Efficacy of Aqueous Extract of the Seeds of Annona muricata L. in the Control of Late Blight (Phytophthora infestans) of Tomato (Lycopersicon esculentum Mill.) in the Field

 

Ramsès Tsala1*, Patrice Zemko Ngatsi1, Nono Carine Temegne1, Sylvere Landry Dida Lontsi1, William Norbert Kuaté Tueguem1, Abdou Nourou Koné Nsangou1, Bekolo Ndongo1

 

1Department of Plant Biology, University of Yaoundé I, Cameroon

 

*Correspondence to: Ramsès Tsala, University of Yaoundé I, XH7P+FMR, Yaounde, Cameroon; E-mail: tsalaramses69@gmail.com

 

DOI: 10.53964/jmab.2022006

 

Abstract

Objective: An experiment was conducted to propose an agroecological alternative to synthetic fungicides for the control of late blight of tomato in field. The aim of this study was to evaluate the effect of aqueous extract of Annona muricata seeds (AqEAM) against late blight and yield parameters of tomato.

 

Methods: Two varieties (Rio Grande and Lindo F1) constituting the main plots and three treatments (aqueous extract of A. muricata, synthetic fungicide Mancozeb 800g/kg and control) represented sub-plots were used in a split-plot design with four replicates. The treatments were applied two weeks after transplanting and the dose of AqEAM used was 70g/L. Incidence, severity of late blight and agronomic parameters were evaluated.

 

Results: The results show that the application of AqEAM significantly reduced the incidence of late blight in the field by 55.84% and the severity by 80.35% compared to the control at 76 days after transplanting (DAT). Furthermore, no significant differences were observed between AqEAM and the synthetic fungicide on the incidence and severity of late blight. In terms of yield (t ha-1), tomatoes treated with AqEAM showed a significant increase of 26.14% and 25.7% respectively compared to the control and the synthetic fungicide. The Lindo F1 variety yielded best (10.80t ha-1) than Rio Grande variety (6.60t ha-1).

 

Conclusion: These results suggest that aqueous seeds extract of Annona muricata is effective as the synthetic fungicide and would therefore be recommended as an alternative in biological control of late blight of tomato.

 

Keywords: Annona muricata extract, antifungal, Lycopersicon esculentum, Phytophthora infestans, yield parameters

 

1 INTRODUCTION

Tomato (Lycopersicon esculentum Mill.) is an herbaceous plant of the Solanaceae family and originated from western coastal part of the South America continent[1]. Due to its high nutritional value, tomatoes are considered to be one of the most economically important vegetable crops globally[2]. It is rich in mineral elements, vitamins A, C, E and phenolic antioxidants[3]. Its consumption reduces the incidence of cardiovascular diseases, various cancers and degenerative diseases associated with old age[4,5]. With a global production of around 120 million tons per year, it is the second most consumed vegetable in the world after potatoes[6]. Tomatoes are highly susceptible to diseases caused by oomycetes, the most important of which is late blight of tomato caused by Phytophthora infestans (Mont.) de Bary. It is one of the most costly diseases worldwide[7]. Its damage in the field affects fruit quality and can lead to tomato yield losses of up to 80%[8]. Recently, it is observed changes in the population structure of P. infestans have led to the advent of new genotypes containing two mating types A1 and A2 that are more aggressive and resistant to synthetic fungicides[9]. Tomato cultivation therefore requires a significant input of synthetic fungicides to reduce field infection of plants by late blight while preserving yield. However, due to their toxicological properties, the abusive use of synthetic fungicides is becoming a real danger for humans and the environment. As soon as they are applied in agriculture, synthetic fungicides contaminate soils, affect biodiversity and are also washed into surface or groundwater during rainfall. Synthetic fungicides can also accumulate in food chains; a small concentration in water can lead to a high concentration in the tissues of consumers in general[10, 11].

 

Faced with this perilous situation, in Agroecology, the search for effective, less costly, non-polluting alternative methods is topical. The formulation of natural substances of plant origin that could have beneficial biostimulator effects in plant protection and production is a promising avenue. Plants with biodegradable pesticide effects synthesize compounds with antifungal, insect repellent, insecticidal and antibacterial properties[12,13]. The plant extracts with their recognized systemic modes of action have already proven to be effective in strengthening the defense system of the plants enabling them to be more vigorous and resistant to diseases[14]. Annona muricata seeds have already been the subject of numerous phytochemical studies, which have demonstrated their insecticidal, fungicidal and bactericidal potential[15-17]. Numerous studies showed that the extract of seeds of A. muricata are rich in secondary metabolites (phenolic compounds, alkaloids, saponins, terpenoids, sterols etc.) which have a pesticide property[18,19]. Nevertheless, very few studies have highlighted the effect of the aqueous extract of A. muricata seeds against late blight in order to optimize tomato yield in the field. Thus, the objective of this study was to evaluate the efficacy of the aqueous extract of Annona muricata seeds on late blight and yield parameters of tomato in the field while preserving tomato yield.

 

2 MATERIALS AND METHODS

2.1 Study Site

The experiment was carried out in a mid-fallow (2 years old) in the locality of Éssazok (03° 46' 00'' North and 12° 15' 00'' East), located in the Centre Region of Cameroon. This locality belongs to the agro-ecological zone 5 of Cameroon (humid forest zone with bimodal rainfall). The zone is characterized by a Congo-Guinean sub-equatorial climate. The average rainfall is 1633mm/year, distributed into a small rainy season (March-June) and a long rainy season (September-November). The average annual temperature is relatively constant (around 23 to 27°C) and the average relative humidity is over 80%. Tomatoes are the main vegetable crop, and the soil is red laterite, sandy, black or clay in some places[20].

 

2.2 Plant and Chemical Material

Plant material consisted of seeds of two tomato varieties (Rio Grande and Lindo F1) was chosen based on of their agronomic performance and different susceptibility to diseases. Both varieties were obtained at Semagri, which is an approved company for the development and sale of agricultural seeds. On the other hand, seeds of Annona muricata obtained from the already ripe fruits at local market reported to the National Herbarium for identification and confirmation. The chemical material consisted mainly of a synthetic fungicide commercially called PENNCOZEB 80 WP which is a contact fungicide, with a very broad spectrum of action, powdery appearance and its active ingredient being Mancozeb 800g/kg.

 

2.3 Nursery and Experimental Design

Two ridges (5m x 1m) were formed using hoes and incorporated poultry manure (two 15kg bags). The duration of the tomato plants in the nursery was 23 days, after which the tomato plants were transplanted to the field in cool weather in afternoon. The experiment was conducted during February to July 2019. A split-plot design with four replications was used. Varieties constituting the main plot randomly in replication with two levels (Rio Grande and F1 Lindo). The treatments represented the sub-plots randomized within the main plot (T0: control, T1: synthetic fungicide and T2: aqueous extract of Annona muricata seeds (AqEAM)). Each experimental unit had 15 tomato plants for a total of 90 plants per block. The experimental units measured 3m x 1.5m and were separated by 1m paths and contained three rows of five seedlings. The four blocks were spaced 1.5m apart.

 

2.4 Preparation and Application of Treatments

For the preparation of the aqueous extract of A. muricata, the seeds isolated from the ripe fruits were dried in the shade for three weeks and kept in an air-permeable container. The dried seeds were crushed with a grinder and 210g of A. muricata seed powder was taken and macerated in 2L of water for at least 24h. The resulting solution was filtered through a cotton cloth and the collected contents were diluted with 1L of soapy water and then introduced into a knapsack sprayer for exclusive use in the eight experimental units involved in the treatment. The soap powder (10g) associated with the extract was used as a wetting agent to reinforce the adhesion of the product on the parts of the plant to be treated. The dose used was 70g/L or 58kg of A. muricata powder for 833 liters of water per hectare[21].

 

For the synthetic fungicide treatment, the rate was in accordance with the recommendations prescribed in the registration, i.e. 5g/L. The mixture obtained was homogenized and then introduced into a sprayer for specific use in the eight experimental units examined.

 

The aqueous extract of A. muricata seeds and the synthetic fungicide were applied five times throughout the experiment at regular intervals of 10 days.

 

2.5 Parameters Measurements

2.5.1 Identification of Late Blight

Late blight of tomato, using various diseased plant samples collected in the field, was identified in the laboratory by microscopic observations of sporocysts[22]. The method consisted in placing a drop of distilled water on a slide, then bringing and dissociating in the drop a sample to be observed; the slide was covered by a slide and the observation was made through a binocular optical microscope of the brand OLYMPUS CH-2 at 40X magnification.

 

2.5.2 Assessment of the Incidence and Severity of Late Blight

The incidence of disease was recorded 40 days after transplantation at 12 days intervals in different experimental units using formula proposed by Tchoumakov and Zaharova[23].

 

 

With I = Incidence; n = Number of diseased plants; N = Total number of plants

 

The severity of late blight was calculated according to the formula proposed by Tchoumakov and Zaharova[23].

 

With S = Severity; ∑ (ab) = sum of multiplications of the number of diseased plants (a) by the corresponding degree of infection (b); N = total number of diseased plants.

 

Degree of infection was attributed using the scale varying from 0 to 5 with modification (Table 1)[24]. The score was assigned by the plant pathologist based on their eye estimation.

 

Table 1. Field Key to Estimate the Degree of Severity of Late Blight[24]

 

2.5.3 Assessment of Growth and Development Parameters

Data collection was carried out weekly from 12 days after transplanting (DAT) until the end of the experiment on seven randomly selected tomato plants per experimental unit for growth parameters. The height of the tomato plants was measured with a ruler. The leaves and the flowers per tomato plant were assessed by counting. The fruit set rate was calculated using the formula used by Tikarrouchine[25]:

 

 

2.6 Assessment of Yield Parameters

The means of number of fruits, fruit mass and fruit diameter of tomato plants were evaluated considering fruits damaged by late blight. Tomato yield in tons per hectare was expressed from the following formula[26, 27]:

 

 

With NF = Mean number of fruits per plot; MF = Mean mass of fruits per plot (g); S = Plot area (m2)

 

2.7 Statistical Analysis

The data obtained were subjected to a one-and two-ways analysis of variance (ANOVA) using IBM SPSS Statistic 20.0 software. Normality (Shapiro-Wilk test; P˃0.05) and homogeneity of variance (Levene test; P˃0.05) were verified. Then a multiple comparison of means using the Student-Newman-Keuls (SNK) test at the 5% threshold was determined.

 

3 RESULTS

3.1 Identification of Late Blight of Tomato

Light microscopic observations of the late blight (Figure 1) structures from the various samples obtained in the field confirmed the effective presence of late blight on tomato plants during the experiment (Figure 1A). Morphological study under the microscope showed that the sporocysts of Phytophthora infestans were ovoid-ellipsoid to limoniform in shape with one pedicel and one papilla each. The mean lengths of the sporocysts ranged from 43.35μm to 51.85μm and the mean widths of the sporocysts from 23.96μm to 35.30μm (Figure 1B).

 

Figure 1. Late blight of tomato. (A): Symptoms observed on a tomato plant; (B): Sporocysts of Phytophthora infestans observed under a binocular optical microscope (40 X magnification)

 

3.2 Epidemiological Parameters of Late Blight in the Field

3.2.1 Incidence of Late Blight

The results reveal significant differences (P<0.05) between the treatments for the incidence of late blight in the field at 40, 52, 64 and 76 DAT (Table 2). The highest incidence of 61.73%, 59.62%, 61.48% and 61.53% was showed in the control compared to the AqEAM treatment which recorded the lowest incidence of 29.65%, 26.13%, 24.32% and 27.80% at 40, 52, 64 and 76 DAT respectively. Regarding the variety effect, no significant difference (P˃0.05) in incidence between the two tomato varieties was observed.

 

Table 2. Effect of Antifungal Treatments and Varieties on the Incidence (%) of Late Blight

Notes: P: 0 '***' 0.001 '**' 0.01 '*' 0.05; ns: not significant. In each column, the values (means ± standard deviations) followed by the same letters do not differ significantly using the Student-Newman-Keuls (SNK) test at the 5% threshold. T0: Control; T1: Synthetic fungicide; T2: AqEAM; V1: Rio Grande; V2: F1 Lindo; DAT: Days after transplanting.

 

3.2.2 Severity of Late Blight

The data on late blight severity are presented in Table 3. A highly significant difference (P<0.01) is recorded between varieties and treatments at 40, 52, 64 and 76 DAT. The AqEAM treatment showed the lowest severity of 8.1%, 5.93%, 5% and 7.23% followed by the fungicide treatment (10.7%, 6.82%, 6.52% and 8.63%) at 40, 52, 64 and 76 DAT respectively. The control treatment recorded the highest severity in all periods. Regarding the variety effect, the variety V2 (Lindo F1) showed the lowest severity compared to the variety V1 (Rio Grande) in all periods.

 

Table 3. Effect of Antifungal Treatments and Varieties on the Severity (%) of Late Blight

Notes: P: 0 '***' 0.001 '**' 0.01 '*' 0.05; ns: not significant. In each column, the values (means ± standard deviations) followed by the same letters do not differ significantly using the Student-Newman-Keuls (SNK) test at the 5% threshold. T0: Control, without any treatment; T1: Synthetic fungicide; T2: AqEAM; V1: Rio Grande; V2: F1 Lindo; DAT: Days after transplanting.

 

3.3 Effect of Treatments and Varieties on Tomato Growth Parameters

The plant height and number of leaves of the two varieties in all treatments are presented in Table 4. No significant difference (P˃0.05) between treatments for plant height was observed. However, a very highly significant difference (P<0.01) was showed between the varieties. The Lindo F1 variety (58.31±3.28cm) presented the highest plant height compared to the Rio Grande variety (42.05±7.59cm) at 50 DAT. For the number of leaves, there significant difference (P<0.05) at 50 DAR between treatments was observed. Plot treated with AqEAM recorded the highest number of leaves (37.50±4.57) compared to the synthetic fungicide (32.60±3.44) and the control (31.50±3.34). No significant difference (P˃0.05) was recorded between the varieties for the number of leaves.

 

Table 4. Evolution of Tomato Plant Growth in Relation to Antifungal Treatments and Varieties

Notes: P: 0 '***' 0.001 '**' 0.01 '*' 0.05; ns: not significant. In each column, the values (means ± standard deviations) followed by the same letters do not differ significantly using the Student-Newman-Keuls (SNK) test at the 5% threshold. T0: Control, without any treatment; T1: Synthetic fungicide; T2: AqEAM; V1: Rio Grande; V2: F1 Lindo; DAT: Days after transplanting.

 

3.4 Effect of Treatments and Varieties on Tomato Development Parameters

The results of the mean number of flowers show a significant difference (P<0.05) between the AqEAM (65.19±5.89) and the control (57.46±8.99) at 59 DAT. On the other hand, at 80 DAT, there was no significant difference (P>0.05) between the treatments. For the varieties, there was no significant difference (P>0.05) during the experiment. Regarding the fruit set rate, there were significant differences between the treatments at 86 (P<0.05) and 105 (P<0.001) DAT. Overall, the AqEAM treatment recorded better fruit set rates of 59.38% and 65.19% compared to the control 33.83% and 57.46% respectively at 86 and 105 DAT. The variety Lindo F1 recorded significantly higher fruit set rates than the variety Rio Grande during the experiment (Table 5).

 

Table 5. Effect of Antifungal Treatments and Varieties on Tomato Development

Notes: P: 0 '***' 0.001 '**' 0.01 '*' 0.05; ns: not significant. In each column, the values (means ± standard deviations) followed by the same letters do not differ significantly using the Student-Newman-Keuls (SNK) test at the 5% threshold. T0: Control, without any treatment; T1: Synthetic fungicide; T2: AqEAM; V1: Rio Grande; V2: F1 Lindo; DAT: Days after transplanting.

 

3.5 Effect of Treatments on Yield-related Parameters

3.5.1 Number of Fruits

The number of fruits was significantly higher in the AqEAM treatment (6.1±1.37) compared to the synthetic fungicide treatment (4.8±0.92) and the control (4.7±1.56) at 93 DAT. For the variety effect, a significant difference (P<0.01) was recorded at 93 and 106 DAT. The Lindo F1 variety had the highest number of fruits (5.1±1.37 and 9.75±2.33) during these two periods (Table 6).

 

Table 6. Effect of Antifungal Treatments and Varieties on the Number of Tomato Fruits

Notes: P: 0 '***' 0.001 '**' 0.01 '*' 0.05; ns: not significant. In each column, the values (means ± standard deviations) followed by the same letters do not differ significantly using the Student-Newman-Keuls (SNK) test at the 5% threshold. T0: Control, without any treatment; T1: Synthetic fungicide; T2: AqEAM; V1: Rio Grande; V2: F1 Lindo; DAT: Days after transplanting.

 

3.5.2 Effect of Treatments and Varieties on Yield

The effect of treatments and varieties on mean fruit diameter per plant, mean fruit mass per plant and yield were presented in Table 7. Indeed, the AqEAM treatment with 6±0.59cm recorded better diameters compared to the synthetic fungicide treatment (5.35±0.38cm) and the control (4.96±0.61cm). The results on the mean fruit diameter per plant showed no significant difference (P>0.05) between the two varieties. In terms of mean fruit mass per plant and yield in tons per hectare, the AqEAM treatment recorded the best values (52.34± 11.25g and 11.40t ha-1) compared to the synthetic fungicide (46.80±3.72g and 8.47t ha-1) and the control (44.19±5.94g and 8.42t ha-1). The variety Lindo F1 had significantly better fruit weight (54.7±7.44g) and yield (10.8t ha-1) than the variety Rio Grande (41.80±2.61g and 6.60t ha-1).

 

Table 7. Variation in Mean Fruit Diameter, Mean Fruit Mass and Tomato Yield in Tons Per Hectare According to Antifungal Treatments and Varieties

Notes: P: 0 '***' 0.001 '**' 0.01 '*' 0.05; ns: not significant. In each column, the values (means ± standard deviations) followed by the same letters do not differ significantly using the Student-Newman-Keuls (SNK) test at the 5% threshold. T0: Control, without any treatment; T1: Synthetic fungicide; T2: AqEAM; V1: Rio Grande; V2: F1 Lindo; MFD: Means fruit diameter; MFM: Means fruit mass.

 

4 DISCUSSION

The assessment of the efficacy of the aqueous extract of A. muricata seeds on the epidemiological parameters revealed a significant decrease in the incidence and severity of late blight of tomato compared to the control. This result would be due to annonain which is an acetogenin contained in the seeds of A. muricata and which would have antifungal properties. Thus, this secondary metabolite would have inhibited the development of Phytophtora infestans spores and consequently, significantly limited the expansion of late blight of tomato in the field. Le Ven[16] demonstrated by analysing the properties of the phytochemical components of A. muricata that the annonain, terpenoids and phenolic acid contained in the seeds would have antifungal potentialities. These results are similar to those obtained on the antifungal activities of acetogenins from Annona squamosal against various plant pathogens[28]. Similarly, Rizwana et al.[29]  show that extract of A. muricata contain important bioactive compounds that possess antifungal activity when they evaluated the antifungal activities of A. muricata on tomato Alternaria. Also, Naik and Sellappan[30] and Boli et al.[31] demonstrate that phytochemical screening of the aqueous extract of A. muricata seeds shows that it is rich in phenols, terpenoids, glycosides, saponins, flavonoids, alkaloids and sterols. The use of aqueous extract of A. muricata seeds (AqEAM) in the protection of tomato plants resulted in significant improvements in leaf number. These effects of AqEAM are believed to be due to its composition of acetogenins, amino acids, vitamins, cytokinin and auxin. Indeed, these substances affect the cellular metabolism of plants and contribute considerably to increasing their productivity[5,32]. Furthermore, statistical analyses did not reveal significant differences in plant height between all treatments. This could be explained by the fact that the height growth of tomato plants is mainly influenced by the physio-chemical composition of the soil, as the poultry manure were added to the soil to enrich it with nitrogen plays an important role in plant growth. Indeed, Hanitriniony[33] when assessing the efficacy of Fourcroya gigantea in the control of Alternaria and late blight in tomato, observed a homogeneity of the growth in height of tomato plants according to the treatments applied. Similarly, Aghofack-Nguemezi et al.[5] had no significant effects for height when applying Spirulina plantensis and Jatropha curcas extracts to tomato plants. On the order hand, Fangue et al.[34] demonstrate that extracts of Tithonia diversifolia and Thevetia peruviana affected significantly plant height of tomatoes in field. Other studies also showed that crude extract of Gleicheni linearis at the rate of 100mg/l was the most effective in increasing plant height[35]. Regarding the fruit set rate, a good development of tomato plants treated with AqEAM was observed compared to the control. These results can be explained by the fact that the annonain contained in the seeds of A. muricata would act against the fungal diseases that cause dysfunctions capable of causing flower bud abortion and poor fruit set. Indeed, Hanitriniony[33], in assessing the effectiveness of Fourcroya gigantea against Alternaria and late blight of tomato, noted that the formation of floral clusters was favoured by the decrease of fungal diseases. Regarding the number of flowers, no significant difference was observed between treatments. These results could be due to the fact that phytohormones such as gibberellin, ethylene and cytokinin involved in flowering induction acted independently of the treatments applied[36]. Comparing the mean fruit weights and diameters as well as the yield per hectare obtained at the different treatments, it was found that overall the AqEAM-treated plots showed significantly better values than the other treatments. This result could support the fact that AqEAM is effective from a phytotechnical point of view. Indeed, the decrease of pests contributes to the improvement of the quantity and quality of the crop yields. In addition, the mean number of fruits per plant in each treatment did not reveal significant differences between AqEAM and the other treatments. Tounou et al.[37] showed that plant extracts applied to cowpea plants did not result in significant differences between treatments on the average number of cowpea pods in southern Togo. The seeds of A. muricata due to their insecticidal, fungicidal, and bactericidal properties[15,16], their richness in acetogenins, essential oils, amino acids, vitamins, auxin and cytokinin as demonstrated by Le Ven[16] in his analysis of the phytochemical components of A. muricata, would favour by the combination of these factors, the obtaining of a good durable phytosanitary follow-up and consequently contribute to the obtaining of a bigger growth, a better development and a higher yield of the crops. During the trial, a better varietal response of the Lindo F1 variety was observed overall compared to Rio Grande both in epidemiological, growth, development and yield parameters. On the one hand, this could be due to genetic modifications that allow the introduction of genes of interest to obtain tomato cultivars that perform as well as Lindo F1, or on the other hand, the cultivar Lindo F1 was simply more adapted to the growing conditions presented during the experiment.

 

5 CONCLUSION

In view of the results obtained and the analyses that follow from this trial whose objective was to evaluate in the field, the effect of the aqueous extract of Annona muricata seeds against late blight of tomato and yield parameters, it can be maintained that, the aqueous extract of A. muricata seeds had remarkable effects on the reduction of the incidence and severity of late blight in comparison with the control. The application of aqueous extract of A. muricata seeds contributed to improve the growth, development and yield of tomato especially in terms of number of leaves, number of flowers, average fruit diameter per plant and average fruit mass per plant. Regarding the varietal effect, the tomato variety F1 Lindo is a recommendable variety for tomato cultivation based on the results obtained. The seeds of A. muricata could be a natural resource for sustainable agriculture. Thus, the aqueous extract of Annona muricata seeds could be used as an alternative method to synthetic fungicides; thus, falling within the framework of the agroecological transition, which nowadays remains a major concern. The further development of this trial in an in vitro environment would constitute an axis for future research.

 

Acknowledgements

The authors would like to express their gratitude to the entire team of the Phytopathology and Plant Protection Research Unit of the Biotechnologies and Environment Laboratory of the Faculty of Science of the University of Yaoundé I for their methodological and technical contributions during the experiment.

 

Conflicts of Interest

The authors declared no conflict of interest.

 

Author Contribution

This work realized with the collaboration of all authors. Ndongo B. designed the study; Tsala R collected data and wrote the first draft of manuscript; Ngatsi PZ coordinated the field and lab study and reviewed the manuscript; Temegne NC performed the statistical analyses; Dida Lontsi SL, Tueguem WNK and Nsangou ANK reviewed the manuscript. All authors approved the final version.

 

Abbreviation List

AqEAM, Aqueous extract of Annona muricata seeds

DAT, Day(s) after transplanting

MFD, Means fruit diameter

MFM, Means fruit mass

MF, Mass of fruits

NF, Number of fruits

 

References

[1] Naika S, De Jeudej JVL, De Goffau M et al. Cultivation of tomato: production, processing and marketing. Agromisa Foundation and CTA: Wageningen, The Netherlands, 2005.

[2] Frusciante L, Carli P, Ercolano MR et al. Antioxidant nutritional quality of tomato. Mol Nutr Food Res, 2007; 51: 609-617. DOI: 10.1002/mnfr.200600158

[3] Habou ZA, Ibrahim MC, Zabeirou H et al. Efficacy of neem oil (Azadirachta indica) and Bacillus thuringiensis (Biobit 2X) on the population dynamics of Bemisiatabaci (Gennadius 1889) and Helicoverpa armigera (Hubner, 1808) in a tomato plantation in Niger. Int J Biol Chem Sci, 2016; 10: 497-505. DOI: 10.4314/ijbcs.v10i2.4

[4] Lee JE, Giovannucci E, Smith-Warner SA et al. Intakes of fruit, vegetable, vitamins A, C and E, and caroitenoids and risk of renal cancer. Cancer Epidemiol Biomarkers Prev, 2006; 15: 2445-2452. DOI: 10.1158/1055-9965.EPI-06-0553

[5] Aghofack J, Schinzoumka PA, Tatchago V. Effets des extraits ou de la poudre de Spirulina platensis et Jatropha curcas sur la croissance et le développement de la tomate, J Appl Biosci, 2015; 90: 8413-8420. DOI: 10.4314/jab.v90i1.2

[6] Planetoscope. Real-time statistics. ConsoGlobe, 2019.

[7] Fry WE, Goodwin SB. Resurgence of the Irish potato famine fungus. Bioscience, 1997; 47: 363-371. DOI: 10.2307/1313151

[8] Tindo M, Tagne A, Mpe JM et al. Technical guide on pests of plantain, maize, cassava and tomato. FAO, 2016; 43-65.

[9] Cooke LR, Schepers H, Hermansen A et al. Epidemiology and Integrated Control of Potato Late Blight in Europe. Potato Res, 2011; 54: 183-222. DOI: 10.1007/s11540-011-9187-0

[10] Gnago JA, Danho M, Atcham TA et al. Efficacité des extraits de neem (Azadirachta indica) et de papayer (Carica papaya) dans la lutte contre les insectes ravageurs du gombo (Abelmoschus esculentus) et du chou (Brassica oleracea) en Côte d’Ivoire. Int J Biol Chem Sci, 2010; 4: 953-966. DOI: 10.4314/ijbcs.v4i4.63035

[11] Cruz JM. Etude de la contamination par les pesticides des milieux eau, air et sols : développement de nouveaux outils et application à l’estuaire de la Gironde [Doctor’s thesis]. Bordeaux, Nouvelle-Aquitaine: University of Bordeaux; 2015.

[12] Amadioha AC, Uchendu PN. Post harvest control of tomato fruit rot caused by fusarium solani with extracts of azadirachta indica. Discov Innov, 2003; 15: 83-86. DOI: 10.4314/dai.v15i1.15629

[13] Opara EU, Wokocha RC. Efficacy of some Plant Extracts on the in vitro and in vivo control of xanthomonas campestris Pv. vesicatoria. Agric J, 2008; 3: 163-170.

[14] Mbega ER, Mabagala RB, Adriko J et al. Five Species of Xanthomonas Associated with Bacterial Leaf Spot Symptoms in Tomato from Tanzania. Plant Dis, 2012; 96: 760-761. DOI: 10.1094/PDIS-01-12-0105-PDN

[15] Haustant W. The soursop fruit. JP Morgan Chase & Co. 2008; 7 (in French).

[16] Le Ven J. Contribution to the study between Annonaceae and Parkinsonism: identification and quantification of acetogenins by dereplication; phase I metabolism and annonacin distribution approach [Thesis]. Orsay, France: University of Paris Sud-Paris XI; 2012.

[17] Togo. Africa Top Success. Les vertus insoupçonnées du corossol: ne le consommez plus au hasard! Available at https://www.africatopsuccess.com/les-vertus-insoupconnees-du-corossol-ne-le-consommez-plus-au-hasard

[18] Ojezele OJ, Ojezele MO, Adeosun AM. Comparative phytochemistry and antioxidant activities of water and ethanol extract of Annona muricata leaf seed and fruit. J Adv Biol Res, 2016; 10: 230-235.

[19] Naik, AV, Sellappan K. Physiochimical and phytochemical analysis of different plant parts of Annona muricata L. (Annonaceae). Pharm Methods, 2019; 10: 70-78. DOI: 10.5530/PHM.2019.2.13

[20] PCD-Mfou. Mfou Communal Development Plan. (CCD)(PNDP), 2016; 22-25.

[21] RECA-Niger. Technical sheet: preparation of an aqueous solution of neem against pests of vegetable crops, 2013; 1-4.

[22] Hsieh WH, Goh TK. Cercospora and similar fungi from Taiwan. Maw Chang Book Company: Taipei, 1990.

[23] Tchoumakov A, Zaharova. Statistic of disease development. Disease damages caused in crop production. Agro Prom Izdat: Moscou, Russia, 1990; 53.

[24] Henfling JW. Late blight of potato: Phytophthora infestans. International Potato Center: Lima, Peru, 1987.

[25] Tikarrouchine R. Agronomic and technological characterization of 17 F1 hybrids of tomato "Lycopersicum esculentum" obtained by crossing [Master’s Thesis]. El Harrach, Algeria: ENSA Alger; 2009.

[26] Svecnjak Z, Varga B, Butorac J. Yield components of apical and subapical ear contributing to the grain yiel responses of prolific maize at high and low plant populations. J Agron Crop Sci, 2006; 192: 37-42. DOI: 10.1111/j.1439-037X.2006.00188.x.

[27] Kamau J, Melis R, Laing M et al. Farmers’ participatory selection for early bulking cassava genotypes in semi-arid Eastern Kenya. J Pl Br Crop Sci, 2011; 3: 44-52. DOI: 10.5897/JPBCS.9000053

[28] Dang QL, Kim WK, Nguyen CM et al. Nematicidal and antifungal activities of anonaceous acetogenins of Annona squamosa against various plant pathogens. J Agric Food Chem, 2011; 59: 11160-11167. DOI: 10.1021/jf203017f

[29] Rizwana H, Bokahri NA, Alsahli SA et al. Postharvest disease management of Alternaria spots on tomato fruit by Annona muricata fruit extracts. Saudi J Biol Sci, 2021; 28: 2236-2244. DOI: 10.1016/j.sjbs.2021.01.014

[30] Naik AV, Sellappan K. Physiochimical and phytochemical Analysis of different plant parts of Annona muricata L. (Annonaceae). Pharm Methods, 2019; 10: 70-78. DOI: 10.5530/phm.2019.2.13

[31] Bolie H, Ndongo B, Ngatsi PZ et al.  Antifungal activity of Annona muricata seed extracts against Cercospora malayensis, causal agent of cercospora leaf spot disease of okra (Abelmoschus esculentus L.), Int J Pathog Res, 2021; 6: 12-24. DOI: 10.9734/IJPR/2021/v6i430167

[32] Angèle NP, Zachée A, Tchadjoko NR et al. Effect of aqueous extracts of neem seeds (Azadirachta indica) on the development of Asian Rust of soybean in the Center Region of Cameroun. Int J Environ Agr Biotechnol, 2018; 3: 956-964. DOI: 10.22161/ijeab/3.3.31

[33] Ramavomboahangy H. Contribution à l'étude d'un biopesticide d'origine végétale, le Fourcroya gigantea pour la lutte contre l'alternariose et le mildiou de la tomate Lycopersicum esculentum. ARSIE: Antananarivo, Madagascar, 2000.

[34] Fangue-Yapseu GY, Mouafo-Tchinda RA, Kenne MF et al. Allelopathic effect of three wild plants (Azadirachta indica, Tithonia diversifolia and Thevetia peruviana) on tomato (Lycopersicum esculentum Mill.) growth and stimulation of metabolites involved in plant resistance. Am J Plant Sci, 2021; 12, 285-299. DOI: 10.4236/ajps.2021.123018

[35] Aulya NR, Noli ZA, Bakhtiar A et al. Effect of plant extracts on growth and yield of maize (Zea mays L.). Pertanika J Trop Agr Sci, 2018; 41: 1193-1205.

[36] Regnautlt-Roger C, Philogène BJR, Vincent C. Biopesticides of plant origin, 2nd ed. Éditon TEC & DOC: Paris, French, 2008.

[37] Tounou AK, Sokame BM, Akpavi S et al. Effets des extraits vegetaux sur la dynamique de populations des insectes ravageurs de niebe, Vigna unguiculata,/i> walp, dans le Sud du Togo. Journal de la Recherche Scientifique de l'Université de Lomé, 2012; 14: 25-34.

 

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