Journal of Agricultural Science and Practice

Volume 3. Page 38-45
Published 20th April, 2018
ISSN 2536-7072

Full Length Research

Effectiveness of systemic and contact fungicides against Alternaria citri the causal organism of citrus brown spot disease in citrus mangroves of Pakistan

Muhammad Farooq1*, Naila Ilyas2, Moses Kwaku Golly3*, Bakhshah Zib4, Ismail khan4, Shoaib Khan5, Iltaf Khan6, Muhammad Bakhtiar7 and Nabeela Ilyas8

1Institute of Food Science and Technology, Sindh Agriculture University, Tando Jam, Pakistan.
2Department of Plant Pathology, Bahauddin Zakariya University, Multan, Pakistan.
3Faculty of Applied Sciences and Technology, Sunyani Technical University, Sunyani, Ghana.
4Department of Agronomy, University of Agriculture Faisalabad, Pakistan.
5Department of Horticulture, The University of Agriculture Peshawar, Pakistan.
6Department of Chemistry, Abdul Wali Khan University Mardan, Pakistan.
7Department of Agronomy, University of Agriculture Peshawar, Pakistan.
8Department of Environmental Sciences, Bahauddin Zakariya University, Multan, Pakistan.

Received 26th March, 2018; Accepted 16th April, 2018

*Correspondence: Dr. Muhammad Farooq and Dr. Moses Kwaku Golly, Institute of Food Science and Technology, Sindh Agriculture University, Tando Jam, Pakistan; and Faculty of Applied Sciences and Technology, Sunyani Technical University, Sunyani, Ghana. Email:,

Copyright © 2018 Farooq et al. This article remains permanently open access under the terms of the Creative Commons Attribution License 4.0, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


Brown spot of citrus caused by Alternaria citri is among several diseases responsible for low crop production in Pakistan. Hence, the present study provides new information about the selection of chemicals for control of citrus brown spot in Pakistan. A. citri was isolated from different diseased samples of citrus plant collected from different orchards of Punjab Province of Pakistan. In vitro efficacy of fungicides was checked against A. citri. Fungicides viz; Thiophenate methyl, Difenoconazole, hexaconazole, Metalaxyl + Mancozeb, Metiram, Mancozeb, Azoxystrobin, Dodine, Chlorothalonil, Fosetyl aluminium were evaluated against tested fungus at various concentrations (25, 50, 100, 200 and 400 ppm) by using poisoned food technique. The results showed that majority of the fungicides exhibited their highest inhibitory activity at a concentration of 400 ppm. Fosetyl aluminium, Metiram, Thiophenate methyl, Mancozeb and Metalaxyl + Mancozeb all exhibited maximum inhibitory mycelial growth of A. citri with 49.55, 52.96, 65.57, 84.86 and 100% inhibtion, respectively at a concentration of 400 ppm whereas, a combination of Azoxystrobin and Difenoconazole exhibited maximum inhibitory mycelial growth of A. citri up to 94.95% at fungicide concentration of 300 ppm. Cholorthalonil, Hexaconazole, Dodine, and Difenoconazole were the most effective in inhibiting A. citri as no mycelial growth was observed at all concentrations and as such they produced 100% decreased in mycelia growth over the control. The study concluded that Fosetyl aluminium was the least effective fungicide against A. citric. The present study provides new information on the selection of chemicals for control of citrus brown spot in Pakistan.

Key words: Chemical control, disease incidence, disease severity, inhibition, mycelia growth.


Citrus (Citrus sinensis) is an important horticultural crop in Pakistan contributing significantly to the Gross Domestic Products (GDP) and foreign exchange earnings for the nation (Haleem et al., 2005). Pakistan ranks 12th worldwide in terms of citrus production with cultivation estimated to cover an area of 0.1922 million hectares with annual production of 2.213 million tons (FAO, 2013). The average yield of citrus is estimated at 12.7 tons per hectare. Fruit production is predisposed to a number of factors amongst which insect/pest infestation is prominent that leads to low yield which in turn results in inferior quality. In addition, numerous other factors such as the development of diseases, non-certified nursery stock, post-harvest fruit losses and poor management practicescontribute to the inferior quality of citrus fruits (Alférez et al., 2003). One prominent causative organism of brown spot of citrus is Alternaria citri (Pierce, 1902). Brown spot symptoms appear on leaf, twigs and fruits, with the characteristic symptom of this disease being circular to oval brown lesions, yellow halo development around the lesions because of toxin production by the pathogen (Dewdney and Timmer, 2012). At initial stages, foliar lesions are circular but having tails and surrounded by leaf vein which makes the lesion to appear as eyespot. The severity of infection depends upon the cultivar and favourable environmental conditions. The most pronounced symptoms can cause defoliation, wilting, dieback and premature fruit drop (Otani et al., 1995). The causal agent of citrus black rot is Alternaria citri which is the first citrus associated Alternaria specie (Pierce, 1902). On the basis of morphological similitude, the pathogen of brown spot of citrus was identified as A. citri (Doidge 1929, Ruehle 1937, Kiely 1964, Pegg 1996). Brown spot mostly infects tangerine and tangerine hybrids leading to fruit drop and reduced yield caused by A. citri. Conidia are produced on all parts of the plant that are susceptible to the disease. For the disease control in general, protectant fungicides are effective in inhibiting spore germination. However, this has been shown to be difficult in humid climate regions like that of Pakistan (Timmer et al., 2003). Nevertheless, chemical control remains the most effective control measure compared with other control strategies due to chemical post-infection activity and availability to growers (Bushong and Timmer, 2000). Chemical control (fungicide use) of the disease is the most common means worldwide and Tebuconazole, Chlorothalonil, Azoxystrobin, Thiophenate methyl, Fosetyl aluminium, and benomyl are some of the fungicides that considerably reduce the severity of brown spot (Timmer and Zitko, 1997). Copper-based fungicides give good results but there are disadvantages of copper as it darkens then blemishes and enhances the attack of lesion causing insects while it’s accumulation in the soil becomes toxic to plants (Whiteside, 1983). Brown spot of citrus is among several diseases responsible for low citrus crop production in Pakistan thus complicating an already problematic situation of pathogen resistance emerging against different fungicides. Though some works have been carried out on the control of A. citri in Pakistan (Johnson, 2006, Fatima et al., 2009, Murtaza et al., 2012, Cevheri, 2017), insufficient research exists specifically on the control of A. citri in citrus plantations in Pakistan. It is at the backdrop of this that the current study was aimed at evaluating the effectiveness of systemic and contact fungicides against A. citri, the causal organism of citrus brown spot disease in citrus mangroves of Pakistan.


Varietal screening

In order to assess disease incidence and severity, a survey was conducted in areas of Khyber Pakhtunkhwa (KPK) and Punjab provinces of Pakistan. Different citrus varieties were selected from different orchards in each area. A total of 102 plants were randomly selected from the different orchards of KPK and Punjab provinces of Pakistan. A sample size of ten (10) plants and fifty (50) fruits were selected from each orchard of Citrus to record disease incidence and severity. Computations were achieved with the help of the following formulae (Safdar et al., 2010);

Disease Incidence (%)= (Number of infected plants)/(Total number of plants) ×100 … Eq. 1

Disease Severity(%)= (No.of infected fruits)/(Total No.of fruits) ×100 … Eq. 2

For assessing disease severity, the rating scale for assessment of leaf spot diseases of citrus as described by (Timmer and Zitko, 1997) (Table 1) was used.

Table 1

Diseased specimen collection

Diseased samples were collected from randomly selected plants of 8 years old orchards to determine the infectious fungi associated with the diseases. The samples (one specific grape variety per location) were collected from twelve different areas (Table 2) resulting in a total of twelve (12) citrus varieties. Samples were aseptically collected and packed in sterile polythene bags and kept in the ice box and then transported to the diagnostic mycology laboratory of Department of Plant Pathology, University of Agriculture Peshawar, Pakistan for further processing within 2 hours after collection.

Table 2

Isolation, purification and identification of pathogenic fungi

Diseased tissues from the samples were cut into small pieces (4 mm) and disinfected with 1% Cholorox solution and washed twice with distilled water and dried on blotter paper and placed on sterilized Petri plates containing potato dextrose agar (PDA) (Bio Basic Inc.) at 25°C with illumination of 600 Lux ((Ploetz and Gregory, 1992). Percentage colonization and relative density were calculated after 7 to 8 days of incubation. The isolated fungi associated with diseased samples were purified by aseptically transferring unto fresh agar slants and incubating as before. For microscopic examination, fungi isolates were prepared by gently lifting the mycelia mat with a sterile inoculation pin into a drop of lactophenol blue on a slide, teased (spreading the mat) and covered with another slip and observed under a microscope. Fungi were identified by morphological characterization and the use of identification keys (Domsch et al. 1980; Samson et al., 1981; Samson et al., 1995).

In vitro screening of fungicide against Alternaria citri

The poisoned food technique described by Das et al. (2010) was employed in the in vitro test of the efficacy of ten selected fungicides (Table 3) against A. citri. The fungicides were tested against A. citri at different concentrations (25, 50, 100, 200 and 400 ppm) by combining appropriate quantities of the fungicides with an autoclaved PDA and mixing very well then plating in sterile Petri dishes and allowed to solidify. With the assistance of a sterile cork borer, a 5 mm mycelia disc of 72 hours old culture of A. citri was taken and aseptically placed in the center of the poisoned media. The experiment was replicated thrice and plates containing only toxicated PDA was used as a control. Inoculated plates were incubated at 250C ±2 for 7 days till the control plate attain growth of 9 cm. Percentage of inhibition was measured with the help of mean colony diameter and computed according to the formula (Eq. 3) (O'Rourke et al., 2009). Percent decrease in mycelial growth was calculated by comparing inhibition zones with respect to control treatment.

Growth inhibition (%)= (X-Y)/X ×100 … Eq. 3

Where X = colony diameter in check and Y = colony diameter on fungicide treated plate.

Table 3

Data analysis

All data recorded (triplicate) were subjected to analysis of variance (ANOVA) using SAS version 2002. Results are presented as means in tables analyzed and compared by applying Fisher’s least significant difference at a confidence interval of 95%.


Disease severity and incidence

From the survey carried out on the brown spot disease incidence and severity as caused by Alternaria citri in different citrus fruits from citrus orchards of Panjabi province, results confirmed the presence of the disease in all orchards surveyed. However, the incidence and severity varied with location. Plate 1 depicts the diseased samples as they were picked from the orchard. The disease severity results are presented in Figure 1, indicating differences in severity of the disease among the citrus varieties correlating with the orchard locations (Table 2). Isolation of pathogen from diseased fruits revealed vividly that the pathogen responsible for the brown spot disease was A. citri as proven by pure cultures using morphological characterization and identification keys (Domsch et al., 1980; Samson et al., 1981; Samson et al., 1995) while Koch’s postulate confirmed the pathogenicity of the isolates. Rangpur lime was the most susceptible variety that was revealing significantly higher (56.0%) infection percentage while Faislabad pride and Valencia late were relatively resistant to A. citri by showing significantly (p<0.05) lower disease severity of 40.0 and 41.0%, respectively. Disease severity of 54.0, 53.0, 53.0 and 51.0% as revealed in Feuterall early, Rio red, Duncan and Coleoptera Riored respectively were not significantly (p>0.05) different to Rangpur lime (Figure 1). Mausambi, Sour orange, Kinnow and Foster were averagely susceptible to the disease with 50.3, 50.0, 47.2 and 45.0% disease severities, respectively (Figure 1). Figure 2 depicts the results of the survey conducted to assess disease incidence of citrus orchards. There was evidence of disease incidence in all the orchards surveyed (Figure 2). The disease incidence ranged between 9.9 and 35.6% with the highest incidence associated with orchards at Sargodha (35.6%) and the least at Jhag (9.9%). More than half (58.33%) of the orchards surveyed recorded diseases incidence of 20% and above.

Plate 1

Figure 1

Figure 2

Screening of fungicides against A. citri

The result of the study suggests that among the ten (10) fungicides evaluated against A. citri, interestingly, Dodine, Hexaconazole, and Cholorthalonil were most effective in controlling A. citri as they exhibited 100% inhibition at all concentrations (Table 4) except for Difenoconazole which was effective (100% inhibition) at lower fungicide concentrations (25, 30 and 50 ppm) while relatively less effective (65.8 and 58.0% inhibition) at higher fungicide concentrations (400 and 200 ppm) respectively. The results of Fosetyl aluminium were almost at par with Metiram with percent average decrease in colony growth of 22.7, 29.4, 29.4, 39.8, as well as 44.5% and 45.4, 45.8, 51.2, 49.6 as well as 52.96% at concentrations of 25, 50,100, 200 and 400 ppm respectively. Mancozeb exhibited high percentage decrease in colony by providing more than 65% growth inhibition at all concentrations (Table 4). In the case of a combination of Metalaxyl and Mancozeb, the result showed that there was relatively significant decrease in colony growth of A. citri over the control with 36.94, 41.99, 51.72, 64.31 and 100% A. citri colony growth inhibition at 25, 50, 100, 200 and 400 ppm concentrations respectively (Table 4). Mixture of Azoxystrobin and Difenoconazole was also effective in controlling reproduction by inhibiting colony of the pathogen (A. citri) at 100, 200 and 400 ppm concentrations with average decrease in colony growth percentages being 91.17, 92. 05 and 94.57 % respectively. On the other hand, the average decrease in colony growth percentages exhibited by Thiophenate Methyl were 41. 61, 47. 61,52.96, 54 and 58.23% at 25, 50, 100, 200 and 400 ppm concentrations respectively (Table 4).

Table 4


Citrus brown spot is an important disease of citrus present throughout the world and the pathogen which was isolated from disease samples was Alternaria citri. In the current study, it was found that A. citri was associated with spread of the citrus brown spot disease. The pathogenicity test of the current study revealed that A. citri was associated with the citrus brown spot disease development and 25 to 300C was suitable temperature for growth and reproduction of conidia as proved by Timmer et al. (2000). Twelve varieties of citrus were evaluated in the study for their susceptibility to the citrus brown spot disease. Rang pur lime citrus variety was most susceptible to infection with 56% disease intensity or severity. While the other varieties were equally susceptible to the disease, some were relatively resistance by showing lower disease severity as in the case of Foster citrus variety. The high disease incidence recorded at Sargodha, Sialkot and Peshawar could be attributed to the climatic factors and the soil condition. One significant observation was that the orchards which were near high ways had higher disease incidence. Similar observation was made by Safdar et al. (2010). In this experiment of fungicides evaluation against the disease, fungicides viz; Metalaxyl and mancozeb, Thiophenate methyl, fosetyl aluminium, metiram, mancozeb, Azoxystobin and difenoconazole inhibited 68% decrease in colony growth of A. citri. The results are in agreement with Timmer and Zitko (1992) in which fosetyl aluminium, mancozeb, azoxystrobin were proved to be the best for management of the disease in citrus orchards. Results in this study revealed that all fungicides greatly inhibited the colony growth of citrus brown spot pathogen. Hexaconazole, difenoconazole belong to triazoles group of fungicides and exhibited 100% decrease in colony growth of pathogen over the control plate in vitro. Dodine, chlorthalonil also gave 100% control against the pathogen. These fungicides (cholorthalonil, dodine, hexaconazole, difenoconazole) were most effective at all concentrations and they totally suppressed growth of pathogen. While Mancozeb, Thiophenate methyl, Metiram, Fosetyl aluminium gave maximum inhibition at 400 ppm concentration, mixture of azoxystrobin and Difenaconazole was also effective and inhibited growth at all concentrations but gave maximum result at 300 ppm. Timmer and Zitko (1997) used similar mixture for suppressing growth of citrus brown spot pathogen. In a similar study, Cholorthalonil an ethylene bisthidiocarbamates fungicide provided control against A. citri in browns spot lesions (Johnson et al., 2003). Various researches have also showed that the mycelia growth of A. citri could be inhibited by mancozeb at 400 ppm concentration (Khanzada et al., 2005; Jamadar and Lingaraju, 2011; Khanzada and Shah, 2012).

Elsewhere, the evaluation of various fungicides revealed that Azoxystrobin, cholorthalonil, hexaconazole, difenoconazole, dodine were highly effective against Alternaria spp. (Timmer et al., 2004). Bhatia et al. (2002) also evaluated mancozeb, metiram against the citrus brown spot pathogen at 200 ppm concentration and proved that the pathogen is suppressed at this concentration in vitro. In view of all the previous studies cited above, the current results are indicative of higher pathogen inhibition as some of the fungicides exhibited growth inhibition of up to 100%. Banik et al. (1998) and Sales (2009) also proved that Difenoconazole was most effective in field disease management. Miles et al. (2005), conducted an experiment on field and evaluated fungicides against brown spot of mandarins and confirmed the causative agent to be A. citri in subtropical areas of Australia. Their results indicated among others that Stroblurens along with copper and Mancozeb were more effective in citrus fungi control which is in consonance with the current study.


This study evaluated the efficacy of selected fungicides at different concentrations in controlling citrus brown spot caused by Alternaria citri. The study has revealed that the selected fungicides (Cholorthalonil, Hexaconazole, Dodine and Difenoconazole) produced 100% decreased mycelia growth over the control, hence were most effective in inhibiting Alternaria citri while Fosetyl Aluminium was the least effective. Thus, these fungicides (Cholorthalonil, Hexaconazole, Dodine and Difenoconazole) have potential for use to control brown spot disease of citrus caused by Alternaria citri in Parkistan.


The authors declare that they have no conflict of interest.


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