Journal of Agricultural Sciences Vol. 61, No. 1, 2016 Pages 57-68

DOI: 10.2298/JAS1601057A UDC: 633.34-248(669)

Original scientific paper

SEED-BORNE FUNGI OF SOYBEANS (GLYCINE MAX [L.] MERR) IN THE GUINEA SAVANNAH AGROECOLOGY OF NIGERIA

Oladimeji Ahmed1*, Olusegun S. Balogun1, Oluyemisi B. Fawole2,

Oluwatoyin A. Fabiyi1, Aliyu T. Hussein1 and Kassoum O. Kassoum1

1Department of Crop Protection, Faculty of Agriculture,

University of Ilorin, Nigeria 2Department of Agronomy, Faculty of Agriculture,

University of Ilorin, Nigeria

Abstract: Seed health testing of fifteen soybean cultivars obtained from five locations in the Guinea Savannah agro-ecology of Nigeria was carried out using two main seed health testing methods described by the International Seed Testing Association (ISTA); the standard blotter and two variants of agar plate incubation method (Potato Dextrose Agar and Czapeck Dox Agar plate methods) to determine the seed infection by fungi. Seed component plating was also carried out to determine the most active site of infection of the seeds by the fungi. Five fungal species were isolated from the cultivars tested. The percentage of seeds infected with Fusarium sp. and Penicillium sp. was significantly different (p<0.05) among the cultivars, with the highest value standing at 15.20 percent of Fusarium sp. and 8.54 percent of Penicillium sp. in cultivars MSJ and FSSBu, respectively. The difference in the methods of isolation was also significant (p<0.05) and the agar (PDA) plate method was the most efficient in the isolation of Aspergillus sp., Penicillium sp. and Phomopsis sp. The efficiency of the other methods of isolation however varied for the different organisms. The cotyledon was observed to be the most active site of infection with thirteen of the fifteen tested cultivars showing 40–100% of infection of the cotyledons. The need for soybean seed health testing before their distribution to farmers is made manifest in this study.

Key words: soybean, seed-borne, mycoflora, Guinea Savannah, component plating.

Introduction

Soybean is one of the world’s most important grain legumes. It is a source of

high quality protein, vegetable oil and other important industrial food-derived products (milk, fibre and phytochemicals) for human and animal consumption *Corresponding author: e-mail: ahmelad2007@yahoo.com

Oladimeji Ahmed et al. 58

(Lusas and Riaz, 1995; Fukushima, 2000; Kerley and Allee, 2003; Palacios et al., 2004). The protein content of soybean is rated as having a protein digestibility-corrected amino acid score (PDCAAS) of 0.99 (the maximum value for individual protein is 1.0 or 100%) (WHO/FAO/UNU, 2007). It is, therefore, a promising substitute for animal protein source supply which is usually inadequate and expensive for poor households in a developing country like Nigeria. The oil is also cholesterol-free, making it one of the healthiest cooking oils.

Soybean is cultivated to a very limited extent in the sub-Saharan Africa, and Nigeria ranks first in the list of producing countries in the region (Laswai et al., 2005; Shurtleff and Aoyagi, 2007). The major soybean producing areas in Nigeria fall within the Guinea and Derived Savannah agroecological zones with Kaduna, Benue, Plateau and Niger states dominating production. Other areas of production include Nasarawa, Kebbi, Kwara, Oyo, Jigawa, Borno, Bauchi, Sokoto, Taraba, Zamfara and Federal Capital Territory (Omotayo et al., 2007). FAO (2009) soybean production record showed that Nigeria contributed 437,000 MT (about 0.3%) of the produce to the total output (about 0.6%) from Africa in 2003. This level of production is very low compared to the one obtained in Brazil, Argentina, USA and China in the same production year.

Disease is one of the factors contributing to the low productivity of soybean in Africa and Nigeria in particular (Osho and Dashiel, 1995). More than 135 microorganisms have been described on soybeans with about 30 species belonging to the group of economically important pathogens (Roy et al., 2000). Some of the pathogens are now known to be transmitted through seeds (Shovan et al., 2008). Seed-borne pathogens represent a major threat to crop establishment and yield. When soybean seeds are sown, seed-borne pathogens may cause disease or death of plants, resulting in crop losses. When used for direct consumption, seed-borne organisms may cause chemical changes, deterioration in seed content or mycotoxin release with the potentially harmful effect on humans and livestock resulting in food waste or famine (Chiarapa and Gambogi, 1986). A knowledge of the type and quantity of pathogens present in a seed sample will be an indication of the risk of disease development in the crop should the seeds be sown under conditions which allow the pathogens to launch a successful attack. Also, if the seeds are to be disinfected to prevent disease establishment, knowledge of the maximum extent of contamination will help to decide how effective such disinfection is likely to be or whether it would be wise to reject the sample for sowing (Malone and Muskett, 1997).

This study was therefore carried out to isolate, quantify and identify seed-borne fungi associated with the seeds of soybean cultivars obtained from selected locations in the Guinea Savannah agro-ecology of Nigeria and to evaluate the relative efficiency of two main seed health testing methods (blotter and agar plate methods) and to locate the site of infection of the soybean seeds in the seed components.

Seed-borne fungi of soybeans in the Guinea Savannah agroecology of Nigeria 59

Material and Methods

Sources of seeds Soybean seeds were sourced from five locations within the Guinea Savannah

agroecological zone of Nigeria as follows: 3 locations from Southern Guinea Savannah (SGS) located at latitudes 8°4′ and 11°3′ N and longitudes 2°41′ and 13°33′ E and 2 locations from Northern Guinea Savannah (NGS) located at latitudes 9°10′ and 11°59′ N and longitudes 3°19′ and 13°37′ E. The three locations in the Southern Guinea Savannah agro-ecology and the sample zones include: Benue (Buruku, Gboko, Guma and Vandelkya), Kwara (Ilorin and Shonga) and Niger (Bidda and Lapai). The two locations in the Northern Guinea Savannah agro-ecology and the zones include: Adamawa (Gire and Jimeta) and Kaduna (Mai Lafia, Makarfi and Zaria) (Plate 2). Seeds collected belong to three categories: storage seeds, farmer-saved seeds and market seeds. Some of the seeds are shown in Plate 1. The seeds were bulked in labelled muslin bags to allow an exchange of air during transportation and while seeds await laboratory tests.

Figure 1. Map of Nigeria showing the selected locations for a collection of soybean seeds used for the study.

Oladimeji Ahmed et al. 60

Seed inspection The collected seed samples were examined when dry for evidence of the

production of fungal fruiting structures or the effect of fungal pathogens on the physical appearance of the seeds.

Plate 1. Appearance of some seed samples used for the study. Sterilization Soybean seeds used were surface sterilized using 0.5% sodium hypochlorite

(NaOCl) for 30 seconds and later rinsed in several changes of sterile water. A sterile blotter was prepared by first moistening Whatman filter paper #1 with distilled water. The filter papers were then wrapped in aluminum foil for sterilization in the autoclave before arranging them aseptically into sterile Petri dishes.

Isolation and quantification of fungal pathogens from the seeds Two main methods were used to isolate the soybean seed-borne fungi, the

standard blotter and agar plate methods as described by the International Seed Testing Association in the ISTA (1996) procedures. In the Standard Blotter method, ten seeds pre-treated with 0.5% sodium hypochlorite were placed equidistantly on sterile moistened Whatman filter paper #1 in Petri dishes (90mm diameter). Three replicates were prepared per soybean variety. The plates were incubated at 25 ± 2oC under alternating cycles of 12 hours of light and darkness for 7 days. Potato dextrose agar (39g/litre) and Czapeck Dox agar (49g/litre) were used as replacements for the blotter in the agar plate method. The media were amended with streptomycin to suppress bacterial growth. Incidence of the seed-borne fungi was recorded as percentage of the total population for each of the soybean cultivar.

Component plating Component plating was done in accordance with the method described by

Maden et al. (1975). Soybean seeds were soaked for about three hours in sterile water after which the seeds were separated into testa, cotyledon and embryo using

Seed-borne fungi of soybeans in the Guinea Savannah agroecology of Nigeria 61

sterile forceps and a dissecting knife. These three components were later surface sterilized for about 30 seconds with 0.5% NaOCl solution and then separately arranged and equally spaced on PDA medium in 90mm Petri dishes. The setup was incubated as described earlier.

Preparation of cultures from the isolated fungi Hypha or spores were transferred aseptically unto fresh sterile media with an

ethanol flamed inoculating needle to prepare the pure cultures from each of the fungal isolates. The plates were later incubated for seven days at 25oC ± 2oC. The pure cultures are required for identification of the fungal isolates.

Identification of the fungal isolates Morphological characteristics of the isolates on plates were observed.

Temporary slides were also prepared for each of the isolates. The slides were then observed under a compound microscope. The morphological and microscopic features were recorded. These features were matched with those described in standard references (Kulwant et al., 1994; Malone and Muskett, 1997; Mathur and Kongsdal, 2003) for identification of the isolates. The identities of the isolates were confirmed at the plant pathology laboratory of the International Institute for Tropical Agriculture (IITA), Ibadan, Nigeria.

Data collection and analysis The data collected during the exercise were the incidence of seed-borne fungi

recorded as percentage of the population in the different soybean cultivars using different incubation methods and incidence of seed-borne fungi in the seed components of the different cultivars. The collected data were subjected to analysis of variance using SPSS Version 21 statistical package and the means were separated using Duncan’s new multiple range test at the 5% level of significance.

Results and Discussion

Seed cultivars and their sources A total of fifteen soybean cultivars were collected from the thirteen zones in

the five locations selected for the study (Table 1). Seed inspection Table 1 shows the results of dry seed inspection carried out on the collected

seeds. The samples collected from markets showed the highest proportion of

Oladimeji Ahmed et al. 62

broken and shrivelled seeds followed by those collected by farmers. The largest proportion of undamaged seeds was found in those obtained from storage.

Table 1. Categorization of sources of collected seeds into storage, market and farmer-saved and their status.

Cultivars Source Location Undamaged Discoloured Shrivelled Broken TGX1019-2EN Storage Ilorin 96 1 2 1 TGX1835-10E Storage Ilorin 97 2 1 0 Tom 1 Storage Gboko 95 1 1 3 John Green Storage Gboko 94 2 3 1 MSGi Market Gire 95 1 1 3 MSGu (Local) Market Guma 86 3 6 5 MSJ Market Jimeta 94 1 2 4 MSM Market Mai Lafia 91 1 3 5 MSMk Market Makarfi 89 2 3 6 MSZ Market Zaria 75 3 9 13 FSSBu Farmer-saved Bidda 81 2 5 12 FSSB (Agric) Farmer-saved Buruku 88 4 5 3 FSSLa Farmer-saved Lapai 89 2 3 6 TGX1448-2E Farmer-saved Shonga 89 3 4 4 Tom 2 Farmer-saved Vandelkya 93 2 3 2 Mean±SE 90.18±0.91 2.00±0.2 3.33±0.39 4.49±0.59 Values are means of three replicates (each of which is made up of one hundred seeds). Storage seeds were obtained from agricultural establishments and research stations. Market seeds were bought from sales points where farmers buy their planting seeds (MSGi Market Soybean from Gire, MSGu Market Soybean from Guma also known as Local, MSJ Market Soybean from Jimeta, MSMl Market Soybean from Mai Lafia, MSMk Market Soybean from Makarfi, MSZ Market Soybean from Zaria). Farmer-saved soybean seeds (FSSB Farmer Saved Soybean from Bidda, FSSBu, Farmer Saved Soybean from Buruku also known as Agric, FSSLa Farmer Saved Soybean from Lapai).

Isolation, identification and quantification of seed-borne fungi Five fungal species were isolated from the fifteen soybean cultivars tested.

They included Aspergillus sp., Curvularia sp., Fusarium sp., Penicillium sp. and Phomopsis sp. (Table 2). The morphology of the organisms on plates and their microscopic features are shown in Plate 2.

Fusarium sp. and Penicillium sp. showed the significantly different (p=0.05) percentage occurrence in the different soybean cultivars tested. Cultivar MSJ with the significantly high percentage occurrence (15.2) was obtained from the market. All the fungal isolates appeared on all the soybean cultivars.

The results also showed that PDA performed better than the other methods in isolating Aspergillus sp., Penicillium sp. and Phomopsis sp. and blotter performed significantly (p=0.05) better than the other methods in isolating Fusarium sp. (Table 3).

Seed-borne fungi of soybeans in the Guinea Savannah agroecology of Nigeria 63

Table 2. Occurrence (%) of fungi on seeds of different soybean cultivars.

Cultivars Aspergillus sp. Curvularia sp. *Fusarium sp. *Penicillium sp. Phomopsis sp. TGX1019-2E 4.3 5.1 8.9abc 4.3ab 107 TGX 1835-10E 3.5 10.8 13.1ab 1.3b 4.6 Tom1 3.3 5.6 10.9abc 3.4ab 10.1 John Green 3.6 8.9 8.9abc 1.6ab 9.8 MSGi 1.8 8.5 11.1abc 1.8ab 9.7 MSGu (Local) 7.7 4.1 9.3abc 3.6ab 9.5 MSJ 1.9 3.1 15.2a 4.1ab 9.1 MSM 5.6 5.5 9.5abc 5.7ab 7.0 MSMk 6.2 6.9 5.9abc 3.2ab 11.1 MSZ 4.7 3.1 7.5abc 6.3ab 11.6 FSSB 8.1 4.1 5.7bc 8.5a 6.9 FSSBu (Agric) 8.6 3.3 6.4abc 8.5a 4.9 FSSLa 7.9 8.7 3.3c 7.4ab 6.0 TGX1448-2E 4.1 6.3 10.5abc 4.6ab 7.8 Tom2 3.8 9.5 8.3abc 2.2ab 9.5 NS (Not significantly different at the 5% level of probability). *Significantly different at the 5% level of probability. Values in the same column followed by the same letter(s) are not different significantly at p=0.05 by Duncan’s multiple range test.

Table 3. Relative effectiveness of the methods of isolation of soybean seed-borne fungi. Methods of isolation Aspergillus sp. *Curvularia sp.* *Fusarium sp. Penicillium

sp. Phomopsis sp.

Blotter 5.1 2.7b 17.6a 4.1 3.9b

Czapeck Dox 4.4 9.5a 4.4b 4.2 10.6a

PDA 5.6 6.5a 4.9b 5.1 11.2a *Significantly different at the 5% level of probability. Values are percentages of isolated fungi. Mean values in the same column followed by the same letter (s) are not significantly different at p=0.05.

Infection of the seed components The percentage infection of the soybean seed components is shown in Table 4.

It was observed that the cotyledon was the most active site of infection of the seed components. The data showed the highest infection percentage of the cotyledons for thirteen of the fifteen soybean cultivars with mean values ranging from 40 to 100.

A high proportion of broken and shrivelled market seeds observed in this study indicate that the sellers care less about the status of the seeds they sell to farmers. This might be due to their poor education and awareness of the implication of poorly handled seeds meant for planting. On the other hand, farmers are aware of the risk involved in poor handling of their buffer stocks, so they take adequate care to secure them for planting in the coming season. The same goes for seeds in the research stations and other agricultural establishments.

Oladimeji Ahmed et al. 64

Table 4. Mean percentage infection of soybean seed components. Cultivars Seed components Mean no. of isolates Total Percentage

TGX1019-2EN Testa 1 12.50 Cotyledon 6 8 75.00 Embryo 1 12.50

TGX1835-10E Testa 2 27.57 Cotyledon 3 7 42.86 Embryo 2 28.57

Tom1 Testa 3 25.00 Cotyledon 6 12 50.00 Embryo 3 25.00

John Green Testa 1 10.00 Cotyledon 6 10 60.00 Embryo 3 30.00

MSGi Testa 4 33.33 Cotyledon 5 12 41.67 Embryo 3 25.00

MSGu (Local) Testa 6 43.00 Cotyledon 4 14 28.50 Embryo 4 28.50

MSJ Testa 3 30.00 Cotyledon 4 10 40.00 Embryo 3 30.00

MSM Testa 3 23.08 Cotyledon 4 13 46.15 Embryo 6 30.77

MSMk Testa 3 33.33 Cotyledon 4 9 44.45 Embryo 2 22.22

MSZ Testa 3 37.50 Cotyledon 4 8 58.00 Embryo 1 12.50

FSSBu (Agric) Testa 2 30.00 Cotyledon 3 7 40.00 Embryo 2 30.00

FSSB Testa 3 33.11 Cotyledon 1 9 11.11 Embryo 5 55.78

FSSLa Testa 1 16.67 Cotyledon 3 6 50.00 Embryo 2 33.33

TGX1448-2E Testa 0 0.00 Cotyledon 3 3 100.00 Embryo 0 0.00

Tom2 Testa 3 23.08 Cotyledon 8 13 61.54 Embryo 2 15.38

*A percentage was calculated by expressing the mean number of isolates as a percentage of total number of seeds.

Seed-borne fungi of soybeans in the Guinea Savannah agroecology of Nigeria 65

This study provides an assessment of the diversity of soybean seed-borne fungi within the Guinea Savannah agroecology of Nigeria. The results showed a varying degree of infection of the different soybean cultivars by the fungi with fairly high frequencies observed in regions with a long history of high productive capacity of the crop in Nigeria (Benue and Kaduna states). This might be attributed to favourable weather conditions for their survival in the region.

Plate 2. Fungi isolated from soybean seeds: A–E are the pure cultures of Phomopsis sp., Aspergillus sp., Penicillium sp., Fusarium sp. and Curvularia sp. F – Phomopsis conidia, G – Macroconidia of Curvularia sp.; H – Conidial head of Aspergillus sp.; I – Conidiophores of Penicillium sp.; J – Micro and macroconidia of Fusarium sp.; K – A close up view of the fruiting bodies of Aspergillus sp. as seen in situ on soybean seeds.

All the fungal isolates observed in this study were listed among the eight species isolated from ten soybean cultivars with agar (PDA) plate and blotter methods in India (Khayum et al., 2006) and the thirty-nine species isolated from

A B

I K

C D

E F G H

J

Oladimeji Ahmed et al. 66

one cultivar of soybean using four methods of isolation in Pakistan (Nasreen, 2003). Both studies also found the agar plate method of isolation to perform better than the blotter method in isolating the fungi. This is in partial agreement with the findings in this study which show that the agar plate method supported better isolation of Curvularia sp., Penicillium sp. and Phomopsis sp. while the blotter method promoted better isolation of Fusarium sp. Michail et al. (1981) however found both methods to be equally good for detecting species of fungi other than Fusarium, Myrothecium and Cephalosporium among the isolated fungal species. The isolation of these three fungi (Fusarium, Myrothecium and Cephalosporium) was better on blotter. The performance of PDA and Czapeck Dox agar can be attributed to the fact that they contain substances essential for the growth of the fungi.

The results of soybean seed component plating show that the cotyledon is the most infected component by the fungi. These results are in line with the findings of Ahmed et al. (2006), but for cowpea seeds. The cotyledon of soybean contains food reserve and may have been the reason for a higher degree of colonization of the seed components.

Conclusion

The seeds of soybean cultivars obtained from the Guinea Savannah agro-

ecology of Nigeria were found to be associated with five fungal species namely Aspergillus sp., Curvularia sp., Fusarium sp., Penicillium sp. and Phomopsis sp. The associated fungal flora was most predominant in the cotyledons of most of the soybean cultivars. The agar (PDA) plate isolation method supported the isolation of more of the fungi than the other methods of isolation.

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Received: February 4, 2015 Accepted: July 1, 2015

Oladimeji Ahmed et al. 68

GLJIVE KOJE SE PRENOSE SEMENOM SOJE (GLYCINE MAX [L.] MERR) U AGROEKOLOŠKIM USLOVIMA GVINEJSKE SAVANE U NIGERIJI

Oladimeji Ahmed1*, Olusegun S. Balogun1, Oluyemisi B. Fawole2, Oluwatoyin A. Fabiyi1, Aliyu T. Hussein1 i Kassoum O. Kassoum1

1Odsek za zaštitu bilja, Poljoprivredni fakultet,

Univerzitet u Ilorinu, Nigerija 2Odsek za agronomiju, Poljoprivredni fakultet,

Univerzitet u Ilorinu, Nigerija.

R e z i m e

Ispitivanje zdravstvenog stanja petnaest sorti soje dobijenih sa pet lokacija u agroekološkim uslovima gvinejske savane u Nigeriji sprovedeno je korišćenjem dve glavne metode za testiranje zdravstvenog stanja semena koje je opisala Međunarodna organizacija za ispitivanje semena (International Seed Testing Association – ISTA); standardni filter papir i dve metode inkubacije na podlozi (krompir-dekstrozni agar i Čapek Dox agar) kako bi se odredila zaraza semena gljivama. Zasejavanje delova semena obavljeno je da bi se odredilo najaktivnije mesto zaraze semena gljivama. Pet vrsta gljiva su izolovane iz sorti koje su ispitivane. Procenat semena zaraženih gljivama Fusarium sp. i Penicillium sp. bio je značajno različit (p<0,05) među sortama, sa najvećom vrednošću od 15,20% semena zaraženih gljivom Fusarium sp. i 8,54% semena zaraženih gljivom Penicillium sp. kod sorti MSJ odnosno FSSBu. Razlika u metodama izolacije takođe je bila značajna (p<0,05) i metoda podloge agara (PDA) bila je najefikasnija u izolaciji gljiva Aspergillus sp., Penicillium sp. i Phomopsis sp. Međutim, efikasnost drugih metoda izolacije varirala je za različite organizme. Primećeno je da je kotiledon najaktivnije mesto zaraze kod trinaest od petnaest ispitanih sorti pokazujući 40–100% zaraze kotiledona. Potreba za ispitivanjem zdravlja semena soje pre njihove distribucije do poljoprivrednika postala je očigledna u ovom istraživanju.

Ključne reči: soja, prenošenje semenom, mikoflora, gvinejska savana, zasejavanje delova semena.

Primljeno: 4. februara 2015.

Odobreno: 1. jula 2015.

*Autor za kontakt: e-mail: ahmelad2007@yahoo.com