Abstract
Background: Angular leaf spot and blight, caused by fungi of the genus Alternaria, known as most destructive diseases affecting Cleome gynandra, a potential Indigenous African vegetable, being promoted in Zimbabwe. Information on its disease management is scanty.
Aim: To isolate, evaluate and propose potential management options against the diseases caused by Alternaria alternata and Alternaria senecionicola, obtained and identified from Marondera University of Agricultural Sciences and Technology, Agro Industrial Park (MUAST AIP) and Premier areas of Zimbabwe.
Setting: Efficacy of fungicides, in a CRD (6*2 factorial experiment), Biological Control Agents (3*2 factorial experiment) and organic agent (2*2 factorial experiment), was evaluated against these species on C. gynandra, with three replications.
Methods: Fifteen cm plants under greenhouse conditions at MUAST AIP were inoculated and monitored. Data on incidence and severity were collected every week for 3 weeks.
Results: A. alternata and A. senecionicola Area Under Disease Progress (AUDPs) and disease incidence were effectively suppressed by all test fungicides (p = 0.02) on days 7–14 and AUDPCs on days 14–21 and had no interactions (p = 0.07). There was interaction between Alternaria species and fungicides for % disease incidence for day 7 (p = 0.009), day 14 (p = 0.04) and day 21 (p = 0.04). Biological control using Trichoderma harzianum (T77) and Saccharomyces cerevisiae was effective in reducing disease severity and incidence. There were no interactions on AUDPCs days 7–14 (p = 0.6), but noted on days 14–21 (p = 0.02). The cattle bile was effective, and it was noted without interactive effects on AUDPCs days 7–14 (p = 0.2) and days 14–21 (p = 0.4). % disease incidences lack interactive effects on day 7 (p = 0.3), and noted on day 14 (p = 0.001). There was no interaction on day 21 (p = 0.08).
Conclusion: Two Alternaria species can be managed by fungicides, BCAs and organic agents.
Contribution: Diseases were controlled.
Keywords: fungicides; biological control; agent; organic control; Alternaria.
Introduction
Angular leaf spot and blight, caused by fungi of the genus Alternaria, are one of the most destructive diseases affecting Cleome gynandra, a potential African Indigenous Vegetable crop, being promoted in Zimbabwe. Information about their disease management is scanty. Alternaria genus is a fungal genus that has been divided into 24 sections based on molecular and morphological data (Woudenberg et al. 2014), hence more species can be found to cause diseases on C. gynandra, which requires more research on their prevalence and management. Alternaria species cause leaf spot diseases in many different plant species, and they cause diseases in aerial plant parts (Agrios 2005; Alalade et al. 2017). Alternaria alternata produces mycotoxins, which are responsible for causing the leaf spot disease in plants, and diseases in postharvest in crops (Troncos-Rojas & Tiznado-Hernandez 2014) and in humans, causing asthma.
C. gynandra has become a weed of importance with its demand increasing, being used in different areas, including pharmaceuticals, culinary and traditional medicine, besides being a nutritious traditional leafy vegetable. C. gynandra’s increase in demand has raised interest in working on the diseases that affect its growth, and the need to do commercial production of the plant in provinces of Zimbabwe, a new area of research to ensure its availability and reduce crop loss to diseases. Alternaria species has been identified through morphological, physiological and molecular characterisation during research at MUAST AIP Laboratory to identify pathogens that affect C. gynandra during the 2021–2022 cropping season in Zimbabwe. Four areas were assessed. They included three provinces, that is, Mashonaland East Province’s Marondera University of Agricultural Sciences and Technology, Dozmery area, Manicaland Province’s Premier and Mutanda 2 areas, and Masvingo Province’s Zimuto area. Differences in morphology, physiology and biochemical characteristics have shown that Alternaria has many species that are pathogenic to C. gynandra accessions in Zimbabwe. The effect of the pathogens on C. gynandra plants has not been evaluated and controlled, hence this research.
Quality and quantity of feed, food and fibre produced by farmers in the world need to be maintained by controlling plant diseases (Cwalina-Amboziak, Damszel & Glosek-Sobieraj 2015). The use of chemical control methods was very effective in the past 100 years, but due to their residual effect in the environment causing pollution, the methods are being replaced by alternatives that are environmentally friendly, such as biological control (Cwalina-Amboziak et al. 2015; Pal & McSpadden Gardener 2006; Pandit et al. 2022). Biological control agencies (BCA) have been used to manage pathogens that cause diseases on plants, and they are cheaper and environmentally friendly because they are available in the environment (Chandrashekara et al. 2012).
Alternaria species have been considered an important fungal species that is known to cause early blight disease. The management of pathogens that has been done before, where different plant pathogens have been controlled using Integrated Pest Management (IPM) options, has been successful (Kaliyati, Mapope & Manyangarirwa 2023; Razdan, Gupta & Peshin 2009). Diseases associated with Alternaria species have been managed effectively with the use of chemicals and biological control agents (Grondona et al. 1997). Alternaria leaf spot management has been noted to have low efficacy when using fungicides (Scheufele 2013), hence the need to use different control methods in this research. This research is new in Zimbabwe, and it deployed synthetic fungicides, BCAs and organic control methods to control pathogens affecting C. gynandra. The use of BCAs has gained widespread acceptance as an alternative to the use of pesticides and pesticide resistance in the control of pathogens (Loona et al. 2024; Pandit et al. 2022), though there is still much to be done on their interaction with natural and societal functions to ensure their sustainable development and deployment of the approach for its endorsement (Loona et al. 2024). Biological control agents can control pathogens, though they fail to permanently eradicate the pathogen (Chandrashekara et al. 2012; Mahr, Whitaker & Ridgway 2008). There are natural BCAs that survive in the plant and soil environment, which produce antibiotics (Alalade et al. 2017; Pal & McSpadden Gardener 2006). Sudden disease appearance under greenhouse conditions, leaving little or no room for farmers to take control action, leads to only the use of fungicides as a control measure (Scheufele 2013). The use of Metalaxyl in combination with Dithiocarbamates was shown to be an effective combination that can regulate the growth of fungi in plants (Panek, Helmer & Ali 2022). The management of early blight diseases caused by Alternaria species has been shown to be low, around 60% – 70% under field conditions (Kaliyati et al. 2023). Acylalanine has been shown in vitro to reduce mycelial growth of A. alternata when applied at a rate of 2 kg/ha and had an efficacy rate of 49%, while Dithiocarbamate at a rate of 2 kg/ha had 100%. A combination of Mancozeb + carbedazim (0.2%) was used on seed treatment and then foliar application and proved to be most effective in reducing disease intensity (Meena et al. 2022). Terbuconazole, a Triazole fungicide, was also found to be effective in controlling Alternaria leaf blight both in in vitro and in vivo by inhibiting mycelial growth (100%) and conidial germination (90.7%), on Radish plants (Razdan et al. 2009). A combination of terbuconazole and azoxystrobin was found to be effective in controlling Alternaria pori at 0.1%, followed by pyraclostrobin + epoxiconazole at the same rate (Mushrif et al. 2023). Biological control is one of the solutions that are now being researched as an alternative pathogen control (Alalade et al. 2017; Torres et al. 2017). Trichoderma, a BCA, has been widely used due to its ability to control pathogen growth and populations in crop production (Pandit et al. 2022). Trichoderma harzianum was noted to reduce the incidence and seed infection of Alternaria species on Brassica seeds, thereby increasing seed emergence and decreasing leaf infections (Scheufele 2013).
The aim of this research was to isolate, evaluate and propose potential management options against the diseases caused by Alternaria alternata and Alternaria senecionicola, obtained and identified from Marondera University of Agricultural Sciences and Technology, Agro Industrial Park (MUAST AIP) and Premier areas, after a research that was conducted from three provinces of Zimbabwe, that is, Mashonaland East Province, MUAST AIP area, Manicaland Province Premier and Mutanda 2 areas, and Masvingo Province’s Zimuto area. This research is new in Zimbabwe.
Research methods and design
Site
These trials were run in a greenhouse in Marondera at MUAST AIP.
Biological material
Fungi used in this research were isolated from three provinces of Zimbabwe during a survey to identify pathogens that affect C. gynandra. Mashonaland East Province MUAST AIP, Masvingo Province, Zimuto area, Manicaland Premier area and Mutanda area during the 2020/22 growing season. In vitro cultures of Alternaria alternata and Alternaria senecionicola were done on potato dextrose agar (PDA) and were placed in an incubator for 7 days at 25 °C + −2 °C. The grown fungi were diluted to a concentration of 1 × 10−6 and used to inoculate 6-week-old greenhouse plants at a height of 15 cm.
In vivo experiments
In vitro experiments were conducted to test the efficacy of fungicides, BCAs and organic control agents against fungal isolates found to be pathogenic to C. gynandra accessions. The different concentrations were used to determine the minimum inhibitory concentrations that were later used in in vivo experiments under greenhouse conditions to control the effect of A. alternata and A. senecionicola.
Three trials were conducted in the greenhouse using fungicide concentrations that effectively controlled fungal growth on C. gynandra in vitro. The 6*2 factorial experiment was laid out in a CRD, with three replications. The main plot had a chemical being tested, for example, triazole, against a pathogen inoculated on C. gynandra plants. 3 m × 1 m plots were used as the main plots with the same fungicide being applied on different isolates, each being replicated three times. The experiments were run in a greenhouse where a double layer of nap liner was used to block each main plot to prevent the drifting of chemicals to other plots.
The first trial was a 6*2 factorial experiment laid out in a CRD, with three replications. The six factors consisted of chemical control agents at rates of 3760 ppm Triazole, 10 000 ppm Acylalanine, 2000 ppm Methyl Benzimidazol Carbamate (MBC), 8520 ppm Dithiocarbamate and 520 ppm Triadimenol, and 3760 ppm Pyraclostrobin+epoxiconazole, as indicated in Table 1, whereas the two factors consisted of the two fungal pathogens, Alternaria alternata and Alternaria senecionicola. Plants inoculated with the two pathogens at a rate of 1 × 10−6 were sprayed with the fungicide from the day of inoculation. The second trial was a 3*2 factorial (BCAs that included Trichoderma harzanium (T77) and Saccharomyces cerevisiae that were used at rates of 240 ppm and 11 000 ppm, as indicated in Table 2 and acylalanine control at 10 000 ppm on plants inoculated separately with A. alternata and A. senecionicola) experiment laid out in a CRD. Plants inoculated with the two pathogens at a rate of 1 × 10−6 were sprayed with the fungicide from the day of inoculation. The third trial was a 2*2 factorial (Cattle bile was used at a rate of 5000 ppm as indicated in Table 3 and Acylalanine control at 10 000 ppm on plants inoculated separately with A. alternata and A. senecionicola) experiment laid in a CRD. Plants inoculated with the two pathogens at a rate of 1 × 10−6 were sprayed with the fungicide from the day of inoculation.
| TABLE 1: Fungicide groups used in in vivo experiments. |
| TABLE 2: Biological control agents used in in vivo experiments. |
| TABLE 3: Biopesticide agent used in in vivo experiments. |
Data collection
In planta experiment
After inoculation and spraying, data were collected every 7 days for 21 days, with disease incidence and severity scores being recorded for every inoculated plant.
Data analysis
Normality tests were conducted on incidence and severity scores using the Shapiro-Wilk test through SPSS. The data that did not fit normality were Log10(x + 1) transformed (Malato 2023) before subjecting them to analysis of variance using GenStat version 18. Severity data collected were used to calculate Area Under Disease Progress Curve (AUDPC) using Excel formula (day7 + day14)*7/2 for all the weeks, disease incidence data collected were Arc SIN transformed using Excel, and the data were subjected to a two-way analysis of variance using GenStat 18th edition at 5% significance.
Ethical considerations
This article followed all ethical standards for research without direct contact with human or animal subjects.
Results
Table 4 presents results with AUDPCs and % disease incidence scores that did not fit normality tests, hence were transformed accordingly. On analysis of variance, there was a significant interaction between fungicide and fungal pathogens on AUDPC on day 7–14 interactions p < 0.02, while there was no significant interaction on day 14–21 p = 0.07. There were significant interactions on % disease incidences for day 7, with p = 0.009, day 14, p = 0.04, and day 21, p = 0.04.
| TABLE 4: Response on disease severity as area under disease progress curve for chemical control (fungicides) on isolated pathogens on Cleome gynandra plants. |
On mean separation, there were significant differences on fungicide action on controlling the pathogens on days 7–14 AUDPCs p < 0.001, where Diathiocarbamate and the control were having the highest AUDPC = 7.9 (70% disease severity) against the rest of the fungicides that are not significantly different from each other, where Pyraclostroblin + epoxyconazole and Triazole had AUDPC = 7.1 (10% disease severity) and MBC had AUDPC = 7.2 (15% disease severity), and both Acylalanine (control) and Triademenol had AUDPC = 7.3 (20% disease severity).
Days 14–21, fungicide action was significant, with p < 0.001. Pyroclostrobin + epoxiconazole, Triazole and MBC were not significantly different, with AUDPCs of 7.1 (10% disease severity), 7.1 (10% disease severity), and 7.2 (15% disease severity), respectively, whilst both Acylalanine (control) and Triademinol had AUDPCs of 7.5 (35% disease severity) and were not significantly different. Dithiocarbamate and the control had the highest AUDPC of 7.8 (60% disease severity) and 7.9 (70% disease severity), respectively, and they were significantly different from the rest of the fungicides.
On % disease incidences, the fungicides were significantly different, with p < 0.001, where Pyraclostrobin + epoxiconazole, Triazole, Acylalanine (control) and Triademinol had 5.7% (0% disease incidence), followed by Diathiocarbamate being equal to 6.3%, which was significantly different, and lastly MBC and the control had the highest incidence of 7.3% (100% disease incidence). On day 14, the % disease incidence was significantly different, with p < 0.001, where Pyraclostrobin + epoxiconazole and Triazole were not significantly different from each other, at had 6% and 6.3%, respectively, whilst Triazole, MBC, Acylalanine (control), Triademinol, Dithiocarbamate and control were not significantly different, with % incidences of 6.3%, 7.1%, 7.3%, 7.3%, 6.8% and 7.3%, respectively.
On day 21, there was a significant difference, with p < 0.001. Pyraclostrobin+epoxiconazole, Triazole and Dithiocarbamate had the least % disease incidences of 6.3%, 6% and 6.3%, respectively, whilst MBC, Acylalanine (control), Triademenol, and control had no significant difference, with disease incidences of 7.3%, 7.1%, 7.3% and 7.3%, respectively (Figure 1).
 |
FIGURE 1: Interactive effect of Synthetic fungicides and Alternaria species on disease incidence (%) day 21 at Agro Industrial Park, Marondera University of Agricultural Sciences and Technology 2023. |
|
Fungal pathogens’ response to fungicide treatment was only significant on days 7–14 AUDPCs, with A. alternata being the least, with 7.2 (15% disease severity), and A. senecionicola had a higher AUDPC of 7.4 (20% disease severity). % disease incidences were not significant throughout the research period.
Table 5 results had the AUDPCs and disease incidence scores not fitting normality tests, hence were transformed accordingly. On analysis of variance, there were no significant interactions between BCAs and fungal pathogens on AUDPCs days 7–14, with p = 0.6 and on days 14–21 p = 0.2.
| TABLE 5: Response to disease severity as area under disease progress curve for Biological Control Agents against a chemical control on isolated pathogens on Cleome gynandra plants. |
On disease incidences, there was no significance during the research on day 7 p = 0, day 14 p = 0.1, and day 21, p = 0.3. On mean separation there were significant differences on AUDPCs on days 7–14, with p < 0.001, where S. cerevisiae and Acylalanine control were not significantly different, with 7 (0% disease severity) and 7.1 (10% disease severity), respectively, whilst T. harzianum (T77) had a higher AUDPC of 7.4 (30% disease severity), followed by the control with 7.9 (70% disease severity).
On days 14–21, there was no significant difference for all the BCAs and the control. On % disease incidence for day 7, 14, and 21, there was no significant difference, with p = 0, 0.1 and 0.05, respectively. Fungal pathogen responses on AUDPCs were not significantly different for days 7–14 evaluations, whilst significance was noted on days 14–21, with p = 0.003 and A. alternata having an AUDPC of 7.1 (10% disease severity), whilst A. senecionicola had a higher AUDPC of 7.4 (30% disease severity).
On % disease incidence, there was no significance throughout the research for days 7, 14 and 21, with p = 0, 0.1, 0.3, respectively.
From Table 6, the AUDPCs and % disease incidence scores did not fit normality tests, hence were transformed accordingly. On analysis of variance, there were no significant interactions between organic control and fungal pathogens on AUDPCs days 7–14, with p = 0.2 and days 14–21 p = 0.4.
| TABLE 6: Response to disease severity as area under the disease progress curve for cattle bile against a chemical control on isolated pathogens on Cleome gynandra plants. |
On disease incidences, there was no significance during the research on day 7 p = 0.3, and there was significance on day 14 p = 0.001, and no significance on day 21, p = 0.08. On mean separation, there were no significant differences on AUDPCs on days 7–14, with p = 0.4. On days 14–21, there was no significant difference p = 0.05. On % disease incidence for days 7, 14 and 21, there was no significant difference, with p = 0.3, 0.3 and 0.08, respectively.
Fungal pathogen responses on AUDPCs were not significantly different for days 7–14 and 14–21 evaluations, with p = 0.4 and 0.7. On % disease incidence, there was no significance throughout the research for days 7, 14 and 21, with p = 0.3, 0.3, 0.08, respectively.
Discussion
Alternaria species has been considered an important fungal species that is known to cause early blight disease (He et al. 2021). The control of pathogens that has been done before involved different plant pathogens that have been controlled using IPM options, and the control has been successful (He et al. 2021). This was observed to complement the results obtained during this research, where the trials (fungicide, BCAs, and organic) were successful in controlling the isolates on C. gynandra. Observations made during this research have shown that chemical treatments were able to control the two pathogens from the two provinces of Zimbabwe. Alternaria alternata and Alternaria senecionicola, which have been found to affect C. gynandra were successfully controlled by Triazole, Triademinol, Pyraclostrobin+epoxiconazole, and MBC. Acylalanine was able to control the pathogen establishment on the C. gynandra plants by keeping disease severity low, below 30%. Dithiocarbamate was used and was found not to be very effective, having a disease severity of 80%. Triazole, Triademinol, Pyroclostrobin+epoxiconazole, MBC are the most effective in the control of Alternaria alternata by keeping the pathogen below 10% of the disease severity. In another research, a combination of terbuconazole and azoxystrobin was found to be effective in controlling Alternaria pori at 0.1%, followed by pyraclostrobin + epoxiconazole at the same rate (Mushrif et al. 2023). Terbuconazole, a triazole fungicide, was also found to be effective in controlling Alternaria leaf blight both in in vitro and in vivo by inhibiting mycelial growth (100%) and conidial germination (90.7%) (Razdan et al. 2009), which approves the results found in this research. The use of metalaxyl in combination with Dithiocarbamates was shown to be an effective combination that can regulate the growth of fungi in plants (Panek et al. 2022). In this research, Acylalanine is a combination of Phenylamide-Acylamide + Dithiocarbamate, which is traded as Mancozeb and Metalaxyl. The management of early blight diseases caused by Alternaria species has been shown to be low, around 60% – 70% under field conditions (He et al. 2021). In this study, Acylalanine had a similar suppressive ability of the two species of the C. gynandra plants. Similarly, Acylalanine, which has been shown to reduce mycelial growth of A. alternata when applied at a rate of 2 kg/ha, had an efficacy rate of 49%, while Dithiocarbamate at a rate of 2 kg/ha had 100% effectiveness, yet in this research it was observed that both treatments that were managed under Acylalanine and Dithiocarbamate had some instances where there was total eradication and in some it was not complete. Observations of unsatisfactory fungicide efficacy are attributed to application of less efficient products, their late application and maybe composition of Alternaria populations in different regions (He et al. 2021).
Dithiocarbamate is a protectant fungicide which prevents the establishment of the pathogen under natural conditions. In this research, it has proved to be ineffective since the application of the fungicide and inoculation were done at the same time. Therefore, the fungi were able to successfully establish on the C. gynandra plants.
Application of Trichoderma harzianum (T77) and Saccharomyces cerevisiae may have suppressed disease incidence and AUDPCs through antagonistic and exclusion means (Grondona et al. 1997). T. harzianum and S. cerevicae were noted to control A. alternata as a biological control on lemon fruits as a pathogen of post-harvest rot (Troncos-Rojas & Tiznado-Hernandez 2014). The effect of different species of T. harzianum proved to be very effective in the management of the targeted fungi (He et al. 2021). Trichoderma harzianum was noted to reduce the incidence and seed infection of Alternaria species on Brassica seeds, thereby increasing seed emergence and decreasing leaf infections (Scheufele 2013). This agrees with the results obtained in this research, where the targeted fungal pathogens have been controlled by T. harzianum (T77), as it has antagonistic action and exclusion on the growth of the fungi.
Organic control success was found in the use of cattle bile, which inhibited the growth of the Alternaria species. Organic control using cattle bile has been effective in the control of the Alternaria species, as it has been observed to have been without significant difference to the effect of Acylalanine, a fungicide which is well known to be effective in the management of the Alternaria species (Kaliyati et al. 2023) throughout the evaluation period.
Conclusion
In this new research conducted in Zimbabwe, Alternaria alternata and Alternaria senecionicola, which have been found to affect C. gynandra, were successfully controlled by Triazole, Acylalanine, Triademinol, Pyraclostrobin+epoxiconazole, and MBC, which were significantly superior in controlling the pathogens, followed by Dithiocarbamate. Biological control was successful with the use of Trichoderma harzanium (T77) and Saccharomyces cerevisiae, and they were found to be competitive as the control Acylalanine in their performance. Organic control success was found in the use of cattle bile, which was significant as acylalanine, which was used as the control during the research. Integrated pest management will be beneficial in the control of pathogens to reduce resistance due to the continual use of chemical fungicides. C. gynandra production will be managed at least with the control of pathogens to ensure success in the expected yield. Research should be ongoing to establish the presence of more different Alternaria species and more control treatments that can manage the current pathogens and many more in the production of C. gynandra.
Acknowledgements
I acknowledge the funding I received from the Government of Zimbabwe through the Ministry of Higher and Tertiary Education to conduct my research to fulfil my PhD studies at the Marondera University of Agricultural Sciences and Technology.
This article is based on research originally conducted as part of Joyce R. Kaliyati’s doctoral thesis titled ‘Fungal disease management in Cleome gynandra’, submitted to the Department of Crop Science, Faculty of Plant and Animal Sciences Technology, Marondera University of Agricultural Sciences and Technology in 2026. The thesis is currently unpublished and not publicly available. The thesis was supervised by Nyamande Mapope and Walter Manyangarirwa. The thesis was reworked, revised and adapted into a journal article for publication. The author confirms that the content has not been previously published or disseminated and complies with ethical standards for original publication.
This article is based on data from a larger study. Another article was published from the same thesis. The article focuses on A review of Disease Management in Cleome gynandra, which has been published in the International Journal of Innovative Science and Research Technology, Volume 8, Issue 7. This article is accessible here: https://doi.org/10.5281/zenodo.8304414
Competing interests
The author reported that they received funding from the Ministry of Higher and Tertiary Education, Innovation, Science and Technology Development, Zimbabwe, which may be affected by the research reported in the enclosed publication. The author has disclosed those interests fully and has implemented an approved plan for managing any potential conflicts arising from their involvement. The terms of these funding arrangements have been reviewed and approved by the affiliated University in accordance with its policy on objectivity in research.
CRediT authorship contribution
Joyce R. Kaliyati: Conceptualisation, Methodology, Formal analysis, Investigation, Writing – original draft, Visualisation, Project administration, Software, Data curation, Resources, Writing – review & editing, Funding acquisition. Nyamande Mapope: Formal analysis, Writing – original draft, Visualisation, Project administration, Writing – review & editing, Supervision. Walter Manyangarirwa: Formal analysis, Visualisation, Project administration, Software, Writing – review & editing, Supervision. All authors reviewed the article, contributed to the discussion of results, approved the final version for submission and publication, and take responsibility for the integrity of its findings.
Funding information
The research was funded by the Ministry of Higher and Tertiary Education, Innovation, Science and Technology Development, Zimbabwe, under grant Ref: AIV/2020/03.
Data availability
The authors confirm that the data supporting the findings of this study are available within the article.
Disclaimer
The views and opinions expressed in this article are those of the authors and are the product of professional research. They do not necessarily reflect the official policy or position of any affiliated institution, funder, agency, or that of the publisher. The authors are responsible for this article’s results, findings, and content.
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