UMYU Journal of Microbiology Research

E-ISSN: 2814 – 1822; P-ISSN: 2616 – 0668

ORIGINAL RESEARCH ARTICLE

Characterization of Fungi Inducing Post-Harvest Deterioration and the Factors Predisposing Tomato Fruits to Fungal Induced Spoilage in Zaria, Nigeria.

1*Dayok, O. , 1Whong, C. M, Z., 1Abdullahi, I.O. and 2Kashina, B. D.

1Department of Microbiology, Faculty of Life Sciences, Ahmadu Bello University, Zaria, Nigeria

2Department of Crop Protection, Institute of Agricultural Research, Ahmadu Bello University, Zaria, Nigeria

*Corrresponding author: dayok olukemi5080@gmail.com,+2348036906508

How to cite: Dayok, O., Whong, C. M. Z., Abdullahi, I. O., & Kashina, B. D. Characterization of Fungi Inducing Post-Harvest Deterioration and the Factors Predisposing Tomato Fruits to Fungal Induced Spoilage in Zaria, Nigeria. UMYU Journal of Microbiology Research (UJMR). Retrieved from https://ujmr.umyu.edu.ng/index.php/ujmr/article/view/508

Abstract

This study was carried out to characterize fungi-inducing post-harvest deterioration of tomato fruits and the factors predisposing the tomato fruits to fungal-induced spoilage in Zaria, Nigeria. A total of two hundred and twenty-five spoilt tomatoes of three different cultivars were collected using guided random selection (45 each) from five markets (Dakachi, Danmangaji, Sabon-gari, Samaru, and Basawa) in Zaria, Nigeria. The fungal isolates were isolated using the standard mycological method. The cultural and microscopic characterization of fungi isolated revealed eleven genera belonging to Fusarium, Phomopsis, Phoma, Cladosporium, Alternaria, Helminthosporium, Colletotrichum, Monilia, Curvularia, Rhizotonia, and Aspergillus. The total frequency and percentage occurrence ranged from 16(10.3%) to 42(26.%). The fungal isolate with the highest % frequency of occurrence was F. oxysporum with 23(14.7%), while the fungal isolate with the lowest frequency of occurrence was Curvularia eragrostidis with 3(1.9%). There were statistically significant differences in the mean number of occurrences among the fungal isolates (P = 0.003 < 0.05) and the markets (P = 0.0335 < 0.05). The total frequency and % occurrence of fungal isolates in tomato cultivars U T C, Ronita, and Roma VF ranged from 42(26.9) to 63(40.4%). There were statistically significant differences in the mean number of occurrences among the fungal isolates (p = 0.0000 < 0.05) and the tomato varieties (p = 0.0260 < 0.05). Tomato varieties, sorting, storage condition, packaging material, means of transportation, and nature of damage significantly affected tomato fungal-induced spoilage. Maintaining good sanitation practices in the field and during post-harvest handling of tomato fruits is crucial in minimizing the introduction and spread of fungi.

Keywords: Tomato, Fruits, Deterioration, Cultivars, Fungi and Post-harvest.

INTRODUCTION

Tomato (Solanum lycopersicum) is a member of the Solanaceae family, and it is one of the most popular and versatile fruits worldwide. They are commonly used in cooking, enjoyed for their taste, consumed in various cuisines, and appreciated for their vibrant colour, unique flavour, and numerous health benefits. Their rich nutrient profile, historical significance, and culinary versatility make them an important ingredient in numerous dishes (Rao et al., 2019). Including tomatoes in a well-rounded diet can contribute to overall health and well-being (Rao et al., 2019).

The tomato crop is susceptible to diseases, pests, and environmental factors affecting production output. Inadequate infrastructure for storage and transportation poses challenges to tomato farmers in Zaria and other regions of Nigeria. Despite these challenges, tomato farming remains an important economic activity in Zaria, contributing to local livelihoods and the agricultural sector of Nigeria as a whole. One of the major issues is the prevalence of tomato diseases, including fungal infections (Adedeji and Aduramigba 2016; Akaeze and Aduramigba 2017). These diseases can cause significant crop losses and reduce the quality and quantity of tomato production (Surechain, 2021).

Microbial spoilage of fresh tomatoes leads to waste of the produce and significant economic losses (Akinniran et al., 2020). Fresh tomato fruits' quality and nutritional value are affected by their pre and post-harvest fungal colonization (Akinniran et al., 2020). Fungi are the most important plant pathogens that affect a wide range of economic fruits during storage (Akinniran et al., 2020). Due to the perishable nature of tomato fruits, they decay before reaching final consumers in distant parts of the country. The deteriorative nature of tomatoes cultivated locally is largely responsible for importing tomato paste into Nigeria (Sabo et al., 2017; Akinniran et al., 2020). The work is aimed at characterizing post-harvest deteriorating fungi and factors predisposing tomato fruits to fungal-induced spoilage in Zaria,

MATERIALS AND METHODS

Collection of Samples

Random sampling was used in sample collection. A total of two hundred and twenty-five (225) spoiled samples of tomatoes were collected. These samples were purchased in batches of forty-five (45) from each of the five locations (Samaru, Sabogari, Basawa, Danmagaji, and Dakachi in Zaria metropolis, Kaduna State) and transported to the mycology laboratory of the Dept. of Crop Protection, Institute of Agricultural Research, ABU, Zaria for further analysis. The samples were washed with tap water, then rinsed with distilled water, and stored in labelled containers to isolate and identify the fungi (Kenneth-Obosi, 2017).

Isolation of Fungal Isolates from Spoilt Tomatoes

The spoilt tomato samples were washed under a running tap, dipped in 1% sodium hypochlorite solution for 3 minutes, and rinsed in three changes of sterile distilled water before blotting dry with sterile filter papers. The affected area of the fruits was cut using a sterile scalpel and plated on Potato Dextrose Agar supplemented with streptomycin sulphate solution (Udoh et al., 2015). The culture plates were incubated at 25°C for 72h and observed daily for fungal growth, which was sub-cultured to obtain pure cultures.

Characterization of Fungal Isolates

The pure cultures of the fungal colonies were subjected to macroscopic and microscopic examination for their identification based on growth patterns, the colour of mycelia, and vegetative and reproductive structures using fungal atlases. References were made to existing stock cultures for ease of identification, (Mbajiuka & Emmanuel, 2014). SPSS version 27 using ANOVA was adopted for statistical analysis.

To determine the factors predisposing tomatoes to fungi-induced spoilage in Zaria, Kaduna State, 225 tomato marketers were interviewed using a random sampling method. However, the responses of only 196 marketers were used in the analysis. The data collected include tomato variety, grade, sorting, storage condition, packaging materials, means of transportation, storing before selling, and nature of damage. Regression analysis was employed to determine the factors predisposing tomatoes to fungal-induced spoilage.

RESULTS

The fungi isolated consist of eleven genera, namely Fusarium spp, Phomopsis spp, Phoma spp, Cladosporium spp, Alternaria spp, Helminthoporum spp, Colletotrichum spp, Monilia spp, Curvularia spp, Rhizoctonia spp and Aspergillus spp with Fusarium spp as the predominant genus.

Fungal Isolates Color Texture Edge Shape Reverse Color Diameter Feature Revealed Under Microscope

Fusarium solani

Light Pink Cottony Irregular Orange 40.0 mm Small Oval Microconidia with one septum

Fusarium fujikuroi

White Cottony Irregular Light Orange 63.4 mm

Abundant Crescent Shaped Macroconidia, Singly

Fusarium equiseti

Whit Pinkish Cottony Circular Pinkish Brown 57.0mm

Branched Mycelia with Variable Sizes

Fusarium subglutinans

White Cottony Circular Dark Orange 46.8 mm

Microconidia in Abundance with Macrocondia

Fusarium oxysporum

White Cottony White Orange 48.3 mm Fusiform Pointed at Edge With 4 Septa

Curvularia eragrostidis

White Suede Irregular Dark Brown 58.6 mm Abundant Mycelial

Phomopsis vexans

Dark Ash Suede Circular Brown White 48.0mm Pycnidia Phomopsis Revealed

Phoma destructiva

Dark Brown Granular Irregular Black 62.5 mm Pycnidia of Phoma

Cladosporium cladosporioides

Pale Green Floccose Irregular Brown Black 25.0 mm Branching Chains of Conidia

Alternaria alternata

Dark Brown Cottony Irregular Black 41.0 mm Branched Chain of Conidia with Terminal Beak at Ends

Helminthosporium sativum

Dark Brown Velvety Irregular Black 58.0 mm Cylindrical Conidia, 8 Cells with Fragmented Hyphea
Colletotrichum lindemuthiamum Brown/Peach Granular Irregular Black 33.4 mm Conidia and Spine from one of the Conidia

Monila fructicola

Light Brown Creamy Center Floccose Peach and Brown Center 52.0 mm Conidiophore with rounded Conidia Acropetally

Curvularia lunata

Dark Brown Velvet Circular Black 61.5 mm Conidiophore Bearing Conidia

Rhizoctonia solani

White Patches Velvet Circular Black 54.0 mm Sclerotia and Mycelium

Aspergillus niger

Brownish Black Powdery Irregular Cream 78.5 mm Conidiosphore with Large Black Sporing Heads, Black round Conidia covering surface of Vesticles.

Table1. Fungal Isolates Growth Showed Various Cultural and Morphological Features of the Fungal Isolates Observed at 7 days

KEY: Color, Texture, Edge Shape, Diameter, Microconidia, Conidiosphore, Macroconidia

Table 2. Frequency of Occurrence of Fungal Isolates associated with Tomato samples from the five market locations in Zaria Metropolis

MARKET
DAK DMG SG BSW SAM Total
Fungal isolate N % N % N % N % N % N %

Fusarium solani

2

12.5

4

14.3

4

11.1

2

5.9

3

7.1

15

9.6

Fusarium fujikuroi

3

18.8

3

10.7

6

16.7

6

17.6

4

9.5

22

14.1

Fusarium equiseti

1

6.3

1

3.6

2

5.6

1

2.9

2

4.8

7

4.5

Fusarium subglutinans

0

0.0

4

14.3

3

8.3

0

0.0

2

4.8

9

5.8

Fusarium oxysporum

3

18.8

5

17.9

4

11.1

4

11.8

7

16.7

23

14.7

Curvularia eragrostidis

2

12.5

0

0.0

1

2.8

0

0.0

0

0.0

3

1.9

Phomopsis vexans

1

6.3

1

3.6

0

0.0

7

20.6

1

2.4

10

6.4

Phoma destructiva

1

6.3

2

7.1

1

2.8

2

5.9

2

4.8

8

5.1

Cladosporum cladosporioides

1

6.3

0

0.0

0

0.0

2

5.9

1

2.4

4

2.6

Alternaria alternata

0

0.0

0

0.0

2

5.6

2

5.9

4

9.5

8

5.1

Helminthosporum sativum

0

0.0

0

0.0

0

0.0

2

5.9

2

4.8

4

2.6

Colletotrichum lindemuthiamum

0

0.0

1

3.6

0

0.0

0

0.0

4

9.5

5

3.2

Monilia  fructicola

0

0.0

2

7.1

1

2.8

1

2.9

3

7.1

7

4.5

Curvularia lunata

0

0.0

2

7.1

3

8.3

1

2.9

1

2.4

7

4.5

Rhizoctonia solani

0

0.0

1

3.6

7

19.4

2

5.9

3

7.1

13

8.3

Aspergillus niger

2

12.5

2

7.1

2

5.6

2

5.9

3

7.1

11

7.1

Total

16

10.3

28

17.9

36

23.1

34

21.8

42

26.9

156

100.0

KEY: DAK –Dakachi, DMG -Danmagaji, SG-Sabon Gari, BSW -Basawa, SAM –Samaru; N=number of occurrence of organism, %=Percentage of frequency of occurrences

The total frequency and percentage occurrence of fungal Isolates from Dakachi, Danmangaji, Sabo-Gari, Basawa, and Samaru were 16(10.3%), 28(17.9%), 36(23.1%), 34(21.8%) and 42(26.9%) respectively. The market with the highest frequency of occurrence was Samaru at 42 (26.9%), while the market with the lowest frequency of occurrence was Dakachi at 16 (10.3%). The fungal isolate with the highest frequency of occurrence was Fusarium Oxysporum with 23 (14.7%), while the fungal isolate with the lowest frequency of occurrence was Curvularia eragrostidis with 3 (1.9%). The ANOVA results indicate that there are statistically significant differences in the mean number of occurrences among the fungal isolates (p=0.0003<0.05) and the markets (p = 0.0335 < 0.05). The fungal isolates can be grouped into 4 homogenous groups based on the multiple comparison results, indicating significant differences between some isolates but not within each group. The ANOVA results indicate that there are statistically significant differences in the mean number of occurrences among the fungal isolates (p=0.0003<0.05) and the markets (p=0.0335<0.05). The fungal isolates can be grouped into 4 homogeneous groups based on the multiple comparison results, indicating significant differences between some isolates but not within each group: Group 1: Curvularia eragrostidis, Phomopsis vexans, Phoma destructiva, Cladosporum cladosporiodes, Helminthosporum sativum - These isolates had the lowest mean number of samples (0.6 to 0.8). Group 2: Alternaria alternata, Fusarium equiseti – Had a moderate mean number of occurrences (1.0 to 1.6). Group 3: Fusarium solani, Fusarium subglutinans, Aspergillus niger, Monilia fructicola, Curvularia lunata, Rhizoctonia solani – Had a moderately high mean number of occurrences (2.0 to 2.6). Group 4: Fusarium fujikuroiFusarium oxysporum vii – Had the highest mean occurrence (3.0 and 4.6). The markets were also grouped into 2 homogeneous groups: Group 1: DAK –Had the lowest mean number of isolates (1.0). Group 2: DMG, SG, BSW, SAM - Had moderately higher mean numbers of isolates (1.8 to 2.6), with no significant differences among them. The multiple comparisons show that Fusarium fujikuroi had significantly more occurrence than all other isolates except Fusarium oxysporum, which had significantly more occurrence than all isolates except Fusarium fujikuroi and Fusarium solani. DAK market had significantly fewer samples than the SG and SAM markets. The number of occurrences varied significantly between fungal isolates and markets. Fusarium oxysporum and Fusarium fujikuroi isolates had the most occurrence overall, while Curvularia eragrostidis had the least. The DAK market had significantly fewer isolates than some other markets.

Figure 1. Percentage Occurrence of Fungal Isolates

Table 3: Frequency Occurrence (%) of Fungal Isolates from Spoilt Tomato Fruits Based on Tomato Cultivars

Fungal Isolates

UTC

RONITA

ROMA VF

TOTAL

Fusarium solani

5

11.9

4

7.8

6

9.5

15

9.6

Fusarium fujikuroi

8

19.0

6

11.8

8

12.7

22

14.1

Fusarium equiseti

2

4.8

3

5.9

2

3.2

7

4.5

Fusarium subglutinans

2

4.8

3

5.9

4

6.3

9

5.8

Fusarium oxysporum

6

14.3

7

13.7

10

15.9

23

14.7

Curvularia eragrostidis

1

2.4

1

2.0

1

1.6

3

1.9

Phomopsis vexans

4

9.5

4

7.8

2

3.2

10

6.4

Phoma destructiva

2

4.8

2

3.9

4

6.3

8

5.1

Cladosporium cladosporioides

1

2.4

1

2.0

2

3.2

4

2.6

Alternaria alternata

1

2.4

4

7.8

3

4.8

8

5.1

Helminthosporium sativum

1

2.4

2

3.9

1

1.6

4

2.6

Colletotrichum lindemuthiamum

2

4.8

1

2.0

2

3.2

5

3.2

Monila fructicola

1

2.4

3

5.9

3

4.8

7

4.5

Curvularia lunata

2

4.8

2

3.9

3

4.8

7

4.5

Rhizoctonia solani

3

7.1

6

11.8

4

6.3

13

8.3

Aspergillus niger

1

2.4

2

3.9

8

12.7

11

7.1

Total

42

26.9

51

32.7

63

40.4

156

100.0

key: N=number of occurrence of organism,%=percentage of occurrence of organisms

The total frequency and percentage occurrence of fungal isolates in tomato cultivars UTC, Ronita, and Roma VF are 42 (26.9%), 51 (32.7%), and 63(40.4%). The tomato cultivar with the highest frequency of occurrence of fungal isolates was Roma VF, with 63 (40.4%), while the lowest was UTC with 42(26.9%). The ANOVA showed that there are statistically significant differences in the mean number of occurrences among the fungal isolates (p = 0.0000 <0.05) and the tomato varieties (p=0.0260 < 0.05) (Table 3).

Table 4: Factors that predispose tomato to fungal-induced spoilage

Factors Number of respondents (%) R p-value Inference
Tomato varieties
No response 22 (11.2) 0.200 0.006 S
UTC 77 (39.3)
Roma VF 32 (16.3)
Ronita 10 (5.1)
Griffaton 22 (11.2)
all varieties 33 (16.8)
Grade
No response 9 (4.6) 0.305 0.008 S
Ripe 185 (94.4)
unripe 2 (1.0)
Sorting
Yes 130(66.3) 0.147 0.040 S
No 66 (33.7)
Storage condition
No response 2 (1.0) 0.242 0.001 S
Shade and covering with leaves 76 (38.8)
Storage under shade 101 (51.5)
Sorting before storage 7 (3.6)
Concrete floor 10 (5.1)
Packaging materials
Basket covered with leaves/paper 145(74.0) 0.233 0.001 S
plastics crates 40 (20.4)
Sacks 11 (5.6)
Means of transportation
Pick-up van 32 (16.3) 0.204 0.004 S
Long vehicle 52 (26.5)
Car 75 (38.3)
Motorbike 29 (14.8)
Others 8 (4.1)
Storing before selling
Yes 74 (37.8) 0.230 0.001 S
No 122 (62.2)
Nature of damage
No response 3 (1.5) 0.356 0.000 S
Physical 98 (50.0)
Fungi 53 (27.0)
Insect 11 (5.6)
Over ripe 31 (15.8)

Dependent variable: % fungal spoilage, Independent variables: factors R: Regression

DISCUSSION

Sixteen different species were isolated From the two hundred and twenty-five (225) tomato samples from the five locations at five different times. These include Fusarium solani, Fusarium fujikuroi, Fusarium equiseti, Fusarium subglutinans, Fusarium oxysporum,     Curvularia eragrostidis, Phomopsis vexans, Phoma destuctiva, Cladosporium cladosporioides, Alternaria alternata, Helminthosporium sativum, Colletotichum lindemuthiamum, Monilia fructicola, Curvularia lunata, Rhizoctonia solani, and Aspergillus niger. They were the main fungal species found to be responsible for the post-harvest deterioration of tomato fruits at different frequencies from the five locations. These species were previously reported for causing damage to tomato fruits from different markets in Nigeria (Sinno et al., 2020). Also, Sajad and Jamaluddin (2017) reported that the major post-harvest losses of fruits and vegetables are caused by species of fungi such as Alternaria, Botrytis, Monilia, Penicillium, Fusarium, Geotrichum, Helminthosporium, Curvularia which were similar to findings in this study. Chohan et al. (2016) reported that tomatoes are vulnerable to attack by different fungal pathogens, which are soil-borne, airborne, and seed-borne and inflict heavy losses in producing tomato fruits. The isolated and identified fungal species from tomato fruit rots are mainly caused by several fungi species (Sajad and Jamaluddin 2017). The study of Kvas et al. (2009) reappraised the numerous constituents of this group, including several economically significant plant pathogens and some that may produce secondary metabolite mycotoxins that can be harmful to human and animal health. Members of this group, such as Fusarium solani, Fusarium fujikuroi, Fusarium subglutinans, and other isolates in this study, are of worldwide distribution. Some are commonly saprobic on plant debris and in soil. Some strains are plant pathogens causing seedling blights, root/bulb rots, and vascular wilts. A number of strains have been isolated from human clinical specimens, and some members of this group of fungi isolated in this study are assigned to hazard group 2 by the ACDP (UK). The sixteen fungal species obtained in this study revealed that the market locations studied have diverse fungal species responsible for the post-harvest deterioration of tomato fruits. The frequency and percentage occurrence of fungal isolates from Dakachi, Damangaji, Sabo Gari, Basawa, and Samaru; 16(10.3%), 28(17.9%), 26(23.1%), 34(21.8%) and 42(26.9%) respectively. The market with the highest frequency and percentage occurrence is Samaru 42(26.9%), while the market with the lowest frequency is Dakachi at 16(10.3%).Variation in frequency of occurrence may have stemmed from improved methods of tomato handling and also due to a healthy market environment. Improper handling practices during post-harvest operations and at retail locations can cause mechanical injuries to tomatoes. Even minor injuries can create entry points for fungi to invade the fruits. Inadequate handling equipment and surface sanitation can lead to cross-contamination between healthy and spoilt tomatoes (Yuan et al., 2019). The fungal isolate with the highest percentage frequency of occurrence is Fusarium oxysporum 23(14.7%), while the fungal isolate with the lowest frequency of occurrence is Curvularia eragrostidis with 3(1.9%). Fusarium species are well-known plant pathogens causing diseases in various crops, including tomatoes (Thomma et al., 2011). The presence of Fusarium spp in tomato crops can devastate agriculture by yielding losses (Leslie et al., 2006). These species in this group are widespread and frequently isolated from soil and many different plant species worldwide. Some strains occur as saprobes on plant debris, others cause disease of a wide range of plants, including seedling blight, root/bulb rots, and vascular wilts. Members of this group also occur as contaminants from industrial sources, e.g., in machine cooling fluids, and have been reported as opportunistic pathogens of human eyes and skin (Proctor et al., 2018). The frequency and percentage occurrence of fungal isolates in tomato cultivars UTC, Ronita, and Roma VF were 42 (26.9%), 51 (32.7%), and 63(40.4%), respectively. The tomato cultivar with the highest % frequency of occurrence of fungal isolates is Roma VF 63(40.4%), while the lowest was observed in UTC 42(26.9%). Yousuf et al. (2021) reported that different tomato cultivars are susceptible to fungal infections. Some cultivars may possess genetic traits that make them more susceptible to fungal pathogens, whereas others may display resistance or tolerance. The choice of cultivar can significantly influence the susceptibility of tomato fruits to fungal-induced spoilage. The occurrence varied significantly between fungal isolates but not between the tomato varieties. Fusarium fujikuroi had the highest occurrence, while the organism with the least occurrence in relation to tomato cultivars was Curvularia eragrostidis. Mc colloch et al. (2002) reported that fungi cause different types of deterioration in post-harvest fruits, which occurs largely as blight and fruit rot of market vegetables. Drosophila melanogaster can carry spores and mycelia fragments on its body, from decaying tomatoes to cracks and wounds in healthy ones.                                                                                                                    Tomato varieties had a significant effect on fungal-induced spoilage. In this study, most respondents sold UTC, followed by Roma and other varieties. Their choice of tomato cultivars could be due to their unique characteristics. However, all varieties had varied percentages of fungal occurrence. Apart from unique characteristics, other factors such as grading, sorting, packaging materials, and means of transportation predisposed tomatoes to fungal-induced spoilage. In this study, 94.4% of respondents purchased ripe tomatoes, which are more susceptible to infection by fungal species.  33.7% did not sort their tomatoes, 74.0% used raffia baskets for packaging tomatoes, while a higher percentage of respondents used cars as a means of transportation of tomato fruits, which may not provide all the protection needed for the fruits. These findings align with the report of Ritenour et al. (2017) that inappropriate harvesting practices may cause damage such as wounds, breakage, or squeezing of the cellular and tissue structure. This generally increases the susceptibility of tomato fruits to the invasion and growth of fungi and speeds fungal decay rate. Lima et al. (2020) also stated that if tomatoes are not efficiently separated, fungal spores can spread to healthy fruits, accelerating the spoilage process.

CONCLUSION

Fungi isolates of eleven genera have been isolated, which include Fusarium spp, Phomopsis spp, Phoma spp, Cladosporium spp, Alternaria spp, Helminthosporium spp, Colletotrichum spp, Monilia spp, Curvularia spp, Rhizoctonia spp, and Aspergillus spp have been isolated. The frequency and percentage occurrence of fungal isolates from location ranged from 16(10.3%) – 42 (26.9%). The frequency and percentage occurrence of fungal isolates in UTC, Ronita, and Roma VF ranged from 42(26.9%) to 63 (40.4%), respectively. The frequency and percentage occurrence of fungal isolates in UTC, Ronita, and Roma VF ranged from 42(26.9%) to 63(40.4%), respectively. Tomato varieties, sorting, storage condition, packaging material, means of transportation, and nature of damage significantly affected tomato fungal-induced spoilage.

RECOMMENDATIONS

Maintaining good sanitation practices in the field and during post-harvest handling of tomato fruits is crucial in minimizing the introduction and spread of fungi. Removal and proper disposal of infected plant debris and regular disinfection of equipment can help reduce the risk of fungal-induced spoilage. Inadequate handling equipment and surface sanitation can lead to cross-contamination between healthy and infected tomatoes.

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