Online publication; available at: https://jats-truffles.org/truffology/

Truffology 5 (1): 15–21 (2022)

Original peer-reviewed article （原著論文 ； 査読有）

Tolypocladium bacillisporum (Ophiocordycipitaceae): A new parasite of
Elaphomyces from Japan
国内から採集されたツチダンゴ属生の新種シロアシヒメハナヤスリタケ
Tolypocladium bacillisporum （オフィオコルディセプス科）
Kohei Yamamoto1*, Gen Sugawa2, Keizo Takeda3, Yousuke Degawa2
山本 航平 1*, 須川 元 2, 武田 桂三 3, 出川 洋介 2
1

Tochigi Prefectural Museum, 2-2 Mutsumi-cho, Utsunomiya-shi, Tochigi 320-0865, Japan
栃木県立博物館， 〒 320-0865 栃木県宇都宮市睦町 2-2

2

Sugadaira Research Station, Mountain Science Center, University of Tsukuba, 1278-294 Sugadairakogen, Ueda-shi,
Nagano 386-2204, Japan
筑波大学山岳科学センター菅平高原実験所， 〒 386-2204 長野県上田市菅平高原 1278-294

3Japanese Society of Cordyceps Research, Tsuruoka-shi, Yamagata, Japan
日本冬虫夏草の会，山形県鶴岡市* Corresponding author （主著者）
E-mail: kohei081@yahoo.co.jp

Abstract
The genus Tolypocladium (Ophiocordycipitaceae) includes species that are parasitic on the truﬄe-like ascomycete
Elaphomyces. In addition to the 16 known species of mycoparasitic Tolypocladium from Japan, at least 19
undescribed species have been recorded from there. One of these species, called in Japan as “Shiroashi-himehanayasuri-take”, is a parasite of the Elaphomyces sect. Ceratogaster, and has been collected from Hokkaido Pref.,Japan. We found a new locality for this species in Miyagi Pref., and conducted morphological observations,
isolation, and molecular phylogenetic analyses of the specimens from Japan. The part-spore shape of this species
was different from that of T. jezoense, a macromorphologically similar species and the phylogenies strongly
indicated that “Shiroashi-hime-hanayasuri-take” is an independent species. Accordingly, this undescribed species
is herein proposed as a new species, T. bacillisporum.

要旨
トリポクラジウム属 （オフィオコルディセプス科） には、 トリュフ型の子嚢菌類であるツチダンゴ属に寄生する種が含まれる。
日本国内からは 16 既知種に加え、 少なくとも 19 種の未記載種が報告されている。 その内の一種であるシロアシヒメハナ
ヤスリタケは、 ツチダンゴ属 Ceratogaster 節の一種を宿主とし、 北海道から報告されている。 我々は宮城県内より本種の新産地を見出し、 日本産標本について形態観察、 分離培養、 分子系統解析を行った。 その結果、 本種は子実体の外観が類似するエゾハナヤスリタケとは部分胞子の形が異なり、 系統学的に独立種であることが強く支持された。 以上の結果に基づき、 本種を新種 Tolypocladium bacillisporum として記載した。
Article Info: Submitted: 25 February 2022

© The Japanese Association for Truffle Science (JATS), 2022

Accepted: 24 March 2022

Published: 31 March 2022

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Yamamoto et al.: Tolypocladium bacillisporum, a new parasite of Elaphomyces

Truffology - Volume 5, Issue 1, 2022

Introduction

Nature and Science, Tokyo (TNS) in Japan under TPM-M-9859, 9860,

The family Ophiocordycipitaceae (Hypocreales) described by Sung

9861 and TNS-F-82223, respectively.

et al. (2007), includes not only numerous arthropod pathogens but
also mycoparasites of the truffle-like ectomycorrhizal ascomycete

Isolation and observation of mycelial growth

Elaphomyces (Elaphomycetaceae, Eurotiales). Those mycoparasites

Ascospores discharged from mature perithecia onto potato dextrose

were formerly known as Elaphocordyceps spp., but the genus wasagar (PDA; Nissui, Tokyo, Japan) were used to obtain cultures

recently synonymized into Tolypocladium (Quandt et al., 2014).

(Uchiyama, 1999). Plates were incubated at 20°C in the dark until

Besides mycoparasites of Elaphomyces, Tolypocladium also includes

germination. Germinated ascospores were transferred to anotherinsect pathogens, soil inhabitants, and endophytes (Gazis et al., 2014;

plate. The established isolates, C23 from TPM-M-9859, C53 from

Quandt et al., 2014). Since Nikoh & Fukatsu (2000) suggested that

TPM-M-9860 and 202009-1 from TPM-M-9861, were deposited in

the common ancestor of extant cicada pathogenic and mycoparasitic

the Medical Mycology Research Center, Chiba University (Chiba,

Tolypocladium spp. was likely to be a cicada pathogenic fungus, inter-

Japan) under accession numbers IFM 67757 (for C23), IFM 67758

kingdom host jumping within the genus has been receiving increased(C53), and IFM 67759 (202009-1). Mycelial growth on PDA wasattention (Quandt et al., 2016, 2018).

measured based on Yamamoto et al. (2020).

So far, there are 24 described species of Tolypocladium parasitizing
Elaphomyces (Index Fungorum [http://www.indexfungorum.org/],

DNA sequencing and phylogenetic analyses

accessed on 10 Feb. 2022), and at least 16 known species have been

DNA was extracted from cultured mycelia on PDA, as describedreported from Japan (Kobayasi & Shimizu, 1960; Shimizu, 1997).

by Izumitsu et al. (2012), or CTAB method (Ishida et al., 1999).

Furthermore, Shimizu (1997) and Japanese Society of Cordyceps

PCR was performed using KOD FX Neo (Toyobo, Osaka, Japan) as

Research (2014) suggested that 19 taxonomically unsettled species

described by Yamamoto et al. (2021) or using KOD FX (Toyobo) in awere present in Japan. One of these Tolypocladium species with thetotal volume of 25 μL containing 5 µL dNTPs (0.4 mM each), 0.75 µL

Japanese name “Shiroashi-hime-hanayasuri-take” (from the Japaneseof each primer (0.3 µM each), 12.5 µL 2× PCR buffer for KOD FXshiroashi = whitish stipe, hime = small, and hanayasuri-take = T.

(Toyobo), 0.5 µL 1.0 U μL−1 KOD FX, 1.5 µL template DNA, and 4 µL

ophioglossoides (J.F. Gmel.) C.A. Quandt, Kepler & Spatafora;

sterile distilled water. For C23 and C53, amplification of (1) the small

hereafter referred to as “Shiroashi”), was illustrated in a book (Japanese

subunit (18S)-internal transcribed spacer (ITS)-large subunit (28S) of

Society of Cordyceps Research, 2014). This species is parasitic on

nuclear rDNA operon and (2) the translation elongation factor 1-alphaa species of sect. Ceratogaster, which was tentatively identified as(tef1) was performed using the primer pairs NS1 (White et al., 1990)

Elaphomyces cf. anthracinus Vittad., and known only from Hokkaido

and LR5 (Vilgalys & Hester, 1990), and 983F and 2218R (Rehner &Pref., Japan (Japanese Society of Cordyceps Research, 2014), but was

Buckley, 2005), respectively. For 202009-1, amplification of (3) the

recently also found in Miyagi Pref., Japan by the second author. Here,ITS was performed using ITS5 and ITS4 (White et al., 1990). The

we critically examined the morphology and phylogenetic position

PCR conditions were as follows: (1) 94°C for 2 min and 40 cycles ofof this species from Hokkaido Pref. and Miyagi Pref., and provide a

98°C for 10 s, 51°C for 30 s, and 68°C for 3.5 min; (2) 94°C for 2 min,taxonomic treatment.

10 cycles of 98°C for 10 s, 60°C for 30 s, and 68°C for 1 min 45 s,
followed by 30 cycles of 98°C for 10 s, 55°C for 30 s, and 68°C for

Materials and methods

1 min 45 s; (3) 94°C for 5 min and 10 cycles of 98°C for 10 s, 55°C for

Morphological observations

30 s (0.5°C decrease per cycle), and 68°C for 1 min, followed by 25

Morphological observations were conducted based on fresh and freeze-

cycles of 98°C for 10 s, 50°C for 30 s, and 68°C for 1 min. The PCRdried specimens of “Shiroashi” following the methods of Yamamotoproducts were purified using Illustra™ ExoProStar™ (GE Healthcare,

et al. (2020). Hand-cut sections of ascomata and ascospores discharged

Amersham, UK) or Applied Biosystems™ ExoSAP-IT™ (Thermo

from perithecia were mounted in lactoglycerol and observed under aFisher Scientific, Waltham, MA, USA) and sent to Macrogen Japan

light microscope (BX40; Olympus, Tokyo, Japan). All measurements(Tokyo, Japan) or FASMAC (Kanagawa, Japan) for sequencing, using

were made using PhotoRuler version 1.1.3 (http://inocybe.info/). Afterthe same primers for PCR [except for NS1, NS5, NS6, ITS3, ITS4,

observation and isolation, fresh specimens were freeze-dried and

ITS1 (White et al., 1990), and LR5 for (1)]. The resulting bidirectionaloven-dried at 60°C. The specimens were deposited in the herbarium

sequences were edited using 4Peaks 1.8 (http://nucleobytes.com/4peaks)of Tochigi Prefectural Museum (TPM) and the National Museum ofand assembled using MEGA 11 (Tamura et al., 2021). Newly generated

16© The Japanese Association for Truffle Science (JATS), 2022

Yamamoto et al.: Tolypocladium bacillisporum, a new parasite of Elaphomyces

Truffology - Volume 5, Issue 1, 2022

sequences were deposited in the DNA Data Bank of Japan (http://www.

ectomycorrhizal associations with Elaphomyces (Paz et al. 2017). The

ddbj.nig.ac.jp) under LC684522–LC684526.

host was Elaphomyces cf. anthracinus (Fig. 1E). The perithecia were

For phylogenetic analyses of the combined dataset of 18S, ITS,

vertically immersed in the fertile head (Fig. 1F–G). Mycoparasitic

28S and tef1, all Tolypocladium species parasitic on Elaphomyces

Tolypocladium spp., such as T. guangdongense (Lin et al., 2008),

for which sequences were available, i.e. T. capitatum (Holmsk.) C.A.

T. japonicum, T. jezoense, T. ophioglossoides, T. tenuisporum

Quandt, Kepler & Spatafora, T. cucullae Y.P. Xiao & T.C. Wen, T.

(Mains) C.A. Quandt, Kepler & Spatafora, and Elaphocordyceps

flavonigrum Noisrip., Tasan., Khons. & Luangsa-ard, T. fractum

×jezoensoides (Kobayasi) Hirok. Sato, S. Ban, Masuya & Hosoya(Mains) C.A. Quandt, Kepler & Spatafora, T. guangdongense (T.H.

are characterized by the clavate stromata (Mains 1957; Kobayasi

Li, Q.Y. Lin & B. Song) V. Papp, T. inusitaticapitatum F.M. Yu, Q.

& Shimizu, 1960). Among them, only T. jezoense parasitizes

Zhao & K.D. Hyde, T. japonicum (Lloyd) C.A. Quandt, Kepler &species of sect. Ceratogaster including E. anthracinus (Kobayasi

Spatafora, T. jezoense (S. Imai) C.A. Quandt, Kepler & Spatafora, T.

& Shimizu, 1960), and T. jezoense is macromorphologically very

ophioglossoides, and T. valliforme (Mains) C.A. Quandt, Kepler &similar to “Shiroashi.” However, the latter formed smaller perithecia

Spatafora, were retrieved from the International Nucleotide Sequence(700–720 × 200–250 μm in T. jezoense vs. 480–590 × 195–235

Databases and included. We also included several insect pathogenic

μm in “Shiroashi”) (Kobayasi & Shimizu, 1960; Fig. 1H), shorter

Tolypocladium spp., i.e. T. dujiaolongae Y.P. Cao & C.R. Li, T.

and narrower asci (450–500 × 13–19 μm vs. 220–370 × 8–12 μm)

fumosum Ruszk.-Mich., J. Pawłowska & Wrzosek, T. inegoense(Kobayasi & Shimizu, 1960; Fig. 1I–J), and ascospores with a large(Kobayasi) C.A. Quandt, Kepler & Spatafora, and T. paradoxum

number of septa (15 vs. 31 or 63) (Japanese Society of Cordyceps(Kobayasi) C.A. Quandt, Kepler & Spatafora, which were suggested

Research, 2014; Fig. 1K). Furthermore, there was almost no overlap

to be close to “Shiroashi” based on the results of National Center for

between the length of the part-spore of “Shiroashi” (3.5–12.3 μm;

Biotechnology Information nucleotide BLAST search (https://blast.

Fig. 1L–M) and those in all of the above-mentioned species (≥10

ncbi.nlm.nih.gov/Blast.cgi) and an endophytic species, T. amazonense

μm long) except T. ophioglossoides and T. tenuisporum. These two

Gazis, Skaltsas & P. Chaverri, which is distantly related to the above-

species clearly differ from “Shiroashi” in the length of their perithecia

mentioned species parasitic on Elaphomyces and insects (Gazis et al.,(≥600 μm) (Mains 1957; Kobayasi & Shimizu, 1960). The ascospores2014). Purpureocillium lilacinum (Thom) Luangsa-ard, Houbraken,

of “Shiroashi” germinated on PDA within 1 week and formed whiteHywel-Jones & Samson (Ophiocordycipitaceae) was selected as ancolonies within a month (Fig. 1N–O).

outgroup. The sequences were aligned according to Yamamoto et

18S-ITS-28S rDNA operon (3,395 bp and 2,853 bp) and tef1 (952al. (2020). Topological conflicts with significant support among thebp and 979 bp) sequences were obtained from the isolates C23 andfour trees (18S, 933 bp; ITS, 522 bp; 28S, 859 bp; tef1, 1,006 bp)

C53, respectively. An ITS sequence (498 bp) was obtained fromwere checked directly by topological comparison of the preliminary

the isolates 202009-1. Sequences of each locus were identical except

maximum likelihood (ML) trees. Next, the four datasets were

for the ITS region: a single nucleotide deletion was present in 202009-

combined into a single 3,320 bp dataset and deposited in TreeBASE

1. The BLAST search showed that ITS sequences from Japanese(accession URL: http://purl.org/phylo/treebase/phylows/study/

specimens were most similar to sequences of Tolypocladium spp., but

TB2:S29449). ML analysis of the combined dataset was conducted

the homology was less than 96%. Fig. 2 shows the ML phylogeny ofbased on Yamamoto et al. (2020) using raxmlGUI 2.0 (Edler etthe combined rDNA and tef1 dataset (ln L = −8869.48349). The MPal., 2020) under a general time reversible model of nucleotide

statistics were as follows: tree length = 806, consistency index = 0.65,

substitution, with a discrete gamma distribution (+G) and invariant

retention index = 0.697, and composite index = 0.453. The sequences

sites (+I), as selected by MEGA 11. A maximum parsimony (MP)from isolates of “Shiroashi” and the three abovementioned clavate,

analysis was conducted based on Yamamoto et al. (2020).

mycoparasitic species of Tolypocladium formed a well-supported.

clade (bootstrap support: 94/79). “Shiroashi” is a unique species inResults and Discussion

this clade because it has much smaller part-spores than the otherThe stromata of “Shiroashi” (Fig. 1A–B) were characterized byclosely related species.

the aboveground clavate part, which was olive-colored at maturity

Morphological comparisons and phylogenetic analyses strongly

and yellowish-green when young (Fig. 1C), and undergroundindicated that “Shiroashi” is an undescribed species. Here, we

white rhizomorphs. This species was often found near broad-propose a new name, T. bacillisporum for “Shiroashi” and provide its

leaved trees (Fig. 1D), e.g. Quercus and Carpinus known to formtaxonomic description.

© The Japanese Association for Truffle Science (JATS), 2022

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Yamamoto et al.: Tolypocladium bacillisporum, a new parasite of Elaphomyces

Truffology - Volume 5, Issue 1, 2022

Fig. 1. Tolypocladium bacillisporum collected in Hokkaido Pref. (A, C–G: TPM-M-9860) and Miyagi Pref. (B, H–M: TPM-M-9861), and ex-type culture C23 (N,O). (A–B) Ascomata. (C) Young stromata in natural habitat. (D) Habitat. Arrow indicates the position of ascomata. (E) Host ascoma showing surface (left)
and gleba (right). (F) Fertile head. (G) Longitudinal section of fertile head. (H) Perithecia. (I) Asci. (J) Apical cap of two asci. (K) Ascospore with 63 septa. (L)Tips of two ascospores. (M) Part-spores. (N–O) Upper (N) and reverse (O) sides of colonies on PDA after 30 d. Bars: A–B, E = 1 cm; F–G = 2 mm; H = 200 μm; I,
K = 100 μm; J, L–M = 10 μm; N–O = 2 cm.

Taxonomyanthracinus and its relatives, are common between the species. But

Tolypocladium bacillisporum Koh. Yamam., Sugawa & K. Takeda,

the part-spores are much smaller than the latter.

sp. nov.

Etymology: From the Latin bacilli = bacillus and sporum = spore,[MycoBank ID: MB 843120]

referring to the bacilliform part-spore of this species.
Fig. 1.

Type: JAPAN, Hokkaido Pref., Tohma-cho, Kaimei-ni-ku, ca. 220 m

Diagnosis: This species is most similar to T. jezoense. The stroma

above sea level, on ascomata of E. cf. anthracinus hypogeous underis macromorphologically similar, and the hosts, Elaphomyces

a secondary forest dominated by Quercus dentata Thunb., 20 Sep.

18

© The Japanese Association for Truffle Science (JATS), 2022

Truffology - Volume 5, Issue 1, 2022

Yamamoto et al.: Tolypocladium bacillisporum, a new parasite of Elaphomyces

Kyoto,	
  JP	
  (AB027319/AB027365/AB027365/-­‐)	
100/99	

94/79	

Tolypocladium	
  jezoense	

ND	
  (DQ522547/JN049824/DQ518761/DQ522330)	

Shiga,	
  JP	
  (AB027320/AB027366/AB027366/-­‐)	58/-	
100/99	 CN	
  (-­‐/EU039881/-­‐/-­‐)	  T	
CN	  (-­‐/MT386338/-­‐/-­‐)	62/-	Miyagi,	  JP,	
  202009-­‐1	
  (-­‐/LC684524/-­‐/-­‐)	60/-	
98/99	
 Hokkaido,	
  JP,	  C23	  (LC684522/LC684522/LC684522/LC684525)	
  ET	
Hokkaido,	
  JP,	  C53	  (LC684523/LC684523/LC684523/LC684526)	
Kyoto,	
  JP	
  (JN941731/JN943323/JN941410/AB968599)	
81/78	
Osaka,	
  JP	
  (JN941730/JN943324/JN941411/AB968600)	
Amami	
  Isl.,	
  JP	
  (AB027323/AB027369/AB027369/-­‐)	
68/74	
100/95	
 CN	
  (-­‐/KF696557/-­‐/-­‐)	  T	
87/93	 CN	
  (-­‐/MW199076/-­‐/-­‐)	T.	
  japonicum	
T.	
  guangdongense	
T.	
  bacillisporum	

T.	
  paradoxum	
T.	
  dujiaolongae	

ND	
  (DQ522545/-­‐/DQ518759/DQ522328)	
T.	
  fractum	CN	
  (MW798784/MW798788/MW798786	
  /-­‐)	
  T	
T.	
  cucullae	CN	
  (MW798785/MW798789/MW798787	
  /-­‐)	
NO	  (-­‐/AJ786568/-­‐/-­‐)	
62/-	
T.	
  longisegmentatum	
100/100	
 TH	
  (-­‐/MN338090/MN337287/MN338495)	
  ET	
T.	
  ﬂavonigrum	
58/-	
TH	
  (-­‐/MN338091/MN337288/MN338496)	
57/-	
T.	
  inusita;capitatum	
65/89	
96/96	
100/100	
 CN	
  (MW537734/MW537736/MW537719/MW507528)	
CN	
  (MW537733/MW537735/MW537718/MW507527)	
  T	
100/99	
65/73	ND	
  (-­‐/-­‐/DQ118741/DQ118752)	

Hokkaido,	
  JP	
  (AB027322/AB027368/AB027368/-­‐)	PL	  (-­‐/KU925171/KU985053/-­‐)	
  T	
56/-	
FR	
  (AY489689/-­‐/AY489721/AY489615)	
100/100	
 Osaka,	
  JP	
  (JN941739/JN943314/JN941402/AB968598)	
Kagawa,	
  JP	
  (AB027318/AB027364/AB027364/-­‐)	
99/96	 Osaka,	
  JP	
  (JN941735/JN943319/JN941406/AB968602)	
JP	
  (JN941736/JN943316/JN941405/AB968601)	
US	
  (AY489691/-­‐/AY489723/AY489618)	
96/99	CA	
  (AY245648/AY245640/-­‐/-­‐)	T.	
  amazonense	
  (KF747314/-­‐/KF747134/KF747099)	
  ET	
Purpureocillium	
  lilacinum	
  (AY526475/MH855800/FR775484/EF468792)	
  ET	
99/94	T.	
  inegoense	
T.	
  fumosum	
T.	
  capitatum	

T.	
  ophioglossoides	
T.	
  valliforme	

0.02 substitutions/site	

Fig. 2. Maximum likelihood (ML) phylogenetic tree of the combined dataset of 18S, ITS, 28S, and tef1 sequences of Tolypocladium spp.
parasitic on Elaphomyces (black circle) and their relatives on insects (open rhombus). Purpureocillium lilacinum was used as an outgroup.
GenBank accession numbers for 18S, ITS, 28S, and tef1 are shown in parentheses from left to right. Bootstrap (BS) values (1,000 replicates)≥ 50% from ML (left) and maximum parsimony (MP) (right) analyses are shown near the nodes. Branches supported by BS values ≥ 70%from both ML and MP analyses are depicted as thick lines. CA = Canada; CN = China; FR = France; JP = Japan; ND = no data; NO = Norway;
PL = Poland; TH = Thailand; US = USA. T = type specimen; ET = ex-type culture.

2010, K. Yamamoto (holotype, TPM-M-9859; isotype, TNS-F-82223;

solid; ostioles up to 15 per 1 mm2. Stipe grayish-white with greenish

ex-type culture C23 [IFM 67757]).

or yellowish tinge, cylindrical, surface smooth, narrower than fertile

Gene sequences from ex-type culture: LC684522 (18S), LC684522

head, 1.8–2.7 mm wide; striae sometimes present at the border of(ITS), LC684522 (28S), LC684525 (tef1).

the head. Rhizomorphic part white, partially yellowish, frequently

Description: Stromata arise from 1–3 hosts, often solitary, sometimes

branched, fragile, up to 1 mm wide. Perithecia ovoid, verticallycaespitose; epigeous part clavate, not branched, 30–65 mm long;

immersed, ostiole protuberant, 480–590 × 195–235 μm (mean 528.1

underground part rhizomorphic, 8–75 mm long. Fertile head× 218.1 μm, n = 6); wall 12–17 μm thick, composed of 6–7 layers ofyellowish-green when young, turning olive-green as it matures,textura angularis, cells up to 18 μm wide. Asci hyaline, cylindrical,

ellipsoidal to oblong, 5–16 mm long, 3–4.5 mm wide; inside yellow,

8-spored, 220–370 × 8–12 μm (mean 326.4 × 9.16 μm, n = 21); apical© The Japanese Association for Truffle Science (JATS), 2022

19

Truffology - Volume 5, Issue 1, 2022

Yamamoto et al.: Tolypocladium bacillisporum, a new parasite of Elaphomyces
cap prominent, 2.5–4 μm high, 5–6 μm wide (mean 3.28 × 5.1 μm,

fruiting bodies for PCR. Mycoscience 53: 396–401.

n = 18). Ascospores hyaline, filiform, slightly acute at both ends,

Japanese Society of Cordyceps Research (2014) An illustrated guide

270–355 μm long (mean 313.7 μm, n = 20); septa often 63, rarely 31,

to ecology of Japanese Cordyceps. Seibundo Shinkosha, Tokyo. (infragmenting into part-spores; part-spores cylindrical, bacilliform, 3.5–

Japanese)

12.3 × 1.5–2.5 μm (mean ± SD: 5.6 ± 1.63 × 1.93 ± 0.16 μm, n = 50).
Colonies on PDA growing 11–13 mm within 30 d at 25°C in the dark;
white, surface floccose with aerial hyphae; reverse white to pale yellow.
Distribution, habitat, and fruiting season: On hypogeous ascoma
of Elaphomyces sect. Ceratogaster in broadleaved tree-dominatedforests in the temperate zone of Honshu or subarctic zone of
Hokkaido Pref., Japan. Found in autumn.

Kobayasi Y., Shimizu D. (1960) Monographic studies of Cordyceps. 1.
Group parasitic on Elaphomyces. Bulletin of the National Science
Museum, Tokyo 5: 69–85.
Lin Q.Y., Li T.H., Song B. (2008) Cordyceps guangdongensis sp. nov.
from China. Mycoaxon 103: 371–376.
Mains E.B. (1957) Species of Cordyceps parasitic on Elaphomyces.
Bulletin of the Torrey Botanical Club 84: 243–251.
Nikoh N., Fukatsu T. (2000) Interkingdom host jumping underground:

Other specimens examined: JAPAN, Hokkaido Pref., Tohma-

phylogenetic analysis of entomoparasitic fungi of the genus Cordyceps.

cho, same locality as holotype specimen, on hypogeous ascomata

Molecular Biology and Evolution 17: 629–638.

of E. cf. anthracinus, 11 Sep. 2011, K. Yamamoto (TPM-M-9860;

Paz A., Bellanger J.-M., Lavoise C., Molia A., Ławrynowicz M.,

living culture, C53 [IFM 67758]). Miyagi Pref., Sendai-shi, Taihaku-ku,

Larsson E., Ibarguren I.O., Jeppson M., Læssøe T., Sauve M., Richard

Kagitori, ca. 136 m above sea level, on hypogeous ascomata ofF., Moreau P.-A. (2017) The genus Elaphomyces (Ascomycota,

E. cf. anthracinus under a Carpinus standing by a stream in mixed
forest dominated by Abies ﬁrma Siebold & Zucc., 27 Sep. 2020,
G. Sugawa (TPM-M-9861; living culture, 202009-1 [IFM 67759]).
Note: Ascoma of TPM-M-9860 and microstructures of TPM-M-9859
are illustrated as “Shiroashi-hime-hanayasuri-take” in the page 259 ofJapanese Society of Cordyceps Research (2014).

Acknowledgements

Eurotiales): a ribosomal DNA-based phylogeny and revised systematics
of European ‘deer truffles’. Persoonia 38: 197–239.
Quandt C.A., Di Y., Elser J., Jaiswal P., Spatafora J.W. (2016) Differential
expression of genes involved in host recognition, attachment, anddegradation in the mycoparasite Tolypocladium ophioglossoides. G3
Genes Genomes Genetics 6: 731–741.
Quandt C.A., Kepler R.M., Gams W., Araújo J.P.M., Ban S., Evans H.C.,
Hughes D., Humber R., Hywel-Jones N., Li Z., Luangsa-ard J.J., Rehner
S.A., Sanjuan T., Sato H., Shrestha B., Sung G.-H., Yao Y.-J., Zare R.,

We are grateful to Mr. Yoshitaka Kaitsu (Japanese Society of

Spatafora J.W. (2014) Phylogenetic-based nomenclatural proposals

Cordyceps Research) for obtaining permission for field sampling

for Ophiocordycipitaceae (Hypocreales) with new combinations infrom Tohma Town Office and supporting the field survey conducted

Tolypocladium. IMA Fungus 5: 121–134.

by the first author. We also thank Dr. Kentaro Hosaka for depositing
specimens in TNS.

Quandt C.A., Patterson W., Spatafora J.W. (2018) Harnessing thepower of phylogenomics to disentangle the directionality andsignatures of interkingdom host jumping in the parasitic fungal genus
Tolypocladium. Mycologia 110: 104–117.

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