A cryptic powdery mildew (Golovinomyces hieraciorum sp. nov.) on Hieracium and Pilosella (Compositae)

Abstract

The Golovinomyces cichoracearum complex is morphologically highly variable and causes powdery mildew on a wide range of Compositae, including Hieracium spp. and Lapsana communis. A comprehensive phylogenetic analysis of Golovinomyces, published in 2013, revealed that G. cichoracearum s. str. was confined to Scorzonera and Tragopogon spp. as hosts (Compositae, tribe Lactuceae, subtribe Scorzonerinae). To clarify the phylogeny and taxonomy of Golovinomyces on Hieracium spp. (Compositae, tribe Lactuceae, subtribe Hieraciinae), which is common in Asia and Europe, morphology and phylogenetic analyses of ITS + 28S rDNA sequences were conducted for 57 powdery mildew specimens of Hieracium spp. and Lapsana communis. Golovinomyces on Hieracium spp. in Asia and Europe, previously referred to as G. cichoracearum, is a previously undescribed, cryptic species, which is described here as Golovinomyces hieraciorum sp. nov.. Since a sequence retrieved from a powdery mildew on Lapsana communis in Switzerland clustered in sister position to the G. hieraciorum clade, numerous German specimens identified as G. cichoracearum were included in the present examinations. All the re-examined collections of “G. cichoracearum” on L. communis were misidentified, and were shown to belong to Neoërysiphe nevoi or Podosphaera ergerontis-canadensis.

Full text

Phytopathologia Mediterranea 61(1): 107-117, 2022
Firenze University Press
www.fupress.com/pm
ISSN 0031-9465 (print) | ISSN 1593-2095 (online) | DOI: 10.36253/phyto-12992
Phytopathologia Mediterranea
The international journal of the
Mediterranean Phytopathological Union
Citation: G.-X. Guan, S.-Y. Liu, U.
Braun, P.-L. Qiu, J. Liu, F.-Y. Zhao,
S.-R. Tang, J.-N. Li, V.-N. Nguyen (2022) A
cryptic powdery mildew (Golovinomy-
ces hieraciorum sp. nov.) on Hieracium
and Pilosella (Compositae). Phytopath-
ologia Mediterranea 61(1): 107-117. doi:
10.36253/phyto-12992
Accepted: November 30, 2021
Published: March 25, 2022
Copyright: © 2022 G.-X. Guan, S.-Y. Liu,
U. Braun, P.-L. Qiu, J. Liu, F.-Y. Zhao,
S.-R. Tang, J.-N. Li, V.-N. Nguyen.
This is an open access, peer-reviewed
article published by Firenze Univer-
sity Press (http://www.fupress.com/pm)
and distributed under the terms of the
Creative Commons Attribution License,
which permits unrestricted use, distri-
bution, and reproduction in any medi-
um, provided the original author and
source are credited.
Data Availability Statement: All rel-
evant data are within the paper and its
Supporting Information les.
Competing Interests: The Author(s)
declare(s) no conict of interest.
Editor: Tito Caf, Università Cattolica
del Sacro Cuore, Piacenza , Italy.
Research Papers
A cryptic powdery mildew (Golovinomyces
hieraciorum sp. nov.) on Hieracium and Pilosella
(Compositae)
G-X GUAN1, S-Y LIU1,2,*, U BRAUN3, P-L QIU1, J
LIU1, F-Y ZHAO1, S-R TAN G1, J-N LI1, V-N NGUYEN1
1 Engineering Research Center of Edible and Medicinal Fungi, Ministry of Education, Jilin
Agricultural University, No. 2888 Xincheng Street, Changchun130118, Jilin Province, China
2 Department of Plant Pathology, College of Plant Protection, Jilin Agricultural University,
No. 2888 Xincheng Street, Changchun130118, Jilin Province, China
3 Herbarium, Department of Geobotany and Botanical Garden, Institute for Biology,
Martin Luther University, Halle (Saale), Germany
*Corresponding author. E-mail: liussyan@163.com
Summary. e Golovinomyces cichoracearum complex is morphologically highly vari-
able and causes powdery mildew on a wide range of Compositae, including Hieracium
spp. and Lapsana communis. A comprehensive phylogenetic analysis of Golovinomyces,
published in 2013, revealed that G. cichoracearum s. str. was conned to Scorzonera
and Tragopogon spp. as hosts (Compositae, tribe Lactuceae, subtribe Scorzonerinae). To
clarify the phylogeny and taxonomy of Golovinomyces on Hieracium spp. (Compositae,
tribe Lactuceae, subtribe Hieraciinae), which is common in Asia and Europe, morphol-
ogy and phylogenetic analyses of ITS + 28S rDNA sequences were conducted for 57
powdery mildew specimens of Hieracium spp. and Lapsana communis. Golovinomy-
ces on Hieracium spp. in Asia and Europe, previously referred to as G. cichoracearum,
is a previously undescribed, cryptic species, which is described here as Golovino-
myces hieraciorum sp. nov.. Since a sequence retrieved from a powdery mildew on
Lapsana communis in Switzerland clustered in sister position to the G. hieraciorum
clade, numerous German specimens identied as G. cichoracearum were included in
the present examinations. All the re-examined collections of “G. cichoracearum” on
L. communis were misidentied, and were shown to belong to Neoërysiphe nevoi or
Podosphaera ergerontis-canadensis.
Keywords. Golovinomyces cichoracearum, Erysiphaceae, Ascomycota, taxonomy, phylo-
genetic analysis.
INTRODUCTION
Hieracium L. (Compositae, tribe Lactuceae; hawkweed) is a taxonomical-
ly challenging genus of herbaceous perennial herbs, with ligulate owers and
milky latex in stems and leaves. is genus comprises terrestrial perennial
plants, native to Africa, Asia, Europe and North to South America, which
are used as forage for livestock (Wilson et al., 2006). Hieracium comprises ca.

108 Guan-Xiu Guan et alii
770 sexually producing species, and ca. 5200 apomictic
microspecies, according to e International Compositae
Alliance (TICA) (CWG, 2021). Hieracium is divided into
three subgenera, viz. Pilosella, Hieracium, and Chionora-
cium (Wilson et al., 2006). Subgenus Pilosella is consid-
ered a separate genus, Pilosella, i.e., the former subgenus
Hieracium is treated as Hieracium s. str., and subgenus
Chionoracium is assigned to the genus Crepis (Gask in
and Wilson, 2007). Members of the genera Hieracium
and Pilosella are model plants that are used to study the
mechanisms of apomixis (not involving the fusion of
male and female gametes in reproduction) (Hand et al.,
2015; Płachno et al., 2017; Chrtek et al., 2020). Apomixis
is a key evolutionary mechanism in certain angiosperms,
providing reproductive assurance and isolation (Mráz
and Zdvořák, 2019).
Hieracium spp. are susceptible to powdery mildews.
Six species, viz. Erysiphe lamprocarpa, Golovinomyces
cichoracearum, Leveillula taurica, Podosphaera fusca,
Po. fuliginea, and Po. macularis, have been reported on
Hieracium from many countries (Farr and Rossman,
2021). However, these names do not reflect the cur-
rent taxonomy, i.e., they were based on outdated broad
species concepts. Golovinomyces cichoracearum (basio-
nym: Erysiphe cichoracearum) was originally described
on Scorzonera hispanica and Tragopogon porrifolius (de
Lamarck and de Candolle, 1805). Salmon (1900) widened
the concept of G. cichoracearum by assigning powdery
mildew on numerous hosts of various plant families,
including Boraginaceae and Plantaginaceae, to this spe-
cies. Braun (1987) conned G. cichoracearum to a wide
range of Compositae hosts. Braun and Cook (2012) fur-
ther reduced its circumscription to Golovinomyces on
hosts in the subfamily Cichorioideae of Compositae, but
emphasized that this circumscription still represented
a heterogenic complex species. is is demonstrated by
molecular sequence analyses (Matsuda and Takamatsu,
2003; Lebeda and Mieslerová, 2011), which supported
this compound species comprising at least several for-
mae speciales or possibly cryptic species.
e morphology of G. cichoracearum s. lat. is not
uniform on various hosts, i.e., somewhat lobed hyphal
appressoria and conidiophores with curved foot-cells
are common on Lactuca, Scorzonera, and Tragopogon,
whereas most appressoria are nipple-shaped and the
foot-cells are mostly straight on Hieracium and Picris
(Lebeda and Mieslerová, 2011; Braun and Cook, 2012).
Takamatsu et al. (2013) showed in comprehensive phy-
logenetic analyses that G. cichoracearum s . str. is further
conned to host species of the genera Scorzonera and
Tragopogon (Compositae, Cichorioideae, tribe Lactuceae,
subtribe Scorzonerinae), since the powdery mildews on
hosts of these genera morphologically coincide and are
a clade which is separate from all other clades within
Golovinomyces.
Golovinomyces cichoracearum (or E. cichoracearum)
on Hieracium (tribe Lactuceae, subtribe Hieraciinae)
and L. communis (tribe Lactuceae, subtribe Crepidinae)
is common throughout Europe, North America, and in
parts of Asia (Zeller and Levy, 1995; Braun and Cook,
2012; Farr and Rossman, 2021). Takamatsu et al. (2013)
showed a sequence retrieved from Golovinomyces on
L. communis in Switzerland was genetically distinct
from G. cichoracearum s . str., and forms a separate line-
age. Additional sequences and morphological observa-
tions are required to clarify the relationship between G.
cichoracearum s. str., Golovinomyces collections on Hiera-
cium, and Golovinomyces collections on L. communis.
In 2014 and 2017, Golovinomyces sp. was found
on H. umbellatum in Heihe City, Heilongjiang Prov-
ince, China. To identify the powdery mildew species
involved, morphological and molecular phylogenetic
analyses (based on ITS and 28S rDNA sequences) were
conducted. Morphologically, this fungus is close to G.
cichoracearum as circumscribed in Braun and Cook
(2012), but genetically it clusters far away from G.
cichoracearum s. str. and forms a clade of its own in sis-
ter position to a sequence obtained from Golovinomyces
on L. communis in Europe. erefore, the present study
aimed to: (i) clarify the identity of the causal agent of
the Hieracium powdery mildew based on morphological
re-examinations and molecular analyses, and determine
if this pathogen is distributed and common in Asia and
Europe; and (ii) identify the Golovinomyces on L. com-
munis in Europe.
MATERIALS AND METHODS
Fungal material
A total of 57 specimens were examined from four
countries. Twenty-eight specimens of Hieracium (includ-
ing 14 species) with Golovinomyces were examined,
including two samples collected in China, one specimen
from Russia, one from Slovakia, and 24 additional col-
lections from Germany. One specimen on Pilosella pro-
cera from China was included, and 27 Lapsana commu-
nis specimens from Germany were also examined.
Morphological examination
For morphological observations, dried samples from
herbarium collections were mounted in lactic acid and

109
A cryptic powdery mildew on Hieracium and Pilosella
examined using a light microscope (Zeiss Axio Scope
A1, Germany). Dimensions of at least 30 dierent fungus
anamorph and teleomorph structures were measured for
each sample.
DNA extractions, PCR amplication and sequencing
Whole-cell DNA was extracted from chasmothecia
or conidia and mycelia using the Chelex-100 method
(Walsh et al., 1991; Hirata and Takamatsu, 1996). e
rDNA internal transcribed spacer (ITS) regions includ-
ing the 5.8S rDNA were amplied with primers ITS5
and ITS4 (White et al., 1990), or PM10 and PM2 (Brad-
shaw and Tobin, 2020). And the partial 28S rDNA,
including D1 and D2 domains, was amplified with
primers LSU1 and LSU2 (Scholin et al., 1994; Mori et
al., 2000), or PM28F and PM28R (Bradshaw and Tobin,
2020). e DNA amplication and sequencing were car-
ried out as outlined in Qiu et al. (2018).
Molecular phylogenetic analyses
The obtained sequences, including complete ITS
and partial 28S rDNA, were deposited in GenBank.
e combined dataset of ITS and 28S rDNA sequences
was aligned with closely related sequences of the genus
Golovinomyces (Table S1) (Kiss et al., 2001; Matsuda and
Takamatsu, 2003; Takamatsu et al., 2006; 2008; 2009;
2013; Park et al., 2010; Scholler et al., 2016; Bradshaw et
al., 2017; Braun et al., 2018; 2019; Meeboon et al., 2018;
Ellingham et al., 2019; Qiu et al., 2020). Golovinomyces
inulae was selected as the outgroup taxon (Takamatsu et
al., 2013). Multiple sequence alignments were carried out
using MUSCLE implemented in the MEGA X (Kumar et
al., 2018). Subsequently, the alignments were manually
rened with MEGA X and deposited in TreeBASE (Piel
et al., 2009) under the accession number of S28413. Phy-
logenetic trees were obtained from the generated dataset
using the maximum parsimony (MP), maximum likeli-
hood (ML) and Bayesian Inference (BI) methods. MP
analysis was implemented in PAUP* 4.0 (Swoord, 2002)
with the heuristic search option using the “tree-bisec-
tion-reconnection” (TBR) algorithm with 100 random
sequence additions to nd the global optimum tree. All
sites were treated as unordered and unweighted, with
gaps treated as missing data. e strength of the internal
branches of the resulting trees was tested with bootstrap
(BS) analysis using 1000 replications with the step-wise
addition option set as simple and maximum tree num-
ber as 100 to save analysis time. Tree scores, including
tree length (TL), consistency index (CI), retention index
(RI), and rescaled consistency index (RC), were also cal-
culated. ML analyses were carried out in raxmlGUI 2.0
beta (Edler et al., 2021) under a GTRGAMMA model.
e BS supports and trees were obtained by running
rapid bootstrap analyses of 1000 replicates followed by
a search for the tree with the greatest likelihood. Boot-
strap supports below 75% were discarded for both anal-
yses. In BI analyses, the best-t substitution models for
dierent datasets were estimated by MrModeltest ver. 2.3
based on the implementation of the Akaike information
criterion (AIC) (Nylander, 2004). Four Markov Chain
Monte Carlo (MCMC) were run from random starting
trees for 2,000,000 generations, and trees were sampled
every 100 generations by MrBayes v. 3.2.7 (Ronquist and
Huelsenbeck, 2003). e runs ended when the standard
deviation of split frequencies reached below 0.01. e
rst 25% of all generations were discarded as burn-in
and a majority rule consensus tree of all remaining trees
was calculated to determine the posterior probabilities
for individual branches. e resulting trees were visual-
ized using FigTree 1.3.1 (Rambaut, 2009).
RESULTS
Morphological description
Golovinomyces hieraciorum G.-X. Guan & S.-Y. Liu sp.
nov. (Figure 1).
MycoBank Number: MB10001660
Etymology. Epithet derived from the name of the
host genus, Hieracium, using the plural genitive, mean-
ing “Golovinomyces of Hieracium spp.”
Typificat i on. on Hieracium umbellatum, China.
Heilongjiang Province, Heihe City, Sunwu County, the
south coast of Xunbiela River, 20 Sep. 2014, Feng-Yun
Zhao, Jian Liu, Shu-Rong Tang, Peng-Lei Qiu (holotype,
HMJAU-PM91858; isotype, HMAS249776); GenBank
number: MZ420204 (ITS+28S). Paratype: Heilongji-
ang Province, Heihe City, Sunwu County, 2 Sep. 2017,
Feng-Yun Zhao, Van-Ninh Nguyen, Jia-Ni Li, Jing-Sheng
Lu (HMJAU-PM91859), GenBank number: MZ420205
(ITS+28S).
Description. Mycelium on leaves, amphigenous, and
stems, forming irregular white patches or euse, nally
covering whole leaf surfaces, persistent. Hyphae straight
to sinuous-geniculate, hyaline, thin-walled, septate,
hyphal cells 60–90 µm long and 4–10 µm wide. Later
in the season hyphae becoming pigmented, above and
all around chasmothecia (secondary hyphae). Hyphal
appressoria nipple-shaped, solitary or in opposite pairs,
4–8 µm diam. Conidiophores on the upper surfaces
of hyphal mother cells, erect, position usually towards

110 Guan-Xiu Guan et alii
Figure 1. Golovinomyces hieraciorum on Hieracium umbellatum (HMJAU-PM91858). A and B, symptoms on host plants. C to E, hyphal
appressoria. F and G, conidiophores. H to J, conidia. K, conidium with germ tube. L, chasmothecium. M, peridium cells. N, asci. O and P,
ascospores. Bars = 10 m.

111
A cryptic powdery mildew on Hieracium and Pilosella
one septum of each mother cell, rarely in the middle or
almost so, (40–)47–90(–120) × 9–15 m. Conidiophores
foot-cells cylindrical or slightly increasing in width from
bases to tops, straight, occasionally somewhat curved at
the bases, with basal septae at the junctions (or almost
so) with the hyphal mother cells, occasionally slightly
elevated (5–10 µm), 22–80 × 8–15 m, followed by 1–3
short cells. Conidia formation catenescent, outline of
conidium chains distinctly sinuate. Conidia ellipsoid-
ovoid to doliiform-cylindrical, 22–35(–40) × 11–20 m,
length/width ratio (1.3–)1.5–2.1(–2.7). Germ tubes club-
shaped, produced in perihilar positions, short, without
swollen tips. Euoidium type. Chasmothecia, amphig-
enous, scattered to gregarious, when mature oen sur-
rounded by secondary (pigmented) hyphae, 80–156 m
diam. Peridium cells with irregularly curved-sinuous
walls, (7.4–)10–25 m diam. Appendages numerous,
in the lower half of the ascomata, sometimes also in
the upper half, mycelioid, simple but rarely irregularly
branched and interlaced with each other, 0.2–2.3 times
as long as the chasmothecial diam., 3–9 µm wide, sep-
tate, walls thin, smooth or somewhat rough, at first
hyaline, later brown, paler towards the apices or colour-
less near the apices, shorter appendages may be brown
throughout (differentiation between appendages and
secondary hyphae oen dicult). Asci 6–16 per chasmo-
thecium, clavate to saccate, (28–)45–75(–80) × (18–)20–
40(–45) µm, length/width ratio (1.2–)1.5–2.5(–3.3), usu-
ally with numerous small to moderately large oil drop-
lets, sessile to short-stalked, stalks 5–15 µm long, rarely
longer, to 25 µm, walls thin, 1–2 µm, terminal oculi
inconspicuous, 7–15 µm diam., 2-spored. Ascospores
ellipsoid-ovoid, (11–)15–20(–31) × 11–18 µm, length/
width ratio 1.0–1.9(–2.3), colourless.
Host range and distribution. Compositae (tr ibe
Lactuceae, subtribe Hieraciinae): On Hieracium (albi-
florum, alpinum, amplexicaule, anchusoides, argilla-
ceum, aurantiacum, auricula, belonodontum, bidum,
bombycinum, boreale, bupleuroides, caesium, caespito-
sum, canadense, carpathicum, carpaticum, cinerascens,
cymosum, danubiale, dentatum, echioides, fallax, fla-
gellare, orentinum, ×oribundum, gentile, glaucinum,
glaucum, groenlandicum, hryniawiense, humile, incisum,
integrifolium, jankae, juranum, kotschyanum, lachenalii,
laevicaule, laevigatum, lanatum, lanceolatum, lehbertii,
leucophaeum, longifolium, lycopifolium, murorum, ois-
tophyllum, onosmoides, pallidum, paniculatum, pictum,
pilosella, piloselloides, pleiotrichum, porrifolium, prae-
altum, praecox, pratense, prenanthoides, pulmonarioides,
quercetorum, racemosum, rapunculoides, regelianum,
robustum, rotundatum, rubrum, sabaudum, scabrum,
schmidtii, semisylvaticum, sp., staticifolium, subinuloides,
submurorum, sylvaticum, sylvularum, tenuiorum, trach-
selianum, transylvanicum, tridentatum, tritum, umbel-
latum, vagum, villosum, virosum, viscosum, vulgatum),
and Pilosella (aurantiaca, procera). Asia (Armenia, Chi-
na), Europe (Belarus, Czechoslovakia, Denmark, Esto-
nia, Finland, France, Germany, Hungary, Iceland, Italy,
Netherlands, Norway, Poland, Romania, Russia, Slova-
kia, Spain, Sweden, Switzerland, UK, Ukraine, Yugosla-
via), and North America (Amano, 1986; Braun, 1995;
Farr and Rossman, 2021).
Additional material examined. on H. amplexi-
caule, Germany, Sachsen-Anhalt, Landkreis Jerichower
Land, Burg, 10 June 1997, H. Jage (GLM-F-50151); on H.
bombycinum, Germany, Sachsen, Dresden, Großer Gar-
ten, 27 Sep. 1994, F. Klenke (GLM-F-102977); on H. fal-
lax, Germany, Sachsen-Anhalt, Landkreis Wittenberg,
Kemberg, 25 Aug. 2009, H. Jage (GLM-F-97335); on H.
glaucinum, Germany, Sachsen, Görlitz, 1 Nov. 2009,
H. Boyle (GLM-F-99602); Germany, Sachsen-Anhalt,
Landkreis Mansfeld-Südharz, between Questenberg and
Hainrode, 15 May 2009, A. Hoch (GLM-F-97576); on H.
lachenalii, Germany, Sachsen-Anhalt, Landkreis Anhalt-
Bitterfeld, Gröbzig, 10 Oct. 2006, H. Zimmermann
(GLM-F-95815); on H. laevigatum, Germany, Sachsen-
Anhalt, Sandersdorf, Stakendorfer Busch, 13 Sep. 1977,
U. Braun (HAL 946 F); Germany, Sachsen, landkreis
Görlitz, Boxberg, OT Bärwalde, 26 Aug. 2004, H. Boyle
(GLM-F-53711); Germany, Sachsen-Anhalt, Eisleben,
Steinmetzgrund, 18 Oct. 2001, H. John (GLM-F-54365);
Germany, üringen, Landkreis Gotha, Friedrichroda,
25 Sep. 2004, H. Jage & H. Boyle (GLM-F-64230); on H.
murorum, Germany, Sachsen-Anhalt, Landkreis Wit-
tenberg, north west of Oranienbaum, 20 May 2003, H.
Jage (GLM-F-63253); Germany, Sachsen-Anhalt, Land-
kreis Mansfeld-Südharz, Grillenberg, 9 Nov. 2003,
H. Jage (GLM-F-63260); on H. porrifolium, Slovakia,
Žilinský kraj, Okres Bytča, Súľovské vrchy, 26 Jul. 2011,
F. Klenke (GLM-F-105347); on H. racemosum, Germany,
Nordrhein-Westfalen, Mönchengladbach, Schloß Dyk, 6
Sep. 2003, U. Raabe (GLM-F-63139); on H. sabaudum,
Germany, Sachsen-Anhalt, Dübener Heide, Rotta, 09
Oct. 1976, U. Braun (HAL 953 F), GenBank number:
MZ420213 (28S rDNA); Germany, Sachsen, Bautzen, 15
Oct. 2003, H. Boyle (GLM-F-51367); Germany, Sachsen,
Landkreis Bautzen, Bischofwerda, 12 Jul. 2007, H. Boyle
(GLM-F-81076); Germany, Sachsen, Görlitz, 2 Sep. 2003,
H. Boyle (GLM-F- 51329); Germany, Sachsen, Görlitz, 9
Sep. 2003, S. Hoeich & H. Boyle (GLM-F-51429); Ger-
many, Sachsen, Landkreis Görlitz, Niesky, 16 Nov. 2006,
H. Boyle (GLM-F-78755); Germany, Sachsen, Bautzen, 19
Sep. 2006, H. Boyle (GLM-F-74935); Germany, Sachsen,
Landkreis Görlitz, Herrenhut, 28 June 2007, H. Boyle

112 Guan-Xiu Guan et alii
(GLM-F-79431); Germany, Sachsen, Landkreis Görlitz,
Seiennersdorf, 28 June 2007, H. Boyle & G. Zschi-
eschang (GLM-F-79445); Germany, Sachsen, Landkreis
Bautzen, Großröhrsdorf, 23 Sep. 2009, H. Boyle (GLM-
F-99681); H. schmidtii, Germany, Sachsen-Anhalt, Saal-
ekreis, Gimritzer Porphyrlandschaft, 21 Nov. 2007,
H. John (GLM-F-94444); on Hieracium sp., Germany,
Thüringen, Greiz, Cossengrün, 5 Sep. 1999, H. Jage
(GLM-F-47535); on H. virosum, Russia, Bashkortostan
Tujmazinskij Rayon, south west of Tujmazy, Kandri-
kul Lake, 12 Jul. 1977, U. Braun (HAL 859 F), GenBank
number: MZ420206 (ITS+28S); on Pilosella procera,
China, Xinjiang, Altay, Fuhai, 6 Aug. 1975, Z.Y. Zhao
(HMAS39956).
Notes. Golovinomyces cichoracearum s. lat. (sy n.
Erysiphe cichoracearum) on Hieracium and Pilosella spp.
is common and widespread in Europe, North America
and parts of Asia. Golovinomyces cichoracearum s . str.
does not occur on Hieracium spp. Based on comprehen-
sive phylogenetic examinations, Takamatsu et al. (2013)
demonstrated that G. cichoracearum s. str. is conned to
host species of Scorzonera and Tragopogon. A single re-
examined collection on H. sabaudum (HAL 953 F) was
a mixed infection with G. hieraciorum and Neoërysiphe
nevoi. is is the rst report of the N. nevoi on Hiera-
cium. e asexual stage in this collection was N. nevoi,
conrmed by ITS rDNA sequence data retrieved from
mycelia and conidia, whereas the chasmothecia in this
collection were of G. hieraciorum, which was also con-
rmed by ITS rDNA sequences data obtained from chas-
mothecia.
Golovinomyces cichoracearum on L. communis
has been reported from numerous European countries
(Amano, 1986; Braun, 1995; Farr and Rossman, 2021).
In order to clarify the phylogenetic and taxonomic posi-
tion of this taxon and to nd appropriate material for
additional sequence analyses, all German powdery mil-
dew collections on L. communis, deposited at GLM and
HAL, have been re-examined. All of these collections
were shown to be either misidentied or were powdery
mildew species other than G. cichoracearum s. lat.
e following re-examined collections, including
some originally misidentied as G. cichoracearum, per-
tain to Podosphaera ergerontis-canadensis on L. com-
munis. Germany, Hessen, Schwalm-Eder-Kreis, Bad
Zwesten, 14 Jul. 2007, C. Klencke (GLM-F-104902). Ger-
many, Sachsen, Landkreis Nordsachsen, Zschepplin,
OT Krippehna, 29 Sep. 1997, H. Jage (GLM-F-48602).
Germany, Sachsen, Landkreis Nordsachen, Laußig, OT
Pressel, 22 Oct. 1998, H. Jage (GLM-F-50206). Ger-
many, Sachsen, Oschatz, park, 8 Oct. 2006, H. Jage
(GLM-F-86559). Germany, Sachsen, Landkreis Görlitz,
Oberoderwitz, Kirchweg, 19 Jul. 2007, H. Boyle (GLM-
F-80873). Germany, Sachsen, Landkreis Görlitz, Niesky,
Stannewisch, 5 Jul. 2007, H. Boyle & S. Hoeich (GLM-
F-79525). Germany, Sachsen, Landkreis Görlitz, Box-
berg, Uhyst, 20 Oct. 2005, H. Boyle (GLM-F-70244).
Germany, Sachsen, Görlitz, 26 Aug. 2005, H. Boyle
(GLM-F-70145). Germany, Sachsen, Zittau, Westpark,
9 Aug. 2007, H. Boyle (GLM-F-80893). Germany, Sach-
sen-Anhalt, Landkreis Börde, north east of Samswe-
gen, Heidberg, 16 Oct. 2006, H. Jage (GLM-F-86402).
Germany, Sachsen-Anhalt, Landkreis Wittenberg,
Wörlitz, Wörlitzer Park, 16 Nov. 2000, H. Jage (GLM-
F-47950). Germany, Sachsen-Anhalt, Burgenlandkreis,
Burg Saaleck, 29 Sep. 2003, H. Jage (GLM-F-66171).
Germany, Sachsen-Anhalt, Dessau, Kühnauer Park, 13
Sep. 2001, H. Jage (GLM-F-54331). Germany, Sachsen-
Anhalt, Burgenlandkreis, Osterfeld, east of OT Wal-
dau, 27 Aug. 2003, H. Jage (GLM-F-63279). Germany,
Sachsen-Anhalt, Landkreis Wittenberg, Bleddin, west
of Bleddiner Riß, 31 Oct. 2000, H. Jage (GLM-F-48009).
Germany, Sachsen-Anhalt, Halle (Saale), Herrmann-
Street, 1 Jun. 2020, U. Braun (HAL 3350 F). Other col-
lections (only asexual morphs), mostly identied as G.
cichoracearum, proved to be N. nevoi on L. communis
[Germany, Mecklenburg-Vorpommern, Usedon, east
of Ückeritz, 9 Aug. 1988, H.Jage (GLM-F-58821). Ger-
many, Rheinland-Pfalz, Kreis Cochem, Zell, OT Tellig,
12 Jul. 1999, H. Jage (GLM-F-46819). Germany, Sachsen,
Landkreis Nordsachsen, Laußig, OT Görschlitz, 22 June
1997, H. Jage (GLM-F-50126). Germany, Sachsen, Land-
kreis Nordsachen, Zscheppelin, OT Hohenprießnitz,
10 May 1998, H. Jage et al. (GLM-F-49966). Germany,
Sachsen, Landkreis Görlitz, Bertsdorf, 31 May 2007, H.
Boyle (GLM-F-79245). Germany, Sachsen, Landkreis
Görlitz, Johnsdorf, Hänischmühe, 21 June 2007, H.
Boyle & S. Hoeich (GLM-F-79470). Germany, Sachsen-
Anhalt, Landkreis Wittenberg, Kemberg, 3 Apr. 1999,
H. Jage (GLM-F-46829). Germany, Sachsen-Anhalt, Sal-
zlandkreis, Calbe, 5 May 2001, H. Jage (GLM-F-57042).
Germany, Sachsen-Anhalt, Landkreis Börde, Oscherle-
ben, OT Hadmersleben, 12 June 2002, H. Jage (GLM-
F-57288). Germany, Sachsen-Anhalt, Halle (Saale), Gus-
tav-Anlauf-Street, 2 Jun. 2020, U. Braun (HAL 3349 F).
Germany, üringen, Ilm-Kreis, Arnstadt, 5 June 1997,
H. Jage (GLM-F-50147)].
erefore, reports of G. cichoracearum s. lat. (sy n.
Erysiphe cichoracearum) on L. communis from various
countries [Europe (Belarus, England, France, Hungary,
Italy, Netherlands, Norway, Poland, Romania, Sweden,
Switzerland, Ukraine, United Kingdom, Yugoslavia),
Asia (Armenia)] are doubtful, and need to be reviewed
and conrmed.

113
A cryptic powdery mildew on Hieracium and Pilosella
Phylogenetic analyses
ITS and 28S rDNA sequences were generated from
four Hieracium spp. specimens (highlighted in bold font
in Figure 2). Newly determined sequences were aligned
with other closely related sequences that were retrieved
from DNA databases, and were based on Scholler et al.
(2016), Bradshaw et al. (2017), and Meeboon et al. (2018).
Figure 2. Phylogenetic analysis of the ITS and 28S rDNA regions. e bootstrap support values greater than 75% for maximum parsimony
(MP) and maximum likelihood (ML) are displayed followed by posterior probabilities greater than 0.90 for Bayesian Inference (BI). e
sequences determined in this study were shown in bold font and pink shade. Golovinomyces inulae was used as the outgroup taxon.

114 Guan-Xiu Guan et alii
Golovinomyces inulae was used as the outgroup taxon.
e combined dataset of ITS and 28S rDNA sequences
consisted of 48 sequences including 1488 characters, of
which 108 (7.3%) were parsimony informative and 14
(0.9%) were parsimony-uninformative. e maximum
parsimony tree (TL = 178, CI = 0.8539, RI = 0.9762, RC
= 0.8336) with the greatest likelihood value is shown in
Figure 2. A phylogenetic tree generated from ML and BI
analysis was almost identical to the MP tree, so this tree
is not presented here.
The tree comprises three groups with high reli-
ability, one comprising isolates from Compositae (tribe
Anthemideae) (MP = 95%, ML = 99%, BI = 1.00), the
second representing the G. biocellatus complex clade,
comprising isolates from Lamiaceae with high reliability
(MP =100%, ML = 100%, BI = 1.00), and the third was
a cluster composed of isolates from Compositae (tribe
Lactuceae) also with high reliability (MP =100%, ML =
100%, BI = 1.00). e second and third groups formed a
big clade with high reliability (ML = 87%, BI = 0.97).
Sequences from Hieracium spp. and Pilosella auran-
tiaca as hosts are situated in lineages IX, comprising iso-
lates from Compositae (tribe Lactuceae) with strong reli-
ability (Figure S1). Two sequences from powdery mildew
on Pilosella aurantiaca formed a subclade with strong BS
supports (ML = 90%) (Figure 2).
DISCUSSION
Golovinomyces, with Euoidium as the synonymous
anamorph genus, currently comprises 71 species and
ve varieties (Braun and Cook, 2012; Liu and Wen, 2013;
Bradshaw et al., 2017; Meeboon et al., 2018; Braun et al.,
2019; Qiu et al., 2020). Takamatsu et al. (2013) published
comprehensive phylogenetic analyses of 33 Golovino-
myces spp., which were split into 11 genetically distinct
lineages. Sequences obtained from seven collections
from hosts in tribe Lactuceae of the Compositae were in
two genetically distinct lineages. One was composed of
sequences from collections on Scorzonera and Tragopo-
gon (tribe Lactuceae, subtribe Scorzonerinae), viz. G.
cichoracearum s. str.. e second lineage consisted of a
single sequence from a collection on L. communis (tribe
Lactuceae, subtribe Crepidinae) from Switzerland, which
can currently only be referred to as Golovinomyces sp.
New sequences retrieved from Golovinomyces collections
on Hieracium spp. and Pilosella aurantiaca (tribe Lac-
tuceae, subtribe Hieraciinae) have been generated and
added to the current phylogenetic ITS and 28S rDNA
analyses (Figure S1, including 43 species of Golovinomy-
ces), which signicantly increased the Golovinomyces lin-
eage. is lineage, with high reliability (MP = 100%, ML
= 100%, BI = 1.00), is distant from all other clades within
Golovinomyces, and remains divided into two clades, viz.,
the Hieracium clades (including Pilosella aurantiaca) and
a L. communis clade. e present study supports previous
presumptions of a close co-evolution between Golovino-
myces species and particular host tribes and subtribes of
the Compositae (Matsuda and Takamatsu, 2003; Taka-
matsu et al., 2013; Qiu et al., 2020).
The Hieracium clade, represents a new, hitherto
undescribed species of Golovinomyces, previously hid-
den within G. cichoracearum s. lat., which is described
here as G. hieraciorum. e new species is conned to
Hieracium and Pilosella spp. (tribe Lactuceae, subtribe
Hieraciinae), which reects the close co-evolution of
Golovinomyces with host tribes and subtribes within the
Compositae. Pilosella is phylogenetically close to Hiera-
cium and was previously oen treated as a subgenus of
Hieracium. Fehrer et al. (2007) and Krak et al. (2013)
conducted comprehensive phylogenetic analyses, indicat-
ing that Hieracium and Pilosella should be two distinct
plant genera. e phylogenetically proven occurrence of
G. hieraciorum on Hieracium and Pilosella spp. reects
the close anity of these two host genera.
Golovinomyces on Hieracium and Pilosella spp. is
widespread in Europe, North America, and parts of
Asia. Besides G. hieraciorum, two additional powdery
mildews may occur on Hieracium spp., viz. Neoërysiphe
nevoi and Podosphaera erigerontis-canadensis. Mixed
infections with these two pathogens have to be previ-
ously taken into consideration. One collection on H.
sabaudum from Germany was such a mixed infection
of G. hieraciorum and N. nevoi. is is the rst report
of N. nevoi on Hieracium. Neoërysiphe nevoi and G.
hieraciorum, two powdery mildew species on Composi-
tae, are easily confusable and not easily distinguishable
based on morphology. However, the asci of Neoërysiphe
spp. remain immature, and ascospores do not develop in
2–8-spored asci until aer overwintering. In Golovino-
myces spp., including G. hieraciorum, ascospores mature
in the current season and usually develop in 2-spored
asci. Furthermore, the hyphal appressoria in N. nevoi are
lobed, in contrast to nipple-shaped hyphal appressoria
on G. hieraciorum.
e L. communis clade within Golovinomyces posed
a special problem. Lapsana belongs to subtribe Crepidi-
nae of tribe Lactuceae and is now conned to a single
species, L. communis (Pak and Bremer, 1995). Attempts
failed to solve this problem by tracing additional col-
lections for detailed morphological and phylogenetical
examinations of this powdery mildew. Numerous collec-
tions on L. communis from the herbaria GLM and HAL,

115
A cryptic powdery mildew on Hieracium and Pilosella
identied as Erysiphe cichoracearum or G. cichoracearum,
have been re-examined, but all were misidentied. Most
collections (without chasmothecia) were shown to belong
to N. nevoi (hyphal appressoria lobed, foot-cells of the
conidiophores characteristically short, 20–50 × 9–15 µm,
basal septae of conidiophores foot-cells oen conspicu-
ously constricted, conidia with striate surfaces [as shown
by scanning electron microscopy]). e occurrence of
N. nevoi on L. communis has also been conrmed by
sequence analyses and armed in the rst report of this
species on this host from Germany (Schmidt and Braun,
2020). ere were even some collections with chasmoth-
ecia, originally identied as “Golovinomyces cichoracear-
um”, which turned out to be Po. erigerontis-canadensis
(chasmothecia with single asci). Podosphaera erigerontis-
canadensis is already known on L. communis in Germa-
ny (reported in Jage et al. (2010), under the name Po. fus-
ca). In summary, all collections on L. communis assigned
to G. cichoracearum or E. cichoracearum, including those
reported in Jage et al. (2010), were here shown to be misi-
dentied. erefore, the identity of the true Golovinomy-
ces on L. communis could not be claried in the course
of the present study. Records of G. cichoracearum and
E. cichoracearum, respectively, on Lapsana from various
countries in Europe (Belarus, England, France, Hungary,
Italy, Netherlands, Norway, Poland, Romania, Sweden,
Switzerland, Ukraine, United Kingdom, former Yugosla-
via) and Near East-Caucasus (Armenia) remain unclear
and need to be veried.
ACKNOWLEDGMENTS
e authors thank Susumu Takamatsu for help with
the literature. e curators of the Herbarium Myco-
logicum Academiae Sinicae (HMAS) are acknowledged
for allowing access to specimens for this study. is
research was nancially supported by the National Nat-
ural Science Foundation of China (Nos 31970019 and
31670022).
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Firenze University Press
www.fupress.com/pm
ISSN 0031-9465 (print) | ISSN 1593-2095 (online) | DOI: 10.36253/phyto-12992
Phytopathologia Mediterranea 61(1): 107-117, 2022
G.-X. Guan, S.-Y. Liu, U. Braun, P.-L. Qiu, J. Liu, F.-Y. Zhao, S.-R. Tang, J.-N. Li, V.-N. Nguyen (2022). A cryptic
powdery mildew (Golovinomyces hieraciorum sp. nov.) on Hieracium and Pilosella (Compositae). Phytopathologia
Mediterranea 61(1): 107-117. doi: 10. 36253/phyto-12992
G. sordidus ex Plantago lanceolata MUMH661 Switzerland
G. sordidus ex Plantago sp. AB769467 Argentina
G. sordidus ex Plantago asiatica MUMHn41 Japan
G. cichoracearum ex Scorzonera hispanica MUMH759 Lithuania
G. cichoracearum ex Tragopogon pratensis AB769449 Lithuania
G. orontii ex Valeriana officinalis AB769471 Lithuania
G. orontii ex Viola arvensis AB769472 Switzerland
G. orontii ex Papaver rhoeas AB769466 Switzerland
G. bolayi ex Cucumis sativus AB427187 Japan
G. bolayi ex Arabidopsis thaliana A B769456 Japan
G. bolayi ex Incarvillea mairei AB 769453 Switzerland
G. bolayi ex Kalanchoe sp. LC417096 Germ any
G. bolayi ex Lamium amplexicaule AB427188 Japan
G. bolayi ex Papaver somniferum A B769463 USA
G. tabaci ex Galium spurium AB430815 Japan
G. tabaci ex Galium spurium var. echinospermon AB430816 Japan
G. tabaci ex Galium spurium var. echinospermon AB430817 Japan
G. tabaci ex Inula helenium AB769445 Lithuania
G.t abaci ex Capsella bursa-pastoris LC417098 Japan
G. tabaci ex Galium spurium var. echinospermon AB430818 Japan
G. tabaci ex Capsella bursa-pastoris LC417100 Japan
G. tabaci ex Capsella rubella LC417099 Switzerland
G. tabaci ex Galium aparine AB430813 Ukraine
G. leuceriae ex Leuceria thermarum AB246765 Argentina
G. leuceriae ex Leuceria thermarum AB246766 Argentina
Euoidium reginae ex Mutisia decurrens AB246759 Argentina
Euoidium reginae ex Mutisia decurrens AB246760 Argentina
Euoidium reginae ex Mutisia decurrens AB246761 Argentina
G. adenophorae ex Adenophora triphylla AB769459 Japan
G. sparsus ex Euphorbia collina AB769460 Brazil
G. sparsus ex Euphorbia collina AB769461 Argentina
G. sonchicola ex Sonchus arvensis AB453762 Lithuania
G. sonchicola ex Sonchus oleraceus DNA70 Japan
G. sonchicola ex Sonchus arvensis MUMH683
G.vincae e x Vinca pervinca AB769444 Argentina
G. cynoglossi ex Myosotis sp. AB769455 Australia
G. circumfusus ex Eupatorium cannabinum GLM49501 Germany
G. circumfusus ex Eupatorium cannabinum GLM74796 Germany
G. circumfusus ex Eupatorium cannabinum HAL3300F Germany
G. verbasci exV erbascum densiflorum MUMH958 Lithuania
G. verbasci ex Verbascum thapsus HMJAU-PM91935 China
G.asperifoliorum ex Pulmonaria officinalis MH189691 Germany
G. asperifoliorum ex Symphytum officinale MH189692 Russia
G. fischeri ex Senecio doronicum AB769450 Switzerland
G. calceolariae ex Calceolaria polyrrhiza AB430810 Argentina
G. calceolariae ex Galium aparin AB430812 Argentina
G. magnicellulatus ex Phlox paniculata AB769441 Lithuania
G. magnicellulatus ex Phlox paniculata AB769442 USA
G. magnicellulatus ex Physalis alkekengi HMJAU PM91840 China
Euoidium fuegianum ex Ranunculus sp AB769443 Argentina
Pilosella aurantiaca KY660945 UK
Pilosella aurantiaca KY660935 UK
Hieracium umbellatum HMJAU-PM91858 China
Hieracium umbellatum HMJAU-PM91859 China
Hieracium virosum HAL859F Russia
Hieracium sabaudum HAL953F Germany
Golovinomyces sp. ex Lapsana communis MUMH637 Switzerland
G. longipes ex Petunia hybrida AB769440 Argentina
G. lycopersici ex Lycopesicon esculentum AF229021 Australia
G. neosalviae ex Salvia fructicosa KR M 33266 Germany
G. neosalviae ex Salvia lavandulifolia KR M 39098 Germany
G. neosalviae ex Salvia lavandulifolia KR M 39099 Germany
G. neosalviae ex Salvia officinalis KR M 35012 Germany
G. neosalviae ex Salvia officinalis KR M 38203 Germany
G. biocellatus s. str. ex Lycopus europaeus KR M 27775 Germany
G. biocellatus s. str. ex Lycopus europaeus KR M 35014 Germany
G. biocellatus s. str. ex Glechoma hederacea KR M 21890 Germany
G. biocellatus s. str. ex Glechoma hederacea KR M 21901 Germany
G. salviae ex Salvia nemorosa KR M 46020 Germany
G. salviae ex Salvia pratensis KR M 18634 Germany
G. salviae ex Salvia pratensis MUMH935 Lithuania
G. monardae ex Mentha piperita KR M 39096 Germany
G. monardae ex Monarda citriodora KR M 24044 Germany
G. monardae ex Monarda fistulosa KR M 35023 Germany
G. monardae ex Thymus citriodorus KR M 33259 Germany
G. ocimi ex Ocimum tenuiflorum LC306656 Thailand
G. ocimi ex Ocimum tenuiflorum LC306657 Thailand
G. riedlianus ex Galium ruthenicum AB430814 Ukraine
G. riedlianus ex Galium verum AB430820 Ukraine
G. riedlianus ex Galium verum AB430819 Japan
G. riedlianus ex Galium album AB430811 Switzerland
G. chrysanthemi ex Chrysanthemum morifolium GLM F047617 Germany
G. chrysanthemi ex Chrysanthemum morifolium GLM F048600 Germany
G. chrysanthemi ex Chrysanthemum morifolium MUMH6851 USA
G. chrysanthemi ex Chrysanthemum morifolium JKI 2250 C14 Germany
G. chrysanthemi ex Chrysanthemum morifolium MUMH853 Japan
G. artemisiae exA rtemisia dubia MUMH175 Japan
G. artemisiae ex Artemisia vulgaris MUMH1041 USA
G. artemisiae ex Artemisia montana MUMH519 Japan
G. artemisiae ex Nipponanthemum nipponicum MUMH1084 Japan
G. artemisiae ex Artemisia verlotiorum MUMH1877 Argentina
G. artemisiae ex Artemisia vulgaris MUMH6848 Japan
G. artemisiae ex Artemisia vulgaris MUMH6849 Japan
G. macrocarpus ex Achillea millefolium MUMH939 Lithuania
G. macrocarpus ex Tanacetum sp. VPRI20160 Australia
G. macrocarpus ex Tanacetum vulgare HAL 3153F Germany
G. asperifolii ex Myosotis arvensis MH189704 Germany
G. asperifolii ex Trigonotis peduncularis MH189708 Korea
G. asperifolii ex Cynoglossum officinale MH189702 USA
Golovinomyces sp ex Ageratum conyzoides MUMH6739 Thailand
Golovinomyces sp ex Bidens pilosa MUMH6685 Thailand
Euoidium sp. ex Wedelia glauca AB769423 Argentina
Euoidium sp. ex Wedelia glauca AB769424 Argentina
G. ambrosiae ex Ambrosia artemisiifolia HMJAU-PM91812 China
G. ambrosiae ex Ambrosia trifida HMJAU-PM91813 China
G. ambrosiae ex Aster novi-belgii HMJAU-PM91804 China
G. ambrosiae ex Dahlia pinnata HMJAU-PM91822 China
G. ambrosiae ex Zinnia elegans HMJAU-PM91842 China
G. latisporus ex Helianthus annuus MUMH731 Lithuania
G. latisporus ex Helianthus tuberosus AB769419 Lithuania
Euoidium mutisiae ex Mutisia spinosa AB246762 Argentina
Euoidium mutisiae ex Mutisia spinosa AB246764 Argentina
Euoidium mutisiae ex Mutisia spinosa AB246763 Argentina
G. asterum var. asterum ex Aster sp. AB769416 Australia
G. inulae ex Inula britannica GU143089 Korea
G. inulae ex Inula salicina MUMH1334 Switzerland
G. depressus ex Arctium lappa MUMH696 Hungary
G. depressus ex Arctium lappa MUMH957 Lithuania
G. echinopis ex Echinops exaltatus AB769414 Switzerland
G. montagnei ex Cirsium japonicum AB769413 Japan
G. montagnei ex Serratula coronata AB077656 Japan
Arthrocladiella mougeotii ex Lycium chinense AB329690 Japan
1 change
97
100/100/1
100/100/1
75/-/-
96/991
100/100/1
99/96/1
-/-/0.96
97/98/1
-/-/1
84/-/1
100/100/1
92/94/0.98
100/100/1
94/96/1
-/7/-
100/100/1
90/94/1
-/76/0.96
100/100/1
75/85/-
94/96/1
98/95/1
-/89/0.95
100/100/1
100/100/1
100/100/1
-/78/0.99
86/98/-
98/87/0.90
-/-/0.91
99/100/1
100/100/1
90/95/1
93/96/1
93/92/1
99/100/1
77/82/0.97
85/93/1
88/96/1
100/99/1
100/99/1
75/-/0.95
-/86/0.98
-/-/0.92
-/-0.97
-/-0.91
-/-/1
-/-/0.97
-/-/0.97
ITS+28S rDNA
122 sequences
1194 characters
TL = 538
CI = 0.5818
RI = 0.9196
RC = 0.5350
Lamiaceae
Asteraceae [Trib. Lactuceae]
Solanaceae
Asteraceae [Trib. Anthemideae]
Asteraceae [Trib. Cardueae]
Asteraceae [Trib. Astereae]
Asteraceae [Trib. Inuleae]
Boraginaceae
Rubiaceae
Polemoniaceae
Ranunculaceae
Ⅰ
Ⅱ
Ⅲ
Ⅳ
Ⅴ
Ⅵ
Ⅶ
Ⅷ
Ⅸ
Ⅹ
Ⅺ
Golovinomyces hieraciorum sp. nov.
Figure S1. Phylogenetic analysis from maximum parsimony (MP), maximum likelihood (ML) and Bayesian Inference (BI) analyses of all
available Golovinomyces species, based on combined ITS and 28S rDNA regions. e bootstrap support values greater than 75% for MP and
ML are displayed followed by posterior probabilities greater than 0.90 for BI. e sequences determined in this study are shown in bold font
and pink shade. Arthrocladiella mougeoti was used as the outgroup taxon.

10
Table S1. List of hosts, countries of collection, and accession numbers of the ITS and 28S rDNA sequences used in this study.
Species Host Host family VoucheraCountry of
origin
Accession number Reference
ITS 28S
Arthrocladiella mougeotii Lycium chinense Solanaceae MUMH851 Japan AB329690 AB329690 Takamatsu et al., 2008
Euoidium fuegianum Ranunculus sp. Ranunculaceae BCRU1608 Argentina AB769443 — Takamatsu et al., 2013
Euoidium mutisiae Mutisia spinosa Compositae (Mutisieae) BCRU330 Argentina AB246762 AB246762 Takamatsu et al., 2006
Euoidium mutisiae Mutisia spinosa Compositae (Mutisieae) BCRU4644 Argentina AB246763 AB246763 Takamatsu et al., 2006
Euoidium mutisiae Mutisia spinosa Compositae (Mutisieae) MUMH2457 Argentina AB246764 AB246764 Takamatsu et al., 2006
Euoidium reginae Mutisia decurrens Compositae (Mutisieae) BCRU4645 Argentina AB246759 AB246759 Takamatsu et al., 2006
Euoidium reginae Mutisia decurrens Compositae (Mutisieae) MUMH1882 Argentina AB246760 AB246760 Takamatsu et al., 2006
Euoidium reginae Mutisia decurrens Compositae (Mutisieae) MUMH2458 Argentina AB246761 AB246761 Takamatsu et al., 2006
Euoidium sp. Wedelia glauca Compositae (Heliantheae) MUMH3042 Argentina AB769423 AB769423 Takamatsu et al., 2013
Euoidium sp. Wedelia glauca Compositae (Heliantheae) MUMH3081 Argentina AB769424 AB769424 Takamatsu et al., 2013
G. adenophorae Adenophora triphylla Campanulaceae —Japan AB769459 AB769459 Takamatsu et al., 2013
G. ambrosiae Ambrosia artemisiifolia Compositae (Heliantheae) HMJAU-PM91812 China MK452583 MK452656 Qiu et al., 2020
G. ambrosiae Ambrosia trida Compositae (Heliantheae) HMJAU-PM91813 China MK452584 MK452657 Qiu et al., 2020
G. ambrosiae Aster novi-belgii Compositae (Astereae) HMJAU-PM91804 China MK452575 MK452648 Qiu et al., 2020
G. ambrosiae Dahlia pinnata Compositae (Heliantheae) HMJAU-PM91822 China MK452593 MK452666 Qiu et al., 2020
G. ambrosiae Zinnia elegans Compositae (Heliantheae) HMJAU-PM91842 China MK452612 MK452685 Qiu et al., 2020
G. artemisiae Artemisia montana Compositae (Anthemideae) MUMH519 Japan AB077649 AB077648 Matsuda and Takamatsu, 2003
G. artemisiae Artemisia princeps Compositae (Anthemideae) MUMH175 Japan AB077637 AB077636 Matsuda and Takamatsu, 2003
G. artemisiae Artemisia verlotiorum Compositae (Anthemideae) MUMH1877 Argentina AB769431 AB769431 Takamatsu et al., 2013
G. artemisiae Artemisia vulgaris Compositae (Anthemideae) MUMH1041 USA AB769432 AB769432 Takamatsu et al., 2013
G. artemisiae Artemisia vulgaris Compositae (Anthemideae) MUMH6848 Japan LC217863 LC217863 Bradshaw et al., 2017
G. artemisiae Artemisia vulgaris Compositae (Anthemideae) MUMH6849 Japan LC217864 LC217864 Bradshaw et al., 2017
G. artemisiae Nipponanthemum nipponicum Compositae (Anthemideae) MUMH1084 Japan AB769433 AB769433 Bradshaw et al., 2017
G. asperifolii Cynoglossum ocinale Boraginaceae KUS-F30414 USA MH189702 — Braun et al., 2018
G. asperifolii Myosotis arvensis Boraginaceae GLM-F079306 Germany MH189704 — Braun et al., 2018
G. asperifolii Trigonotis peduncularis Boraginaceae KUS-F29281 Korea MH189708 — Braun et al., 2018
G. asperifoliorum Pulmonaria ocinalis Boraginaceae GLM-F100040 Germany MH189691 MH189691 Braun et al., 2018
G. asperifoliorum Symphytum ocinale Boraginaceae KUS-F28744 Russia MH189692 MH189692 Braun et al., 2018
G. asterum var. asterum Aster sp. Compositae (Astereae) MUMH684 Australia AB769416 AB769416 Takamatsu et al., 2013
G. biocellatus s. str. Glechoma hederacea Lamiaceae KR-M 21890 Germany LC076805 LC076805 Scholler et al., 2016
G. biocellatus s. str. Glechoma hederacea Lamiaceae KR-M 21901 Germany LC076806 LC076806 Scholler et al., 2016
G. biocellatus s. str. Lycopus europaeus Labiatae KR-M 27775 Germany LC076814 LC076814 Scholler et al., 2016
G. biocellatus s. str. Lycopus europaeus Labiatae KR-M 35014 Germany LC076825 LC076825 Scholler et al., 2016
G. bolayi Arabidopsis thaliana Brassicaceae MUMH2603 Japan AB769456 AB769456 Braun et al., 2019
(Continued)

11
Species Host Host family VoucheraCountry of
origin
Accession number Reference
ITS 28S
G. bolayi Cucumis sativus Cucurbitaceae MUMH1978 Japan AB427187 AB427187 Braun et al., 2019
G. bolayi Incarvillea mairei Bignoniaceae MUMH1387 Switzerland AB769453 AB769453 Braun et al., 2019
G. bolayi Kalanchoe sp. Crassulaceae HAL3275F Germany LC417096 LC417096 Braun et al., 2019
G. bolayi Lamium amplexicaule Lamiaceae MUMH2003 Japan AB427188 AB427188 Braun et al., 2019
G. bolayi Papaver somniferum Papaveraceae MUMH1037 USA AB769463 AB769463 Braun et al., 2019
G. calceolariae Calceolaria polyrrhiza Scrophulariaceae MUMH1934 Argentina AB430810 AB430810 Takamatsu et al., 2009
G. calceolariae Galium aparin Rubiaceae MUMH1879 Argentina AB430812 AB430812 Takamatsu et al., 2009
G. chrysanthemi Chrysanthemum morifolium Compositae (Anthemideae) GLM-F047617 Germany LC217866 LC217866 Bradshaw et al., 2017
G. chrysanthemi Chrysanthemum morifolium Compositae (Anthemideae) GLM-F048600 Germany LC217867 LC217867 Bradshaw et al., 2017
G. chrysanthemi Chrysanthemum morifolium Compositae (Anthemideae) JKI-2250-C14 Germany LC217869 LC217869 Bradshaw et al., 2017
G. chrysanthemi Chrysanthemum morifolium Compositae (Anthemideae) HAL3171F USA LC217865 LC217865 Bradshaw et al., 2017
G. chrysanthemi Chrysanthemum morifolium Compositae (Anthemideae) MUMH853 Japan AB077654 AB077653 Bradshaw et al., 2017
G. cichoracearum Scorzonera hispanica Compositae (Lactuceae) MUMH759 Lithuania AB077682 AB077681 Matsuda and Takamatsu, 2003
G. cichoracearum Tragopogon pratensis Compositae (Lactuceae) MUMH937 Lithuania AB769449 AB769449 Takamatsu et al., 2013
G. circumfusus Eupatorium cannabinum Compositae (Eupatorieae) GLM-F49501 Germany MK452630 MK452703 Qiu et al., 2020
G. circumfusus Eupatorium cannabinum Compositae (Eupatorieae) GLM-F74796 Germany MK452629 MK452702 Qiu et al., 2020
G. circumfusus Eupatorium cannabinum Compositae (Eupatorieae) HAL3300F Germany MK452628 MK452701 Qiu et al., 2020
G. cynoglossi Myos otis sp. Boraginaceae VPRI20429 Australia AB769455 AB769455 Takamatsu et al., 2013
G. depressus Arctium lappa Compositae (Cynareae) MUMH696 Hungary AB077675 AB077676 Matsuda and Takamatsu, 2003
G. depressus Arctium lappa Compositae (Cynareae) MUMH957 Lithuania AB769411 AB769412 Takamatsu et al., 2013
G. echinopis Echinops exaltatus Compositae (Cynareae) MUMH1363 Switzerland AB769414 AB769414 Takamatsu et al., 2013
G. scheri Senecio doronicum Compositae (Senecioneae) MUMH1343 Switzerland AB769450 AB769450 Takamatsu et al., 2013
G. hieraciorum Hieracium sabaudum Compositae (Lactuceae) HAL953F Germany — MZ420213 is study
G. hieraciorum Hieracium umbellatum Compositae (Lactuceae) HMJAU-PM91858 China MZ420204 MZ420204 is study
G. hieraciorum Hieracium umbellatum Compositae (Lactuceae) HMJAU-PM91859 China MZ420205 MZ420205 is study
G. hieraciorum Hieracium virosum Compositae (Lactuceae) HAL859F Russia MZ420206 MZ420206 is study
G. hieraciorum Pilosella aurantiaca Compositae (Lactuceae) — UK KY660945 — Ellingham et al., 2019
G. hieraciorum Pilosella aurantiaca Compositae (Lactuceae) — UK KY660935 — Ellingham et al., 2019
G. inulae Inula britannica var. chinensis Compositae (Inuleae) KUS-F24692 Korea GU143089 — Park et al., 2010
G. inulae Inula salicina Compositae (Inuleae) MUMH1334 Switzerland AB769428 AB769428 Takamatsu et al., 2013
G. latisporus Helianthus annuus Compositae (Heliantheae) MUMH731 Lithuania AB077679 AB077680 Matsuda and Takamatsu, 2003
G. latisporus Helianthus tuberosus Compositae (Heliantheae) MUMH3081 Lithuania AB769419 AB769419 Takamatsu et al., 2013
G. leuceriae Leuceria thermarum Compositae (Mutisieae) MUMH1880 Argentina AB246765 AB246765 Takamatsu et al., 2006
Table S1. (Continued).
(Continued)

12
Species Host Host family VoucheraCountry of
origin
Accession number Reference
ITS 28S
G. leuceriae Leuceria thermarum Compositae (Mutisieae) MUMH2527 Argentina AB246766 AB246766 Takamatsu et al., 2006
G. longipes Petunia hybrida Solanaceae MUMH2489 Argentina AB769440 AB769440 Takamatsu et al., 2013
G. lycopersici Lycopesicon esculentum Solanaceae VPRI 19847 Australia AF229021 — Kiss et al., 2001
G. macrocarpus Achillea millefolium Compositae (Anthemideae) MUMH939 Lithuania AB769429 AB769429 Takamatsu et al., 2013
G. macrocarpus Tanacetum sp. Compositae (Anthemideae) VPRI20160 Australia AB769434 AB769435 Takamatsu et al., 2013
G. macrocarpus Tanacetum vulgare Compositae (Anthemideae) HAL3153F Germany LC217868 LC217868 Bradshaw et al., 2017
G. magnicellulatus Phlox paniculata Palemoniaceae MUMH933 Lithuania AB769441 AB769441 Takamatsu et al., 2013
G. magnicellulatus Phlox paniculata Palemoniaceae MUMH1036 USA (AB769441) AB769442 Takamatsu et al., 2013
G. magnicellulatus Physalis alkekengi Solanaceae HMJAU-PM91840 China MK452610 MK452683 Qiu et al., 2020
G. monardae Mentha piperita Labiatae KR-M39096 Germany LC076835 LC076835 Scholler et al., 2016
G. monardae Monarda citriodora Labiatae KR-M24044 Germany LC076809 LC076809 Scholler et al., 2016
G. monardae Monarda stulosa Lamiaceae KR-M35023 Germany LC076830 LC076830 Scholler et al., 2016
G. monardae ymus citriodorus Labiatae KR-M33259 Germany LC076815 LC076815 Scholler et al., 2016
G. montagnei Cirsium japonicum Compositae (Cardueae) MUMH1082 Japan AB769413 AB769413 Takamatsu et al., 2013
G. montagnei Serratula coronata Compositae (Cynareae) YNMH12310 Japan AB077656 AB077656 Matsuda and Takamatsu, 2003
G. neosalviae Salvia fructicosa Lamiaceae KR-M 33266 Germany LC076819 LC076819 Scholler et al., 2016
G. neosalviae Salvia lavandulifolia Lamiaceae KR-M 39098 Germany LC076837 LC076837 Scholler et al., 2016
G. neosalviae Salvia lavandulifolia Lamiaceae KR-M 39099 Germany LC076838 LC076838 Scholler et al., 2016
G. neosalviae Salvia ocinalis Lamiaceae KR-M 35012 Germany LC076823 LC076823 Scholler et al., 2016
G. neosalviae Salvia ocinalis Lamiaceae KR-M 38203 Germany LC076833 LC076833 Scholler et al., 2016
G. ocimi Ocimum tenuiorum Labiatae MUMH1803 ailand LC306656 — Meeboon et al., 2018
G. ocimi Ocimum tenuiorum Labiatae MUMH6621 ailand LC306657 — Meeboon et al., 2018
G. orontii Papaver rhoeas Papaveraceae MUMH1393 Switzerland AB769466 AB769466 Takamatsu et al., 2013
G. orontii Valeriana ocinalis Valerianaceae MUMH938 Lithuania AB769471 AB769471 Takamatsu et al., 2013
G. orontii Viola arvensis Violaceae MUMH1406 Switzerland AB769472 AB769472 Takamatsu et al., 2013
G. riedlianus Galium album Rubiaceae MUMH1301 Switzerland AB430811 AB430811 Takamatsu et al., 2009
G. riedlianus Galium ruthenicum Rubiaceae MUMH3223 Ukraine AB430814 AB430814 Takamatsu et al., 2009
G. riedlianus Galium verum Rubiaceae MUMH1148 Japan AB430819 AB430819 Takamatsu et al., 2009
G. riedlianus Galium verum Rubiaceae MUMH3217 Ukraine AB430820 AB430820 Takamatsu et al., 2009
G. salviae Salvia nemorosa Lamiaceae KR-M 46020 Germany LC100001 LC100001 Scholler et al., 2016
G. salviae Salvia pratensis Lamiaceae KR-M 18634 Germany LC076803 LC076803 Scholler et al., 2016
G. salviae Salvia pratensis Lamiaceae MUMH935 Lithuania AB769437 AB077690 Takamatsu et al., 2013
G. sonchicola Sonchus arvensis Compositae (Lactuceae) MUMH952 Lithuania AB453762 AB453762 Takamatsu et al., 2013
Table S1. (Continued).
(Continued)

13
Species Host Host family VoucheraCountry of
origin
Accession number Reference
ITS 28S
G. sonchicola Sonchus arvensis Compositae (Lactuceae) MUMH683 Hungary AB077673 AB077672 Matsuda and Takamatsu, 2003
G. sonchicola Sonchus oleraceus Compositae (Lactuceae) — Japan AB077623 AB077624 Matsuda and Takamatsu, 2003
G. sordidus Plantago asiatica Plantaginaceae MUMHn41 Japan AB077658 AB077657 Matsuda and Takamatsu, 2003
G. sordidus Plantago lanceolata Plantaginaceae MUMH661 Switzerland AB077665 AB077664 Matsuda and Takamatsu, 2003
G. sordidus Plantago sp. Plantaginaceae MUMH2433 Argentina AB769467 AB769467 Takamatsu et al., 2013
G. sparsus Euphorbia collina Euphorbiaceae MUMH3807 Brazil AB769460 AB769460 Takamatsu et al., 2013
G. sparsus Euphorbia collina Euphorbiaceae BCRU934 Argentina AB769461 AB769461 Takamatsu et al., 2013
G. tabaci Capsella bursa-pastoris Cruciferae MUMH1388 Japan LC417098 LC417098 Braun et al., 2019
G. tabaci Capsella bursa-pastoris Cruciferae HAL2506F Japan LC417100 LC417100 Braun et al., 2019
G. tabaci Capsella rubella Cruciferae — Switzerland LC417099 LC417099 Braun et al., 2019
G. tabaci Galium aparine Rubiaceae MUMH3225 Ukraine AB430813 AB430813 Braun et al., 2019
G. tabaci Galium spurium var. echinospermon Rubiaceae MUMH826 Japan AB430815 AB430815 Braun et al., 2019
G. tabaci Galium spurium var. echinospermon Rubiaceae MUMH2622 Japan AB430816 AB430816 Braun et al., 2019
G. tabaci Galium spurium var. echinospermon Rubiaceae MUMH2623 Japan AB430817 AB430817 Braun et al., 2019
G. tabaci Galium spurium var. echinospermon Rubiaceae MUMH2624 Japan AB430818 AB430818 Takamatsu et al., 2009
G. tabaci Inula helenium Compositae (Inuleae ) MUMH940 Lithuania AB769445 AB769445 Braun et al., 2019
G. verbasci Verbascum densiorum Scrophulariaceae MUMH958 Lithuania AB769468 AB769469 Takamatsu et al., 2013
G. verbasci Verbascum thapsus Scrophulariaceae HMJAU-PM91935 China MZ505461 — is study
G. vincae Vinca pervinca Apocynaceae MUMH2480 Argentina AB769444 AB769444 Takamatsu et al., 2013
Golovinomyces sp. Ageratum conyzoides Compositae (Eupatorieae) MUMH6739 ailand LC306669 — Meeboon et al., 2018
Golovinomyces sp. Bidens pilosa Compositae (Heliantheae) MUMH6685 ailand LC306668 — Meeboon et al., 2018
Golovinomyces sp. Lapsana communis Compositae (Lactuceae) MUMH637 Switzerland AB077662 AB769439 Matsuda and Takamatsu, 2003
a BCRU: Universidad Nacional del Comahue, Argentina; GLM: Senckenberg Gesellscha für Naturforschung: Senckenberg Museum für Naturkunde Görlitz, Görlitz; HAL: Martin
Luther Universität, Institut für Biologie, Bereich Geobotanik und Botanischer Garten, Herbarium, Halle; HMJAU: Herbarium of Mycology of Jilin Agricultural University, China; KR:
Herbarium of State Museum of Natural History, Karlsruhe, Germany; KUS: Korea University, Korea; MUMH: Mie University, Mycological Herbarium, Japan; VPRI: Victorian Depart-
ment of Primary Industries, Australia; YNMH: Yukihiko Nomura Mycological Herbarium, Japan.
Table S1. (Continued).