Mycoscience (2008) 49:185–191
DOI 10.1007/s10267-008-0406-8
© The Mycological Society of Japan and Springer 2008
FULL PAPER
Susumu Takamatsu · Hayato Masuya
Rangsi Divarangkoon · Yukihiko Nomura
Erysiphe fimbriata sp. nov.: a powdery mildew fungus found on
Carpinus laxiflora
Received: August 1, 2007 / Accepted: January 7, 2008
Abstract Ascomata of a powdery mildew-like fungus have
been found on Carpinus laxiflora in Tochigi Prefecture of
Japan since 2003. The morphological and molecular characteristics of this fungus are reported, and a new species,
Erysiphe fimbriata, is proposed. It has large chasmothecia
(200–250 µm in diameter) with long (up to 4–5 mm in
length), fimbriate appendages arising from the upper half
of the chasmothecia and turning upward, and numerous asci
(22–38 per chasmothecium). Erysiphe fimbriata is a unique
fungus both genetically and morphologically.
Key words Betulaceae · Erysiphaceae · Erysiphales ·
Molecular phylogeny · New species
Introduction
The family Betulaceae (Fagales) is composed of six genera
and up to 130 species of anemophilous shrubs and trees.
Most species of the family are distributed in temperate
regions of the Northern Hemisphere, i.e., Asia, Europe, and
North America (Chen et al. 1999). More than 50% of the
total species of the Betulaceae have been reported as hosts
of powdery mildew fungi (Amano 1986). Because the ratio
of hosts of powdery mildew fungi among the total species
S. Takamatsu (*)
Graduate School of Bioresources, Mie University, 1577 Kurimamachiya, Tsu 514-8507, Japan
Tel. +81-59-231-9497; Fax +81-59-231-9540
e-mail: takamatu@bio.mie-u.ac.jp
H. Masuya
Forest Pathology Laboratory, Forestry and Forest Products Research
Institute, Ibaraki, Japan
R. Divarangkoon
Department of Plant Pathology, Faculty of Agriculture, Chiang Mai
University, Chiang Mai, Thailand
Y. Nomura
Yotsukaido, Chiba, Japan
of angiosperms is about 4.5% (Amano 1986), this high ratio
of hosts in the Betulaceae may indicate a close evolutionary
affinity of this plant family with the powdery mildew fungi.
Carpinus is one of the six genera of the Betulaceae (including Corylaceae), which is distributed in Asia, Europe, and
North America, with a divergence center in China. Six
species, i.e., Erysiphe carpinicola (Hara) U. Braun & S.
Takam. [= Uncinula carpinicola (Hara) Hara], E. ellisii
(U. Braun) U. Braun & S. Takam. (= Microsphaera ellisii
U. Braun), E. pseudocarpinicola (Y. Nomura & Tanda) U.
Braun & S. Takam. (= U. pseudocarpinicola Y. Nomura &
Tanda), E. wuyiensis (Z.X. Chen & R.X. Gao) U. Braun &
S. Takam. [= U. wuyiensis (Zhi X. Chen & R.X. Gao) U.
Braun], Oidium carpini Foitzik, and Phyllactinia guttata
(Wallr.) Lév., have been reported to occur on Carpinus
(Braun 1987, 1995; Braun and Takamatsu 2000). Recently,
E. carpinicola was divided into three species, E. arcuata U.
Braun, Heluta & S. Takam. (host: C. betulus L. and C.
tschonoskii Maxim.; anamorph: O. carpini), E. carpinicola
(host: C. japonica Blume), and E. carpini-laxiflorae U.
Braun, Heluta & S. Takam. [host: C. laxiflora (Siebold &
Zucc.) Blume] based on morphological and molecular characteristics (Braun et al. 2006, 2007). Thus, a total of seven
species of the powdery mildew fungi occur on Carpinus
now.
In March 2003, we found powdery mildew-like ascomata
attached to fallen twigs of C. laxiflora in litter of the Mikamoyama Park, Sano-shi, Tochigi Prefecture, Japan (see Fig.
3), which appeared to be strange because powdery mildew
fungi are obligate biotrophs of plants. They usually infect
living host tissues, and do not have saprophytic life stages.
However, both morphological observations and a molecular phylogenetic analysis indicated that this fungus is a
member of the powdery mildews. In this study, we report
the morphological and molecular characteristics of this
fungus that is described as a new species of the powdery
mildew fungi with a unique morphology.
186
Materials and methods
Morphological studies
Specimens on C. laxiflora were examined by standard light
microscopy (Axio Imager; Carl Zeiss, Göttingen, Germany)
and differential-interference-contrast optical instruments
and devices.
The specimens examined are deposited at MUMH (Herbarium, Faculty of Bioresources, Mie University, Tsu,
Japan), TNS (Herbarium of the National Museum of Nature
and Science, Tsukuba, Japan), and HAL [Martin-LutherUniversity, Institute of Biology, Geobotany and Botanical
Garden, Herbarium, Halle (Saale), Germany].
Molecular phylogenetic study
MUMH 3694, a paratype specimen of Erysiphe fimbriata,
was used for molecular analysis. Isolation of whole-cell
DNA was performed using the chelex method (Walsh et al.
1991) as described in Hirata and Takamatsu (1996). The
5′-end of the 28S rDNA, including the domains D1 and D2,
and the internal transcribed spacer (ITS) region, including
the 5.8S rDNA, were amplified by polymerase chain reaction (PCR) and then sequenced using direct sequencing as
described in Takamatsu et al. (2006). DNA sequences
determined in this study were deposited in DDBJ (DNA
databank of Japan) under the accession numbers of
AB333839.
The sequences were initially aligned using the Clustal X
package (Thompson et al. 1997). The alignment was then
visually refined with a word processing program, using
colour-coded nucleotides. The alignments were deposited
in TreeBASE (http://www.treebase.org/) under the accession number of S1942. Phylogenetic trees were obtained
from the data using the maximum-parsimony (MP) method
in PAUP* 4.0 (Swofford 2001) and Bayesian analysis in
MRBAYES 3.1.1 (Huelsenbeck and Ronquist 2001). MP
analyses were performed with the heuristic search option
using the tree-bisection-reconstruction (TBR) algorithm
with 100 random sequence additions to find the global
optimum tree. All sites were treated as unordered and
unweighted, with gaps treated as missing data. The maximum
tree number was set as 104. The strength of the internal
branches of the resulting trees was tested with BS analyses
using 1000 replications with the stepwise addition option set
as simple (Felsenstein 1985). Bootstrap (BS) values higher
than 70% are provided.
For Bayesian phylogenetic analyses, the best-fit evolutionary model was determined for each data set by comparing different evolutionary models via the Akaike information
criterion (AIC) using PAUP* and MrModeltest 2.2
(Nylander 2004). MRBAYES was launched with random
starting trees for 106 generations and the Markov chains
were sampled every 100 generations, which resulted in 104
sampled trees. To ensure that the Markov chain did not
become trapped in local optima, we used the MCMCMC
algorithm, performing the estimation with four incrementally heated Markov chains. Of the resulting 104 trees, the
first 2000 (burn-in) were discarded. The remaining 8000
trees were summarized in a majority-rule consensus tree,
yielding the probabilities of each clade being monophyletic.
Bayesian posterior probability (PP) values higher than 0.95
are provided.
Results
Field observation
The occurrence of powdery mildew on C. laxiflora was
observed from June to December 2006 in the Mikamoyama
Park. No powdery mildew occurrence was found in early
June. White powdery mildew colonies were found on the
leaves of C. laxiflora in late September. The powdery
mildew mainly colonized veins and their surrounding areas
of the lower surface of leaves, and caused necrotic discolorations and distortions of the attacked host tissues. Colonies were not found on the upper leaf surface. Young,
immature chasmothecia were produced on the colonies. In
late October, mature chasmothecia were observed on the
colonies together with immature ones. Long (up to 4–5 mm
in length), fimbriate appendages rose from the upper half
of the chasmothecia, which were easily observable by naked
eye (see Fig. 4). By early December, almost all leaves had
fallen on the ground. Obvious white colonies with mature
chasmothecia were observed on the fallen leaves, but infections of twigs were not found during this period. Conidial
formation was also not observed.
Phylogenetic placement of Carpinus powdery mildew in
the Erysiphaceae: 28S rDNA analysis
A total of 99 sequences of 28S rDNA, including a sequence
from the new Carpinus powdery mildew, were used to
construct the phylogenetic tree of the Erysiphaceae. Byssoascus striatisporus (G.L. Barron & C. Booth) Arx (Myxotrichaceae) was used as an outgroup taxon, based on Mori
et al. (2000). The data set consisted of 831 characters, of
which 245 characters were variable and 189 characters were
phylogenetically informative for parsimony analysis. A
total of 104 equally MP trees with 995 steps (CI = 0.3789,
RI = 0.8014, RC = 0.3037) were constructed by the MP
analysis. To avoid the possibility that the heuristic search
became trapped in local optima, we repeated similar analysis by the parsimony ratchet method (Nixon 1999) using
PAUPRat (Sikes and Lewis 2001). The analysis also generated trees with 995 steps having topologies similar to the
MP trees. Thus, one of the 104 MP trees is shown in Fig. 1.
Most internal branches are supported in the strict consensus
of the 104 trees. Bayesian analysis generated similar tree
topology.
The previous phylogenetic analyses of the Erysiphaceae
demonstrated that five tribes and two basal genera are
included in the family (Mori et al. 2000; Braun and
Erysiphe quercicola ex Quercus AB197135
Erysiphe quercicola ex Quercus AB292691
Erysiphe quercicola ex Quercus AB292694
Erysiphe heraclei ex Daucus AB022391
28S rDNA
Erysiphe friesii ex Rhamnus AB022382
Erysiphe nomurae ex Symplocos MUMH 275
99 sequences
Erysiphe monascogera ex Styrax MUMH 3786
831 characters
Erysiphe alphitoides ex Quercus AB292699
Erysiphe alphitoides ex Quercus AB292707
995 steps
Erysiphe alphitoides ex Quercus AB237811
96
Erysiphe alphitoides ex Quercus AB257431
CI = 0.3789
Erysiphe sp. ex Quercus AB292712
Erysiphe sp. ex Quercus AB292711
RI = 0.8014
Erysiphe hypophylla ex Quercus AB292715
Erysiphe hypophylla ex Quercus AB292716
RC = 0.3037
Erysiphe abbreviata ex Quercus AB271785
84
Erysiphe hypogena ex Quercus AB292725
Erysiphe hypogena ex Quercus AB292727
82
Erysiphe hypogena ex Quercus AB292726
Erysiphe epigena ex Quercus AB292718
Erysiphe epigena ex Quercus AB292717
Tribe
Erysiphe epigena ex Quercus AB292720
1.0 Erysiphe epigena ex Quercus AB292722
Erysipheae
Erysiphe aquilegiae ex Cimicifuga AB022405
Erysiphe pulchra ex Swida AB022389
Erysiphe paeoniae ex Paeonia AB257438
93 Erysiphe carpinicola ex Carpinus AB252469
Erysiphe carpinicola ex Carpinus AB252467
100
Erysiphe carpinicola ex Carpinus AB252468
1.0
Erysiphe sp. ex Carpinus AB252464
Erysiphe
carpi-laxiflorae ex Carpinus AB252472
100
.99
.97
Erysiphe carpi-laxiflorae ex Carpinus AB252471
1.0 Erysiphe carpi-laxiflorae ex Carpinus AB252470
Brasiliomyces trina ex Quercus AB022350
Erysiphe simulans ex Rosa AB022395
Erysiphe gracilis ex Quercus AB022357
73
Typhulochaeta japonica ex Quercus AB022415
1.0
Erysiphe mori ex Morus AB022418
100 Erysiphe pseudocarpinicola ex Carpinus AB252465
1.0 Erysiphe pseudocarpinicola ex Carpinus AB252466
96
Erysiphe glycines ex Desmodium AB022397
MUMH3694 Carpinus laxiflora
Erysiphe arcuata ex Carpinus AB252463
Erysiphe arcuata ex Carpinus AB252474
Erysiphe arcuata ex Carpinus AB252473
Erysiphe adunca ex Salix AB022374
Erysiphe australiana ex Lagerstroemia AB022407
86
Golovinomyces orontii ex Veronica AB077651
Golovinomyces sordidus ex Plantago AB077657
Golovinomyces orontii ex Rubia AB077634
87
77
Golovinomyces orontii ex Nicotiana AB022412
Golovinomyces adenophorae ex Adenophora AB077632
Golovinomyces orontii ex Physalis AB077646
96
1.0 98 Golovinomyces cichoracearum ex Dahlia AB077628
Golovinomyces cichoracearum ex Aster AB077641
79
1.0
Golovinomyces cichoracearum ex Eupatorium AB022387
Tribe
1.0
Golovinomyces
cichoracearum ex Solidago AB077650
100
Arthrocladiella mougeotii ex Lycium AB329690
Golovinomyceteae
1.0
Arthrocladiella mougeotii ex Lycium AB022379
92 Neoerysiphe galeopsidis ex Lamium AB329674
Neoerysiphe galeopsidis ex Chelonopsis AB022369
83
Neoerysiphe galeopsidis ex Acanthus AB329670
100
1.0
Neoerysiphe galii ex Galium AB329681
1.0 Neoerysiphe galii ex Galium AB329682
75
Oidium maquii ex Aristotelia AB329686
98
Oidium aloysiae ex Aloysia AB329683
1.0
Neoerysiphe cumminsiana ex Cacalia AB329669
Oidium baccharidis ex Baccharis AB329684
100 Oidium phyllanthi ex Phyllanthus AB120755
Oidium subgen.
100
1.0 Oidium phyllanthi ex Phyllanthus AB120754
1.0
Microidium
Oidium phyllanthi ex Phyllanthus AB120758
94
Phyllactinia guttata ex Alnus AB080452
98
Phyllactinia
guttata
ex
Euptelea
AB080388
1.0
75
Phyllactinia guttata ex Morus AB080372
1.0 100
Phyllactinia guttata ex Diospyros AB022372
78
Tribe
Phyllactinia guttata ex Hamamelis AB080410
1.0
.97
99
Phyllactinia fraxini ex Fraxinus AB080451
100
Phyllactinieae
Phyllactinia fraxini ex Syringa AB080436
.95
1.0
Leveillula taurica ex Artemisia AB080470
98
Leveillula guilanensis ex Chondrilla AB080478
Leveillula saxaouli ex Haloxylon AB080469
1.0
Pleochaeta turbiana ex Platycyamus AB218773
.99
Pleochaeta shiraiana ex Celtis AB022403
99 Podosphaera longiseta ex Prunus AB022423
71
Podosphaera tridactyla ex Prunus AB022393
98 .99 1.0
Podosphaera xanthii ex Melothria AB022410
1.0 92 Podosphaera pannosa ex Rosa AB022347
Tribe
100
1.0 Podosphaera filipendulae ex Filipendula AB022384
Cystotheceae
100
Sawadaea polyfida ex Acer AB022364
1.0
82 1.0 Sawadaea tulasnei ex Acer AB022366
73
100
Cystotheca wrightii ex Quercus AB022355
.99
Cystotheca lanestris ex Quercus AB022353
1.0
Blumeria
graminis ex Hordeum AB022399
100
Tribe Blumerieae
Blumeria graminis ex Triticum AB022376
1.0
Blumeria
graminis
ex Bromus AB022362
100
Parauncinula septata ex Quercus AB022420
1.0
Parauncinula septata ex Quercus AB183533
Basal group
Caespitotheca forestalis ex Schinopsis AB193467
Byssoascus striatisporus U17912
73
5 changes
Fig. 1. Phylogenetic analysis of the divergent domains D1 and D2
sequences of the 28S rDNA for 99 sequences from the Erysiphaceae
covering all known tribes and one outgroup taxon. The tree is a phylogram of the maximum-likelihood tree among the 104 most parsimonious trees with 995 steps, which was obtained by a heuristic search
employing the random stepwise addition option of PAUP*. Gaps were
treated as missing data. Horizontal branch lengths are proportional to
the number of nucleotide substitutions that were inferred to have
occurred along a particular branch of the tree. Percentage bootstrap
support (1000 replications; >70%) and posterior probability (>0.95) are
shown on and under branches, respectively
188
Takamatsu 2000; Takamatsu et al. 2005a,b). The present
analysis supports the monophyly of four tribes, i.e., the
tribes Blumerieae, Erysipheae, Cystotheceae, and Phyllactinieae. The tribe Golovinomyceteae groups with Oidium
subgenus Microidium To-anun & S. Takam. (To-anun et al.
2005) to form a clade together. Caespitotheca S. Takam. &
U. Braun and Parauncinula S. Takam. & U. Braun take
basal positions within the Erysiphaceae. The fungus MUMH
3694 on C. laxiflora is placed in the genus Erysiphe DC. and
groups with E. pseudocarpinicola (= Uncinula pseudocarpinicola) from C. cordata Blume and E. glycines F.L. Tai
var. glycines from Desmodium podocarpum DC. subsp.
oxyphyllum (DC.) Ohashi, but this is supported by neither
BS nor PP values.
tive for parsimony analysis. A total of 106 equally MP trees
with 639 steps (CI = 0.5540, RI = 0.7209, RC = 0.3994) were
constructed by the MP analysis. A tree with the highest
likelihood score among the 106 MP trees is shown in Fig. 2.
Most internal branches are supported in the strict consensus
of the 106 trees. Bayesian analysis generated similar tree
topology.
The ITS sequence from MUMH3694 on C. laxiflora is
sister to all Erysiphe species excluding E. australiana
(McAlpine) U. Braun & S. Takam. (= U. australiana
McAlpine) and E. adunca (Wallr.) Fr. var. adunca [= U.
adunca (Wallr.) Lév. var. adunca], but this is supported by
neither BS nor PP values.
Phylogeny within Erysiphe: ITS analysis
Taxonomy
A total of 31 ITS sequences from Erysiphe, including a
sequence from the new Carpinus powdery mildew, were
used to construct the phylogenetic Erysiphe tree. The data
set consisted of 711 characters, of which 212 characters were
removed from the analysis because of ambiguous alignment. Of the remaining 499 characters, 225 characters were
variable, and 161 characters were phylogenetically informa-
Erysiphe fimbriata S. Takam., Masuya & Y. Nomura, sp.
nov.
Figs. 3–9
MycoBank no.: MB511033
Mycelio hypophyllo, in venis et prope venas habitanti,
hyalino, persistensi; discolorationem cum necrose et torsionem folii efficienti; chasmotheciis hypophyllis, dispersis vel
subgregariis, fusco-brunneis, 200–250 µm diametro; peridiis
Fig. 2. Phylogenetic analysis of
the nucleotide sequences of the
internal transcribed spacer (ITS)
region including 5.8S rDNA for
31 sequences from Erysiphe.
The tree is a phylogram of the
maximum-likelihood tree among
the 106 most parsimonious trees
with 639 steps, which was
obtained by a heuristic search
employing the random stepwise
addition option of PAUP*. Gaps
were treated as missing data.
This tree is also the maximumlikelihood tree among the 106
most parsimonious trees.
Horizontal branch lengths are
proportional to the number of
nucleotide substitutions that
were inferred to have occurred
along a particular branch of the
tree. Percentage bootstrap
support (1000 replications;
>70%) and posterior probability
(>0.95) are shown on and under
branches, respectively
Erysiphe arcuata ex Carpinus AB252463
Erysiphe arcuata ex Carpinus AB252473
Erysiphe arcuata ex Carpinus AB252474
100 Erysiphe pseudocarpinicola ex Carpinus AB252466
1.0 Erysiphe pseudocarpinicola ex Carpinus AB252465
Erysiphe glycines ex Desmodium AB015927
Erysiphe
heraclei ex Daucus AB000942
97
1.0
Erysiphe friesii ex Rhamnus AB000939
1.0
Erysiphe aquilegiae ex Cimicifuga AB000944
Erysiphe japonica ex Swida AB000941
Erysiphe carpinicola ex Carpinus AB252469
100
Erysiphe carpinicola ex Carpinus AB252467
1.0
100
Erysiphe carpinicola ex Carpinus AB252468
77 1.0
Erysiphe sp. ex Carpinus AB252464
100
Erysiphe togashiana ex Styrax AB091775
1.0
Erysiphe carpi-laxiflorae ex Carpinus AB252472
100
Erysiphe carpi-laxiflorae ex Carpinus AB252471
1.0
Erysiphe carpi-laxiflorae ex Carpinus AB252470
Typhulochaeta japonica ex Quercus AB022416
Brasiliomyces trina ex Quercus AB022351
.98
Erysiphe gracilis ex Quercus AB022358
Erysiphe wadae ex Fagus AB091776
Erysiphe simulans ex Rosa AB015926
92
Erysiphe flexuosa ex Aesculus AB091774
1.0
Erysiphe prunastri ex Prunus AB046983
Erysiphe mori ex Morus AB000946
Erysiphe necator ex Vitis AF073346
MUMH3694 Carpinus laxiflora
100
Erysiphe adunca ex Populus AF011324
1.0
Erysiphe adunca ex Salix D84383
Erysiphe australiana ex Lagerstroemia AB022408
10 changes
ITS
31 sequences
499 characters
639 steps
CI = 0.5540
RI = 0.7209
RC = 0.3994
100
1.0
189
Figs. 3–8. Erysiphe fimbriata. 3 Chasmothecia attaching on a twig of Carpinus laxiflora. 4 Long, fimbriate appendages growing upward from leaf
surface. 5 Chasmothecia with long appendages. 6 Anchoring hyphae arising from whole surface of young, immature chasmothecia. 7, 8 Asci and
ascospores. Bars 3–7 100 µm; 8 20 µm
ex cellulis angulatis vel irregularibus 20–25 × 15–17.5 µm
compositis; appendicibus ex parte superne chasmothecii
oriundis, surgentibus, (17–)20–50, simplicibus, mycelioidibus, rectis, interdum sinuosis vel geniculatis, interdum torulosis, raro ramosis, (3–)4–8(–12.5) µm latis, 4–5 mm longis,
septatis, crassitunicatis, hyalinis, raro ad basim pallide brunneis; hyphis anchoriformibus ex superficie omnino chasmothecii oriundis, intertextis; ascis numerosis, 22–38,
pedunculatis, 75–105 × 35–37.5 µm, ellipsoideis vel ovoideis;
ascosporis 6–8, late ellipsoideis vel ovoideis, hyalinis, 20–25
× 12.5–17.5 µm.
Typus: Japan, Tochigi Prefecture, Sano-shi, Mikamoyama Park, on fallen leaves of Carpinus laxiflora (Siebold
& Zucc.) Blume (Betulaceae), 4 Dec 2006, leg. S. Takamatsu (Holotypus, TNS-F-16170; isotypus, MUMH 4592
and HAL 2051 F).
Etymology: “fimbriata” refers to the long, fimbriate
appendages.
190
MUMH 4303; 22 Oct 2006, leg. S. Takamatsu, Y. Shiroya,
and M. Ito, MUMH 4416.
Discussion
Fig. 9. Erysiphe fimbriata. A Chasmothecium. B Peridial cells. C
Appendages. D Asci and ascospores. E Ascospores. Bars A 100 µm;
E 20 µm (for B–E)
Mycelia hypophyllous, colonizing veins and the surrounding leaf area, hyaline, persistent, causing necrotic discoloration and distortion of the attacked host tissue.
Chasmothecia hypophyllous, scattered to subgregarious,
blackish brown, 200–250 µm diameter, peridial cells angularirregular in outline, 20–25 × 15–17.5 µm. Appendages (17–)
20–50, arising from the upper part of chasmothecia, turning
upward, simple, mycelioid, straight, sometimes slightly
sinuous to geniculate, sometimes having small projections,
rarely branched, (3–)4–8(–12.5) µm wide, long (up to 4–
5 mm), aseptate, thick-walled, hyaline, rarely pale brown at
the base. Anchoring hyphae arise from whole surface of
chasmothecia, interwoven with vegetative hyphae. Asci
numerous, 22–38 per chasmothecium, stalked, 75–105 ×
35–37.5 µm, ellipsoid to ovoid, (6–)8-spored. Ascospores
broadly ellipsoid to ovoid, colorless, 20–25 × 12.5–17.5 µm.
Anamorph unkown.
Host range and distribution: On the leaves of Carpinus
laxiflora, Asia, Japan.
Additional materials examined: Japan, Tochigi Prefecture, Sano-shi, Mikamoyama Park, on Carpinus laxiflora, 19
Mar 2003, leg. H. Masuya, MUMH 3694; 4 Mar 2006, leg.
H. Masuya, MUMH 3813; 20 Sep 2006, leg. S. Takamatsu,
Of the seven powdery mildew species known to occur on
Carpinus, five belong to Erysiphe section Uncinula (Lév.)
U. Braun & Shishkoff, which has appendages with uncinatecircinate apex. Erysiphe ellisii belongs to the section Microsphaera (Lév.) U. Braun & Shishkoff, which has appendages
with apex dichotomously branched several times. Erysiphe
fimbriata, having simple, mycelioid appendages, belongs to
the section Erysiphe. Thus, Carpinus is affected by Erysiphe
species of all sections known. However, appendages of
species of the section Erysiphe usually arise from the lower
part of the chasmothecia and are interwoven with hyphae
on the surface of the leaves. In contrast, appendages of E.
fimbriata arise from the upper part of chasmothecia and
turn upward, which is quite different from the appendages
of most species of the section Erysiphe, except for some
species that are intermediate between the sections Erysiphe
and Microsphaera, as, for instance, Erysiphe tortilis (Wallr.)
Link: Fr. and E. trifolii Grev., and allied species in which
the appendages turn upward (toward one direction). The
phylogenetic analysis also supports that E. fimbriata belongs
to the lineage of section Uncinula, but not to section Erysiphe. In species of Erysiphe section Uncinula, the appendages mostly arise equatorially, but in Uncinula forestalis
Mena, now Caespitotheca forestalis (Mena) S. Takam. & U.
Braun, the terminal appendages turn toward one direction.
Moreover, the large size of chasmothecia and numerous
asci of E. fimbriata demonstrate that this species is a unique fungus among the genus Erysiphe. Phyllactinia guttata
(Wallr.: Fr.) Lév., one of the powdery mildews that infect
Carpinus, also has large chasmothecia (150–250 µm diameter). This fungus has needle-shaped appendages with a
bulbous base, which is quite different from the mycelioid
appendages of E. fimbriata. Therefore, E. fimbriata differs
from any other powdery mildew species known to occur on
Carpinus, and also differs from any other powdery mildew
species. We thus propose E. fimbriata as a new species of
the Erysiphaceae.
Molecular phylogenetic analyses support that E. fimbriata belongs to the genus Erysiphe, which is consistent with
the morphological characteristics of this fungus having
multi-asci chasmothecia and mycelioid appendages. Molecular analyses also demonstrate that the phylogenetic position of E. fimbriata is ambiguous within Erysiphe, i.e., there
is no Erysiphe species closely related to E. fimbriata. Erysiphe species most closely allied to E. fimbriata are E. paeoniae R.Y. Zheng & G.Q. Chen and E. arcuata in 28S
rDNA (97.5% similarity). ITS sequence similarities of E.
fimbriata are less than 90% to all other Erysiphe species
used in this study. Sequence similarity of E. fimbriata to
Erysiphe species parasitic on Carpinus are 95.3%–97.5% in
the 28S rDNA and 77.4%–87.3% in ITS regions, which
indicates that E. fimbriata is distantly related to all other
191
Erysiphe species reported on Carpinus. These data suggest
that E. fimbriata is a unique fungus genetically as well as
morphologically.
Erysiphe fimbriata was first found as chasmothecia
attached on twigs of C. laxiflora in litter. Our first assumption was that E. fimbriata colonized the twigs of C. laxiflora
and later formed chasmothecia there. To confirm this
assumption, we visited the Mikamoyama Park several times
from May to December in 2006. However, we failed to
observe the fungus colonizing on twigs during this period.
Therefore, the chasmothecia might be transferred from
leaves to twigs after maturation in some unknown way. The
evidence that the chasmothecia are attached to the twigs
upside down may support this assumption. The long appendages turning upward from the chasmothecia might have
some function in the dispersal process.
Erysiphe carpini-laxiflorae also occurs on C. laxiflora in
the Mikamoyama Park. Erysiphe carpini-laxiflorae usually
occurs on young seedlings of C. laxiflora, but not on the
adult tree, whereas E. fimbriata occurs on a large tree, about
15–20 m tall. Thus, the two powdery mildews that occur on
C. laxiflora seem to have different ecological niches.
However, additional detailed ecological studies of these
fungi are required.
Acknowledgments We thank Dr. Uwe Braun for critical reading of
the manuscript and Dr. Chiharu Nakashima for the Latin
description.
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