Mycopathologia (2007) 164:127–134 DOI 10.1007/s11046-007-9017-8
Fumonisins production by Fusarium proliferatum strains isolated from asparagus crown Chenglan Liu Æ Wenna Xu Æ Fengmao Liu Æ Shuren Jiang
Received: 28 November 2006 / Accepted: 2 April 2007 / Published online: 13 July 2007 Springer Science+Business Media B.V. 2007
Abstract The present work deals with the capability for producing fumonisin by Fusarium proliferatum strains isolated from asparagus in China. Fifty of F. proliferatum strains were randomly selected and incubated on cultures of maize grain and asparagus spear, respectively. Fumonisin levels (FB1 and FB2) were determined by high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry (HPLC-ESI-MS/MS). The results showed that all 50 strains produced fumonisins in maize culture within a wide range of concentrations, 10–11,499 mg/g and 2–6,598 mg/g for FB1 and FB2, respectively. On culture of asparagus spear,48 strains (96%) produced fumonisins in the range 0.2–781.6 mg/g and no detected to 40.3 mg/g Electronic supplementary material The online version of this article (doi: 10.1007/s11046-007-9017-8) contains supplementary material, which is available to authorized users. C. Liu F. Liu S. Jiang (&) Department of Applied Chemistry, College of Science, China Agricultural University, Beijing 100094, P.R. China e-mail:
[email protected] C. Liu Key Lab of Pesticide and Chemical Biology, Ministry of Education, South China Agricultural University, Guangzhou 510642, P.R. China W. Xu Institute of Vegetable and Ornamental Crops, Grossbeeren 14979, Germany
for FB1 and FB2, respectively. All of F. proliferatum strains produced much higher levels of FB1, FB2 and total fumonisins (FB1 + FB2) in maize grain culture than in asparagus spear culture. Meanwhile, fumonisin B3 (FB3) was identified in all maize culture extracts and most of asparagus spear culture extracts. This is the first study carried out the fumonisinproducing ability of F. proliferatum strains isolated from asparagus in China. The information obtained is useful for assessing the risk of fumonisins contamination in asparagus spear. Keywords Asparagus China Fumonisin Mycotoxin Fusarium proliferatum
Introduction The Fumonisins are a group of structurally related mycotoxins isolated initially from corn culture material of Fusarium verticillioides (Sacc.) Nirenberg (former named as F. moniliforme J. Sheldon) [1]. The elucidation of the chemical structure of the fumonisins was carried out by Bezuidenhout et al. [2]. F. verticillioides and F. proliferatum (Matsushima) Nirenberg have been recognized as the highest fumonisin producers, and the most isolates of these two species are able to produce fumonisins [3]. Fumonisins are responsible for serious diseases affecting humans and animals. The most abundant fumonisin produced in nature is fumonisin B1 that
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causes leukoencephalomalacia (LEM) in horses, pulmonary edema syndrome (PES) and hydrothorax in pigs, and liver cancer in rats [4–6], and hypercholesterolemia, and a number of immunological alterations in several animal species [7]. Although the effects of fumonisin on humans are difficult to determine, epidemiological studies suggest a correlation between the consumption of corn contaminated with F. verticillioides and a high incidence of human esophageal cancer [8–13]. On the basis of available toxicological evidence, the International Agency for Research on Cancer (IARC) in 2002 [14] classified FB1 as possibly carcinogenic to humans (class 2B carcinogen). Asparagus (Asparagus officinalis L.) has recently received increased worldwide interest because of its unique taste, high nutritional value, and the presence of biotic compounds [15]. China is one of the largest country of producing and exporting of asparagus in the world, where Shandong province occupies the top rank. The largest part of the asparagus products from China is exported to the countries, such as Japan and Germany. Fusarium species infected with asparagus plants has been reported in several countries, as causal pathogens of stem and crown rot of asparagus [16–20]. In China, a systemic monitoring of latent Fusarium infection of asparagus plants was carried out by Xu et al. (article submitted for publication), and the results showed that the most plants samples in Caoxian county, Shandong province were infected with F. proliferatum. Further study demonstrated a light fumonisin contamination of asparagus spears in this region [21]. However, only limited data on the ability of local fungal strains to produce mycotoxins are available. The aim of the present work was to evaluate the ability of F. proliferatum strains isolated from asparagus crowns sampled from in the northwestern Shandong province, the main asparagus-producing region of China, to produce fumonisins in vitro.
Mycopathologia (2007) 164:127–134
the province of Shandong (China), were analyzed for fumonisins production in cultures of maize grain and asparagus spear, respectively. A spore suspension of each strain was prepared in sterilized distilled water and after enumeration of conidia, a dilution containing 107 conidia per milliliter was used to inoculate on maize grain and asparagus spear substrate, respectively. All treatments were replicated two times. Corn grain cultures Thirty gram of coarsely cracked maize were placed in Erlenmeyer flasks (300 ml), 30 ml of distilled water added, autoclaved at 1218C for 1 h and allowed to stand overnight. Each flask was inoculated with 2 ml of the spore suspension described above, and incubated in the dark at 25 ± 18C for 30 days and shaken once or twice daily for 3 days to aid in even distribution of the inoculum. Harvested maize cultures were frozen at 798C for 60 min, then lyophilized and packed in plastic bags, labeled and stored at 208C for fumonisin analysis. Asparagus spear cultures The asparagus spears (‘‘UC 157’’ green, bought from Bureau of plant protection of Beijing, China), which the asparagus spears were not infected with mycotoxigenic Fusarium strains such as F. proliferatum or F. moniliforrme, were washed in tap water, surfacedisinfected with 3% solution of sodium hypochlorite for 3 min, and rinsed in distilled water for 3 min. A transverse slice of the spear approximately 2–5 mm wide was cut approximately 2 cm from apical and basal ends of each spear segment. Segments were removed to the surface, and immerged into the spore suspension for 60 min and then dredged. Each Petri dish (15 cm of diameter) was put into 20 species of segment, and incubated at 25 ± 18C in the dark for 10 days. Harvested spear cultures were lyophilized and stored under the same conditions as those for the maize culture.
Materials and methods Fumonisins extraction and clean-up Strains and Mycotoxin production A total of 50 strains of F. proliferatum, which isolated from different asparagus crowns collected in eight fields of asparagus located in Caoxian county,
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Fumonisins were extracted from fungal cultures by the method described in our previous study [21]. Samples (0.5 g, dry weight) were extracted by blending for 5 min with 15 ml of methanol/water
Mycopathologia (2007) 164:127–134
(3:1, v:v) in an Ultra-Turrax T18 basic disperser followed by centrifugation at 4,000 g for 15 min. The supernatant was adjusted to pH 5.8–6.5 with 0.25 M NaOH, and 8 ml was applied to a strong anion exchange (SAX) cartridge (Agilent Co., USA) preconditioned with 8 ml of methanol followed by 8 ml of methanol/water (3:1, v:v) at a flow rate of 2 ml/ min. The cartridge was washed with 8 ml methanol/ water (3:1, v:v), followed by 8 ml of methanol. Finally, fumonisins were eluted at a flow rate of 1 ml/min with 10 ml of 1% methanolic acetic acid. The eluate was evaporated to dryness at 408C under a stream of nitrogen and redissolved in 1 ml methanol/water (60:40, v:v), filtered through a 0.22 mm solvent resistant membrane, then stored at 48C until HPLC-ESI-MS/MS analysis. HPLC-ESI-MS/MS analysis Fumonisin standards were purchased from Sigma Chemical Co. (St Louis, MO, USA). Standard solutions were prepared containing FB1 (100 mg/ml) and FB2 (100 mg/ml) in methanol/water (60:40, v:v). Fumonisins (FB1 and FB2) were quantified according to the method described by Liu et al. [21]. An aliquot (20 ml) of the purified extract was analyzed by high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. The LC/MS system was equipped with Agilent 1100 HPLC (Agilent Co., USA) including a gradient pump, solvent degasser and autosampler, and Agilent 1100 LC/MSD ION TRAP VL mass spectrometer with an ESI interface (Agilent Co., USA). Chromatographic separations were carried out on an Agilent C 8 column (150 · 4.6 mm i.d., 5 mm; Agilent, USA) using a binary gradient. Solvent A was 0.05% trifluoroacetic acid (TFA) in water (v/v), and solvent B was 0.05% TFA in methanol (v/v). For fumonisins’ analysis the gradient program was: 0–3 min, 63% B; 3–10 min linear gradient to 100% B; hold 100% B for 6 min; 16–17 min linear gradient from 100% B to 63% B; hold 63% B for 1 min. Total runtime was 18 min. The flow rate was 0.8 ml/min. The outlet of the HPLC column was split (6:4) to the ESI interface of the mass analyzer. For pneumatically assisted ESI, the spray capillary voltage was set to 3.5 kV. Nitrogen served as the nebulizer gas (40 psi), and the drying gas nitrogen was set at a flow rate of 8 l/
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min at 3508C. The mass spectrometer was operated in positive-ion mode. MS-MS was operated at a fragmentation amplitude of 2.75 eV in the MRM mode. For the identification and quantitative analysis of the protonated molecular ion [M + H]+ of FB1 (m/z 722) and FB2 (m/z 706), the following fragment ions were chosen: ions at m/z 352 [M + H-2TCA-H2O]+, 528 [M + H-TCA-H2O]+, and 546 [M + H-TCA]+ for FB1, ions at m/z 336 [M + H-2TCA-H2O]+, 512 [M + H-TCA-H2O]+, and 530 [M + H-TCA]+ for FB2. Standard curves for FB1 and FB2 were linear in the range 0.01–10.0 mg/ g. The detection limits for FB1 and FB2 were 0.01 mg/g and 0.005 mg/g, respectively. The recoveries ranged from 90.8 to 96.3% for FB1 and from 82.8 to 110% for FB2, and the repeatabilities, expressed as RSD, were in the range 2.2–13.4% for FB1 and 4.5–14.2% for FB2.
Results Analysis of the toxin-producing activity of F. proliferatum showed that all 50 strains tested in the present study could produce FB1 and FB2 in maize grain. The levels obtained ranged from 10 to 11499 mg/g of dried culture for FB1, and from 2 to 6,598 mg/g for FB2. Forty-three of the 50 strains produced more than 500 mg/g of fumonisin B1 range from 802 to 11499 mg/g (Table 1). In culture of asparagus spears, 48 out of 50 strains of F. proliferatum (96%) produced FB1 in the range from 0.2 to 781.6 mg/g, 92% (46) of F. proliferatum strains produced FB2 in the range from 0.1 to 40.3 mg/g, but only three strains produced over 500 mg/g of fumonisin B1 range from 503.2 to 781.6 mg/g (Table 1). At the same time, fumonisin B3 (FB3) was identified in all maize grain cultures and the most of asparagus spear cultures (No quantified for not FB3 standard). All of F. proliferatum strains tested were produced more FB 1 , FB 2 , and total fumonisins (FB1 + FB2) on maize grain than on asparagus spear (Table 1). The average levels of FB1, FB2 and total fumonisins (FB1 + FB2) found in cultures of maize grain were 3,420, 945, and 4,365 mg/g, respectively. But on asparagus spear cultures, the average levels of FB1, FB2 and total fumonisins (FB1 + FB2) were 116.7, 9.1, and 125.4 mg/g, respectively (Table 1; Figs. 1–3).
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Mycopathologia (2007) 164:127–134
Table 1 Fumonisin production (mg/g)a on maize grains and asparagus spears by F. proliferatum strains isolated from asparagus crowns collected from Shandong province, China, in 2003 Strain No.
Maize grain cultures FB1
Asparagus spear cultures
FB2
Total
FB1
FB2
Total
SCZI1A3
2,297
425
2,722
26.0
3.1
29.1
SCZI2B1
7,416
1,048
8,464
231
15.1
246.1
SCZI3A1 SCZI4B1
1,759 7,200
218 654
1,977 7,854
64.4 70.0
4.6 5.1
69 75.1
SCZI5B2
4,728
2,396
7,124
142.2
21.0
163.2
SCZI6B1
9,948
6,598
16546
29.3
4.7
34
SCZI7B1
1,528
460
1,988
8.9
0.7
9.6
SCZI8A2
5,602
945
6,547
59.4
6.2
65.6
SCZI9A2
2,827
375
3,202
827
149
976
SKZI2A1
4,518
840
SKZI3A3
3,844
484
SKZI4A3
1,798
SKZI5A2 SKZI6A3a
8.9
0.9
9.8
31.8
2
33.8
5,358
316.9
30.4
347.3
4,328
14.0
0.5
14.5
234
2,032
9.2
1.5
10.7
9,891
2,896
12787
503.2
40.1
543.3
2,598
834
3,432
52.4
2.9
55.3
SKZI7A3
1,446
685
2,131
109.3
10
119.3
SKZI8A1
9,733
1,963
11696
617.7
36.0
653.7
SKZI9B3 SKZI10A2
3,642 4,919
965 1,398
4,607 6,317
67.7 110
5.8 9.2
73.5 119.2
SZSLI2A3
918
169
1,087
25.1
1.3
26.4
SZSLI3A1
1,145
185
1,330
20.3
2.0
22.3
SZSLI8B2
6,516
1,683
8,199
0.6
0.1
0.7
SZSLI9A3
2,676
508
3,184
2.3
0.2
2.5
SSWI1A1
802
369
1,171
21.7
1.6
23.3
SCZI10B1
SSWI2A1
918
169
1,087
66.7
15.0
81.7
SSWI3A1
7,067
1,999
9,066
0.3
NDb
0.3
SSWI4B3a
3,451
713
4,164
144.6
3.2
147.8
SSWI5B2
3,943
2,848
6,791
310.8
22.7
333.5
SSWI6A1
169
24
193
42.3
2.9
45.2
SSWI7B2
11499
6,406
17905
11.2
0.4
11.6
SSWI8B2
3,362
1,103
4,465
418.7
40.3
459
SSWI9A3
4,931
1,723
6,654
126.7
9.6
136.3
SSWI10A22
8,207
930
9,137
781.6
35.8
817.4
SYDLII SYDLII5B3
1,127 4,460
127 700
1,254 5,160
191.4 10
8.3 0.5
199.7 10.5 27.4
SYDLII6A2
888
122
1,010
26.0
1.4
SYDLI2A2
1,810
291
2,101
2.6
0.1
2.7
SYDLI6B2
10
2
12
ND
ND
ND
SYDLI7B3
45
6
51
19
2.1
21.1
SYDLI9B3
3,451
713
4,164
103
13
116
ND
ND
ND
33.2
6.1
39.3
SCZII3B1
16
3
19
SCZII4A3
1,311
237
1,548
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Mycopathologia (2007) 164:127–134
131
Table 1 continued Strain No.
Maize grain cultures
Asparagus spear cultures
FB1
FB2
Total
FB1
FB2
Total
SCZII5B3
7,929
1,375
9,304
106.7
7.9
114.6
SCZII7B5
1,512
337
1,849
44.2
3.6
47.8
SCZII9B1
49
28
77
1.2
0.2
1.4
SCZII10B1
146
33
179
0.2
ND
0.2
SSWII3A3
262
91
353
12.2
2.3
14.5
SSWII5B2
820
112
932
319
12.5
331.5
SSWII7A2 SSWII8A3
3,921 1,120
545 130
4,466 1,250
265 21.5
23.1 1.1
288.1 22.6
Mean
3,420
945
4,365
116.7
9.1
125.4
a
Based on dry weight
b
ND, not detected. The concentrations of fumonisins were 0.25 mg/g for FB1, 0.04 mg/g for FB2 in control of maize and no detected for FB1, FB2 in control of asparagus spear, respectively
Attach file 1 Intens. x10 5 6
FB2
5
FB1 4
3
2
FB3
1
0 5
6
7
8
9
10
11
12
13
Time [min]
Fig. 1 Total ion current chromatograms of FB1, FB2 and FB3 in maize grain culture and asparagus spear culture
Discussion Analysis of 50 strains of F. proliferatum from asparagus indicated that 100% and 96% of the strains produced fumonisins in culture of maize grain and asparagus spear, respectively. This is the first time to our knowledge that fumonisins production of F. proliferatum isolated from asparagus in China has been reported. Similar results for fumonisins production by F. proliferatum isolated from asparagus plants found in other studies [20, 22, 23]. Logriceo et al. [22] showed that F. proliferatum isolated from
asparagus crown and stem tissues collected from in Italy produced FB1 in maize grain. Seefelder et al. [23] reported that F. proliferatum strains from asparagus in Germany produced FB1 in the garlic bulbs, and Weber et al. [20] reported F. proliferatum strains isolated from asparagus in Germany produced FB1 on maize kernels. These results showed that F. proliferatum strains isolated from asparagus plants could also produce fumonisin as those strains isolated from maize grain. There was a high degree of variability in the amount of fumonisins produced by different strains of
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132
Mycopathologia (2007) 164:127–134 x10 5
+MS, 9.4mi n #727
706.2 4
3
397.2 2
430.7
1 369.2 313.1
577.3 485.1
345.0
728.1 750.2
521.4
603.3
0 300
350
400
450
500
550
600
650
700
750
m/z
Fig. 2 Positive electrospray mass spectra of FB3
Intens. x10 4
+MS2(706.0), 8.8min #386 512.2
5
4
530.2 336.2
3
2
354.2 318.2
670.2
1
494.2
706.2
548.2
0 300
350
400
450
500
550
600
650
700
750
m/z
Fig. 3 Product ion spectra of FB3 obtained by collision induced dissociation (CID)
F. proliferatum. In the present study, all the strains of F. proliferatum tested produced FB1 and FB2 in the wide range 10–11499 mg/g and 2–6,598 mg/g in maize culture, and produced FB1 (no detected to 781.6 mg/g) and FB2 (no detected to 40.3 mg/g) in asparagus spear culture, respectively. A similar variability in fumonisins production was observed in strains from the other crops [24–27]. The different capability of fumonisin production by F. proliferatum would be influenced by different source of strains and environmental conditions (such as medium, temperature, and water activity).
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Nelson et al. [28] considered strains producing less than 50 mg/g of FB1 to be low producers, those producing 50–500 mg/g to be intermediate producers, and those producing more than 500 mg/g to be high producers. In our study, when these strains grown on maize grain substrate, most of strains (forty-three) would be included in high producers. These strains, be similar to many strains of F. proliferatum isolated from other crops [28–31], have a high potential for fumonisin production in culture of maize grain. But, in culture on asparagus spear, only three strains produced more than 500 mg/g of FB1, most of strains
Mycopathologia (2007) 164:127–134
would be included in low and intermediate producers, twenty-seven strains produced FB1 less than 50 mg/g, twenty strains produced FB1 in the range 52.4– 418.7 mg/g. This result is in contrast to that almost all strains produced high level of FB1 (500 mg/g) on maize grain. Our results demonstrated that the potential for produced fumonisins of F. proliferatum have significant difference on different substrates. Although only fumonisin B1, B2 and, B3 were qualified in this study, it is likely that many F. proliferatum strains produce additional mycotoxins and other secondary metabolites. Strains of F. proliferatum isolated from maize in Canada have been reported to produce the mutagenic fusarins [32], strains of F. proliferatum isolated from rice in American can produce moniliformin [33], and strains of F. proliferatum isolated from maize, wheat, asparagus, and rice in Italy have been reported to produce the cyclic peptide toxin beauvericin [34, 35]. In conclusion, our study shows that 100% (50) and 96% (48) of F. proliferatum strains tested produced fumonisins in cultures of maize grain and asparagus spear, respectively. However, the high capability for producing fumonisins on maize grain and asparagus spear cultures of F. proliferatum strains isolated from asparagus in China was due to incubated on optimal conditions. In fact, the level of fumonisins on the asparagus spear in China is very low [21]. Acknowledgements The authors wish to acknowledge financial support from The Sino-German Center for Research Promotion (GZ051–7(151)).
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