Fungicide sensitivity of selected Verticillium fungicola isolates from Agaricus bisporus farms
ABSTRACT Five isolates of Verticillium fungicola, isolated from diseased fruiting bodies of Agaricus bisporus collected from mushroom farms in Serbia during 2002-2003, were studied. By observing their colony morphology under different growth conditions and their pathogenic characteristics, the isolates were identified as V. fungicola var. fungicola. The peat/lime casing was the primary source of infection. Testing of sensitivity to selected fungicides showed that all isolates were highly resistant to benomyl (EC50 values were higher than 200.00 mg/l), moderately sensitive to iprodione (EC50 values were between 11.93 and 22.80 mg/l), and highly sensitive to prochloraz-Mn (EC50 values were less than 3.00 mg/l).
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ABSTRACT: Symptoms of brown blotch were observed on cultivated Agaricus bisporus on several mushroom farms in Serbia. Subsequently, samples were collected from nine localities during 2006–2010 and fluorescent Gram-negative bacterial strains were isolated. All strains caused sunken brown lesions on A. bisporus tissue blocks after artificial inoculation. Isolated strains showed the LOPAT characteristics of the group Va being negative for levan production; the ability to produce a hypersensitivity reaction in tobacco; were oxidase and arginine dihydrolase positive; and lacked pectolytic activity. The results from other tests were as follows: oxidative metabolism of glucose; catalase activity positive; aesculin hydrolisis negative; Tween 80 hydrolysis positive; casein hydrolysis positive; gelatine hydrolysis and nitrate reduction negative; mannitol, erythritol, sorbitol, inositol and trehalose were used as a carbon source but not sucrose, arabinose and D(-) tartrate. Based on these features bacterial strains were identified as Pseudomonas tolaasii. The identity of isolated strains was confirmed by polymerase chain reaction. This is the first report of P. tolaasii in Serbia.Phytoparasitica 40(3). · 0.72 Impact Factor
Agaricus bisporus (Lange) Imbach is the most com-
monly cultivated mushroom species (royse, 1996).
the production of fruiting bodies is severely afflict-
ed by fungal, bacterial, and viral pathogens that can
cause diseases which have an effect on yield and
quality. Verticillium fungicola (Preuss) Hassebrauk,
with two varieties, fungicola, widespread in Europe,
and aleophilum, widespread in north America, is a
major A. bisporus pathogen and a causal agent of
the disease commonly known as “dry bubble”. A.
bisporus – V. fungicola interaction is of an invasive
necrotrophic nature. the disease severity and symp-
toms depend on the stage of mushroom develop-
ment at the time of infection (north and Wuest,
1993, Grogan et al., 2000), and the symptoms are
necrotic lesions with brown colored spots or streaks,
stipe blow-out, and undifferentiated structures con-
taining mycelia of both host and pathogen (Savoie
and Largeteau, 2004).
In recent years, the usual method of controlling
of “dry bubble” disease on farms worldwide is based
on the use of fungicides. The most commonly used
fungicides on mushroom farms are: benomyl (2,2-di-
phenyl-1-picrylhydrazyl cineole chamazulene); ipro-
ainc salt); and prochloraz-Mn (1-(n-propyl-n-(2-
(Gea et al., 1997). However, development of patho-
gen resistance to fungicides after frequent applica-
tion (Bonnen and Hopkins, 1997; Gea et al.,
1997, 2003; Grogan et al., 2000) and host sensitiv-
ity to fungicides (diamantopoulou et al., 2006)
are a serious problems.
the aims of this study were to isolate and iden-
tify the causal agent of ”dry bubble” in Serbia, and
examine variation of the pathogen as evidenced by
morphology of its colonies under different growth
conditions and their pathogenic characteristics.
Sensitivity of the pathogen to benomyl, iprodione
and procholoraz-Mn was also tested.
FUNGICIDE SENSITIVITY OF SELECTED VERTICILLIUM FUNGICOLA ISOLATES
FROM AGARICUS BISPORUS FARMS
IVAnA PotoČnIK1, JELEnA VuKoJEVIĆ2, MIrJAnA StAJIĆ2,
BrAnKIcA tAnoVIĆ1, and BILJAnA todoroVIĆ1
1ARI Serbia, Pesticide and Environmental Research Center, 11080 Belgrade, Serbia
2Institute of Botany, Faculty of Biology, University of Belgrade, 11000 Belgrade, Serbia
Abstract — Five isolates of Verticillium fungicola, isolated from diseased fruiting bodies of Agaricus bisporus collected
from mushroom farms in Serbia during 2002-2003, were studied. By observing their colony morphology under different
growth conditions and their pathogenic characteristics, the isolates were identified as V. fungicola var. fungicola. the peat/
lime casing was the primary source of infection. testing of sensitivity to selected fungicides showed that all isolates were
highly resistant to benomyl (Ec50 values were higher than 200.00 mg/l), moderately sensitive to iprodione (Ec50 values
were between 11.93 and 22.80 mg/l), and highly sensitive to prochloraz-Mn (Ec50 values were less than 3.00 mg/l).
Key words: Verticillium fungicola var. fungicola, fungicides, benomyl, iprodione, prochloraz-Mn, sensitivity
Arch. Biol. Sci., Belgrade, 60 (1), 151-157, 2008 doI:10.2298/ABS0801151P
I. PotoČnIK Et AL.
MAtErIALS And MEtHodS
Isolates and growth conditions
Isolates of V. fungicola obtained from diseased
fruiting bodies of A. bisporus collected during 2002-
2003 in Serbia are shown in table 1. Isolation
was done by taking small pieces (2 x 2 x 5 mm)
of fruiting bodies with ”dry bubble” symptoms,
immersing them a 1% sodium hypochlorite solu-
tion (for 1 min), and placing them on Potato dex-
trose agar medium (PdA). the isolates are main-
tained on PdA at 5oc in the culture collection of
the Pesticide and Environmental research center's
Phytopathology Laboratory in Belgrade. Verticillium
fungicola var. fungicola 182 (obtained from the
collection of Horticulture research International,
Wellesbourne, uK) and V. fungicola var. aleophi-
lum dc-170 (obtained from the Plant Pathology
department, Penn State university, uSA) were used
the morphology of colonies of all V. fungicola
isolates was studied by observing their growth on
PdA, malt agar medium (MA), mushroom dextrose
agar medium (MdA), water agar medium (WA),
and czapek agar medium (czA) for 7 days at 20oc.
the dimensions of 30 conidia per isolate formed on
PdA were measured and compared. temperature
influence was investigated on V. fungicola isolates
cultivated on the optimal medium for 7 days at 20,
27 and 30oc. three replicates per treatment and per
isolate were used for statistical analysis.
Spawn-run compost (A. bisporus Sylvan A 15),
produced by uca & co., Vranovo, Serbia, was
used for the pathogenicity test. compost bags were
encased with a 40 – 50-mm layer of black peat/lime
casing ("Makadam" co., Belgrade), which was arti-
ficially inoculated with the studied isolates of V.
fungicola. the casing inoculation was done by spore
Varietycode of isolates
originYear of isolation
V. fungicola var. fungicola
V. fungicola var. aleophilum
Table 1. Isolates of Verticillium fungicola.
suspension spraying (approximately 106 conidia/ml)
3 days after encasement. Bags were incubated at
25oc during spawn-running of the casing (for 7
days), after which temperature was lowered to 18oc.
the inoculated black peat/lime casing was removed
and replaced with new sterile one 30 days after the
Testing of sensitivity to selected fungicides
Sensitivity analysis was done with isolates
grown on PdA amended with the following fun-
gicides: benomyl (Benfungin WP, 50%, Galenika-
Fitofarmacija); iprodione (Kidan Ec, 25.5%, Bayer);
and prochloraz-Mn (octave WP, 50%, Bayer). the
preliminary concentrations of all selected fungicides
were 0.01, 0.10, 1.00, 10.00, 100.00, and 1000.00 mg/l.
testing of sensitivity to iprodione and prochloraz-
Mn was repeated with concentrations of 0.1, 0.5, 1.5,
10.0, 50.0, and 100.0 mg/l; and 0.078, 0.156, 0.312,
0.625, 1.250, 2.500, and 5.000 mg/l, respectively.
the plates were inoculated with an inverted
mycelial agar disk (10 mm) taken from the edge
of 14-day-old culture of V. fungicola var. fungicola
isolates, placed centrally on fungicide-amended and
fungicide-free medium (control) and incubated at
20oc. three replicates per treatment and per isolate
were done. colony diameter was measured after 7
days of growth. Growth of colonies on the fungi-
FunGIcIdE SEnSItIVItY oF VERTICIllIUm FUngIColA
Fig. 1. Spotting of Agaricus bisporus cap artificially induced by
Verticillium fungicola var. fungicola VV2.
Fig. 2. Deformation of Agaricus bisporus fruiting body artifi-
cially induced by Verticillium fungicola var. fungicola VV2
Fig. 3. Influence of medium composition on growth of Verti-
cilium fungicola var. fungicola VV2. From left to right: upper
row - PDA, MA, and MDA; lower row - PDA, CzA, and WA.
cide-amended medium was given as a percentage
of the control. Ec50 and Ec90 (fungicide concentra-
tions which inhibit mycelial growth by 50 and 90%,
respectively) were determined for each isolate by
interpolation from computer-generated log-probit
plots of fungicide concentration and relative inhibi-
tion (Leroux and Gredt, 1972). the effect of fungi-
cides was studied by analyzing means and variance
of Ec by the multiple range test (Finney, 1964).
Symptoms of “dry bubble“ disease
Single or clusters of undifferentiated fruiting
bodies of A. bisporus with symptoms similar to those
caused by V. fungicola were observed in screening of
mushroom farms in Serbia during 2002-2003. Large
brown spots with a fuzzy grayish tint were noticed
on fully differentiated fruiting bodies after 12 days
(Fig. 1), and undifferentiated fruiting bodies were
found 18 days after artificial inoculation of casing
with the pathogen (Fig. 2).
Identification of isolates identification
the following morphological characteristics
were recorded in the analyzed isolates: dense white
aerial mycelia; absence of pigment production; hya-
line, erect conidiophores with groups of divergent
phialides of verticilliate form; hyaline, cylindri-
cal phialides with slightly inflated base and acute
tip; and hyaline, unicellular, ellipsoid to cylindrical
conidia produced in a gelatinous matrix. conidia in
all studied isolates measured 2.95-7.38 x 1.97-2.46
µm. After comparing our isolates with control iso-
lates, we concluded that all Serbian isolates were V.
fungicola var. fungicola.
the diameter of colonies of all isolates after
7 days of growth showed significant differences
depending on composition of the medium (Fig. 3),
ranging between 10.25 mm on MdA (ViV1) and
14.17 mm on PdA (P2V3).
Serbian as well as uK V. fungicola isolates grew
only at 20oc; growth was absent at 27 and 30oc.
However, V. fungicola var. aleophilum dc-170 grew
at all investigated temperatures, the optimal one
I. PotoČnIK Et AL.
Fruiting bodies with split stems and grayish-
brown spots on the whole surface of the cap were
noticed 12 days after inoculation of the casing with
isolates VV2 and P2V3; and 13 days after inoculation
with isolates ViV1, raV1, and BeV1 (Fig. 1).
undifferentiated masses of fruiting bodies with
a dry surface covered with a dusty gray layer of
conidia were observed on the 18th day after inocula-
tion with isolates VV2 and P2V3; on the 19th day after
inoculation with ViV1 and raV1; and on the 20th
day after inoculation with BeV1 (Fig. 2). However,
fruiting bodies with "dry bubble" symptoms were
not recorded after replacing the infected casing with
a sterile new one.
Testing of sensitivity to selected fungicides
In these in vitro investigations of the sensitivity
of V. fungicola var. fungicola isolates to the selected
fungicides, all studied isolates showed high resis-
tance to benomyl (Ec50 values were between 234.55
to 359.95 mg/l); moderate sensitivity to iprodione
(Ec50 values were in the range from 11.93 to 22.80
mg/l); and high sensitivity to prochloraz-Mn (Ec50
values were in the range from 1.11 to 2.51 mg/l);
to judge from taxonomic criteria based on the
optimal growth temperature (Gams and Van
Zaayen, 1982; nair and Macauley, 1987), all
V. fungicola isolates from Serbian A. bisporus farms
were V. fungicola var. fungicola. Gams and Van
Zaayen (1982) emphasized V. fungicola varieties
differ significantly with respect to the optimal tem-
perature for mycelial growth (20-240c for var. fun-
gicola and 300c for var. aleophilum). Bonnen and
Hopkins (1997) observed a high level of homoge-
nicity in colony morphology, virulence, and fungi-
cide response among analyzed V. fungicola isolates
from north America and placed them in the same
rAPd group. But in investigations of hydrolytic en-
zyme production and genetic variability between two
2273.47-12347.75 48187.94-16268E+4 7308.98-12560E+1
Ec50 and Ec90 expressed in mg/L
b = regression coefficient
Table 2. In vitro sensitivity of Veriticillium fungicola var. fungicola isolates to selected fungicides.
FunGIcIdE SEnSItIVItY oF VERTICIllIUm FUngIColA
V. fungicola isolates originating from north Ameri-
ca, Bidochka et al. (1999) showed the presence of
49% divergence in the rdnA sequence of their ItS1,
which was confirmed using rAPd and AFLP mark-
ers (Juarez del carmen et al., 2002; Large-
teau et al., 2006). contrary to the situation with
var. aleophilum, Largeteau et al. (2006) showed
the presence of significant differences of physiologi-
cal and pathogenicity traits among var. fungicola iso-
the noted symptoms on A. bisporus fruiting
bodies caused by V. fungicola var. fungicola iso-
lates on Sebian farms were similar to ones pre-
viously described on farms worldwide (nairn
and Macauley, 1987; Staunton and dunne,
1990; north and Wuest, 1993; Savoie and
Largeteau, 2004). the results of this study con-
firm the results of Wong and Preece (1987), and
north and Wuest (1993), who showed the peat/
lime casing to be the primary source of V. fungicola,
and that the earliest possible infection occurred dur-
ing the encasement period, but not before, because
conidia which were present in spawned compost
were not able to cause development of the disease.
using electron microscopy, dragt et al. (1996)
showed that V. fungicola grows both outside and in-
side the hyphae of A. bisporus fruiting bodies, and
emphasized that the pathogen penetrates host chi-
tin cell walls by the combined effect of mechanical
pressure and wall-lytic enzymes. Mills et al. (2000)
isolated and identified β-1-6-glucanases, chitinases,
serine proteinase, stearase, and esterase from cul-
ture filtrates of V. fungicola grown in the presence
of A. bisporus cell wall, and Athey-Pollard et
al. (2003) isolated the cap-binding protein (eIF4E)
from A. bisporus and V. fungicola and described its
gene nucleotide and amino acid composition.
Agaricus species can protect themselves from
V. fungicola invasion by production of extracellu-
lar phenoloxidases, H2o2, and antibiotics (Large-
teau et al., 2006; Score et al., 1997; Savoie et
al., 2004), but efficiency of self-defense depends on
the level of resistance of Agaricus species (and even
strainstrains) to V. fungicola, as well as on sensitivity
of the pathogen to host metabolites (Savoie and
Largeteau, 2004; dragt et al., 1995; Jaurez
del carmen et al., 2002). Thus, Gea et al. (2003)
noted that 26-47% of fruiting bodies on A. bisporus
farms but only 4-12% on A. bitorquis farms were
infected, while Savoie and Largeteau (2004)
showed that the majority of V. fungicola isolates were
susceptible to lower H2o2 concentration. In recent
decades, a common method of pathogen control on
farms worldwide is application of various fungicides.
For improvement of crop protection and reduction
of production costs, the effects of some new fungi-
cides are being tested. However, fungicide efficien-
cy depends on frequency of usage (Bonnen and
Hopkins, 1997), as well as on the persistence of
fungicides in high concentrations in the casing dur-
ing cultivation (Grogan and Jekes, 2003).
According to the criteria established by Gea et
al. (2003, 2005), V. fungicola isolates from Serbian
A. bisporus farms were highly resistant to benomyl,
moderately sensitive to iprodione, and highly sensi-
tive to prochloraz-Mn. Bonnen and Hopkins
(1997) also showed absence of benomyl sensitivity
in isolates obtained after the year 1979. However,
contrary to the situation with Serbian V. fungicola
isolates, Spanish isolates were resistant to iprodione
with Ec50 values higher than 50.00 mg/L (Gea et
al., 1997). In the case of resistance to prochloraz-Mn,
the picture is very different from strain to strain of
V. fungicola. to be specific, 70% of pathogen isolates
from Great Britain and Spain were moderately sen-
sitive to prochloraz-Mn with Ec50 values ranging
from 5.0 to 8.0 mg/L (Grogan et al., 2000; Gea
et al., 2003), and some farms reported unsatisfac-
tory levels of control by that fungicide, which was
explained by the fact that resistance was developed
with the passage of time (Gea et al. 2005). Those au-
thors analyzed 105 V. fungicola var. fungicola isolates
from Spanish mushroom crops collected in the pe-
riod between 1992 and 1999 and demonstrated that
their resistance ranged from low (Ec50 value of 0.8
mg/l) in 1992 to moderate (Ec50 value of 8.8 mg/l) in
1998. In the case of isolates from 1999, 29.86% were
sensitive (Ec50 value of 5.0 mg/l) and 14% slightly
tolerant (Ec50 values equal to or above 5.0 mg/l),
while 60% grew at a fungicide concentration of 50.0
mg/l and 40% at 100.0 mg/l.
I. PotoČnIK Et AL.
Bernardo et al. (2002, 2004) noted that pro-
chloraz-Mn alters structure of the cell wall, as well as
the ratio of cell wall components and their structure
in both V. fungicola and A. bisporus, which can be
attributed to the fungicide's inhibitory effect on ste-
rol biosynthesis. diamantopoulou et al. (2006)
confirmed the adverse effects of fungicides in test-
ing of tebuconazole, a new fungicide, which caused
pileus deformations and severe reduction of total
yield at a concentration of 0.8 g/m2 and deviation in
sporophore color at a concentration of 1.2 g/m2. ow-
ing to everything mentioned above and despite the
existence of some efficient fungicides for V. fungicola
control, special attention is now being paid to ge-
netic reduction of pathogen virulence by generation
of mutants with diminished ability to utilize chitin
as a carbon source (Amey et al., 2003), as well as
to the possibility of using natural products (such as
essential oils of different plants) to inhibit pathogen
activity (Soković et al., 2006).
Ackowledgments – the authors thank H. M. Grogan of
Horticulture research International, Wellesbourne, Warwick,
uK; and d. M. Beyer of the Plant Pathology department, Penn
State university, uSA, for supplying isolates. this research
was performed at the deparment of Applied Plant Pathology
of Pesticide and Environmental research center; and of the
Faculty of Biology, university of Belgrade (Grant 143041).
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OСЕТЉИВОСТ НА ФУНГИЦИДЕ ОДАБРАНИХ ИЗОЛАТА VERTICILLIUM FUNGICOLA
ИЗ ГАЈИЛИШТА AGARICUS BISPORUS
ИВАНА ПОТОЧНИК1, ЈЕЛЕНА ВУКОЈЕВИЋ2,, МИРЈАНА СТАЈИЋ2,
БРАНКИЦА ТАНОВИЋ1 и БИЉАНА ТОДОРОВИЋ1
1АРИ Србија, Центар за пестициде и заштиту животне средине, 11080 Београд, Србија
2Институт за ботанику, Биолошки факултет, Универзитет у Београду, 11000 Београд, Србија
Проучавано је пет изолата Verticillium fungico-
la, изолованих са оболелих плодоносних тела Aga-
ricus bisporus сакупљених у гајилиштима Србије у
току 2002-2003. На основу мор�ологије колонија,На основу мор�ологије колонија,
гајених под различитим условима, и патогених
карактеристика, изолати су иденти�иковани као
V. fungicola. fungicolafungicola var.var. . fungicola. Примарни извор ин�ек-
ције била је покривка од тресета и креча. Тест осе-
тљивости на одабране �унгициде је показао да су
сви изолати високо резистентни на беномил (Ec50
вредности више од 200.00 mg/l), умерено осетљи-
ви на ипродион (Ec50 вредности између 11.93 и
22.80 mg/l), и високо осетљиви на прохлораз-Mn
(Ec50 вредности мање од 3.00 mg/l).