutipes var. filiformis is
characterized by the ochraceous to yellowish
basidiomata and the suprapellis composed of
slender hyphae and fusoid‐lanceolate pileocystidia.
The typically orange‐red‐brown to dark‐red‐brown F.
velutipes var. velutipes differs from the new variety
by its frequently branched ixohyphidia and larger
basidiospores (Bas 1983; our own study on materials
collected from Germany).
Flammulina velutipes var. lactea, originally
described from Netherlands, differs from the new
variety by having ivory basidiomata which become
white when dried, and larger cylindrical
basidiospores measuring 7.3–10.1 × 2.9–4.0µm (Bas
1983). Flammulina velutipes var. lupinicola, originally
described from Western United States, differs from F.
velutipes var. filiformis in having larger spores
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7.3–10.1 × 2.9–4.0µm and its limited distribution
area largely on a specific host Lupinus arboreus
native to California coastal dunes (Redhead &
Petersen 1999).
Flammulina velutipes var. himalayana Z.W. Ge,
Kuan Zhao & Zhu L. Yang, var. nov. Fig. 1D, Fig. 6
Fungal Name Number: FN570169
Holotypus: China: Yunnan Province, Shangri‐la
County, Luoji Xiang, alt. 3 500m, 3 September 2013,
K. Zhao 404 (HKAS 80829).
Etymology: himalayana refers to the region
where the type of this variety was collected.
Pileus (Fig. 1D) 2–4cm in diam., plano‐convex;
surface ochraceous, paler toward margin, viscid
when wet; context white. Lamellae adnate to
sinuate, whitish, 0.3–0.4cm in height, with 2 tires of
lamellulae, edge even. Stipe 3–4 × 0.5–0.7cm,
densely covered with yellow brownish tiny hairs.
Basidiospores (Fig. 6a) [40/2/1] 6–7 × 3–4µm (x
= 6.48 ± 0.45 × 3.34 ± 0.39µm), Q = (1.63)1.71–2.33,
(Q =1.96 ± 0.20), elongate ellipsoid, smooth, hyaline,
thin‐walled, non‐amyloid. Basidia (Fig. 6b) 20–26 ×
4–5µm, narrowly clavate, hyaline, thin‐walled,
4‐spored, occasionally 2‐spored; sterigmata up to
4µm long. Pleurocystidia (Fig. 6b) lageniform to
ventricose, projecting up to 25µm beyond the
surface of the hymenium, 35–46 × 12–15µm,
brownish, slightly thick‐walled. Cheilocystidia (Fig.
6c) rare, similar to pleurocystidia in size and shape.
Lamellar trama regular, composed of colorless,
thin‐walled filamentous hyphae. Suprapellis (Fig. 6d)
an ixotrichoderm layer embedded in gelatinous
substances, composed of i xohyphydia and
filamentous hyphae derived from ixohyphydia
interspersed with pileocystidia. Filamentous hyphae
1–2µm, branches not very often, hyal ine;
Fig. 6 Flammulina velutipes var. himalayana (HKAS 80829). a: Basidiospores; b: Basidia and a pleurocystidium; c: Cheilocystidia; d:
Elements of suprapellis.
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ixohyphidia 3–4µm, hyaline or yellow browish,
sometimes inflated to subclavate elements (6–7µm)
with protruding apicals. Pileocystidia
elongate‐fusiform to lanceolate (60–90 × 7–10µm),
slightly thick‐walled, yellowish to brownish. Clamp
connections common in all tissue.
Habitat: Clustered on the stump of Betulaceae
in mixed forest dominated by Picea and Abies.
Note: Flammulina velutipes var. himalayana is
characterized by the ochraceous basidiomata on the
whole, and so far only known from Himalaya regions.
Besides the type collection, there is a sequence
(DQ978219) generated from material collected from
North Western Himalaya, India which was only 7
base pairs difference from the sequence of the type.
Flammulina velutipes var. himalayana differs
from F. velutipes var. filiformis by the moderately
differentiated suprapellis composed of an
ixotrichodermium of irregular, filamentous hyphae
derived from fusoid or very irregular thorny hyphidia.
The European F. velutipes var. lactea differs from the
new variety by its ivory basidiomata and cylindrical
basidiospores measuring 7.3–10.1 × 2.9–4.0µm (Bas
1983). The American F. velutipes var. lupinicola
differs from the new variety by its larger spores
7–14.8 × 3.7–6.5µm and geographic distribution
restricted to California coastal dunes and the pacific
host Lupinus arboreus (Redhead & Petersen 1999).
Key to the taxa of Flammulina in China
1. Suprapellis an ixotrichodermium of erect, filamentous, narrowly fusoid or very irregular thorny elements ..... 2 (variants of F. velutipes)
1. Suprapellis hymeniform to subhymeniform, composed of clavate cells intermixed with a few to many fusiform,
strangulate‐fusiform or forked ascending hyphal tips and pileocystidia ..................................................................................... 3
2. Suprapellis an ixotrichoderm of erect slender filamentous hyphae, widely distributed in subtropical and temperate regions of
East Asia and North America ................................................................................................................ F. velutipes var. filiformis
2. Suprapellis an ixotrichoderm of irregular, filamentous hyphae derived from differentiated hyphidia which are fusoid or very
irregular thorny, in subalpine regions in the Himalaya...................................................................... F. velutipes var. himalayana
3. Suprapellis composed by clavate to subclavate cells without moniliform hyphal tips or protruding branched hyphae;
basidiospores less than 9µm in length ....................................................................................................................................... 4
3. Suprapellis composed mostly by clavate to subclavate cells with moniliform hyphal tips or protruding branched hyphae;
basidiospores 8.5–10 × 4–5µm, ellipsoid to oblong ellipsoid ........................................................................................ F. rossica
4. Basidiomata stout, associated with Populus or Pinus, temperate regions in Northern China ..................................... F. populicola
4. Basidiomata slender, often associated with fagaceous plants or Schima, warm regions in Southwestern China ..... F. yunnanensis
3 DISCUSSION
Flammulina velutipes is reported to produce
basidiomata in low temperature ≤ 15°C, although its
optimal temperature for vegetative growth ranges
from 22°C to 26°C (Aschan 1954; Fultz 1988).
Cultivars tolerate to relatively high temperature are
preferable since application of these cultivars could
reduce the cost in commercial production, especially
in Summer time. Here we revealed that there are
two novel F. velutipes varieties and one additional
new record of Flammulina for China, thus provided
ISSN1672‐6472 CN11‐5180/Q Mycosystema July 15, 2015 Vol. 34 No. 4
http://journals‐myco.im.ac.cn
602
further information on candidate genetic resources
for improvements of this economically important
mushroom.
Among the vouchers examined in study, several
specimens from Hunan (HKAS 47768 and HKAS
51988) and Yunnan (HKAS 85819, HKAS 85820, HKAS
85821 and HKAS 85822) were fruiting in the field
when average temperatures at local sites were
above 20°C. China could, thus, harbors strains
potentially tolerant to relatively high temperatures.
Flammulina yunnanensis was collected from
subtropical areas, and could be a promising
candidate for screening cultivars tolerate to high
temperatures.
In this study we have included several
cultivated strains that are commonly used in
Flammulina industry in China and found that these
strains are all F. velutipes var. filiformis (Fig. 3, clade
C). This finding suggests that strains other than F.
velutipes var. filiformis could be of considerable
interest for screening strains for industrial use.
Relationships among the species within
Flammulina have not been fully resolved based on ITS
data only (Fig. 3), and there is a new species remains
to be described when future field trips with mature
materials obtained for Flammulina sp. HKAS 51191
(Fig. 3). Future field trips should be focused on
regions less collected during the past years. Other
informative loci including the second largest subunit
of RNA polymerase II (rpb2), and the elongation
factor 1‐a (tef‐1a) would be helpful to resolve the
phylogeny and biogeographic inferences in the future.
Acknowledgements: Special thanks go to Dr. P. Zhang (Hunan
Normal University) and Xiang‐Hua Wang (KIB, China) for
providing specimens and/or color image. We thank professor
D.H. Pfister (Farlow Herbarium, FH) for allowing the first
author to examine F. velutipes deposited in FH for
comparison. Thanks also go to Ms. Shu Yao for assistance
with the lab work.
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