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Journal of Applied Research in Plant Protection 12 (3): 239–256 (2023)-Research Article
How to cite:
Artand S, Mehrabi-Koushki M, Tabein S, 2023. Identification of some fungal species in Chaetomiaceae and
Didymellaceae families associated with foliar and trunk diseases symptoms on forest trees in the Zagrosian region.
Journal of Applied Research in Plant Protection 12 (3): 239–256.
https://dx.doi.org/10.22034/arpp.2023.16635
ChaetomiaceaeDidymellaceae
mhdmhrb@scu.ac.ir
PDA
OAPDAITS-rDNA
tub2rpb2
NCBI
Chaetomium anastomosans
C. ascotrichoides
C. subglobosum
Didymella pomorum
D. prolaticolla
Paramicrosphaeropsis iranica
C. anastomosans
C. subglobosum
D. prolaticolla
C. anastomosans C. ascotrichoides C.
subglobosum
P. iranica
ChaetomiumDidymellaParamicrosphaeropsis
Identification of some fungal species in Chaetomiaceae and Didymellaceae families associated
with foliar and trunk diseases symptoms on forest trees in the Zagrosian region
Saeid Artand1, Mehdi Mehrabi-Koushki2 and Saeid Tabein3
1Department of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran. 2Department
of Plant Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran. 3Department of Plant
Protection, Faculty of Agriculture, Shahid Chamran University of Ahvaz, Ahvaz, Iran.
mhdmhrb@scu.ac.ir
Received: 4 July 2022 Revised: 18 December 2022 Accepted: 20 December 2022
Abstract
Mountains of Shahiyoon and Salandkooh (Dezful, Khuzestan), Kabirkooh (Abdanan, Ilam) and ZazoMahroo
(Aligoodarz, Lorestan) constitute small parts of the Zagrosian forests in Iran. During 2020-2022, 50 symptomatic samples
from forest trees including Acer sp., Amygdalus scoparia, Crataegus sp., Pistacia atlantica, Quercus brantii and Ziziphus
sp., showing leaf blight, leaf spot, fruit rot, decline and dieback, were collected. Totally, 153 fungal isolates were obtained
on potato–dextrose–agar medium (PDA), of which 17 were identified at species level based on combination of
morphological characteristics and sequence data of marker genes. Morphological characteristics and growth rate were
evaluated on oat -meal - agar (OA) and PDA. The ITS-rDNA region (in some isolates) and part of the tub2 (in all isolates)
and rpb2 (in some isolates) genes were amplified and sequenced. The obtained sequences were compared using BLASTn
search algorithm in NCBI database and their phylogenetic analyses were performed based on single or multiple genomic
regions. Accordingly, the isolates were identified as follow: Chaetomium anastomosans, C. ascotrichoides, C.
subglobosum, Didymella pomorum, D. prolaticolla, and Paramicrosphaeropsis iranica. Based on literature, this is the
first record of C. anastomosans, C. subglobosum and D. prolaticolla for the mycobiota of Iran. In addition, new hosts for
C. anastomosans (P. atlantica, Q. brantii and Crataegus sp.), C. ascotrichoides (Acer sp.), C. subglobosum (Q. brantii)
and P. iranica (A. scoparia and P. atlantica) are reported.
Keywords: Didymella, Chaetomium, Fungal Diversity, Molecular Phylogeny, Paramicrosphaeropsis.
240
J Appl Res Plant Prot
Sabernasab et al. 2019
Ghobad-Nejad
2016
Sabernasab et al. 2019
Acer sp. Amygdalus scoparia
SpachQuercus brantii Lindl.Pistacia
atlantica Desf.Daphne sp.Crataegus
sp.P. khinjuk StocksGhobad-Nejad
2016
Tubakia sp.(Lee et al.
2018)Inonotus krawtzewii
(Pilát) PilátGhobad-Nejad 2016Libertella quercina
Grove
Mehrabi & Hemati 2013 Cytospora
intermedia Sacc.
(Fotouhifar et al. 2010)
Neoscytalidium dimidiatum (Penz.) Crous &
SlippersObolarina persica Mirabolfathy, Ju, Hsieh &
RogersAlidadi et al. 2019
Biscogniauxia mediterranea (De Not.) Kuntze
Arzanlou et al. 2016
Ghasemi-Esfahlan et al.
2019
Wilsonomyces carpophilus (Lév.) Adask, J.M. Ogawa &
E.E. ButlerThyrostroma cornicola Crous & H.D. Shin
Collophorina paarla (Damm & Crous) Damm & Crous
B. mediterranea
Rostamian et al.
2016; Mirabdolahi-shamsi et al. 2019Eremothecium
coryli (Peglion) Kurtzman(Ershad
2022)
W. carpophilus
Ahmadpour et al. 2011
Colletotrichum gloeosporioides (Penz.)
Penz. & Sacc.Nieto-López et al. 2018
Neofusicoccum luteum (Pennycook
& Samuels) Crous, Slippers & A.J.L. Phillips
(Adesemoye et al. 2013)
Alternaria arborescens E.G.
Simmons Fusarium equiseti (Corda) Sacc.
Gymnosporangium globosum (Farl.) Farl. G.
Cooke & Peck clavipes
Monilinia johnsonii (Ellis & Everh.) Honey
(Salazar-Cerezo et al. 2020)
Acaulospora Gerdemann & Trappe
Glomus
Tulasne & C. Tulasne
Crataegus pontica
Mirzaei et al. 2014
Valsaria insitiva (Tode) Ces. & De Not.
Massaria vindobonensis Voglmayr & JaklitschM.
mediterranea Voglmayr & JaklitschStegonsporium
opalus (Voglmayr & Jaklitsch) Voglmayr & Jaklitsch
Taphrina inositophila (Á. Fonseca, J. Inácio & M.G.
Rodrigues) Yurkov & BuzzinErysiphe paradoxa
(Simonyan) U. Braun & S. TakamSawadaea bicornis
(Wallr.) Homma
S. tulasnei (Fuckel) Homma
Voglmayr & Jaklitsch. 2011, 2014; Jiang et al.
2018 Alternaria
alternata (Fries) KeisslerBotryosphaeria obtusa
(Schwein.) ShoemakerVerticillium dahlia Klebahn
Morgan et al. 1992; Swart et al. 1995;
Ozkilinc et al. 2017
J Appl Res Plant Prot
ChaetomiaceaeDidymellaceae
-Potato Dextrose Agar
PDA
Alexopoulos & Beneke 1962; Paripour et al. 2023
–Oatmeal AgarOAPDA
OA
±
DNA
PDA
DNA Raeder & Broda (1985
Ahmadpour et al. 2017a
18S ITS15.8S ITS2
28S rDNA ITS-
rDNA
Didymellaceae
ITS1White et al. 1990NL4
O’Donnell 1993
T1/Btub4Rd
Chaetomium KunzeBtub2Fd/T2
DidymellaParamicrosphaeropsis
O’Donnell & Cigelnik 1997; Groenewald et al.
2013RNA
II Paramicrosphaeropsis L.W. Hou,
L. Cai & Crous RPB2-5F2
fRPB2-
7cR
Liu et al. 1999; Sung et al. 2007
Polymerase
chain reactionPCR
ITS
tub2 rpb2
Safi et al. 2020,
2021; Aghyl et al. 2022; Ahmadpour et al. 2022b
PCR
Geneall
biotechnology
BioEdit ver 4.0.6.2Hall 1999
DNA Baser ver3.5.0www.DnaBaser.com
242
J Appl Res Plant Prot
ML, Maximum liklihood
MP, Maximum parsimony BI,
Bayesian inference
ChaetomiumAsgari & Zare 2011; Wang et al. 2016a,
b; Aghyl et al. 2021 Didymella
ParamicrosphaeropsisChen et al. 2015, 2017; Hou et
al. 2020; Ahmadpour et al. 2022a
NCBI .
RAxMLGUI 2.0Edler et al. 2021
MEGATamura et al. 2013
MrBayes v.3.2.6Ronquist et al.
2012
jModelTest 2Darriba et
al. 2012
Bootstrapping, BS
Posterior probability, BPP
BS
BPP
Chaetomiaceae
Didymellaceae
Chaetomium anastomosans M. Raza & L. CaiC.
ascotrichoides CalvielloC. subglobosum Wang et al.
Didymella pomorum (Thum) Chen & L. CaiD.
prolaticolla L.W. Hou, L. Cai & Crous
Paramicrosphaeropsis iranica Ahmadpour et al.
NCBI
Table 1. Data of the isolates under study and their accession numbers in NCBI GenBank.
NCBIChaetomium
tub2rpb2
Species name
Isolate numbers
Isolation source
origin
accession numbers in NCBI
Chaetomium anastomosans
SCUA-Ar-B9B
Quercus brantii
Zaz and Mahroo
-
ON383186
-
C. anastomosans
SCUA-Ar-SK1C
Pistacia atlantica
Dezful-Sardasht
-
ON383187
-
C. anastomosans
SCUA-Ar-SK12A
Pistacia atlantica
Dezful-Sardasht
-
ON383188
-
C. anastomosans
SCUA-Ar-Z8A
Crataegus sp.
Zaz and Mahroo
-
ON383189
-
C. anastomosans
SCUA-Ar-Z8B
Crataegus sp.
Zaz and Mahroo
-
ON383190
-
C. subglobosum
SCUA-Ar-Kb6B2
Quercus brantii
Abdanan-Kaberkooh
-
ON383192
-
C. ascotrichoides
SCUA-Ar-KK4A
Acer sp.
Abdanan-Kaberkooh
-
ON383191
-
Didymella pomorum
SCUA-Ar-S4B
Ziziphus sp.
Dezful-Sardasht
ON847318
ON383195
-
D. prolaticolla
SCUA-Ar-S9A
Unknown plant
Dezful-Sardasht
ON847319
ON383196
-
Paramicrosphaeropsis iranica
SCUA-Ar-K11A
Pistacia atlantica
Zaz and Mahroo
-
MZ747189
-
P. iranica
SCUA-Ar-KS6-7
Quercus brantii
Dezful-Shahiyoon
-
MZ747191
-
P. iranica
SCUA-Ar-K12C
Pistacia atlantica
Zaz and Mahroo
MZ746104
MZ747185
MZ747198
P. iranica
SCUA-Ar-B7DA
Quercus brantii
Zaz and Mahroo
-
MZ747188
-
P. iranica
SCUA-Ar-SB5B
Quercus brantii
Dezful-Sardasht
-
MZ747192
-
P. iranica
SCUA-Ar-KB1A
Amygdalus scoparia
Abdanan-Kaberkooh
-
MZ747190
-
P. iranica
SCUA-Ar-B2F2
Quercus brantii
Zaz and Mahroo
-
MZ747187
-
P. iranica
SCUA-Ar-B2A1
Quercus brantii
Zaz and Mahroo
-
MZ747186
-
J Appl Res Plant Prot
Didymella Sacc.Paramicrosphaeropsis
ITStub2rpb2
Chaetomiumtub2rpb2
≥(MLMP
≥BPP
Amesia
atrobrunnea
T
Figure 1. Phylogenetic tree constructed for Chatomium isolates based on combination of tub2 and rpb2 sequences. The
isolates in this study are indicated with red-color filled circles. Bootstrap values obtained in maximum likelihood (ML)
and maximum parsimony (MP) analyses ≥50% and Bayesian posterior probability values (BPP) ≥0.95 are shown at the
nodes, respectively. The tree was rooted with Amesia atrobrunnea. Letter T indicates the type strain.
244
J Appl Res Plant Prot
DidymellaITStub2rpb2
≥(MLMP≥
BPP
Neoascochyta argentina
T
Figure 2. Phylogenetic tree constructed for Didymella isolates based onITS, tub2 and rpb2 sequences. The isolates in
this study are indicated with red-color filled circles. Bootstrap values obtained in maximum likelihood (ML) and
maximum parsimony (MP) analyses ≥50% and Bayesian posterior probability values (BPP) ≥0.95 are shown at the nodes,
respectively. The tree was rooted with Neoascochyta argentina. Letter T indicates the type strain.
J Appl Res Plant Prot
ParamicrosphaeropsisITStub2rpb2
≥(MLMP
≥BPP
Ascochyta
rabiei
T
Figure 3. Phylogenetic tree constructed for Paramicrosphaeropsisisolates based on ITS, tub2 and rpb2 sequences. The
isolates in this study are indicated with red-color filled circles. Bootstrap values obtained in maximum likelihood (ML)
and maximum parsimony (MP) analyses ≥50% and Bayesian posterior probability values (BPP) ≥0.95 are shown at the
nodes, respectively. The tree was rooted with Ascochyta rabiei. Letter T indicates the type strain.
Chaetomium anastomosans M. Raza & L. Cai,
Fungal Diversity 99: 78 (2019)
OA
±
SCUA-Ar-SK1C
SCUA-Ar-SK12ASCUA-Ar-
B98SCUA-Ar-Z8A
SCUA-Ar-Z8B
tub2
C. anastomosans
CGMCC3.19350
tub2rpb2
246
J Appl Res Plant Prot
LC 13503
CGMCC 3.19350
MLBP: 86%, MPBP: 94%, BPP: 0.97
CGMCC 3.19350
Raza et al. 2019
Raza et al. 2019
Walther et al. 2021
C.
anastomosans
Chaetomium anastomosans
SCUA-Ar-SK1CA-CD-E
OAFGFG
Figure 4. Chaetomium anastomosans (SCUA-Ar-SK1C): A-C. Substrates (Pistacia atlantica, Quercus brantii
and Crataegus sp.), D-E Colony on OA after 8 days from above and below, F Ascocarps, G. Ascospores (Scale bars: F
= 500 µm, G = 20 µm).
Chaetomium ascotrichoides Calviello, Bernardino
Rivadavia 3: 372 (1972)
tub2
CBS 113.83
tub2rpb2
CGMCC 3.11378CBS
110.83
MLBP: 97%, MPBP: 100%, BPP: 1.0
CBS 113.83
Wang et al.
2016b
J Appl Res Plant Prot
SCUA-Ar-KK4A
C. ascotrichoides
Wang et al. 2016b
Larki et al. 2019
C. ascotrichoides
Chaetomium ascotrichoides
SCUA-Ar-KK4A
AB-C
OAD-FG)DEFG
(
Figure 5. Chaetomium ascotrichoides (SCUA-Ar-KK4A): A Host (Acer sp.), B-C. Colony on OA after 8 days from
above and below, D-F. Ascomata, G. Ascospores (Scale bars: D = 500 µm, E = 200 µm, F = 105 µm, G = 20 µm).
Chaetomium subglobosum Wang et al, Perssonia 36: 83-133 (2016)
OA±
SCUA-
Ar-Kb6B2 .
248
J Appl Res Plant Prot
Chaetomium subglobosum
SCUA-Ar-Kb6B2
A-BC-D
OAE-GHIE-FGH-I
Figure 6. Chaetomium subglobosum (SCUA-Ar-Kb6B2): A-B. Host (Quercus brantii), C-D. Colony on OA after 8 days
from above and below, E-G. Ascomata, H. Ascospores, I. Ascus(Scale bars: E-F = 500 µm, G = 200 µm, H-I = 20 µm)
tub2
C. subglobosum MCUL
18694
tub2rpb2
MCUL 18694
MLBP: 100%, MPBP: 97%, BPP: 1.0
MCUL
18694
Wang et al. 2016b
C. subglobosum
Didymella pomorum (Thum) Chen & L. Cai, Studies
in Mycology 82: 179 (2015)
Boerema et al. (2004)
ITS
tub2D. pomorum CBS 286.76
ITStub2
rpb2
CBS 286.76
MLBP: 100%,
MPBP: 100%
CBS 539.66Boerema et al. 2004
SCUA-Ar-S4B
D. pomorum
Phoma Pomorum
J Appl Res Plant Prot
Thüm.Boerema et al. 2004
DidymellaChen et al. 2015
Chen et al. 2015
Ershad 2022
D. pomorum
Malus spp.Rosa spp.
Havenga et al. 2019; Ilyukhin 2022
Didymella pomorum
SCUA-Ar-S4B
A-BC-DOA
E-FGEFG
Figure 7. Didymella pomorum (SCUA-Ar-S4B): A-B Host (Ziziphus sp.), C-D. Colony on OA after 8 days from above
and below, E-F. Pycnidia, G. Conidia (Scale bars: E = 200 µm, F = 50 µm, G = 20 µm).
Didymella prolaticolla L.W. Hou, L. Cai & Crous,
Studies in Mycology 82: 357 (2020)
OA±
SCUA-Ar-S9A
250
J Appl Res Plant Prot
ITS
tub2 D.
prolaticolla CBS 126182
ITS
tub2
rpb2
CBS 126182
MLBP: 100%, MPBP: 87%, BPP: 0.99
Hou et al. 2020
Hou et al. 2020
D. prolaticolla
Didymella prolaticolla
SCUA-Ar-S9AAB-COA
D-FGHDEF
G-H
Figure 8. Didymella prolaticolla (SCUA-Ar-S9A): A. Host (Daphne sp.), B-C. Colony on OA after 8days from above
and below, D-F. Pycnidia, G. Conidiogenous cells, H. Conidia. Scale bars: D = 500 µm, E = 200 µm, F = 105 µm, G-H
= 20 µm.
Paramicrosphaeropsis iranica Ahmadpour et al,
Mycological Progress 21:28 (2022)
ITS
tub2rpb2
IRAN 2929C
MLBP: 96%, MPBP: 85%
IRAN 2929C
SCUA-Ar-K12C
SCUA-Ar-K11A
J Appl Res Plant Prot
SCUA-Ar-B2A1SCUA-Ar-B2F2SCUA-Ar-
B7DASCUA-Ar-KS6-7
SCUA-Ar-Kb1A
SCUA-Ar-SB5B
Paramicrosphaeropsis iranica
Ahmadpour et al.
2022a
Paramicrosphaeropsis
Quercus ilex L.
Crataegus sp.Nerium
oleander L.
Pistacia atlantica
P. khinjuk
Quercus
brantii
Ziziphus sp.
Amygdalus
scopariaCrataegus sp.
Q. brantii
Hou et al. 2020; Ahmadpour et al. 2022a;
Artand et al. 2022
Paramicrosphaeropsis iranica
SCUA-Ar-K12CA-CD-G
OAD-EPDAF-GH-IJ HI
J
Figure 9. Paramicrosphaeropsis iranica (SCUA-Ar-K12C): A-C. Hosts (Amgydalus
scoparia, Quercus brantii and
Pistacia atlantica), D-G. Colony on OA (D-E)and PDA (F-G) after 8-days from above and below, H-I. Pycnidia, J.
Conidia. Scale bars: H = 500 µm, I = 200 µm, J = 20 µm
C. anastomosans
C.
ascotrichoides
C. subglobosumDidymella pomorum
Dprolaticolla
P. iranica
Chaetomium
Kamat et al.
2020
Fatima et al. 2016
Chaetomium
Soytong et al. 2001
C. ascotrichoides CavielloC.
circinatum ChiversC. crispatum (Fuckel) FuckelC.
cruentatum SörgelC. elatum KunzeC. globisporum
252
J Appl Res Plant Prot
LodhaC. globosum KunzeC. grande Asgari & Zare
C. hispanicum Guarro & ArxC. interruptum Asgari &
ZareC. iranicum M. Mehrabi-Koushki, Aghyl & M.
EsfandC. madrasense NatarajanC. megalocarpum
BainierC. osmaniae P. Rama Rao & Ram ReddyC.
rectangulare Asgari & ZareC. spiralotrichum Lodha
C. undulatulum Asgari & ZareAghyl
et al. 2021; Ershad 2022 Chaetomium
Chaetomium
Piontelli 2006
Di Pietro et al. 1992
Didymella
D. exigua (Niessl) Sacc.
Holm 1975; Corlett 1981
Mycosphaerellaceae
Pleosporaceae Phaeosphaeriaceae
Venturiaceae
Pleosporales
DidymellaceaePleosporales
DothideomycetesDidymella
Aveskamp et al. 2008, 2010
D. acetosellae (A.L. Sm. &
Ramsb.) Qian Chen & L. CaiD. azollae E. Shams, F.
Dehghanizadeh, A. Pordel & M. Javan-NikkhahD.
bellidis (Neerg.) Qian Chen & L. CaiD. cousiniae Petr
D. cylindrica S.A. Ahmadp., M. Mehrabi-Koushki,
Farokhinejad & AsgariD. glomerata (Corda) Qian
Chen & L. CaiD. iranica PetrD. microchlamydospora
(Aveskamp & Verkley) Qian Chen & L. CaiD.
pinodella (L.K. Jones) Qian Chen & L. CaiD. pisi
Chilvers, J.D. Rogers & PeeverD. tanaceti (R.G.
Shivas, S.J. Pethybr. & S.J. Jones) T.L. Pearce, J.B.
Scott, Crous, S.J. Pethybr. & F.S. Hay
Ahmadpour et al. 2017b, 2022a; Ershad 2022
Microsphaeropsis
Didymellaceae
Microsphaeropsis
Montagnulaceae
MicrosphaeropsidaceaeChen et al. 2015
MicrosphaeropsisDidymellaceae
Neomicrosphaeropsis Thambug., Camporesi & K.D.
HydeParamicrosphaeropsisHou et al. 2020
Paramicrosphaeropsis
Microsphaeropsis Sousa da Câmara,
Oliveira & Luz Didymellaceae
Hou et al. 2020
Paramicrosphaeropsis
P. amygdalus M. Mehrabi-Koushki, S. Artand, K.D.
Hyde & Jayaward.P. ellipsoidea L.W. Hou, L. Cai &
CrousP. iranicaP. pistacicola M. Mehrabi-Koushki,
S. Artand, K.D. Hyde & JayawardP. salandica M.
Mehrabi-Koushki, S. Artand, K.D. Hyde & Jayaward
P. zagrosensis M. Mehrabi-Koushki, S. Artand, K.D.
Hyde & JayawardHou et al. 2020; Ahmadpour et
al. 2022a; Artand et al. 2022P.
ellipsoidea
Hou et al. 2020
J Appl Res Plant Prot
SCU.AP1400.294
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