Mycologia Iranica 2(1): 46 – 58, 2015
Original Article
A further contribution to the knowledge of sooty mould
fungi from Iran
S. A. Khodaparast
F. Byrami
M. J. Pourmoghadam
Department of Plant Protection, Faculty of
Agricultural Sciences, University of Guilan,
Rasht, Iran
A. R. Amirmijani
Department of Plant Protection, Faculty of
Agriculture, University of Jiroft, Jiroft, Iran
M. Salimi
Department of Plant Protection, Faculty of
Agricultural Sciences, University of Guilan,
Rasht, Iran
Abstract: Sooty mold fungi are often associated with
honeydew which insects secrete while feeding on the
plant. A great variety of these fungi occur in the
North of Iran, especially on Citrus spp which is one
of the most widely cultivated fruit trees in this region.
During last 10 years, several collections of these fungi
examined and 15 species have been recorded. In this
paper seven previously unreported species are treated
and described for the first time from Iran. The treated
species include Catenuloxyphium heterosporum (on
Salix aegiptiaca and Alnus glutinosa); Echinothecium
sp. (on Eriobotrya japonica and Passiflora sp.); cf.
Denisiella sp. (On Citrus sinensis and Malus pumila);
Fumagospora capnodioides (on Alnus glutinosa,
Populus deltoids, Salix aegyptiaca and Zelkova
carpinifolia); Leptoxyphium fumago (on Alnus
glutinosa, Rubus sp. and Phytolacca americana);
Tripospermum juglandis (on Ligustrum sp.) and
Scorias spongiosa (on Citrus sinensis).
Key words: Capnodiales, Capnodiaceae, Chaetothyriaceae, Scorias, Fumagospora.
INTRODUCTION
Sooty mould fungi are a diverse group of
ascomycetes that are common on the leaves, stems,
twigs and fruits of many plants. These fungi are
saprobic on the exudates produced by several insects
living on the surface of plant structures (Hughes
1976; Chomnunti et al. 2011, 2014). Sooty mould
fungi produce dark pigmented hyphae, usually with
Submitted 3 April 2015, accepted for publication 5 June 2015
Corresponding author: Email: khodaparast@guilan.ac.ir
© 2015, Published by the Iranian Mycological Society
http://mi.iranjournals.ir
mucilaginous outer walls that form a thin network on
the plant surface. Such thin network may be peeled
readily from the surface with or without some
treatment such as collodion solution (Hughes 1976).
These fungi are common in tropical, humid
subtropical or temperate climate. The first
comprehensive monographic literature on these fungi
extends back to over 50 years ago (Batista and Ciferri
1962; 1963a, b), however, taxonomy of the sooty
mould fungi is much complicated and needs more
studies. Identification of these fungi is largely based
on the old literatures and new taxonomic treatments
are rather scanty. However, some investigations and
new approaches to solve taxonomic problems of these
fungi have recently been done by some researcher
(Cheewangkoon et al. 2009; Chomnunti et al. 2011,
2012, 2014; Bose et al. 2014; Yang et al. 2014). In
north of Iran including Guilan, Gorgan and
Mazandaran provinces, sooty moulds are common on
living leaves of a great variety of plants (Khodaparast
1986, Byrami et al. 2013). According to previous
studies about 15 species have been reported from
Iran. This paper reports and describes more species of
sooty mould found from this region.
MATERIALS AND METHODS
Infected plant materials were initially examined
visually using stereomicroscope for mycelial
appearance and development. Fungal structures were
mounted in 50% lactic acid and examined using a
BH2 Olympus light microscope equipped with a Sony
digital Camera (DSC-HX1). Measurements were
taken in lactic acid (50%) mounts, based on at least
25-30 conidiophores, conidia, etc. Morphological
characters of fungal structures including hyphal type,
conidia and conidiomata, ascoma, asci and
ascospores, if present, were studied. Identifications of
the taxa were largely based on the keys and
descriptions available in several literatures including
Batista, and Ciferri (1962;1963 a,b), Hughes (1976),
Von Arx and Muller (1975), Kwee (1988), Reynolds
(1999, 2000, 2010), Reynolds and Gilbert (2005,
2006), Chomnunti et al. (2011). Species descriptions,
photographs of the conidiophores and conidia,
ascoma, asci etc. are provided. Isolation of some
sooty mould species was also attempted on water
agar, potato dextrose agar (PDA) and 2 % malt
KHODAPARAST ET AL.: A further contribution to the knowledge of sooty mould fungi from Iran
extract agar (MEA). For isolation, a part of plant
material containing pycnidia were incubated in a
moist chamber for up to 14 h. Oozed conidial mass on
top of ostiole of one pycnidium were removed with a
sterile needle and streaked on agar containing media.
Growing colonies were sub-cultured onto potatodextrose PDA or MEA.
All collected specimens were deposited in the
fungal collection of the Department of Plant Protection, Faculty of Agricultural sciences, University of
Guilan (GUMC).
RESULTS AND DISCUSSION
Seven species of sooty mould fungi were
identified, all of them are described as new records
from Iran.
Catenuloxyphium heterosporum Bat., Nascim. &
Cif., in Batista & Ciferri, Quad. Lab. crittogam.,
Pavia 31: 55 (1963)
Saprobic on insect exudates and producing a black
sooty-like covering on the surface of leaves.
Mycelium consisting of a network of superficial
brown septate hyphae. Hypahal cells cylindrical to
subcylindrical, constricted at septa, measured 6-21 x
3.5-5 µm. Conidiomata pycnidial, superficial,
scattered, brown, flask-shaped to cylindrical, without
conspicuous stalk or stalk very short, wider at base or
near the base, sometimes with oval fruiting zone at
middle, tapering to the apex, producing ostiole at the
apex, ostiole surrounded by hyaline hyphae, up to 35
μm in length, wall consisting of oblong cells, about 624 x 3-6 μm, total pycnidium length 200-350 (-420)
μm, 36 -56 (-70) μm at wider part (usually near the
base), Conidiogenous cells arising from the inner cell
wall of the fruiting zone. Conidia ellipsoid, ovoid to
cylindric, at first hyaline, aseptate or with 1-3 (usually
1) septa, 6.5-15 x 3-4 (-4.5) μm; mature conidia
brown, with 1-3 (usually 1) septa, 10-17 x 5-7 μm
(Fig. 1, 2).
Specimen examined: on Salix aegiptiaca L.,
Ramsar, Mazandaran Province, Iran, 27 Jul. 2007, S.
A. Khodaparast (GUM 1309); on Alnus glutinosa (L.)
Gaertn., Tonekabon, Mazandaran Province, Iran, 17
Jun. 2011, F. Byrami (GUM 1310).
In our specimen, pycnidia are longer and fimbriate
versus shorter and not fimbriated ostiole which has
been described in Batista and Ciferri (1963b) for
Catenuloxyphium heterosporum.
Cf. Dennisiella sp.
Mycelium consisting of superficial hyaline,
septate hyphae. Hyphae are more or less cylindric,
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about 3-4 μm wide. Hyphae frequently become
compact and form cushion of cells which are
pigmented and develop two to several setae around
cushion. Setae are nonseptate, thick-walled, subulate,
robust and straight or sometimes curved and slightly
flexible, usually pointed at apex, with a bulbous,
lobed base, 50-250 μm long and 6-10 μm wide near
the base.
Some setae are encircled by hyphae bearing
conidia. The conidia are globose to subglobose,
hyaline, about 3.5-6 μm (Figs. 3, 4). According to
Hughes (1976) fungus with such conidia assigned to
Microxiphium (anamorphic state of Dennisiella),
however, It was difficult to discriminate if there was
conidial state of this fungus or contamination from
other fungi. No ascomatal state has been discovered
during this study, however, it seems this specimen
belong to Dennisiella.
Specimen examined: On Citrus sinensis Pers.,
Guilan, Sumaehsara 7 Feb. 2014, S.A. Khodaparast
(GUM 1306); Malus pumila Mill., Guilan, Sumaehsara 16 Nov. 2011, S.A. Khodaparast (GUM 1307).
Echinothecium sp.
Mycelium consisting of superficial pale brown to
olivaceous brown septate hyphae. Hyphae are
cylindric, constricted at septa. Ascoma globose,
subglobose, setose, 65-180 μm, Peridium consisting
of pale brown to olivaceous brown cells forming a
textura angularis, setae dark brown, usually produced
at upper part of ascoma, measured 13-95 x 2.5-9 μm,
Asci elongate, fusiform, bitunictae, 50-90 x 8-20 μm,
8-spored, Ascospores fusiform, hyaline, 2-celled, 920 x 2.5-5.5 μm (Fig. 5).
Specimen examined: Eriobotrya japonica (Thunb.)
Lindl., Mazandaran Province, Nashtaroud, Iran, 17
Jun. 2011, F. Byrami (GUM 1320); on Passiflora sp.,
Guilan Province, Rasht, Iran, 25 Oct. 2009, F. Byrami
(GUM 1321).
According to Batista and Ciferri (1963a) this
species is very close to Capnobatistia serrulata Cif.
& Leal. This genus have been transferred to
Echinothecium by von arx and Muller (1975).
Fumagospora capnodioides G. Arnaud, Annals
d'École National d'Agric. de Montpellier, Série 2
10(4): 326 (1911)
Saprobic on insect exudates and producing a black
sooty-like covering on the surface of leaves.
Mycelium consisting of a network of superficial
brown septate hyphae. Pycnidia variable in shape,
mostly cylindrical to subcylindrical, rarely flask
shaped, with or without stalk, simple or branched,
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usually 200-400 μm total length, fruiting zone 25-60
μm wide, stalk 25-95 x 25-46 μm, about 18-35 (-46)
μm wide near the ostiole, ostiole with hyaline hyphae
with 14-25 μm in length, conidia ellipsoid, at first
hyaline, becoming pigmented at maturity, 2-3 (-4)
transverse and 1-3 longitudinal septa, measured 15-25
x 8-11 μm (Fig. 6).
Specimen examined: on Alnus glutinosa (L.)
Gaertn., Guilan, Poonel, 8 Aug. 2012, S. A. Khodaparst
Mycologia Iranica - Vol. 2, 2015
(GUM 1326); Populus deltoides W. Bartram ex
Marshall, Sumaehsara, Guilan province, 20 Sept.
2007, S. A. Khodaparast (GUM 1318); Salix
aegyptiaca L., Sumaehsara, Guilan Province, 28 Jun.
1997, S. A. Khodaparast (GUM 1316); L., Zelkova
carpinifolia Dippel, Rasht, 7 Oct. 1997, S.A.
Khodaparast (GUM 1317).
Fig. 1. Catenuloxyphium heterosporum: a-c. pycnidia, scale= 200 μm; d-e. Ostioles and mass of conidia, scale for D=20 μm,
for E=30 μm.
KHODAPARAST ET AL.: A further contribution to the knowledge of sooty mould fungi from Iran
Fig. 2. Catenuloxyphium heterosporum: a-f. Different type of conidia, scale = 20 μm.
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Mycologia Iranica - Vol. 2, 2015
Fig 3. Cf. Dennisiella sp. a-b Setae on the mycelium, scale for A =200 μm, for B = 100 μm; c. mycelium, d. conidia, scale 20 μm.
Leptoxyphium fumago (Woron.) R.C. Srivast., Arch.
Protistenk. 125 (1-4): 333 (1982)
Saprobic on insect exudates and producing a black
sooty-like covering on the surface of leaves. Mycelium
consisting of a network of cylindrical and septate
hyphae.
Conidioma a synnematal-like structure (pycnidia as
stated by some authors such as Chomnunti et al. 2011),
comprising 10-12 parallel, septate hyphae, cylindrical
but usually slightly tapering toward apex, with long
stalk, and a cup-like fruiting zone at the apex, total
length up to 500 μm, usually proliferate to produce new
conidiogenous zone, 13-55 μm at the base, cup-like
fruiting zone measured 18-50 μm in wide.
Conidiogenous cells arising from the inner cell wall of
the fruiting zone. Conidia at first hyaline, ellipsoid,
continuous, measuring 5-10 x 2-3 (-4) µm, finally they
may enlarge, become 1-septate and pigmented on the
host plant leaves (Fig. 7).
Specimen examined: On Alnus glutinosa (L.)
Gaertn., Katalom-Tonekabon road, Mazandaran
Province, Iran, 21 Nov., F. Byrami (GUM 1324);
Rubus sp. Ramsar, Mazandaran Province, Iran, 21
Nov., F. Byrami (GUM 1308); Phytolacca americana
L., Guilan Province, Sumaehsara, Iran, 27 Oct. 2007,
S.A. Khodaparast (GUM 1325).
KHODAPARAST ET AL.: A further contribution to the knowledge of sooty mould fungi from Iran
51
Fig. 4. Cf. Dennisiella sp. a. Lobed basal cell of setae on the mycelium, b-c. Conidia around setae assigned to Microxiphium
(anamorphic state of Dennisiella), d-e. Colony on the leaf surface, scale 20 μm.
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Mycologia Iranica - Vol. 2, 2015
Fig. 5. Echinothecium sp.: a. Ascoma, b. ascospores, c. Asci, scale for A=50 μm, B=10 μm, C=20 μm.
Tripospermum juglandis (Thüm.) Speg., Physis, Rev.
Soc. Arg. Cienc. Nat. 4 (no. 17): 294
A dematiaceous Hyphomycetes that occurs solely or
usually together with other sooty moulds as a
superficial mycelium consisting of olivaceous septate
hyphae on leaf surfaces that already infested with insect
exudates. Hyphae are more or less cylindrical,
constricted at septa, composed of cylindrical or barrel
shape cells. Each conidium arises from a pyriform,
stalked cell 5-15 µm long and 3-6 µm wide. Conidia
are brown to olivaceous, star-shaped with four
divergent arms which are wide at the base and
attenuated toward apex, apex rounded, longest arm
measures 23-55 µm and shortest arms 12-30 µm (Fig.
8).
KHODAPARAST ET AL.: A further contribution to the knowledge of sooty mould fungi from Iran
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Fig. 6. Fumagospora capnodioides: a. Branched pycnidium, scale 50 μm, b. drawing of pycnidium, scale= 100 μm and
conidia, scale =25 μm.
Specimen examined: Ligustrum sp., KatalomTonekabon road, Mazandaran Province, Iran, 22 Oct.
2010, F. Byrami (GUM 1323).
Scorias spongiosa (Schwein.) Fr., Syst. mycol.
(Lundae) 3(2): 291 (1832)
Saprobic on insect exudates and producing a black
sooty-like covering on the surface of leaves. Mycelium
consisting of a network of cylindrical and septate
hyphae. Conidiomata pycnidial, scattered, brown to
blackish brown, wall synnematous, comprising mostly
of cylindrical cells, tapering to the apex, flask–shaped,
total pycnidium length 250-550 μm, with a flattened
stalk, stalks about 80-170 x 35-140 μm, continue to a
conidiogenous zone, conidiogenous zone sub-ellipsoid,
darker than other parts, (50-) 75-112 x 36-62 μm,
extended into a neck, neck subcylindrical, 92-275 μm
long, about 12-20 μm wide at base, and 10-13 μm apex;
ostiole surrounded by hyaline hyphae about 10-25 μm.
Conidia gathered in a slimy mass around ostiole,
hyaline, ellipsoid, cylindric to subcylindric, rounded at
both ends or pointed at the base, smooth, 1-celled, 2
guttules, 3.5-5.5 x 1.5-2 μm (Fig. 9).
Culture characteristics: Colony becoming up to 7 mm
diam at 25 °C on PDA after 10 days, about 17.3 mm on
MEA after 14 days in the darkness; superficial, flat,
with entire edge, olivaceous to green, producing a
characteristic spreading red –purple pigment in plate,
showed a color change of the medium away from the
original plate after subculturing; aerial hyphae at fiest
with thin and inconspicuous septa, usually not
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constricted, branched, smooth to slightly verrucose,
pale brown to brown, cylindrical to sub-cylindrical,
hyphae becoming thick-walled, pale broun to
olivaceous, constricted at septa, about 3–5 μm wide.
Total pycnidium length 450-900 μm, stalks 120-600
μm long, and 50-125 μm wide, conidiogenous zone
usually conspicuous, darked, sub-ellipsoid, ellipsoid,
150-230 x 55-150 μm, neck 137-375 μm long, 17- 30
Mycologia Iranica - Vol. 2, 2015
near the base, tapering toward the apex, apex about 1118 μm wide, hyaline hyphae around ostioles about 1737 μm long. Conidia gathered in a slimy mass around
ostiole, hyaline, ellipsoid, cylindric, subcylindric, 2
guttules, (-2.5) 3-4 x 1-2 (-2.5) μm. Pycnidia produced
abundantly on the surface of the MEA plate (Fig. 10).
Specimen examined: On Citrus sinensis Pers.,
Sumaehsara, Guilan Province, Iran, 24 Jan. 2013, S. A.
Khodaparast (GUM 1301).
Fig. 7. Leptoxyphium fumago: a-b. Synnema, scale 50 µm, c. hyaline and immature conidia, scale 10 µm; d. mature
pigmented conidia, scale 10 µm.
KHODAPARAST ET AL.: A further contribution to the knowledge of sooty mould fungi from Iran
55
Fig. 8. Tripospermum juglandis: Conidia, scale =50 µm.
Fig. 9. Scorias spongiosa: a. pycnidial, some immature ascoma around pycnidial, scale= 100 μm; b-c. pycnidial, scale= 100
μm; d. Conidia scale =20 μm; e. pycnidium neck, scale =50 μm.
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Mycologia Iranica - Vol. 2, 2015
Fig. 10. Scorias spongiosa: a-d. Different type of pycnidia produced on Malt Extract Agar, scale for a, b and d = 100 μm,
c = 200 μm; e. conidia, scale 5 μm.
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Q, Peršoh D, Dhami MK, Hyde KD. 2014. The
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Hughes SJ. 1976. Sooty moulds. Mycologia 4: 693820.
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fungi in Guilan province, Iran. Rostaniha 7: 59-65.
Kwee LT. 1988. Studies on some sooty moulds on
Guava in Malaysia. Pertanika 11: 349-355.
Reynolds DR. 1999. Foliicolous fungi 8: Vietnam.
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Gardens Bulletin Singapore 51: 71-84.
Reynolds DR. 2000. The Capnodium citri mould
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اطالعات جدید در مورد قارچ های مولد کپک دوده ای در ایران
سیداکبر خداپرست ، 1فریبا بایرامی ،1محمد جواد پورمقدم ، 1امیررضا امیرمیجانی 2و مهدی سلیمی
1
- 1گروه گیاهپزشکی ،دانشکده علوم کشاورزی ،دانشگاه گیالن ،رشت
- 2گروه گیاهپزشکی ،دانشکده کشاورزی ،دانشگاه جیرفت ،جیرفت
چکیده :قارچهای مولد کپک دودهای اغلب همراه با ترشحات عسلی حشراتی هستند که از گیاهان تغذیه میکنند .تعداد زیادی از
این قارچ ها در شمال ایران به ویژه روی مرکبات گسترش دارند که از محصوالت کشاورزی مهم این منطقه به شمار میآیند .طی ده
سال گذشته نمونههای زیادی از این قارچها مطالعه شدهاند و 15گونه از این منطقه گزارش شده است .در این مقاله نیز هفت گونه
جدید از ایران گزارش می شود که عبارتند از :
Catenuloxyphium heterosporum (on Salix aegiptiaca and Alnus glutinosa); Echinothecium sp. (on Eriobotrya
japonica and Passiflora sp.); cf. Denisiella sp. (On Citrus sinensis and Malus pumila); Fumagospora capnodioides
(on Alnus glutinosa, Populus deltoids, Salix aegyptiaca and Zelkova carpinifolia); Leptoxyphium fumago (on Alnus
glutinosa, Rubus sp. and Phytolacca americana); Tripospermum juglandis (on Ligustrum sp.) and Scorias spongiosa
(on Citrus sinensis).
کلمات کلیدیFumagospora ،Scorias ،Chaetothyriaceae ،Capnodiaceae ،Capnodiales :
مکاتبه کننده :سیداکبر خداپرست Email: khodaparast@guilan.ac.ir
تاریخ دریافت1394/01/14 :
تاریخ پذیرش1394/03/15 :