New records of citrus sooty mold fungi from North of Iran

Abstract

Sooty molds are a group of fungi with dark-coloured hyphae, which grow saprophytically on various living plant organs and sometimes on non-living substrates and produce brown to black superficial colonies, black pellicles or pseudoparenchymatous crust. In north of Iran including Guilan and Mazandaran provinces, sooty molds are common on living leaves of a great variety of plants especially Citrus spp. There are a few sporadic reports of sooty mold fungi from Iran in the literature. In continuation of an earlier investigation, sooty molds from different citrus species collected from western parts of Mazandaran province and specimens obtained from fungal collection at University of Guilan were studied. As a result, five mitosporic species viz., Chaetasbolisia falcata, Cylindroxyphium virginianum, Fumiglobus citrinus, Fumiglobus foedus and Polychaeton tenellum, and one ascomyceteous species Phaeosaccardinula epicarpa, were identified as causal agents of sooty mold on citrus plants in this region. According to the literature, all of the above mentioned taxa are new to Iran mycobiota.

Full text

J. Crop Prot. 2013, 2 (3): 369-374______________________________________________________
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New records of citrus sooty mold fungi from North of Iran
Fariba Byrami, Seyed Akbar Khodaparast* and Hassan Pedramfar
Department of Plant protection College of Agriculture University of Guilan P. O. Box: 41635-1314, Rasht, Iran.
Abstract: Sooty molds are a group of fungi with dark-coloured hyphae, which grow
saprophytically on various living plant organs and sometimes on non-living
substrates and produce brown to black superficial colonies, black pellicles or
pseudoparenchymatous crust. In north of Iran including Guilan and Mazandaran
provinces, sooty molds are common on living leaves of a great variety of plants
especially Citrus spp. There are a few sporadic reports of sooty mold fungi from Iran
in the literature. In continuation of an earlier investigation, sooty molds from different
citrus species collected from western parts of Mazandaran province and specimens
obtained from fungal collection at University of Guilan were studied. As a result, five
mitosporic species viz., Chaetasbolisia falcata, Cylindroxyphium virginianum,
Fumiglobus citrinus, Fumiglobus foedus and Polychaeton tenellum, and one
ascomyceteous species Phaeosaccardinula epicarpa, were identified as causal agents
of sooty mold on citrus plants in this region. According to the literature, all of the
above mentioned taxa are new to Iran mycobiota.
Keyword: Cylindroxyphium, Fumiglobus, Chaetasbolisia, Phaeosaccardinula,
Polychaeton, taxonomy
Introduction12
Sooty molds represent different fungi belonging
to the anamorphic and teleomorphic
ascomycetes, living on plant surfaces as
saprobes (Kwee 1988). These fungi are
common on the leaves, stems, twigs and
sometimes fruits of many crops in regions with
tropical, humid subtropical or temperate climate
such as occur in Guilan and Mazandaran, north
of Iran. This region is characterized by high
rainfalls and rich fungal diversity. Sooty mold
fungi are often associated with honeydew which
insects secrete while feeding on the plant, but
they can also occur without them (Hughes
1976). Scale insects and aphids are abundant on
citrus trees which provide a good habitat for
sooty molds. There is considerable evidence
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Handling Editor: Dr. Vahe Minassian
________________________________
* Corresponding author, e-mail: khodaparast@guilan.ac.ir
Received: 6 November 2012; Accepted: 19 June 2013
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that most sooty molds display no host
preference, however some evidences show that
particular species may be restricted to certain or
a few related hosts (Hughes 1976).
The monographic literature on these fungi
extends back to over 50 years ago (Batista
1959, Batista and Ciferri 1962; 1963a, b),
however, taxonomy of the sooty mold fungi is
much complicated for which there are several
reasons that are discussed by Hughes (1976)
and Reynolds and Gilbert (2005, 2006).
In north of Iran including Guilan and
Mazandaran provinces, sooty molds are common
on living leaves of a great variety of plants
especially Citrus spp. There are a few brief
reports of sooty mold fungi from Iran in the
literature (Ershad 2009). The only comprehensive
study of sooty mold fungi in Iran has been by
Khodaparast (2006). He reported nine species of
these fungi just from Guilan province viz.
Trichomerium grandisporum, Polychaeton
artocarpi, Aithaloderma ferrugineum,
Conidiocarpus penzigi, C. caucasicus,

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Tripospermum roupalae, Leptoxyphium sp.,
Chaetasbolisia microglobulosa and Polychaeton
sp. all on citrus. The objective of this study was to
investigate the species diversity of sooty mold
fungi in a wider area of citrus orchards in north of
Iran. This paper reports only part of results that
relate to our findings on this group of molds on
citrus species.
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, when and if present were studied.
Identifications of the taxa were based on the
keys and descriptions available in several sources
including Kwee (1988), Hughes (1976) Batista,
and Ciferri (1962; 1963a, b), Reynolds (1999,
2000, 2010), Reynolds and Gilbert (2005, 2006),
Von Arx and Muller (1975) and some other
related papers cited in the references. Species
descriptions, photographs of the conidiophores
and conidia, ascoma, asci and etc. are provided.
All collected specimens were deposited in the
fungal collection of the Department of Plant
Protection, College of Agriculture, University of
Guilan. Reference numbers are presented in
parentheses after collector name.
Result and discussion
In this study, six species were determined. Brief
descriptions of identified taxa are presented.
Chaetasbolisia falcata V. A. M. Mill. & Bonar,
University of Calif. Publ. Bot. 19: 413 (1941)
Colonies composed of a network of pale
brown hyphae. Hyphae are composed of
subcylindrical to cylindrical cells which vary in
size. Pycnidia globose, sessile, superficial or
partially immersed, ostiole rounded, up to 20-
35 (-50) µm in diam., with rigid, brown-black
setae around ostioles, setae right to curved,
continuous, 4-14 in number, 20-40 × 4-7µm,
pycnidiospores hyaline, subcylindric to bacillar,
non septate, 3.5-6 × 1.5-2 µm (Fig. 1 A-D)
Specimen examined: On Citrus sinensis,
Langroud, Guilan province, S. A. Khodaparast,
14 Aug. 2012 (942).
Cylindroxyphium virginianum Bat. & Cif.,
Quad. Lab. crittogam., Pavia 31: 77 (1963)
Mycelium epiphyllous, superficial, made of
brown hyphae irregularly branched, septate,
constricted, composed of cylindrical cells.
Pycnidia superficial on the mycelium, 80-130 μm
high with a more or less cylindrical, short or long
stalk, the stalk expands into an ellipsoidal or
obovoid conidiogenous zone. Pycnidial wall
pseudoparenchymatous, composed of several cell
layers. Some scattered cells of the wall around the
ostiole have developed dark brown to almost
black thick-walled, nonseptate, subulate, straight,
setae which are 13-30 μm long and 2.5-5 μm
wide (Fig 2A). Conidia are hyaline, ellipsoid to
bacillar, 2.5-4.5 × 1.5-2.5 μm.
Specimen examined: On Citrus sinensis,
Nashtarood, Mazandaran province, F. Byrami,
16 June. 2012 (937).
Fumiglobus citrinus (Bat. & Cif.) D. R.
Reynolds & G. S. Gilbert, Cryptogamie
Mycologie, 27 (3): 254 (2006)
Mycelium epiphyllous, blackish, hyphae brown,
composed of an irregular network. Pycnidia
pyriform to globoid, superficial on the
mycelium, gregarious, brown, 25-91 × 22-75
µm, wall composed of polygonal cells (Fig.
2B). Pycnidiospores cylindrical, continuous,
hyaline, 2.5-5 × 1.2-2.5 μm (Fig. 2C).
Hughes (1976) considered the name
Asbolisia as dubious. Reynolds and Gilbert
(2006) created the name Fumiglobus to
accommodate this ambiguity and recognized
the concept for the genus as defined by Batista
and Ciferri (1963b) for Asbolisia.
Specimen examined: On Citrus sinensis,
Ramsar, Mazandaran province, S. A.
Khodaparast, 22 Jun. 2003 (951).

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Figure 1 Chaetasbolisia falcata: Pycnidia, with conspicuous ostiole (A), scale bar = 50 µm, Pycnidium with rigid,
curved setae (B), scale bar = 20 µm Hyphal network (C), scale bar = 50 µm Conidia (D), scale bar = 10 µm.
Fumiglobus foedus (Sacc.) D. R. Reynolds &
G. S. Gilbert, Cryptogamie Mycologie, 27
(3): 254 (2006)
Mycelium superficial, brownish, hyphae septate,
constricted, composed of cells 7.5-15 × 3-6 µm.
Pycnidia subglobose, sessile, gregarious, 35-79
μm in height, 51-70 μm wide, with walls made
up of polygonal cells. Pycnidiospores globose,
hyaline, 2.5-3 μm (Fig. 3 A and B).
Specimen examined: On Citrus sinensis,
Ramsar, Mazandaran province, H. Pedramfar,
27 Mar. 2011 (944).
Polychaeton tenellum (Sacc.) D. R. Reynolds,
Gdns' Bull., Singapore 61 (2): 422 (2010)
Mycelium epiphyllous, superficial, formed by
irregularly branched, septate brown hyphae,
hyphae composed of cylindrical or oblong cells.
The short stalk varies from broad cylindrical to
ellipsoid. Pycnidia superficial, 70-150 μm long,
13-6o μm wide at the base and 20-60 μm wide
at the top, 35-50 μm cylindrical swelling.
Pycnidiospores hyaline, ellipsoid to bacillar,
2.5-4.5 × 1.2-2 μm (Fig. 4)
Figure 2 Cylindroxyphium virginianum: Pycnidia,
scale bar = 20 μm (A), Fumiglobus citrinus,
pycnidium (B) Conidia (C), scale bar for B and C =
10 μm.

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Figure 3 Fumiglobus foedus: Pycnidia, scale bar =
20 μm (A), Conidia, scale bar = 10 μm (B).
Figure 4 Polychaeton tenellum; Pycnidium, scale
bar = 50µm (A), Terminal part of pycnidium and
conidia, scale bar =10 μm (B).
According to Batista and Ciferri (1963b) this
fungus was identified as Microxiphium
atmosphaericum. Several species have been
described as Microxiphium (= Microxyphium)
in Batista and Ciferri (1963b), most of them are
synonyms of Polychaeton (Reynolds 2010).
Specimens examined: On Citrus sinensis,
Nashtarood, 16 June 2011 (945), Ramsar 20
Nov. 2011 (949), Tonekabon, 20 Nov. 2010
(948); on Rubus sp., Ramsar 20 Nov. 2011
(946), on Phytolacca americana, Ramsar 20
Nov. 2011 (947), F. Byrami.
Phaeosaccardinula epicarpa Bat., Nasc. &
Cif. (1962)
Mycelium superficial, blackish brown,
pelliculose, composed of cylindric hyphae with
subglobose cells, constricted, nonsetose.
Perithecia developed beneath the mycelial
pellicle. Perithecia globose to subglobose, 160-
230 μm diam, with pseudo-ostiole, glabrous,
blackish brown, nonsetose. Asci ellipsoid, 6-8
spores, sessile, 50-74 × 24-36 μm,
aparaphysate. Ascospores ellipsoid, muriform,
transversely with 5-7 and 1-4 longitudinal
septa, at first hyaline, then yellowish- brown,
25-45 μm long and 6-15 μm wide (Fig. 5).
Figure 5 Phaeosaccardinula epicarpa cross section
of ascoma, scale bar=100 µm (A), Asci with six
ascospores, scale bar=20 µm (B), Ascospores, scale
bar =10 µm (C).
Specimens examined: On Citrus sinensis,
Sumaehsara 18 May 2003 (952), Lahijan, 20
July 2003 (953), 20 May 2003 (954), 7 June
2004 (956), Roodsar, 20 July 2003 (955);
Ramsar, 14 May 2007 (943), S. A. Khodaparast.
Acknowledgments
This work was funded by a grant from the
Deputy of Research and Technology of The
University of Guilan, Iran.
References
Batista, A. 1959. Monografia dos fungos
Micropeltaceae. Instuto de Micologia,
Universidade do Recife Publicaço, 56: 1-519.
Batista, A. C. and Ciferri, R. 1962. The
Chaetothyriale. Sydowia, 3: 1-129.

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Batista, A. C. and Ciferri, R. 1963a.
Capnodiales. Saccardoa 2: 1-296.
Batista, A.C. and Ciferri, R. 1963b.The sooty
molds of the family Asbolisiaceae.
Quaternion, 31: 1-229.
Ershad, D. 2009. Fungi of Iran. Iranian
Research Institute of Plant Protection,
Tehran. 531 pp.
Hughes, S. J. 1976. Sooty molds. Mycologia, 4:
693-820.
Khodaparast, S. A. 2006. A survey on citrus
sooty mold fungi in Guilan province, Iran.
Rostaniha, 7 (1): 59-65.
Kwee, L. T. 1988. Studies on some sooty
moulds on Guava in Malaysia. Pertanika, 11
(3): 349-355.
Reynolds, D. R. 1999. Foliicolous fungi 8:
Vietnam. Gardens Bulletin Singapore 51:
71-84.
Reynolds, D. R. 2000. The Capnodium citri
mold complex. Mycotaxon, 148: 141-147.
Reynolds, D. R. 2010. Epifoliar Fungi of
Singapore. Gardens Bulletin Singapore, 61
(2): 401-435.
Reynolds, D. R. and Gilbert, G. S. 2005.
Epifoliar fungi from Queensland,
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Reynolds, D. R. and Gilbert, G. S. 2006.
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شراﺰﮔﻪﻳارآ يﺎﻫچرﺎﻗ زا ﺪﻳﺪﺟ ناﺮﻳا لﺎﻤﺷ زا تﺎﺒﻛﺮﻣ هدود ﺪﻟﻮﻣ يﺎﻫ
ﻣاﺮﻳﺎﺑ ﺎﺒﻳﺮﻓﺖﺳﺮﭘاﺪﺧ ﺮﺒﻛا ﺪﻴﺳ ،ﻲ
*
مارﺪﭘ ﻦﺴﺣ و ﺮﻓ
هﺎﻴﮔ هوﺮﮔﺷﺰﭘﻼﻴﮔ هﺎﮕﺸﻧاد يزروﺎﺸﻛ هﺪﻜﺸﻧاد ﻲﻜناﺮﻳا ،ﺖﺷر ،ن
*ﻪﺒﺗﺎﻜﻣ لﻮﺌﺴﻣ هﺪﻨﺴﻳﻮﻧ ﻲﻜﻴﻧوﺮﺘﻜﻟا ﺖﺴﭘ :
khodaparast@guilan.ac.ir
ﺖﻓﺎﻳرد :16نﺎﺑآ 1391شﺮﻳﺬﭘ ؛ :29 دادﺮﺧ 1392
هﺪﻴﻜﭼ: چرﺎﻗ ﻲﻳﺎﺳﺎﻨﺷ ﻪﻣادا ردﻪﻧﻮﻤﻧ ،ناﺮﻳا لﺎﻤﺷ رد تﺎﺒﻛﺮﻣ هدود ﺪﻟﻮﻣ يﺎﻫ يدﺪﻌﺘﻣ يﺎﻫزا بﺮﻏ
ﻊﻤﺟ نارﺪﻧزﺎﻣ نﺎﺘﺳاﻪﻧﻮﻤﻧ ﺎﺑ هاﺮﻤﻫ و يروآﺪﻧﺪﺷ ﻲﺳرﺮﺑ نﻼﻴﮔ هﺎﮕﺸﻧاد مﻮﻳرﺎﺑﺮﻫ رد دﻮﺟﻮﻣ يﺎﻫ . ﻦﻳا رد
ﺑ ﻞﻣﺎﺷ ﻚﻳرﻮﭙﺳﻮﺘﻴﻣ چرﺎﻗ ﻪﻧﻮﮔ ﺞﻨﭘ ﻲﺳرﺮ
Chaetasbolisia falcata ،Cylindroxyphium virginianum ،
Fumiglobus citrinus، Fumiglobus foedusو Polychaeton tenellum وﻪﺑ ﺖﺴﻴﻣﻮﻜﺳآ ﻪﻧﻮﮔ ﻚﻳ مﺎﻧ
Phaeosaccardinula epicarpaﺪﺷ ﻲﻳﺎﺳﺎﻨﺷ ﺪﻧ.ﻪﻧﻮﮔ ﺑ ﻪﻟﺎﻘﻣ ﻦﻳا رد هﺪﺷ ﻲﻳﺎﺳﺎﻨﺷ يﺎﻫﻪﻮﻃ ﺮﺼﺘﺨﻣ ر
ﻲﻣ ﻒﻴﺻﻮﺗ ﺪﻧﻮﺷ.ﻪﻧﻮﮔ ﻪﻴﻠﻛ ﻲﻣ ﺪﻳﺪﺟ ناﺮﻳا يﺎﺗﻮﻴﺑﻮﻜﻴﻣ ياﺮﺑ ﺎﻫﺪﻨﺷﺎﺑ.
يﺪﻴﻠﻛ نﺎﮔژاو:ﻲﻣﻮﻧﻮﺴﻛﺎﺗ ،
Cylindroxyphium
،
Fumiglobus
،
Chaetasbolisia
،
Phaeosaccardinula
،
Polychaeton