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https://doi.org/10.1007/s10658-022-02599-3
Abstract Powdery mildew is one of the most important combination of both in four commercial fields at various
diseases that causes significant economic losses in melon. sampling times [30, 90 and 120 days after the first fungi-
Chemical fungicides and tolerant melon varieties, which cide application (DAFA)]. Both fungicide mixture
may reduce pathogen severity and encourage positive plant azoxystrobin + chlorothalonil and fungicide thiophanate-
responses, are viable techniques for controlling this disease. methyl reduced the disease index of powdery mildew on
The study objectives were to investigate the effectiveness melon varieties compared to the untreated control (disease
of contact fungicides, systemic fungicides and a index 1.70–2.13 and 0.83–1.75, respectively at 120
DAFA), reduced the disease severity (24.79–31.5% and
A. Rhouma (*) 19.06–21.88%, respectively at 120 DAFA) and the per-
Regional Centre of Agricultural Research of Sidi Bouzid, CRRA, centage of leaf area covered by powdery mildew (27–
Gafsa Road Km 6, B.P. 357, 9100 Sidi Bouzid, Tunisia 43.75% and 8.25–39%, respectively at 120 DAFA). Fur-
e-mail: abdelhak.rhouma@gmail.com
thermore, melon plants treated with azoxystrobin +
M. S. Mehaoua chlorothalonil showed a larger yield increase (63.31–
Laboratory of Genetics, Biotechnology and Valorization of 71.40%), polar (15.43–17.59 cm) and equatorial (24.71–
Bio-resources, Department of Agronomic Sciences, University of 29.61 cm) diameter, yield (2.23–3.18 fruits number/plant;
Biskra, Biskra, Algeria
27.67–52.22 t/ha) and mean weight (2411.25–3289.5 g).
Azoxystrobin + chlorothalonil and thiophanate-methyl not
I. Mougou only reduced the disease index and disease severity index,
Higher Agronomic Institute of Chott Mariem Sousse, University but also promoted a yield increase of all melon varieties.
of Sousse, Sousse, Tunisia
More attention should be given to the effectiveness of
chemical fungicide control in view of expected climate
H. Rhouma changes. But fungicides continuous application following
Faculty of Science of Gabes, University of Gabes, Gabes, Tunisia a fixed schedule is unsustainable and could lead to high
resistance development in PM fungi.
K. K. Shah
Institute of Agriculture and Animal Science, Gokuleshwor Keywords Azoxystrobin . Chlorothalonil . Melon
College, Tribhuvan University, Baitadi, Nepal varieties . Powdery mildew . Thiophanate-methyl
H. Bedjaoui Introduction
Laboratory of Promotion of Innovation of Agriculture in Arid
Regions, Department of Agronomic Sciences, University of
Biskra, Biskra, Algeria Powdery mildew is a devastating disease that affects melon
production and fruit quality in both fields and greenhouse
190 Eur J Plant Pathol (2023) 165:189–201
environments (Saharan et al., 2019). This disease is caused severity were observed for several varietal resistance-
by two fungal species: Podosphaera xanthii (syn. fungicide application combinations. Casey Barickman
Sphaerotheca fuliginea) and Golovinomyces et al. (2017) found that pumpkin cultivar Mustang treated
cichoracearum (syn. Erysiphe cichoracearum) (Cohen with chlorothalonil and azoxystrobin had less disease
et al., 2004; Howlader et al., 2020). Romdhani and El severity and greater fruit yield. Aly et al. (2021) observed
Mahjoub (1991) showed that P. xanthii (syn. that foliar treatment of flax (Sakha 3, Sakha 4, Giza 10
S. fuliginea) was the causal agent of powdery mildew and Istro cultivars) with boscalid and pyraclostrobin
on melon and some other cucurbits in Tunisia. Their against powdery mildew reduced disease incidence and
identification was based on the occurrence of fibrosin increased straw and seed yield.
bodies in conidia. Powdery mildew is known for its For the successful control of powdery mildew, an
flour-like powder that coats the leaves of infected plants integrated program comprising the above-mentioned
as a result of fungal sporulation. The infection begins management strategies represents the ideal approach.
with white patches on the lower surface of the leaf, then The objectives of the present work were to assess the
advance to the upper side of the leaf eventually covering efficiency of contact, systemic and a combination of
the whole surface, causing the browning and wrinkling both contact and systemic fungicides currently regis-
of leaves and leaf death (Cohen et al., 2004; Rhouma tered against cucurbit powdery mildew, to evaluate the
et al., 2021a). Powdery mildew may grow in practically effect of fungicide treatments on morpho-productive
every season due to favorable weather conditions. The characters of melon varieties, and to determine the re-
infection may be exacerbated by hot to humid circum- sistance level of these treatments towards powdery mil-
stances, but it can also occur in dry weather (Baiswar dew under field conditions.
et al., 2015; Lebeda et al., 2016).
Cucurbit powdery mildew is a serious production
problem in many areas of the world, and fungicides Materials and methods
are a key tool for its control (Matheron & Porchas,
2013). Keinath and DuBose (2004) found that pow- Study area
dery mildew decreased non-treated watermelon yields
by 34% compared to fungicide-treated plants. Most All commercial field trials were conducted in Chott Sidi
systemic fungicides or those with translaminar activ- Abdel Salam oasis, southeastern Tunisia. The Chott Sidi
ity have a site specific mechanism of action (Naidu Abdel Salam oasis with an area of approximately 100 ha
et al., 2012). Along with its fast absorption and strong is located in in the East part of the Gabes Governorate
translaminar action, strobilurin and thiophanate- (Medina Gabes 33°89′ to 33°91’N and 10°10′ to 10°11′
methyl are recommended for the management of cu- E). The oasis has a predominantly arid Mediterranean
curbit powdery mildew (Bhat et al., 2018; Yousaf climate with a dry season lasting from June to August
et al., 2020; Jung et al., 2020). and characterized by a hot climate with an average
In several pathosystems, integration of resistant varie- annual temperature of 21.4 °C recorded in 2020
ties and fungicide application has been advocated as an (Rhouma et al., 2020). Rhouma et al. (2020) found that
alternative sustainable strategy for the control of cucurbit the monthly air temperature in Gabes for the period
powdery mildew (Fondevilla & Rubiales, 2012). Genetic 1979–2018 show changes characterized by a decreasing
selection programs in several countries have resulted in temperature from October to March followed by an
the release of numerous varieties resistant to powdery increasing temperature starting from March. Precipita-
mildew (Vielba-Fernández et al., 2020). Multiple resis- tion is scanty, with the greatest rainfall occurring in
tance genes have been reported in different melon varie- November and March. Rain occurs only rarely during
ties (Charentais, Galia, Afamia, etc.) which increase their the dry season (June to August). Over the years, precip-
resistance to powdery mildew (McCreight, 2006). Cohen itation levels in this oasis have shown a highly erratic
et al. (2004), and Howlader et al. (2020) noted that 43 pattern in which relatively moist years with more than
genotypes reacted as resistant to P. xanthii (Pobeditel, 400 mm (1990, 1994, 1995 and 2006) of rain alternate
Georgia and Neon, etc.), while 19 melon genotypes were with dry years in which less than 100 mm (2016 and
susceptible (GL329, Delicious 51 US and BK/1–5-5, 2018) of precipitation are observed. With a negative
etc.). An increase in fruit yield and a decrease in disease water balance, drought conditions are a dominant
Eur J Plant Pathol (2023) 165:189–201 191
feature of the climate (Rhouma et al., 2020). The soils (stage 7), fruit and seed maturation (stage 8) and ending
are gypsiferous and saline with a sandy texture (Rhouma with senescence (stage 9) (Lancashire et al., 1991;
et al., 2019; Rhouma et al., 2021b). Jacinto et al., 2022).
Table 1 Local name, hybrid or local variety, resistance to powdery mildew and fungicides application timings of the different melon
varieties used in this research
Abbreviation Local name Hybrid or local variety Resistance to powdery mildew Fungicides application timings
NT not available
Statistical analysis last sample, all varieties showed a small disease index
values after several applications of thiophanate-methyl
Statistical analysis was performed using the mean on the varieties Mekkaoui and Galia. While the highest
values of the replicates. The data were analyzed by disease indexes were registered for untreated control
ANOVA using SPSS version 20.0 statistical software plots for all four varieties (Table 3). Thiophanate-meth-
(SPSS, SAS Institute, USA). Homogeneity of variances yl was significantly more effective in reducing the
and normality were checked by applying Duncan’s powdery mildew index at 120 days after the first
Multiple Range Test. Differences between treatments treatment than the other treatments. However the
were determined by Duncan’s Multiple Range Test. plots treated with sulfur showed the highest DI for
All statistical tests were performed with a significance varieties Galia and Calipso. It is worth noting that on
level of 5% (P ≤ 0.05). the variety Mekkaoui both the lowest (for the plots
treated with thiophanate-methyl) and the highest (for
the untreated plots) disease indexes were observed
Results (Table 3). Statistical analysis showed a highly signif-
icant difference (P < 0.01) between both sample periods
The evaluation of fungicide effectiveness in controlling and fungicides treatments. The ANOVA classified the
powdery mildew on four melon varieties treated with two fungicides, azoxystrobin + chlorothalonil and
fungicides showed that the powdery mildew disease thiophanate-methyl into the same homogeneous group
indexes were significantly lower compared to the un- for the different samples of the four varieties in compar-
treated control plots (Table 3). For the first sample (30 ison with untreated plots and plots treated with sulfur. In
DAFA), the lowest disease indexes (DI) were observed the same sense, interactions occurred between melon
in Mekkaoui, Calipso and Galia plots using thiophanate- variety and fungicide treatment and also between sam-
methyl and in plots cultivated with variety Lobnani and ple moments and fungicide treatment (Table 3).
treated with azoxystrobin + chlorothalonil. During the ANOVA showed significant differences (P < 0.01)
second sample (90 DAFA), the lowest DI were obtained in the disease severity index (DSI) observed between the
from the varieties Makkaoui and Calipso treated with treated and control plots, for each variety at each sam-
thiophanate-methyl and for the varieties Lobnani and ple (Table 4). All fungicide applications significantly
Galia treated with azoxystrobin + chlorothalonil. For the (P < 0.01) decreased the powdery mildew disease
Table 2 Fungicides evaluated to control powdery mildew on melon plant under field condition
Abbreviation Trade name Active ingredient Chemical families Action Formulation Product rate
(recommended dose)
Block 1
V1xT1 V1xT2 V1xT3 V1xT0
V2xT1 V2xT2 V2xT3 V2xT0
V3xT1 V3xT2 V3xT3 V3xT0
V4xT1 V4xT2 V4xT3 V4xT0
Block 2
V1xT2 V2xT2 V2xT0 V2xT1
V3xT0 V4xT1 V1xT1 V3xT3
V4xT2 V4xT3 V3xT2 V3xT1
V1xT0 V2xT3 V4xT0 V1xT3
Block 3
V4xT0 V3xT1 V3xT3 V4xT3
V2xT2 V1xT1 V3xT0 V2xT0
V3xT2 V1xT2 V4xT2 V1xT3
V2xT1 V1xT0 V4xT1 V2xT3
V2xT3
5m
0.8 m
0.5 m
3m
Melon plant
Fig. 1 Field layout for a randomized complete block design with fungicides (T0 = Untreated control; T1 = Azoxystrobin +
four melon varieties (V1 = Calipso; V2 = Galia; V3 = Lobnani; chlorothalonil; T2 = Sulfur; T3 = Thiophanate-methyl)
V4 = Mekkaoui) each treated separately with three commercial
severity index. The three samples showed a signifi- The applications of azoxystrobin + chlorothalonil
cant reduction of the disease severity index on the and thiophanate-methyl reduced the percentages of the
four melon varieties treated with thiophanate-methyl, leaf area covered by powdery mildew (Table 5).
followed by azoxystrobin + chlorothalonil. Data pre- Thiophanate-methyl was more effective on the variety
sented in Table 4 show that the lowest severity Mekkaoui than on the other varieties. This variety
indexes were recorded for the variety Calipso treated proved to be the most sensitive having the highest
with thiophanate-methyl followed by the variety percentage of the leaf area infected by powdery mildew
Mekkaoui. Taking into account the disease severity in the control plots. The lowest percentage of PLA
index recorded on different varieties it appears that (2.5%) was also observed at the first sampling moment
the repeated applications of thiophanate-methyl were (30 DAFA) in plots cultivated with the variety Calipso
more effective than other treatments. Sulfur was the and treated with azoxystrobin + chlorothalonil fungi-
least effective (Table 4). cide. Statistical analysis revealed a high significant dif-
The effectiveness of the treatment using fungicides ference (P < 0.01) between melon varieties (MV),
and melon varieties was variable (Table 4). The treat- fungicide treatments (FT), sampling moments (SM),
ment with thiophanate-methyl revealed its ability to and their interactions (MV*FT and SM*FT) for the
protect the four melon varieties against powdery mildew PLA (Table 5).
at different sample times. The same results were obtain- Our results showed that the number of fruits per plant
ed after several treatments with azoxystrobin + increased significantly (P < 0.01) after applications with
chlorothalonil on plots cultivated with the variety Galia. thiophanate-methyl and azoxystrobin + chlorothalonil.
However all treatments using sulfur have shown their According to Table 6, the highest number of fruits per
ineffectiveness in reducing powdery mildew attacks at plant was recorded on the variety Lobnani treated with
all samples. Thus all the control plots were highly sen- azoxystrobin + chlorothalonil followed by the variety
sitive to powdery mildew (Table 4). Galia (Table 6). Foliar treatment with azoxystrobin +
194 Eur J Plant Pathol (2023) 165:189–201
Table 3 Effect of fungicide treatments on disease index in four melon varieties grown in open field conditions at different samples (30, 90
and 120 days after the first fungicide application)
chlorothalonil and thiophanate-methyl significantly en- The different measurements carried out on the fruits
hanced melon yield (P < 0.01) in comparison with revealed that the largest polar diameters of melon fruits
untreated control and sulfur. The highest percentages of were obtained on the variety Mekkaoui, varieties Galia
yield increase were recorded on all varieties treated with and Calipso treated with azoxystrobin + chlorothalonil
azoxystrobin + chlorothalonil (Table 6). The same was and on Lobnani treated with thiophanate-methyl.
observed for fruit weight with a highly significant differ- Whereas, the largest equatorial fruit diameters were
ence between the four varieties (Table 6). obtained in all plots subjected to several applications
Eur J Plant Pathol (2023) 165:189–201 195
Table 4 Effect of fungicide treatments on disease severity index and resistance level in four melon varieties grown in open field conditions
at different samples (30, 90 and 120 days after the first fungicide application)
Table 5 Effect of fungicide treatments on percentage of leaf area covered by powdery mildew in four melon varieties grown in open field
conditions at different sampling moments (30, 90 and 120 days after the first fungicide application)
Table 6 Effect of fungicide treatments on morpho-productive and qualitative characters in four melon varieties grown in open field
conditions
mopho-production characteristics in comparison to the effective than all other non-conventional treatments
untreated control. Our results supported those of (Candido et al., 2014).
Matheron and Porchas (2008) who found that fungicide Both azoxystrobin + chlorothalonil and thiophanate-
treatments of melon varieties reduce the percentage of methyl controlled the disease index comparing to the
leaf area covered by powdery mildew compared to untreated plots by 70–90%. Our results are close to
untreated control. Conventional fungicides were more those obtained by Matheron and Porchas (2008), who
198 Eur J Plant Pathol (2023) 165:189–201
gave an average reduction of disease index of 90% in is therefore necessary to delay the development of pow-
experiments on cantaloupe treated by fungicides such as dery mildew (Keinath & DuBose, 2004).
azoxystrobin, chlorothalonil, sulfur and thiophanate- In cucumber plants, Anand et al. (2007) confirmed
methyl. The same authors confirmed a maximal reduc- that azoxystrobin increased the activity of defense en-
tion of the disease severity index of powdery mildew on zymes such as peroxidase, polyphenol oxidase, phenyl-
cantaloupe by 69.5 and 44.2% after spraying of alanine ammonia lyase and chitinase. Furthermore,
azoxystrobin and thiophanate-methyl, respectively thiophanate-methyl treatment increased peroxydase ac-
(Matheron & Porchas, 2013). tivity and the total phenolic contains (El-Wahab et al.,
Leaf application on cucumber plants with thiophanate- 2016). They also reported that the reduction in the
methyl, reduced significantly the severity index of pow- disease severity index was positively correlated to
dery mildew significantly compared to non treated plants peroxydase activity and the total phenolic content. All
(El-Wahab et al., 2016) and mango cultivars (Nasir et al., these pieces of evidence agree with the effectiveness of
2017b). These results are in agreement with our data after the two fungicides in the control of melon powdery
the application with thiophanate-methyl. Preventive mildew in the present study. Thiophanate-methyl ap-
sprays of thiophanate-methyl against powdery mildew pears to have an active role, possibly as a signal to
of apple showed a reduction of 76.88% of disease. When induce defense reactions (Fawe et al., 1998).
applied curatively, the treatment led to a reduction of The low efficacy of sulfur observed in this study is
68.51% (Nasir et al., 2017a). As a broad-spectrum fun- probably due to the long-time interval between treat-
gicide, thiophanate-methyl acts as a contact and as a ments (15 days) which enable powdery mildew spores
systemic fungicide. It binds with ß-tubulin and prevents to germinate and aggravate disease proliferation. In tests
the production of microtubules during cell division (ß- aiming to control melon powdery mildew using sulfur
tubulin assembly in mitosis). This action will lead to a applications, Abo Ogiela and El-Shoraky (2020) found
morphological alteration of the fungal hyphae (Vielba- a high efficacy whatever the applied sulfur dose. The
Fernández et al., 2020). studies of Konstantinidou-Doltsinis and Schmit (1998),
The use of azoxystrobin against powdery mildew and Keinath and Dubose (2012) found that the applica-
of cucumber by Anand et al. (2008) showed that this tion of sulfur on cucurbit plants infected with powdery
fungicide stopped disease progression successfully. mildew significantly reduces the average percentage of
Similarly, Anesiadis et al. (2003) found that leave area covered by powdery mildew. In addition,
azoxystrobin gave an excellent protection against Abo Ogiela and El-Shoraky (2020), reported that fungi-
both Cercospora leaf-spot and powdery mildew of cides containing sulfur, thiophanate-methyl could re-
sugar beet. El-Mougy et al. (2014) found a very low duce up to 90% the powdery mildew in tree apples.
disease severity index after four applications of Sulphur is a natural mineral substance often used as a
azoxystrobin in association with difenoconazole on fungicide in organic farming. It acts by contact and
cantaloupe. On the other hand, on pumpkin, the vapor on the respiratory system of the fungus and pre-
combination of the fungicides chlorothalonil and vents fungal spores from germinating (Cohen et al.,
difenconazole reduced powdery mildew incidence 2004).
by 60% (Maryam et al., 2020). While, on apple trees The current results revealed that the powdery mildew
Abo Ogiela and El-Shoraky (2020) found that the treatments affected all productivity parameters of the
application of azoxystrobin and metalaxy-m four melon varieties. The variety factor determined sig-
inhibited powdery mildew completely. These results nificant changes in quantitative yield parameters. How-
show that fungicides containing strobilurins reduce ever, it is clear that the highest morpho-productive traits
the powdery mildew severity index considerably (average number of fruits per plant, average yield per
(Keinath & DuBose, 2004). hectare, percentage yield increase and average fruit
In this present study, the efficacy of azoxystrobin + weight) were recorded in the plots treated with
chlorothalonil and thiophanate-methyl fungicides to azoxystrobin + chlorothalonil. From our comparison of
powdery mildew on melon varieties is probably due to the three applied fungicides and taking into account the
their systemic and translaminar action, which ensure a considerable variation in their effectiveness and in the
long protection of the leaves that emerge after the appli- varietal sensitivity, it appears that the two fungicides to
cation of the fungicides. The use of systemic fungicides be recommended against melon powdery mildew in
Eur J Plant Pathol (2023) 165:189–201 199
Tunisia are azoxystrobin + chlorothalonil and Ethics approval and consent to participate Not applicable.
thiophanate-methyl. Indeed, according to our findings,
Consent for publication Not applicable.
we found a very valuable reduction of more than 90% of
the disease severity index and a more than 70% increase
Conflict of interest The authors declare that they have no con-
in yield. Our results are comparable to Candido et al. flict of interest.
(2014). Many studies highlights the effect of powdery
mildew on the primary metabolism in different crops by
reducing the green leaf area and the contents of chloro-
phyll in infected parts (Swarbrick et al., 2006). As a
result of the reduction in organic matter synthesis and References
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