Journal of Phytopathology and Pest Management 8(1): 106-116, 2021
pISSN:2356-8577 eISSN: 2356-6507
Journal homepage: http://ppmj.net/
∗Corresponding author: Mansour M. El-Fawy,
E-mail:
mansour_mazen@hotmail.com
106
Copyright © 2021
Utilizing certain disinfectants as alternatives to fungicides
to manage
Macrophomina
root rot in sugar beet
Ayman S. Saeed1, Rabee A. Emam2, Mansour M. El-Fawy1*
1Agricultural Botany Department, Plant Pathology Branch, Faculty of Agriculture, Al-Azhar University
(Assiut Branch), Assiut 71524, Egypt
2Plant Protection Department, Faculty of Agriculture, Al-Azhar University (Assiut Branch), Assiut, Egypt
Abstract
Keywords: Beta vulgaris, Macrophomina phaseolina, root rot, disinfectants, total soluble solids, sugar percent.
This study aimed to determine the fungicidal effects of certain disinfectants, namely hydrogen peroxide
(H2O2), n-alkyldimethylbenzylammonium chloride (n-ADBAC), and potassium permanganate (KMnO₄), on
M. phaseolina, the causal pathogen of root rot in sugar beet (Beta vulgaris L.), in vitro and under greenhouse
conditions. Mycelial growth of the pathogen was inhibited with different concentrations (0.00, 100, 200, 400,
and 600 ppm) of the tested compounds. KMnO₄ at 600 ppm was the most effective in inhibiting the growth
of the pathogen (77.41%) when compared to other treatments. In greenhouse tests, treating pathogen-
infested soil with these disinfectants reduced the disease severity of Macrophomina root rot in sugar beet.
The highest reduction in disease severity was achieved with 600 ppm KMnO4. In addition, all treatments
improved root agronomic characteristics, such as total soluble solids (TSS) and sugar percentage. These
findings suggest that these disinfectants could serve as promising alternatives to traditional fungicides for
managing Macrophomina root rot in sugar beet.
Saeed et al., 2021
107
1. Introduction
Sugar beet (Beta vulgaris L.) belongs to the
Chenopodiaceae family and has a high sucrose
concentration, which is used for sugar
production (Zicari et al., 2019). Sugar
extracted from sugarcane and sugar beet is
used as a sweetener in domestic food and as an
ingredient in the food industry for sweet-
flavored substances. Sugar is mainly referred
to as sucrose and, to some extent, as glucose
and fructose (Duraisam et al. 2017).
Macrophomina phaseolina is a soil-borne,
necrotrophic pathogen present worldwide that
affects more than 500 plant species (Abass et
al., 2021; Marquez et al., 2021; Babu et al.,
2007). M. phaseolina is a facultative
saprophyte that survives in the soil through the
formation of microsclerotia, which are
pseudoparenchymatous tissue masses resistant
to adverse environmental conditions (Shaner et
al., 1999). Disinfectants are of great
importance in eliminating microbes in various
applications. Hydrogen peroxide (H2O2) is
used for surface sterilization and is highly
effective at inhibiting microbes. All H2O2
concentrations significantly reduced the linear
growth of all the tested fungi. However, a 2%
concentration completely inhibited the growth
of Rhizoctonia solani, Pythium sp., and
Fusarium solani (Ali, 2018). H2O2 participates
in many resistance mechanisms, including
reinforcement of the plant cell wall,
phytoalexin production, and enhancement of
resistance to various stresses (Quan et al.,
2008). It can also be used to control plant
diseases, such as root rot and wilt disease in
thyme (Ali, 2018) and alfalfa rust disease
(Abdel-Monaim et al., 2012). Kyeong-Hwan et
al. (2014) utilized hydrogen peroxide vapor in
the agricultural field to inhibit the growth of
pathogenic microorganisms. This was due to
the fact that hydrogen peroxide could enter the
microbial interior and react with lipid double
bonds in the cell wall, affecting proteins,
lipids, and polysaccharides, changing cell
permeability, and ultimately causing cell lysis
and death (McDonell and Russell, 2001).
However, multiple studies have demonstrated
the significance of H2O2 in promoting plant
growth and increasing productivity
(Khandaker et al., 2012). Orabi et al. (2015)
stated that a lower level of treatment with H2O2
can have a significant positive effect on plant
growth, growth regulators, antioxidant
enzyme activity, fruit yield and quality of
tomato. Quaternary ammonium compounds
(QACs) are surfactants that penetrate the
membranes of microorganisms, destroying
proteins and nucleic acids, and leading to cell
death (Gerba, 2015). Numerous studies have
reported the effectiveness of QACs in
controlling bacterial, fungal, and viral plant
diseases (Bennett et al., 2011; Strobel, 2006;
Tubajika, 2006). Among QACs, n-ADBAC is
well-known for its strong antibacterial and
antifungal properties (Oblak et al., 2013; Ohta
et al., 2008). The textile industry has also
utilized it as an antibacterial agent or
insecticide (Kim and Sun, 2001). Studies have
demonstrated that BAC, a potent bactericidal
and fungicidal agent, reduces the size of
organisms in multi-dose containers (Noecker
and Miller, 2011). However, Izquierdo-García
et al. (2021) and Nguyen et al. (2019) utilized
a 1:100 dilution to completely prevent the
survival of all F. oxysporum f. sp. cubense
propagules over the length of all contact times,
whether or not soil was present. QAC products
have been reported to be effective against
fungal plant pathogens (Bika et al., 2021;
Baysal-Gurel et al., 2015). In a similar study,
Tubajika (2006) showed that the colony
diameter and mycelial dry weight of
Physalospora vaccinii were reduced at 1,000
ppm ADBAC in in vitro growth tests.
Potassium permanganate (KMnO₄) is a
powerful oxidizing agent that can be used to
Saeed et al., 2021
108
control plant diseases (Goutam and Bajpai,
2019). It acts as a disinfectant and fungicide,
helping to eliminate pathogens such as fungi
and bacteria. It is used for seed treatment, soil
disinfection, and to control diseases such as
damping-off, powdery mildew, and wilt in
various crops (Sanchez-Saldana and Saenz,
2002). It can also be used as a fungicide to
control a wide range of fungal infections
(Goutam and Bajpai, 2019). Additionally, it
can help reduce disease pressure and promote
healthy root development in plants. This study
aimed to determine the fungicidal effects of
certain disinfectants, that is, hydrogen
peroxide, n-alkyldimethylbenzylammonium
chloride, and potassium permanganate, on M.
phaseolina, the causal pathogen of root rot in
sugar beet, in vitro and under greenhouse
experiments. In addition, the impact of these
treatments on yield parameters, such as total
soluble solids (TSS) and sugar percentage, was
investigated.
2. Materials and methods
2.1 Isolation and identification of the causal
pathogen
Samples of naturally infected sugar beet plants
were collected from various locations within
the Assiut and El-Behera governorates in
Egypt. Additionally, the collar portion of the
infected plants was cut into 3-5 mm thick tissue
sections, sterilized with 1% sodium hypochlorite
solution for two minutes, rinsed thrice in
sterilized distilled water, and dried on
sterilized filter paper at room temperature. The
developing hyphae were examined under a
microscope at low magnification for typical
hyphal growth of M. phaseolina and incubated
at 25°C for 15 days. The purified fungi were
identified based on their morphological and
microscopic characteristics, as described by
Sneh et al. (1991). Hyphal tips were
transferred to PDA medium. Hyphal-tipped
isolates identified as M. phaseolina were
transferred to PDA slants and stored for further
studies.
2.2 Pathogenicity assay
2.2.1 Inoculum production
Barley medium (75 g barley, 25 g clean sand,
2 g sucrose, 0.1 g yeast, and 100 ml distilled
water) was used in the experiments. The barley
medium was autoclaved for 20 min at 121°C
on two separate days (Imran et al., 2021). M.
phaseolina isolates were grown on potato
dextrose agar (PDA) for 7 days. Each barley
medium bottle was inoculated with two plugs
(5 mm diameter) taken from the margin of a 1-
week-old culture of the isolates grown on PDA
medium in Petri dish. The bottles were then
incubated at 25°C in the dark for two weeks.
2.2.2 Plant material and inoculation
Sand clay soil and plastic pots (30 cm Ø) were
sterilized with a 5% formaldehyde solution
and allowed to dry. Inoculum of each pathogen
isolate was added to the soil in pots at 1%
(w/w), one week before sowing (1 g
inoculum/100 g soil), mixed well, and
thoroughly irrigated. Three Pleno cultivar
sugar beet seeds were sown in each pot. Three
replicates were used for each isolate. Pots
containing non-infested soil mixed with 1%
barley grain medium were used as controls.
The Agricultural Botany Department, Plant
Pathology Branch, Faculty of Agriculture, Al-
Azhar University (Assiut Branch), Assiut,
Egypt, conducted the experiment in a
greenhouse during the 2018/2019 growing
season. The pots were irrigated and fertilized
regularly in a greenhouse. Disease severity
was recorded 120 days after sowing.
Saeed et al., 2021
109
2.2.3 Assessment of root-rot severity
The severity of infection by root rot was
assessed using the devised 0-7 scale by
Engelkes and Windels (1996) as follows: 0 =
No visible lesions, 1 = Arrested lesions at point
of inoculation, 2 = Less than 5% shallow, dry
rot canker, 3 = 5 to 24% deep, dry rot canker,
4 = 25 to 49% extensive rot, 5 = 50 to 89% rot
extensive into interior root, 6 = 90 to less than
100%, most dead foliage, 7 = 100% dead plants.
2.2.3 Source of disinfectants
Hydrogen peroxide (H2O2) and potassium
permanganate (KMnO4) were obtained from El
Nasr Pharmaceutical Chemicals Company,
Abu Zaabal, Egypt. The n-
alkyldimethylbenzylammonium chloride
product was purchased from United
Promotions, Inc. (Atlanta, USA).
2.4 Impacts of H2O2, n-ADBAC and KMnO4
on M. phaseolina mycelial growth
The effectiveness of H2O2, n-ADBAC, and
KMnO4 at various concentrations (0.00, 100,
200, 400, and 600 ppm) on the mycelial growth
of the pathogen was assessed in vitro. The
concentrations were added to the PDA
medium. 8-mm plugs of M. phaseolina culture
grown on PDA plates were placed in the
middle of PDA plates with the added
compounds. Three replicate Petri dishes were
used for each concentration. PDA Petri dishes
without treatment served as controls. After a 7-
day incubation period, the colony diameter of
each plate was measured. The average length
of the longest and shortest diameters was used
to calculate the colony diameter. The following
formula was used to determine the inhibition
of mycelial growth: [(control radial growth –
disinfectant-amended radial growth)/control
radial growth] × 100.
2.5 Impact of H2O2, n-ADBAC and KMnO4
soil treatments on managing root rot
diseases under greenhouse conditions
The experiment was conducted during the
2019/2020 and 2020/2021 seasons at the Plant
Pathology Branch of the Agricultural Botany
Department at Al-Azhar University (Assiut
Branch), Assiut, Egypt. M. phaseolina inocula
were prepared and added to the soil, as
mentioned before. Three Peleno sugar beet
seeds were planted in sterile soil. One month
after planting, each tested compound at a
concentration of 600 ppm was added as a soil
drenching. The treatments were applied twice
at four-week intervals. The fungicide Double
56% {(Hymexazol 16% WP (W/W);
Thiophanate Methyl 40% WP (W/W)}
obtained from Shora Company for
Agricultural Chemicals, Egypt, was applied at
a concentration of 1 g/l water. The treatment
with these compounds was repeated 90 days
after the initial treatment. Control was
achieved by planting sugar beet seeds in
infected soil without treatment. Three pots
were used as replicates for each treatment. As
mentioned earlier, disease severity was
calculated 120 days after planting. A hand
refractometer was used to measure the T.S.S.
percentage in the juice of fresh roots. Sugar
content was measured at the sugar factory
laboratory (Nobaryia Sugar Refining
Company) using the standard polarimetric
method described by Schneider et al. (2002).
2.6 Statistical analysis
MSTAT-C (1991) version 2.10 was used for
all statistical analyses. The data were analyzed
using one-way analysis. The results are
presented as the mean and standard deviation
(mean ± SD), and all measurements were
performed in triplicate. The means were
compared using Bartlett's test. The statistical
Saeed et al., 2021
110
significance threshold was set at P = 0.05
(Gomez and Gomez, 1984).
3. Results
3.1 Isolation and identification of the causal
pathogen
From diseased sugar beet plants (Figure 1A
and B) gathered from various locations in the
El-Behera and Assiut Governorates, 11 fungal
isolates of M. phaseolina were obtained: seven
and four isolates, respectively. The obtained
isolates were identified as M. phaseolina by
microscopic and cultural examinations. The
isolates were identified based on the
morphological and microscopic features of the
mycelium (Figure 1C).
Figure 1: (A) Symptoms of Macrophomina root rot disease on sugar beet root, (B) cross-section of sugar
beet root infected with M. phaseolina, and (C) mycelial growth of M. phaseolina on potato dextrose agar.
3.2 Pathogenicity test of M. phaseolina
isolates on sugar beet plants
All M. phaseolina isolates infected the sugar
beet cultivar and caused typical symptoms of
root rot disease, as shown in Figure (2). The
isolates tested for their ability to cause root rot
in sugar beet plants varied greatly in terms of
their disease severity. Isolate No. 8 (66.93%)
was responsible for the greatest percentage of
disease severity, followed by isolate No. 3
(58.43%) and No. 1 (52.56%). In comparison,
isolates No. 9 and No. 10 were the least likely
to cause infections (27.15 and 29.00%,
respectively), with isolate No. 6 coming in
following (34.44%). Based on the
aforementioned findings, isolate No. 8 was
used in subsequent tests.
3.3 Inhibitory effect of certain disinfectants
on M. phaseolina mycelial growth in vitro
The effects of H2O2, n-ADBAC, and KMnO4
on M. phaseolina mycelial growth were
assessed in vitro using PDA medium (Table
1). Compared to the control, the addition of all
tested compounds to the medium significantly
inhibited the growth of M. phaseolina.
Pathogen growth was most significantly
inhibited by the addition of KMnO4 at a 600
ppm concentration, which was followed by n-
ADBAC. In contrast, H2O2 reduced mycelial
growth the least. Furthermore, increasing the
concentration of these compounds gradually
increased the reduction in mycelial growth of
the pathogen, with higher concentrations being
more effective.
Saeed et al., 2021
111
Figure 2: (A) Pathogenicity tests of M. phaseolina isolates on sugar beet plants under greenhouse
conditions. The values are the mean ± standard deviation of three replicates. The same letters
following column values are not significant according to Bartlett's test (P ≤ 0.05).
Table 1: Effects of different H2O2, n-ADBAC, and KMnO4 concentrations on M. phaseolina
mycelial growth in vitro.
Concentration (ppm)
Growth inhibition (%)
H2O2
n-ADBAC
0 (control)
0.00±0.00a
0.00±0.00a
100
21.11±1.11b
24.81±1.70b
200
38.89±1.11c
44.07±0.64c
400
54.81±0.65d
58.89±1.11d
600
64.03±2.32e
68.52±3.21e
The values are the three replicates' mean ± standard deviation. The same letters following column values are not significant,
according to the Bartlett's test (P ≤ 0.05).
3.4 Impact of disinfectants compounds and
Double fungicide on sugar beet root rot caused
by M. phaseolina in greenhouse experiments
The results in Table (2) show that all the
disinfectant compounds tested and the double
fungicide significantly reduced the severity of
root rot in sugar beet plants caused by M.
phaseolina. The findings of this study showed
that compared to the control, the addition of
KMnO₄ resulted in the least disease severity
and the highest disease protection, with disease
severity percentages of 17.33±2.11 and
16.71±2.11 in the 2019/2020 and 2020/2021
seasons, respectively. Generally, the fungicide
Double 56% had the highest effect on
controlling the disease. In contrast, H₂O₂
resulted in the least reduction in disease
severity and disease protection, at 21.45±2.55
and 23.15±2.44% in both seasons. In addition,
the data revealed significant differences
among all treatments in the disease severity
percentage in both seasons.
3.5 Impacts of disinfectants compounds and
Double fungicide on TSS and sugar
percentage in sugar beet roots
All treatments, including H₂O₂, n-ADBAC,
and KMnO₄, increased TSS and sugar
percentage in the 2019–2020 and 2020–2021
seasons compared to the untreated control
Saeed et al., 2021
112
plants, as demonstrated by the results in Table
3. Data revealed that n-ADBAC recorded the
highest percentages of TSS and sugar in sugar
beet roots, which were 32.10±1.10 and
34.40±1.90 in both seasons, respectively. In
contrast, Double fungicide resulted in the
lowest values of TSS and sugar percentage,
which were 23.70±1.45 and 22.50±1.60 in
both seasons, respectively. The results indicate
that there are no significant differences
between H₂O₂ and n-ADBAC in their effects
on TSS. In addition, there were no significant
differences between n-ADBAC and KMnO₄ in
their effects on sugar content.
Table 2: Effects of H2O2, n-ADBAC, KMnO4 and Double fungicide on sugar beet root rot caused
by M. phaseolina in greenhouse trials.
Treatments
Season 2019/2020
Season 2020/2021
Disease severity (%)
Disease reduction (%)
Disease severity (%)
Disease reduction (%)
H2O2
21.45±2.55b
66.59
23.15±2.44b
59.01
n-ADBAC
17.33±2.11bc
73.01
20.32±1.88bc
64.02
KMnO4
14.07±1.99cd
78.09
16.71±2.11cd
70.41
Double 56%
10.18±2.22d
84.15
12.45±2.12d
77.96
Control
64.21±2.66a
-
56.48±3.11a
-
The values are the three replicates' mean ± standard deviation. The same letters following column values are not significant,
according to the Bartlett's test (P ≤ 0.05).
Table 3: Effects of KMnO4, n-ADBAC, H2O2, and double fungicide on the sugar and TSS content
of sugar beet roots.
Treatments
TSS (%)
Sugar (%)
Season 2019/2020
Season 2020/2021
Season 2019/2020
Season 2020/2021
H2O2
29.20±1.40a
31.30±3.15a
19.15±0.88a
18.51±1.33b
n-ADBAC
32.10±1.10.a
34.40±1.90a
20.31±0.77a
21.46±1.09a
KMnO4
25.40±1.30b
23.10±1.60b
20.07±0.88a
20.71±1.11a
Double 56%
23.70±1.45bc
22.50±1.60b
17.52±1.22b
18.24±1.44b
Control
22.00±1.80c
23.60±1.30b
15.61±1.11c
15.36±1.11c
The values are the three replicates' mean ± standard deviation. The same letters following column values are not significant,
according to the Bartlett's test (P ≤ 0.05)
4. Discussion
Sugar beet is cultivated for its high sucrose
content, making it a major source of sugar
production worldwide (Abou-Elwafa et al.,
2020). Root rot diseases in sugar beet can
cause significant yield loss, impacting both the
quantity and quality of the harvest (Harveson,
2007). These diseases can lead to reduced root
weight, lower sucrose content, and decreased
juice purity, ultimately affecting the
profitability of sugar beet production (El-
Mansoub et al., 2020). In this study, the
efficacy of H₂O₂, n-ADBAC, and KMnO₄
against root rot disease in sugar beet was
investigated in vitro and in greenhouse
experiments. The effects of H2O2, n-ADBAC,
and KMnO4 on M. phaseolina mycelial growth
were assessed in vitro. In comparison to the
control, each tested compound significantly
slowed growth when added to the medium. In
the current study, the data indicated that
KMnO4 had the strongest effect on the
pathogen at a concentration of 600 ppm
(77.41%), followed by n-ADBAC. These
results are consistent with Goutam and Bajpai
(2019), who showed that KMnO4 inhibited the
growth of fungi associated with mustard seeds
such as Aspergillus niger, Rhizopus
nigricansis, A. flavus, A. fumigates, and A.
Saeed et al., 2021
113
luchuansis compared to the control. KMnO4 is
a powerful oxidizing agent that alters the cell
walls of pathogenic microorganisms, interferes
with their DNA structure, and exerts effective
antimicrobial activity against protozoa, fungi,
bacteria, and viruses (Sanchez-Saldana and
Saenz, 2002). In a similar study, Tubajika
(2006) showed that the colony diameter and
mycelial dry weight of Physalospora vaccinii
were reduced at 1,000 ppm ADBAC in vitro
growth tests. Mild or no reduction in fungal
growth and mycelial dry weight was observed
at concentrations less than 100 ppm compared
to the control. H₂O₂ exhibited the lowest
inhibition of pathogen growth. Previous
studies have also shown that it can trigger the
plant's defense systems, such as increasing the
activity of enzymes such as chitinase and
peroxidase, leading to a significant increase in
lignin and suberin. Furthermore, Copes (2009)
noted that H2O2 is crucial for lignification and
strengthening of cell walls where pathogens
attack. QACs are cationic surfactants that
penetrate the cell membranes of microorganisms
(bacteria, fungi, and enveloped viruses),
destroying proteins and nucleic acids, and
causing cell lysis and death (Gerba, 2015;
McDonell, 2007). The results of this study
show that all the tested compounds and double
fungicide significantly reduced the severity of
root rot on sugar beet plants caused by M.
phaseolina. The findings of this study showed
that the addition of KMnO₄ resulted in the
lowest disease severity and the highest disease
protection compared to the control. These
findings align with those of previous studies by
Goutam and Bajpai (2019), who suggested the
possible application of KMnO4 as a
disinfectant for mustard seeds to reduce seed
fungal infection. Generally, the fungicide
Double 56% had the highest effect in
controlling the disease. Similar results with
two QACs disinfectants showed 100% biocide
activity against F. oxysporum f. sp. cubense
TR4 microconidia in the absence of soil but at
different exposure times of 5, 10, and 15 min.
(Nel et al., 2007). In another study, the use of
QACs showed high efficacy against spores of
the cotton pathogen F. oxysporum f. sp.
vasifectum (Bennett et al., 2011). Also, using
H₂O₂ to successfully combat certain plant
diseases, such as wilting tomato plant disease
(Ojha and Chatterjee, 2012), chickpeas
(Sarwa et al., 2005), root and stalk rot disease
of cucumber caused by the pathogenic fungus
F. oxysporum f. sp. radices cucumerinum
(Yousefi et al., 2012), and blight in wheat
caused by the fungal pathogen F.
graminearum (Fe-Qi et al., 2012). In
comparison to the control plants, the results
indicated that all treatments (H₂O₂, n-ADBAC,
and KMnO₄) improved sugar beet agronomic
traits, including TSS and sugar percentage, in
both seasons. The highest percentages of TSS
and sugar in roots were found in n-ADBAC.
These results were consistent with those of
Leilah and Khan (2005), who found that the
application of plant growth retardants, such as
quaternary ammonium salts, affected the sugar
percentage and root yield more than the
control. However, the TSS and sugar
percentage were the lowest in the double
fungicide treatment. Mostafa (2021) observed
that the application of 20 mM H2O2 treatment
significantly increased the content of
carotenoids, phenol, and total sugar. Yield,
productivity, and fruit quality of mangoes
under field conditions. Duman et al. (2013)
observed that fruit thickness, titratable acidity
(TA), and flesh color were considerably
affected by all hydrogen peroxide applications.
5. Conclusion
Considering the previous results, it seems
pertinent to indicate that the application of
H₂O₂, n-ADBAC, and KMnO₄ was beneficial
for reducing Macrophomina root rot in sugar
Saeed et al., 2021
114
beet under greenhouse conditions. Moreover,
these treatments increased the TSS and sugar
percentage in the roots. Based on our results,
we conclude that these treatments can be a
good alternative to fungicides.
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