stored maize grains fungi and fumonisin b1 production · 3- detection of fumonisin b1 (fb1)...

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J.Agric.&Env.Sci.Alex.Univ.,Egypt Vol.8 (2)2009

STORED MAIZE GRAINS FUNGI AND FUMONISIN B1

PRODUCTION

EL-SHEIKH, M.A*., S.I.ATTA-ALLA*., M.M.RAHAL ** AND

R.M.El-TAHAN **.

* Plant Path. Dept., Fac.Agric., Damanhour, Alex.Univ.

** Plant Path.Res.Inst., Agric.Res.Station, Etay El-Barood.

ABSTRACT

Samples of some maize hybrid grains were taken from

five localities at Elbehera governorate and analyzed for

various ear-rot fungi and Fusarium mycotoxins during the

growing season 2007. Fusarium spp were the most common

fungal isolates followed by Aspergillus spp and Penicillium

spp with averages of 20.3, 10.4 and 10.1 %, respectively.

Among Fusarium spp., F. verticillioides was the most

dominant with an average of 13.5 %. The frequency of

Fusarium spp were higher than the other isolated fungi from

grains of maize hybrids stored four months at (5 C◦ + 73 %

RH), (10 C◦ + 64 % RH), (15 C

◦ + 50 % RH) or at room

temperature (23±2+70% RH).The frequency of Penicillium

spp and Aspergillus spp were differed according to the

storage conditions. Maize hybrid grains stored at (room

conditions) had the highest oil and starch contents with

averages of 3.65 and 54.56 %, respectively. The visual

intense of fumonisin B1 (FB1) was varied among Fusarium

species and within the same species. The highest potency was

in case of F.verticillioides isolate No.27, however, Kom

Hamada, Etay Elbaroud and Damanhur isolates were the

highest in this concern .

Keywords: maize, storage, relative humidity, temperature, Fusarium, oil,

starch, fumonisin B1.

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INTRODUCTION

Maize (Zea maize L.) along with rice and wheat are the three

most important stable food grains all over the world (Sobhi, 1991) for

human and animal consumption (Diab et al.,1989). Also, grains and

ears are liable to be infected by several pathogens in both field and

during storage.The highest frequency of isolated fungi from corn

grains were Fusarium spp, Aspergillus spp, Helminthosporium spp,

Alternaria spp and Penicillium spp (Elsayed,1996). In general, at

temperature ranged from 5 to 10 C ˚, storage molds grow very slowly;

while at 27 to 44 C˚, growth is very fast (Pierce and Thompson, 1985).

Many toxigenic mold spp produce mycotoxins in their substrates

depending on microclimatic conditions. In the past three decades,

research showed variability of the frequency of toxigenic molds and

their secondary metabolite mycotoxins in cereals and diet (5-58 %)

from year to year depending on their harvest and post harvest

conditions (Abol Alea, 1996; Shanhan et al., 2003; Pepeljnjak, 2005

and Suksoon et al., 2006). Also, storage types and duration have an

obvious role on mycotoxins productivity (Paster and Menasherov,

1988 and Ghewande et al., 1993).Mycotoxins are mainly produced by

three genera of fungi, i.e; Aspegillus, Penicillium and Fusarium that

grow on almost every kind of nourishing medium (Schoental, 1985).

Aflatoxins produced mainly by Aspergillus flavus and A. parasiticus

and fumonisin produced by Fusarium verticillioides and F.

proliferatum are considered the most serious and dangerous

mycotoxins contaminating maize commodities in significant amounts

( Mohamed, 1999 and Vincelli and Parker, 2002).

The metabolites of F. verticillioides , the fumonisins, have

received much attention since they were discovered in 1988 in

southeastern part of South Africa, where correlation was found

between the occurrence of human oesophageal cancer and the rate of

fumonisin concentration of cereals (Marsas et al., 1988 and Rheeder et

al., 1992) and liver cancer ( Ueno et al.,1997). In this respect,

Desjardins et al., (2002) reported that maize inoculated with

fumonisin producing Fusarium isolates showed a high frequency of

kernel infections without visible symptoms, but fumonisin levels in

symptomless kernels were generally low. El-Assiuty et al., (2007)

reported that infection with F.verticillioides led to the accumulation of

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this mycotoxin in the molded (discolored) and the adjacent

(symptomless) kernels of non treated ears (29.0 and 14.0 ppm,

respectively).

MATERIALS AND METHODS

1- Survey: 1-1- Samples collection:

Fresh maize ear samples were collected from five localities at

El-Behera governorate; namely Abo Hommos, Damanhour, Etay

Elbaroud, Kafr Eldawar and kom Hamada at harvest time during the

growing season (2007). Kernels at each location and cultivar were

mixed together and 500 g sub-samples were taken at random for

fungal isolation and determination of fumonisin B1 (FB1). 1-2- Isolation:

Maize grains were surface sterilized by 5 % sodium hypochlorite

solution for 2 min, rinsed twice in sterilized distilled water and left to

dry on sterilized filter paper. Isolation was carried out by seeding ten

kernels on PDA and ten replicates were used for each location. Plates

were incubated at 25 – 27 C˚ for 7 days and growing fungi were

transformed into PDA plates and then purified using single spore

and/or hyphal tip techniques according to Hansen (1926), preserved in

15 % glycerol and kept at -80 C˚ for these studies. 1-3- Identification of causal agents:

Isolated fungi were identified according to Burnett, (1960) and

Nelson et al., (1983). Identification of Fusarium spp was done using

manual described by Gerlach and Nirenberg, (1982), Nelson et al.,

(1983), Burgess et al., (1994) and Summerell et al., (2003).

2- Storage of maize grains:

Grain samples, 850 g of maize hybrids, local SC 124, SC 155,

TWC 352, SC 10, SC 129, SC 122, TWC 310 and TWC 314 were

taken randomly from grain lots produced at Sakha Agric, Exp. State.,

Kafr El-Sheikh governorate, Egypt, during 2005 season.Average

moisture content of grains ranged between 12-14.2 % and each hybrid

grains were subdivided into four samples and kept in a sterile cloth

bags, sealed and put in plastic box containing 2 cups; the first had 20

ml H2O and the second had 20 ml of 30, 40 or 50 % KOH for gettins

73, 64 and 50 % relative humidity (RH) (Solomon, 1951). Samples

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were transferred immediately to three refrigerators and kept at 5, 10

and 15 C˚, while the fourth sample kept under room conditions (23 + 2

C + 70 % RH) and all of them stored four months. At the termination

of the storage period, isolation, identification for grain borne fungi

were carried out. Moreover, grain oil and starch contents were

determined according to Walker et al. (1972) and AOAC. (1980)

respectively.

3- Detection of fumonisin B1 (FB1) produced by Fusarium spp

isolates:

The properties of 50 different Fusarium spp isolates to produce

FB1 were measured after their culturing on maize grains according to

Dupuy et al., (1993). All Fusarium isolates recovered from different

localities were subjected to visual qualitative detection on TCL plates.

Toxigenic isolates were grouped according to their fluorescence

intensity into low to high (from + to + + + + +) and the signal ( - )

referring to non potent isolates.

RESULTS

Survey:

Results recorded in ( Table 1 ) show that, Fusarium spp. were

the most common fungal isolates recovered from the maize ears at the

chosen localities with general average of 20.3 % followed by

Aspergillus spp and Penicillium spp with averages of 10.4 and 10.1 %,

respectively. Generally, Fusarium spp could be found in high

frequency in Abo Hommos and Etay Elbaroud localities compared

with the other localities with averages of 27.25 and 24.15 %,

respectively. At the same time, Aspergillus spp had the highest

frequency in Etay Elbaroud followed by Kom Hamada and Abo

Hommos with averages of 19.00, 15.50 and 9.62 %, respectively. In

case of Penicillium spp Etay Elbaroud had the highest frequency

followed by koum Hamada and Damanhour with averages of 22.5, 9.0

and 2.0 %, respectively. On the other hand, Kafr Eldawar showed the

highest value in case of Alternaria spp followed by Etay Elbaroud

with averages of 15.0 and 8.0 %, respectively. Finally, it was noticed

that isolates of Rhizopus spp appeared at low frequency. Among

Fusarium spp F.verticillioides was the most dominant species with

general average of 13.5 %. Abo Hommos had the highest value

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followed by Etay Elbaroud, Kom Hamada, Kafr Eldawar and

Damanhour with averages of 20.5, 13.5, 11.0, 10.0 and 8.0 %,

respectively. F. proliferatum occurred in low frequency and the same

trend appeared in case of F. semitectum, F. oxysporum, and F. solani.

Concerning Aspergillus spp; A. niger appeared at high frequency

followed by A. flavus with general averages of 6.9 and 3.7 %,

respectively. In case of Penicillium spp, it was isolated from the all

samples with general average of 10.1 %. Alternaria spp were isolated

at high frequency only in case of samples obtained from Kafr Eldawar.

Finally, Rhizopus spp were isolated only from Abo Hommos and Kafr

Eldawar maize grain samples.

Results obtained in ( Table 2 ) show the frequency of the isolated fungi

from some maize cultivars grains stored four months under four

storage conditions; (5 C˚ + 73 % RH), (10 C˚ + 64 % RH), (15 C˚ + 50

% RH) and room temperature (23+ 2 C˚ + 70 % RH).

Storage of maize grains at (5 C˚ + 73 % RH)

Data in (Table 2) showed that, the isolation frequency of

Fusarium spp was 21.02 %. The occurrence of Penicillium spp and

Aspergillus flavus averages were 3.70 and 0.38 %, respectively. In

case of Fusarium spp the highest frequency appeared in case of the

cultivar SC129 and the lowest one with the cultivar TWC 310 with

averages of 27.50 and 10.20 %, respectively. On the other hand, TWC

310 had the highest frequency of Penicillium spp and Aspergillus

niger was isolated from TWC 352 and SC 129 and A. flavus was

isolated from SC 10 and SC 122. Finally, Rhizopus was isolated only

in case of SC 124.


From (Table 2), (10 C + 64 % RH) treatment had the same trend

as in the treatment of (5 C + 70 % RH) where the frequency of

Fusarium spp was the highest compared with the other isolated fungi

with an average of 22.05 %. Concerning Fusarium spp, the highest

frequency appeared with SC 124 and the lowest one showed in case of

the cultivar SC129 with averages of 29.60 and 10.20 %, respectively.

Penicillium spp were detected only with SC10 and TWC 314. A. niger

was isolated from TWC 352 and TWC 310 and A. flavus from SC

10, TWC 314, SC 155, TWC 352, SC 124 and TWC 314.

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Data in (Table 2) showed that, the same trend was observed in

case of Fusarium spp where it had the highest value. In case of cultivar

TWC 352, Fusarium spp exhibited the highest value (27.43 %)

followed by SC 124, SC 122, SC 129, SC 10, TWC 314, SC 155 and

TWC 310. A. niger was isolated from the most cultivars except in

case of TWC 352. In addition, A. Flavus was only isolated from SC

124 and TWC314. Finally, Rhizopus was isolated from SC 155 only.

Storage of maize grains at (23 + 2 + 70 % RH).:

Data presented in (Table 2) showed the high frequency

of Fusarium spp followed by A. flavus, A. niger, Penicillium spp and

Rhizopus, respectively. In addition, Fusarium spp exhibited the

highest frequency (31.60%) in case of SC 124 followed by TWC 310,

TWC 314, SC 10, SC 122, TWC 352, SC 129 and SC 155,

respectively. Penicillium spp was isolated from SC 129, SC 155 and

SC 124. A. niger was recovered from TWC 352, SC 10, SC 122, TWC

310 and TWC 314, respectively. Additionally, A. flavus was isolated

from SC 122, SC 129, SC 124 and SC 10. Finally, Rhizopus was

isolated only in case of TWC 314 and TWC 352

Oil determination:

Data in (Table 3) show that, maize hybrid grains stored for four

months at different conditions showed variance in oil content. When

grains were stored at (5 C˚ + 73 % RH), Sc 122 and SC 129 had the

highest oil content with averages of 4.16 and 4.00 %, respectively. On

the other hand, grains stored at (10 C˚ + 64 % RH) exhibited the

highest values of oil content in case of SC 129 and TWC 310 with an

average of 4.13 % for the two cultivars. When grains were stored at

(15 C˚ + 50 % RH), the oil content percentages decreased in case of

the all tested hybrids compared to its oil percentages in case of the

storage condition (10 C˚ + 64 % RH). In case of grains stored at (room

temperature) the cultivar Sc 122 had the highest oil content followed

by SC 129 with average of 4.33 and 3.90 %, respectively. Generally, it

is clear that maize hybrid grains stored at (room temperature) had

the highest oil content with an average of 3.65 %.

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Starch determination:

Data in (Table 4) show that, maize hybrid grains stored for four

months at different storage conditions had different starch content

percentages. Storage at (5 C˚ + 73 % RH) showed that SC 155 and

TWC 352 had the highest starch content with averages of 59.63 and

56.17 %, respectively. When grains were stored at (10 C˚ +64 % RH),

TWC 310 and SC 129 had considerable starch percentages with

averages of 60.47 and 58.47 % respectively. Meantime, TWC 310

followed by SC 122 had the highest values when the hybrid grains

stored at (15 C˚ + 50 % RH) with averages of 54.72 and 49.98 %,

respectively. Finally, room conditions were the favorable conditions to

SC 124 and TWC 310 where they had starch content with averages of

61.60 and 58.70 %, respectively.

Detection of Fumonisin B1 (FB1):

Results in (Table 5) indicate a clear correlation between the

intensity of the fluorescence under UV visual scanning and the visual

intense of fumonisin B1. It could be noticed that F. verticillioides was

the dominant isolate recovered from all localities. The visual intense

of fumonisin varied from Fusarium species to another and within the

same species. The highest visual intense appeared in case of

F.verticillioides isolate No.27 (+++++) which was isolated from

SC 10 at Damanhour followed by F. proliferatum isolate No.7 from

SC 10 at Kafr Eldawar and F. verticillioides No.38 from 30K08 at

Koum Hamada (++++). The visual intense (+++) was noticed in case

of F. verticillioides isolates No.20 from SC 122 at Abo Hommos, No.

26 and 28 from Sc 10 at Damanhour. In addition, the same intensity

observed with isolates No.36, 37 and 39 from 30K08 at Koum

Hamada, No.42 and 43 from SC 52 and No.49 from 30K08 at Etay

Elbaroud. Generally, Fusarium isolated from Koum Hamada, Etay

Elbaroud and Damanhour localities have the potential to produce the

highest fluorescence intensity compared with the isolates from the

other two localities.

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DISCUSSION Survey of fungal genera was done throughout this investigation

showed that, Fusarium spp were the major residents that isolated from

the maize ears in all studied localities from El-Behera governorate

followed by Aspergillus spp and Penicillium spp with averages of

20.3, 10.4, and 10.1 %, respectively. This result is in agreement with

the findings of Elshabrawi 2001 and 2007 who reported that Fusarium

spp and Aspergillus spp are cosmopolitan fungi that could be

recovered from infected or even healthy maize ears.

The highest frequency of isolated fungi appeared in case of cvs.

SC52 and 30K08 cultivated in Etay Elbaroud with averages of 17.56

and 11.90 %, respectively. Generally, the isolated pathogenic fungi

from maize grains were differed in their frequency according to the

cultivar and locality. In this concern, Limonard, (1968) and Sobhi,

(1991) mentioned that species and frequency of pathogenic fungi

differed depending upon host cultivar and the environmental

conditions. Among Fusarium spp, F. verticillioides was the most

dominant species recovered from the maize ear samples followed by

F. oxysporum , F. solani, F. semitectum, and F. proliferatum with

averages of 13.5, 2.6, 1.5, 1.4 and 1.2 %, respectively. This result is in

harmony with the findings of Nelson et al. (1983), and Elshabrawi

(2001). Yates and Jaworski, (2000) reported that F. verticillioides

growth on maize is dependent on tissue type, age and conditions.

The differences between cultivars with the isolated fungi may be

due to water availability in the grain and temperature (Mangan and

Lacey, 1987) and maize pericarp and aleurone layer containing

phenolic compounds which shown some antifungal effects ( Rouau et

al., 2003 and Strebova et al., 2004).

Results appeared that Fusarium spp had the highest frequency

under the tested storage conditions, but the frequency varied between

the hybrids. At the storage condition (23C˚±2 + 70 % RH) it can

be noticed that Fusarium spp had the highest frequency followed by

(10 C˚ + 64 % RH), (5 C˚ + 73 % RH) and (15 C˚ + 50 % RH) with

general average of 25.19, 22.05, 21.02, and 15.03 %, respectively.

In this respect, El-Shabrawi, (2001) mentioned that the optimum

temperature for recovering Fusarium spp was (17-27 C˚). Results

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showed that the highest frequency of Penicillium spp exhibited in case

of (5 C˚ + 73 % RH) followed by (15 C˚ + 50% RH), (room

conditions) and (10 C˚ + 64% RH) with general average of 3.70, 2.87,

1.30 and 0.96 % respectively, Concerning Aspergillus spp, data

appeared that A. niger was isolated more than A. flavus and the

hybrids differed in its contamination with them. Majunder et al.,

(1965) classified A. flavus as a thermophilic fungus with an optimum

growth temperature between 36 -38 C˚. These results explain the low

frequency of A. flavus in grains stored at any storage condition tested

in our investigation. Also, the importance of temperature, relative

humidity and storage periods on the isolated fungi frequency was

mentioned by Ono et al., (2002) and Pezzini et al., (2005).

Our results are in harmony with Shamsuddin (2002) who

showed that temperature, relative humidity and moisture content of

seeds should be kept minimum, and the grains of corn may be stored

safe at temperature of 18 C˚ or less, where he added that the

temperature range of 21-27 C˚ is most conducive to fungal activity. In

addition, he found that at high relative humidity, the life of seed is

reduced, while the viability capacity decreases. Such results were in

agreement with those obtained in the present study. Consequently, it

could be recommend storing maize grains at temperature of 15 C˚ and

50 % relative humidity, where the recovering of Fusarium spp was

noticed at low frequency. When hybrids grains were stored at the four

storage conditions mentioned before, grains oil and starch contents

increased at room conditions and (10 C˚ + 64 % RH). Lim et al.,

(1998) reported that after 48 h of storage at both 25 and 50 % RH, a

slight change in the physical properties of the corn starch was

apparent.

Concerning the production of fumonisin B1 by Fusarium spp, it

could be concluded that contaminated grains of maize hybrids showed

different levels according to fungal isolates. Samples taken from Kafr

Eldawar and Abo Hommos showed the lowest intense fluorescence.

In contrast, samples from Kom Hamada, Etay Elbaroud and

Damanhour showed the highest intense fluorescence (+++++) than the

other isolates. In this respect, some factors as geographical area and

harvest season (Viquez et al., 1996), drastic oscillations in rainfall and

relative humidity near harvest (Visconti, 1996 and Ueno et al., 1997)

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and the prevailing environmental conditions (Ono et al., 2002

and Fandohan et al., 2005) affect fumonisins production and

concentration. The fumonisins have found to occur naturally in corn

based associated with animal toxicoses (Ross et al., 1992) and corn

based human food stuffs (Pittet el al., 1992).

Further studies are needed to investigate the effect of different

storage conditions on the contamination of maize hybrids grains

with fumonisins B1, and much attention must focused due to the

correlation between the occurrence of human cancer and

concentration of the toxin secreted in cereals.

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الملخص العربي

. 1فطريات حبوب األذرة المخزنة وانتاج السم فيومونيسين ب

*محمد أحمد الشيخ ،*سعيد ابراهيم عطاهللا ،**محمد مجدي رحال ، **رشا ممدوح الطحان * قسى أيشاض انثاخ ، كهيح انضساعح تذيس ، خايعح االسكذسيح.

.نثاخ ، يحطح انثحز انضساعيح ، إيراي انثاسد** يعذ تحز أيشاض ا

** ذى أخز عياخ عشائي ي حثب تعط د األرسج ي خسح يشاكض ذاتعح نحافظح انثحيشج

أسفشخ عهياخ انعضل ي ز انعياخ ع أ فطش انفيصاسيو أكثش 6776خالل انسى

% عهي انراني . 67.6، 67.6، 67.6يو تسة انفطشياخ ذاخذا يهي فطش االسثشخهس انثسيه

% . نقذ 66.6قذ خذ أ انع فيصاسيو فيشذيسهيذص أكثش أاع انفيصاسيو عضال تسثح

ظش ي رائح انعضل ا أاع انفطش فيصاسيو ي األكثش ذكشاسا ع تاقي انفطشياخ انعضنح ي

نخضح نذج أستعح شس ذحد ظشف ي انحشاسج انشطتح حثب اند انخرهفح ي األرس ا

66% ( ذحد ظشف انغشفح ) 67˚+ و66% ( ، ) 16˚ + و67% ( ، ) 66˚ + و6انسثي ي )

% ( . قذ اخرهف ذكشاس فطشياخ انثسيهيو االسثشخهس ذثعا نظشف انرخضي كا 67+ ±6

انغشف كاد األعهي في يحراا ي انضيد انشا خذ أ حثب د األرسج انخضح ذحد ظشف

% عهي انراني . 66.61، 6.16تسة

ي ع آلخش ي فطش 6عالج عهي رنك فقذ اخرهفد انكثافح انشئيح نهركسي فيييسي ب

ي فطش 66انفيصاسيو أيضا داخم فس انع . قذ نحظد أعهي كثافح يشئيح في حانح انعضن

سيو فيشذيسهيذص . تصسج عايح خذ أ عضالخ انفيصاسيو انعضن ي ياطق كو حاد فيصا

، ايراي انثاسد ، ديس نا انقذسج عهي اراج أعهي كثافح ي انفهسج كذنيم عهي قذسج ز انعضالخ

عهي اراج انرشكيض االعهي ي انركسي .

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stored maize grains fungi and fumonisin b1 production · 3- detection of fumonisin b1 (fb1)...

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