A preliminary study on the genus Fusicladium s. l. in Iran

Abstract

During 2011, twigs, leaves and fruits of symptomatic hosts containing Fusicladium species from Guilan, Mazandaran, Qazvin and Ardabil provinces were sampled and examined. Five species including F. carpophilum, F. fraxini, F. oleagineum, F. pomi and F. pyrorum were identified based on morphological data. Of these, F. carpophilum and F. fraxini are identified as new records for the mycobiota of Iran. Fraxinus sp., Prunus persica var. nectarina, Pyracantha sp., red apple cultivar of Malus pumila and Khoj (local variety of Pyrus communis in Guilan province) are identified as new hosts for the genus Fusicladium in Iran. Cultures of F. fraxini, F. pomi and F. pyrorum are deposited at fungal culture collection of Iranian Research Institute of Plant Protection. A brief description and illustration and a key to Fusicladium species reported from Iran are provided.

Full text

Mycologia Iranica 1(1): 27 – 33, 2014
Submitted 26 June 2013, accepted for publication 20 November 2013

Corresponding Author. E-mail: khodaparast@guilan.ac.ir
© 2014, Published by the Iranian Mycological Society
http://mi.iranjournals.ir
Original Article
A preliminary study on the genus Fusicladium s. l. in Iran
S. A. Hashemi
S. A. Khodaparast

S. A. Elahinia
Department of Plant Protection, Faculty of
Agriculture, University of Guilan, Rasht, Iran
R. Zare
Department of Botany, Iranian Research Institute
of Plant Protection (IRIPP), Tehran, Iran
M. Mousakhah
Clinic of Plant Protection, Astaneh Ashrafieh,
Guilan, Iran
Abstract: During 2011, twigs, leaves and fruits of
symptomatic hosts containing Fusicladium species
from Guilan, Mazandaran, Qazvin and Ardabil
provinces were sampled and examined. Five species
including F. carpophilum, F. fraxini, F. oleagineum,
F. pomi and F. pyrorum were identified based on
morphological data. Of these, F. carpophilum and
F. fraxini are identified as new records for the
mycobiota of Iran. Fraxinus sp., Prunus persica var.
nectarina, Pyracantha sp., red apple cultivar of Malus
pumila and Khoj (local variety of Pyrus communis in
Guilan province) are identified as new hosts for the
genus Fusicladium in Iran. Cultures of F. fraxini, F. pomi
and F. pyrorum are deposited at fungal culture
collection of Iranian Research Institute of Plant
Protection. A brief description and illustration and a
key to Fusicladium species reported from Iran are
provided.
Key words: Fusicladium carpophilum, Fusicladium
fraxini, scab, Spilocaea, Venturia
INTRODUCTION
Fusicladium Bonord. was established to accommo-
date Venturia Sacc. (Ascomycota, Pleosporales,
Venturiaceae E. Müll. & Arx ex M. E. Barr)
anamorphs with sympodial (denticulate) or percurrent
(annellate) conidiogenous cells. Three genera were
later distinguished based on the proliferation mode:
Fusicladium with sympodial proliferation, Pollaccia E.
Bald. & Cif. with monoblastic, determinate to percur-
rent conidiogenous cells (with few rather inconspicu-
ous annellations) and Spilocaea Fr. with percurrent
proliferation and numerous, conspicuous annellations.
Braun et al. (2002) suggested that the separation of
these anamorphic genera is not tenable since the
conidiogenesis and structure of the conidiogenous loci
are uniform. Molecular examinations clearly showed
that Venturia is a monophyletic clade that can not be
separated into sub-clades relevant to these anamorphic
genera (Beck et al. 2005). Therefore, it is proposed that
these genera to be merged in one anamorphic genus.
Hence, the name Fusicladium was conserved against
other names (Braun 2005). In this new concept,
Fusicladium s. l. includes Fusicladium, Spilocaea,
Pollaccia, Cycloconium and Pseudocladosporium
(Braun et al. 2002, Braun 2005, Crous et al. 2007).
They are phytopathologically relevant pathogens,
causing leaf spot, necrosis, scab diseases as well as leaf
and fruit deformations of at least 52 angiospermous
plant genera. These fungi are host specific, mostly
confined to a single host genus or allied host genera in
a single family, e.g. Fusicladium pomi attacks
members of Rosaceae (Schubert et al. 2003). A world
monograph of the genus Fusicladium s. l. Bonord. em.
Schubert, Ritschel et U. Braun was published in 2003
and 57 taxa belonging to the anamorphic genus were
described (Schubert et al. 2003). Some genera such as
Cladosporium are taxonomically related to
Fusicladium. The structure of the conidiogenous loci
and conidial hila proved to be the basic feature for a
natural classification (David 1997), which could be
confirmed by molecular examinations (Braun et al.
2003). True species of Cladosporium are characterized
by having pigmented conidiophores with coronate
conidiogenous loci, i.e. composed of a central convex
dome surrounded by a raised periclinal rim, and
pigmented conidia formed in acropetal chains (David
1997, Braun et al. 2003). Therefore, in a series of
taxonomic studies of the genus Cladosporium s. l.
several new species and new combinations are
proposed in the genus Fusicladium (Schubert 2005,
Schubert & Braun 2005a, b, Schubert & Braun 2007,
Braun et. al. 2008, Crous et al. 2007, 2010a, b).
Although several species of the genus Fusicladium
including F. pomi, F. pyrorum, F. oleagineum,
F. eriobotryae, F. heterosporum, F. crataegi, F.
dendritichum (= F. pomi), F. virescens (= F. pyrorum)
and F. cerasiare so far reported from Iran (Hedjaroude
& Abbasi 2000, Mahdian 2006, Ershad 2009, Askari &
Ghaderi 2010, Sanei & Razavi 2011), but most of them
are not adequately described based on Iranian
materials. This paper presents a primary finding on the
genus Fusicladium species and their hosts in Iran.

28 Mycologia Iranica - Vol. 1, 2014
MATERIALS AND METHODS
Plant parts (twigs, leaves, fruits) showing
Fusicladium spp. symptoms were collected from
Guilan, Mazandaran, Qazvin and Ardabil provinces of
Iran. Moreover, all Fusicladium specimens preserved
at fungal collection of the University of Guilan were
reexamined. VANOX AHBS3 Olympus light
microscope was used to examine fungal structures, and
a BH2 Olympus light microscope equipped with a
SONY DSCHX1 digital camera was used for
photography. Structures were mounted in lactic acid,
and 30 and 10 measurements (× 1000 magnification)
determined for conidia and conidiophores respectively,
with the extremes of spore measurements given in
parentheses. The identification of fungal species was
determined according to Schubert et al. (2003). Host
plants were identified according to Mozaffarian
(1998). All collected specimens were deposited in the
fungal collection of the Department of Plant
Protection, Faculty of Agriculture, University of
Guilan, Iran.
RESULTS AND DISCUSSION
In our study, five species including F. carpophilum,
F. fraxini, F. pomi, F. pyrorum and F. oleagineum
were identified from newly collected plant materials in
four provinces of Iran (Guilan, Qazvin, Ardabil and
Mazandaran). F. carpophilum and F. fraxini are
reported for the first time from Iran. Two species; F.
cerasi and F. crataegi, which have already been
reported from Iran (Schubert et al. 2003, Khabiri 1952,
Esfandiari 1948a, Scharif & Ershad 1966) were not
found in this study. A brief description of identified
taxa and a key to Fusicladium species reported from
Iran are presented.
Fusicladium carpophilum (Thüm.) Oudem., Verh.
Kon. Ned. Akad. Wetensch., Afd. Natuurk.: 388
(1900) Fig. 1A, 2A
On fruits and twigs, patches on the fruits
superficial, circular to oval, small, greenish brown,
conidiophores solitary, erect, somewhat flexuous or
straight, unbranched, 29–105 × 4–6.2 μm, septate,
medium brown, smooth, sometimes swollen at the
base, walls somewhat thickened. Conidiogenous cells
integrated, terminal, 19–26 μm long, with 3–7
denticulate loci, 1–2 μm wide, unthickened, not
darkened. Conidia catenate, cylindrical to fusiform,
straight, 12.5–20(–22) × 4–5 μm, aseptate, pale
olivaceous, smooth, hila truncate, 1–1.5(–2) μm wide,
unthickened, somewhat darkened.
Specimens examined: IRAN, Tajan Gokeh village,
Astaneh Ashrafieh, Guilan Province, on fruits of
Prunus persica var. nectarine, 12 Jun. 2012, M.
Mousakhah, (1029).
Fig. 1. Scab disease symptoms caused by Fusicladium s. l. species on leaves and fruits of few hosts in natural condition on:
(A) Prunus persica var. nectarine, (B) Fraxinus sp., (C) and (D) Malus pumila, (E) Pyracantha coccinea, (F) Eriobotrya
japonica, (G) Pyrus communis, (H) Khoj (local variety of Pyrus communis in Guilan Province, Iran), and (I) Olea europaea.

HASHEMI ET AL.: A preliminary study on the genus Fusicladium s. l. in Iran 29
Fig. 2. Conidia and conidiophores of Fusicladium carpophilum (A) and F. fraxini (B). Scale bars = 10 μm.
Notes: According to Schubert et al. (2003) four
species, F. pomi, F. obducens, F. cerasi and
F. carpophilum, have been reported on Prunus species.
In F. obducens and F. cerasi the conidia often are not
catenate. The latter three species have sympodial
conidiogenesis. F. carpophilum differs from F. cerasi,
a previously reported species from Iran, by having
catenate conidia, longer conidiophores (25–100 μm)
than those of F. cerasi [(10–)20–40(–60) μm] and its
broad host range (rarely occurring on Prunus cerasus)
compared with F. cerasi with narrow host range,
mostly occurring on Prunus cerasus. Fusicladium
carpophilum is a new record for the mycobiota of Iran.
Fusicladium fraxini Aderh.,Nova Hedwigia 36: 74, 83
(1897) Fig. 1B, 2B
Leaf spots amphigenous, circular to irregular, about
5 mm wide, olivaceous-brown on the upper leaf
surface, conidiophores mostly erect, straight to
geniculate, flexuous, often unbranched, sometimes
branched, (18–)26–45(–50)  4–7 μm, 0(–1) septate,
pale olivaceous to medium brown, smooth, often
conspicuously lobed at the base. Conidiogenous cells
integrated, terminal or conidiophores usually reduced
to conidiogenous cells, proliferation sympodial with 5–
10(–14) loci, loci sub-denticulate, 1(–2) μm wide,
minutely thickened. Conidia solitary, fusiform to
obclavate, straight, (12–)14–17(–18)  (4–)5–6 μm,
1(–2)-septate, not or only slightly constricted at the
septa, septa somewhat in the lower half, hila 1(–2) μm
wide, unthickened.
Specimens examined: IRAN, Faculty of
Agricultural Science, University of Guilan, Rasht, on
leaves of Fraxinus sp., 6 Jul. 2011, S. A. Hashemi,
(1026), and IRAN, Ghalehroodkhan, Fuman, Guilan
Province, on leaves of Fraxinus sp., 4 Aug. 2005, S. A.
Khodaparast, (1025).
Notes: So far two species have been described on
Fraxinus; Fusicladium fraxini and F. nebulosum that
can be separated in conidiophore size, proliferation,
colour, etc. (Schubert et al. 2003). F. fraxini is a new
record for mycobiota of Iran. Conidiophores of Iranian
isolates of F. fraxini are conspicuously lobed at the
base. This character was not mentioned in Schubert et
al. (2003). Further studies on these isolates are in
progress to evaluate this character value in terms of
taxonomy.
Fusicladium pomi (Fr.) Lind, Danish fungi: 521
(1913) Fig. 1C-F, 3A-C
On living leaves and fruits, spots amphigenous,
sub-circular to irregular, up to 10 mm wide, pale
olivaceous-brown, becoming greyish black, on leaves
sometimes surrounded by a yellowish halo, often
around the main midrib, occasionally covering large
leaf segments. On fruits forming small, circular to
irregular spots, sub-cuticular, margin indefinite,
olivaceous-brown.
Conidiophores mostly in loose to dense fascicles,
erumpent through the cuticle, erect, straight to slightly
flexuous, cylindrical to ampulliform, unbranched, 14–
22  7–10 μm, aseptate (on yellow apple), 19–31 × 7
μm, aseptate (on red apple), 10–25  5–7 μm, aseptate
(on Eriobotrya japonica) and (14–)24–58  5–6 μm,
(0–)1 septate (on Pyracantha sp.), walls thickened,
often swollen at the base.
Conidiogenous cells integrated, terminal, with a
single locus, proliferation percurrent, with conspicuous
annellations, loci truncate, 4–5μm wide, unthickened,
not darkened. Conidia solitary, shape variable, ovoid to
obpyriform or obclavate, straight, (12–)16–25 (–26) ×
7–9 μm, 0(–1) septate (on yellow apple), (13–)17–24
(–26) × 7 μm, 0(–1) septate (on red apple), (11–)13–
18 7–9 μm, aseptate (on Eriobotrya japonica) and
12–18  7–10 μm, 0(–1) septate (on Pyracantha sp.),
walls somewhat thickened, narrowly pointed or
broadly rounded at the apex, truncate at the base.
Hilum (3–)4–5(–6) μm (on yellow apple), (3.5–)4–5(–
6) μm (on red apple), 4–5(–6) μm (on Eriobotrya
japonica) and 2.5–5 μm (on Pyracantha sp.) wide,
truncate, unthickened to occasionally very slightly
thickened, not darkened.

30 Mycologia Iranica - Vol. 1, 2014
Fig. 3. Conidia and conidiophores of Fusicladium pomi on Malus pumila (A), on Pyracantha sp. (B) and on Eriobotrya
japonica (C), F. pyrorum (D) and F. oleagineum (E). Scale bars = 10 μm.
Specimens examined: On fruit of Malus pumila:
IRAN, Khalkhal, Ardabil Province, 8 Jul. 2011, R.
Ebrahimi, (1010); IRAN, Faculty of Agriculture,
University of Guilan, Rasht, S. A. Khodaparast,
(1011); IRAN, Eghbalieh, Qazvin, 17 Jul. 2011, S. A.
Hashemi, (1013); IRAN, Eghbalieh,Takestan, Qazvin,
17 Jul. 2011, S. A. Hashemi, (1012); IRAN, fruit shop,
Rasht, Guilan Province, 23 Jul. 2011, S. A. Hashemi,
(1014); on fruit of red apple: IRAN, fruit shop, Rasht,
Guilan Province, 14 Dec. 2011, S. A. Hashemi, (1030);
on fruits of Pyracantha sp.: IRAN, Faculty of
Agriculture, University of Guilan, Rasht, 17 Oct. 2011,
S.A.Hashemi, (1027); IRAN, Faculty of Agriculture,
University of Guilan, Rasht, 31 Oct. 2011, S. A.
Hashemi, (1028); on leaves and fruits of Eriobotrya
japonica: IRAN, Some-eh-sara, Guilan Province, 22
May 2007, S. A. Khodaparast, (1021); IRAN, Sarvelat,
Guilan Province, 29 May 2009, S. A. Khodaparast,
(1022); IRAN, Sost, Leisar, Hashtpar, Guilan
Province, 25 Oct. 2011, S. A. Hashemi, (1023); IRAN,
Ramsar, Mazandaran Province, 30 Dec. 2011, S.A.
Elahinia, (1024).
Notes: Three Fusicladium species from Malus;
F. pomi, F. pyrorum and F. asperatum, are different by
having percurrent or sympodial conidiogenous cells,
different conidial size and possessing solitary or
catenate conidia. Schubert et al. (2003) reduced
Spilocaea amelanchieris, S. eriobotryae, S. photinicola
and S. pyracanthae to synonyms of Fusicladium pomi.
This species has previously been reported from Iran as
F. pomi (Spilocaea pomi) on Malus pumila and
F. eriobotryae (= Spilocaea pyracanthae) on
Eriobotrya japonica (Ershad 2009, Askari & Ghaderi
2010) and here it is reported from yellow and red apple
cultivars of Malus pumila, Eriobotrya japonica and
Pyracantha sp. Some authors reported this species as
F. eriobotryae on Eriobotrya japonica (Sánchez-
Torres et al. 2009) and as F. pyracanthae on
Pyracantha sp. (Raabe & Gardner 1972, Juhásová et
al. 2004), but according to Schubert et al. (2003) all of
them belong to F. pomi. Conidia from E. japonica and
Pyracantha specimens are slightly, thought not
significantly, shorter on average.Pyracantha sp. and
red apple cultivar of Malus pumila are reported as new
hosts for F. pomi in Iran. In this study, conidiophores
on Pyracantha sp. are longer than those of the two
other hosts. Conidia on Malus pumila are slightly
longer than those of the two other hosts and hila from
Pyracantha sp. are slightly shorter than others but, all
of them fall in the range of F. pomi.
Fusicladium pyrorum (Lib.) Fuckel, Jahrb. Nassauisc-
hen Vereins Naturk. 23–24: 357 ‘1869’ (1870) Fig.
1G-H, 3D

HASHEMI ET AL.: A preliminary study on the genus Fusicladium s. l. in Iran 31
On fruits and leaves, leaf spots amphigenous,
diffuse, sub-circular to somewhat irregular, olivaceous
to dark brown, surrounded by a paler brown halo.
Conidiophores solitary or in loose fascicles, erect,
straight to flexuous, unbranched, 17–32 × 4–5 μm, and
aseptate (on Pyrus communis), (12–)20–37(–41) × 5–
8(–10) μm, (0–)1(–2) septate (on Khoj, a local
varietyof Pyrus communis in Guilan Province),
olivaceous, thick-walled. Conidiogenous cells
integrated, terminal, 17–32 μm long (on Pyrus
communis) and 9–25(–37) μm long (on Khoj), with
numerous conidiogenous loci (2–4 loci on Pyrusc
ommunisand 2–5(–10) loci on Khoj), proliferation
sympodial, loci denticulate, 2(–3)μm wide (on Pyrus
communis) and (1–)2–3(–4) μm wide (on Khoj), walls
unthickened. Conidia solitary, fusiform to pyriform,
ellipsoid to obovoid, straight, 14–26 × 6–7.5(–8) μm,
0(–1) septate (on Pyrus communis), (11–)13–23 × 8–
10(–11) μm, 0(–1) septate (on Khoj), olivaceous, hila
(1.5–)2(–4) μm wide (on Pyrus communis) and 2–3(–
4) μm wide (on Khoj), unthickened or slightly
thickened.
Specimens examined: On Pyrus communis:IRAN,
Qazvin, S. A. Khodaparast, (1015); IRAN, Qazvin, 26
May 2011, S. A. Khodaparast, (1016); on Khoj fruits:
IRAN, Lahijan, Guilan Province, 5 Jul. 2011, S. A.
Hashemi, (1017); IRAN, Lahijan, Guilan Province, 21
Aug. 2011, S. A. Hashemi, (1018).
Notes: Fusicladium pyrorum occurs on some host
species in the Rosaceae (Aronia, Chaenomeles,
Eriobotrya, Malus and Pyrus) and except of
F. pyrorum other three species of Fusicladium occur
on Pyrus (F. ahmadii, F. pomi and F. nashicola).
These species differ in possessing percurrent or
sympodial conidiogenous cells and specific host of
Pyrus species (Schubert et al. 2003). In this study,
F. pyrorum on Khoj has broader conidiophores and
conidia compared with specimens on Pyrus communis,
but all of them fall in the range of F. pyrorum. The
Khoj variety of Pyrus communis is reported as a new
host of F. pyrorum in Iran.
Fusicladium oleagineum (Castagne) Ritschel & U.
Braun, Schlechtendalia 9: 70 (2003) Fig. 1I, 3E
On living leaves, leaf spots 5–10 mm wide, dark to
greyish brown. Mycelium mostly superficial.
Conidiophores solitary, sub-globoseor ampulliform,
17–33(–37) × 7–13 μm, erect, straight, unbranched,
mostly aseptate, usually thick-walled, conidiophores
reduced to conidiogenous cells, with a single
conidiogenous loci, proliferation percurrent, with 4–
6(–7) conspicuous annellations, loci 5.5–6 μm wide,
unthickened, not darkened. Conidia solitary, obclavate,
straight or occasionally slightly curved, (16–)19–27(–
29) × 8–11(–12) μm, 1(–2) septate, medium to dark
olivaceous-brown, thick-walled, apex rounded, hila
(5–)6(–7.5) μm wide, unthickened, not darkened.
Specimens examined: IRAN, Rice Research
Institute, Rasht, Guilan Province, on leaves of Olea
europaea, 25 Feb. 2011, N. Zareian, (1019); IRAN,
Rice Research Institute, Rasht, Guilan Province, on
leaves of Olea europaea, 12 Dec. 2011, S. A.
Hashemi, (1020).
Notes: This species occurs only on Olea (Schubert
et al. 2003) and is a common species in olive growing
regions of Iran. Olive scab and its causal agent (F.
oleagineum) have been studied previously in different
locations of Iran such as Mazandaran, Golestan and
Guilan Provinces, Iran (Mahdian 2006, Ershad
2009,Sanei & Razavi 2011).
Furthermore, three species of Fusicladium such as
F. crataegi on Crataegus melanocarpa (from Gorgan,
Iran), F. cerasi on Prunus domestica (from Babolsar &
Borujerd, Iran) and F. heterosporum (and related
teleomorph Venturia adusta) on Epilobium hirsutum
(from Shahrestanak, Iran) have been reported from Iran
(Ershad 2009, Hedjaroude & Abbasi 2000), but were
not found in this study. Fusicladium heterosporum is
already transferred to the genus Passalora (Schubert et
al. 2003).
Key to Fusicladium species reported from Iran:
1a. Conidiogenous cells sympodial …………………. 2
b. Conidiogenous cells percurrent ……...….………. 6 6
2a. Conidia catenate, conidiophores 29–105 μm long,
conidia 12.5–20(–22) × 4–5 μm, on fruits of Prunus
persica var. nectarine ….……….... F. carpophilum
b. Conidia not catenate or rarely in chains; if so
conidia 0–1(–3)-septate………………...………... 3
3a. Conidia 1(–2), sometimes 3-septate …………...... 4
b. Conidia 0–1-septate ……………………………... 5
4a. Conidiophores with distinct lobed foot cell, conidia
1(–2) septate, more or less thickened and darkened
at septa, 14–18 × 5 μm, conidiophores 26–45 μm
long, on Fraxinus sp. ……………….…... F. fraxini
b. Conidiophores without distinct lobed foot cell,
conidia 0–2 septate, 10–25 × 4–6 μm,
conidiophores 20–54 μm long, on Crataegus spp.
……………………………....………. F. crataegi
5a Conidia 0(–1)-septate, 13–26 × 6–10 μm,
conidiophores 9–32 μm long, on Pyrus communis
and Khoj (local cultivar of P. communisin Guilan
Province) ………………….……...…... F. pyrurum
b. Conidia solitary, rarely in chains, 0–1(–3)-septate,
11–25× 4–7μm,conidiophores (10–)20–40(–60) μm
long, with narrow host range, mostly on Prunus
cerasus …………………….……...…...… F. cerasi
6a. Conidia usually without septa, 12–25 × 7–10 μm,
conidiophores 10–58 μm long, on Malus sp.,
Pyracantha sp. and Eriobotrya japonica ….F. pomi
b. Conidia 1(–2)-septate, 19–27 × 8–11 μm,
conidiophores 17–33 μm long, on Olea sp.
………………………...…….……... F. oleagineum
ACKNOWLEDGMENTS
We wish to thank Prof. Uwe Braun (Germany) who
kindly sent the monograph of the genus Fusicladium to
us.

32 Mycologia Iranica - Vol. 1, 2014
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HASHEMI ET AL.: A preliminary study on the genus Fusicladium s. l. in Iran 33
Fusicladium s. l.
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




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
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
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



FusicladiumSpilocaeaPollacciaVenturia
FusicladiumCycloconium PollacciaSpilocaeaPseudocladosporium
Fusicladium s. l.-

F. fraxiniF. carpophilumFraxinus
sp.   (Prunus persica var. nectarine)     Fraxinus sp. 
Pyracantha sp.Prunus persica var. nectarina
F. fraxiniF. pomiF. pomi

F. pyrorumF. carpophilum

Fusicladium s. l.F. pyrorumF. pomiF. crataegiF. carpophilum
F. fraxiniF. oleagineumF. cerasi
Fusicladium



Fusicladium fraxiniFusicladium carpophilum

SpilocaeaVenturia






 khodaparast@guilan.ac.ir E-mail: