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Comprehensive evaluation of malt volatile compounds contaminated by

Fusarium graminearum during malting

Article in Journal- Institute of Brewing · September 2017

DOI: 10.1002/jib.453

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Research article Institute of Brewing & Distilling

Received: 22 November 2016 Revised: 4 May 2017 Accepted: 14 July 2017 Published online in Wiley Online Library

(wileyonlinelibrary.com) DOI 10.1002/jib.453

Comprehensive evaluation of malt volatile

compounds contaminated by Fusarium
graminearum during malting
Yan Chen,1 Zhe Zhou,1 Kai Xu,2 Han Zhang,1 Megan Thornton,3 Liming Sun,1
Zhenyu Wang,1 Xianbing Xu1 and Liang Dong1*
Fusarium graminearum is the most important filamentous fungi in the malting process, and greatly affects malting performance
and malt quality. Analysis of the emitted volatiles from F. graminearum mycelium was used to evaluate the malt flavour contam-
inated by F. graminearum during malting based on solid-phase microextraction combined with gas chromatography–mass spec-
trometry. GC–MS analysis of different mycelium samples revealed a broad spectrum of volatile compounds including aldehydes,
ketones, alcohols, organic acids and aromatics, which were highly similar to those of barley and malt. Statistical assessment of the
data via principal component analysis demonstrated that the major contributors to the time-dependent dynamic changes in the
volatiles were the volatile aldehyde, alcohol and ketone fractions in the contaminated malting process. The results showed that
volatile concentration was modulated by the -metabolism of the green malt and F. graminearum. Volatile compounds from green
malt were influenced by F. graminearum fungi contamination during malting, although some were probably generated by this
fungus. Copyright © 2017 The Institute of Brewing & Distilling

Keywords: Fusarium graminearum; flavour; malting; volatiles

Introduction by the fungi or impacting the volatile concentration of the green

malt.
Beer is a popular alcoholic malt beverage resulting from a fermen-
tation of the aqueous extract of malted barley with hops (1). Malt is
the kilned and roasted product of barley, in which the flavour Materials and methods
compounds or their precursors often originate from raw barley
(2). The genus Fusarium comprises some of the most important Materials
filamentous fungus in the malting process (3–7), including F.
The barley cultivar used in this study, Metcalfe, was gifted by
graminearum, F. poae, F. culmorum and F. sporotrichioides. The
COFCO Malt (Dalian) Co. Ltd (China), and was harvested in
production of mycotoxins and gushing factors are well known
France in 2015. The F. graminearum strain was originally isolated
negative effects (8–16) of contamination with Fusarium. Among
from brewing barley by the authors. All reagents used in the fol-
these species, F. graminearum greatly affects malting performance
lowing analyses were of at least analytical grade.
and malt quality, and thus has a correspondingly important impact
on beer quality (13,16,17).
Malt flavour is composed of a series of volatile compounds
Fungal spore suspension preparation
including aldehydes, ketones, alcohols, aromatic compounds and
furans (18,19). Although many studies have performed on the F. graminearum spore suspensions were prepared according to the
influences of Fusarium fungi on barley and malt quality, contami- method described by Mauch et al. (21). Briefly, the fungus was
nation of the malt flavour by these fungus has been neglected. cultivated on potato dextrose agar (PDA) plates at 25°C for six days
In our previous work, volatile metabolic changes over the course (22). Small pieces of F. graminearum-inoculated PDA were transferred
of a malting process contaminated by F. poae were investigated
to assess its influence on malt flavour. The results showed that
volatile metabolites from green malt were influenced by contami-
nation with F. poae fungi during malting to an extent, especially for * Correspondence to: Liang Dong, National Engineering Research Center of
Seafood, School of Food Science and Technology, Dalian Polytechnic Univer-
the volatile aldehyde fractions (20). sity, Dalian, Liaoning 116034, China. E-mail: dongliang@dlpu.edu.cn
This study aims to evaluating the contamination of malt flavour
1
by F. graminearum during malting, focusing on the emission of National Engineering Research Center of Seafood, School of Food Science and
volatile compounds from F. graminearum and the dynamics of Technology, Dalian Polytechnic University, Dalian, Liaoning, 116034, China
the volatile compounds contaminated by F. graminearum during 2
COFCO Malt (Dalian) Co. LtdDalian, Liaoning, 116000, China
the malting process. By comparing these two volatile composi-
tions, the influence of F. graminearum on the malt flavour could 3
Centre for Advanced Sensory Science, School of Exercise and Nutrition Sci-
be judged to come from the new flavour compounds contributed ences, Deakin University, Burwood, VIC, Australia

J. Inst. Brew. 2017 Copyright © 2017 The Institute of Brewing & Distilling
Comprehensive evaluation of malt volatile compounds contaminated by Fusarium graminearum during malting
into 500 mL of synthetic nutrient-poor bouillon. The fungal spore
suspension was normally incubated with continuous shaking
(120 rpm) for 6 h to induce spore germination at room temperature
overnight. The concentration of germinating spores was determined
using a haemocytometer. Concentrations of 106 organism/mL were
obtained (23).
F. graminearum mycelium collection
F. graminearum was cultivated on PDA plates at 25°C for 5 days. F.
graminearum mycelium collection was carried out by glass spread-
ing at three and five days respectively. Then mycelium collection
was divided into two parts, both parts were about 2 g in weight,
and cell disruption operation was carried out using one part. The
collected mycelium and cell extraction were stored at 18°C until
analyzed.
Malting procedure and grain inoculation
The barley grains were subjected to a micro-malting procedure.
The grains were soaked in 3% sodium hypochlorite (v/v) for
5 min to remove the microorganisms on the grain surface, and
were then washed with sterile water. The steeping stage
comprised a 5 h wet stage, a 19 h air stage and a 4 h wet stage,
followed by a 20 h air stage. The fungal suspensions (250 mL/kg
barley), including cells and spent medium, were added to both
steeping waters. The germination stage lasted for four days, during
which the grains were moved to perforated stainless steel
germination boxes to ensure aeration. Air and germination stages
were carried out in a humidity-controlled chamber with a specific
humidity of 98%. To compare the effects of F. graminearum on the
malt quality, a control malting experiment was carried out at the
same time using sterile water instead of the fungal suspensions
under the same procedure.
Sample preparation
The germinated barley grains were frozen in liquid nitrogen and
freeze-dried for 48 h. The barley grains and germinated barley
were milled and freeze-dried again for 48 h. The milled flours were
stored at 18°C until analyzed.
Volatile compounds detecting and identifying
The headspace solid-phase microextraction (SPME) technique was
employed to identify and quantify the barley volatile compounds.
In this study, the temperature was maintained at 18 ± 1°C to avoid
the formation of flavour compound artefacts. The barley slurry was
prepared by blending freshly ground flour (3.0 g) and 20% sodium
chloride solution (2 mL) in a 20 mL flask with a cap and Teflon-
faced silicone rubber septa (Supelco, Co., Bellefonte, PA, USA).
The flask containing the sodium chloride, flour and water was
placed on a magnetic stirring plate (model PC-220; Corning Inc.,
Corning, NY, USA) and stirred at 1100 rpm for 20 min. An SPME fi-
bre (DVB/CAR/PDMS) was then exposed to the headspace of the
barley slurry for 1 h in a water bath at 18 ± 1°C (24).
The GC–MS analyses were conducted using an Agilent
6890/5975c Mass Selective Detector (Santa Clara, CA, USA). The
desorption time was 5 min in the injection port at 250°C, and
an HP-5 ms column was used (30 m × 0.25 mm i.d., 0.25 μm film
thickness; J&W Scientific). The temperature was programmed to
be held at 40°C for 5 min, increased to 50°C at a rate of
J. Inst. Brew. 2017 Copyright © 2017 The Institute of Brewing & Distilling
Institute of Brewing & Distilling
2°C/min, and then finally increased to 250°C at a rate of
5°C/min. The carrier gas was helium, which was delivered at a lin-
ear velocity of 2 mL/min. The mass selective detector was oper-
ated in the electron impact ionization mode at 70 eV, in the
scan range m/z 40–400. The interface temperature was 230°C,
and the retention time of each volatile was converted to the
Kovats retention index using n-alkanes (Supelco, Co.) as refer-
ences. The volatile compounds were tentatively identified by
matching the mass spectra with the spectra of the reference com-
pounds in both the Wiley mass spectra (MS) library (8th edn) and
the NIST/EPA/NIH MS library (version 1.5a), and verified on the ba-
sis of mass spectra obtained from the literature and comparison
of Kovats retention indices with those reported in the literature.
The results from the volatile analyses are provided in the peak
area counts of the compounds identified (25). All experiments
were performed in triplicate.
Multivariate data analysis
Barley samples at different malting stages were analysed in tripli-
cate. The peak areas of each volatile compound were standard-
ized. Analysis of variance and principal component analysis (PCA)
were performed using the SPSS system for Windows (version 8;
SPSS, Inc., Chicago, IL, USA).
Results and discussion
Analysis of volatile compounds emitted from F. graminearum
In this work, volatile compounds from the filamentous fungi
during two crucial physiological periods - unsporulated and
sporulated F. graminearum - were detected by culturing them to
3 and 5 days separately. The mycelium was directly collected from
the plates by glass spreading operation to avoid the interference
of volatile compounds from the substrate. Meanwhile, to evaluate
the influence of the autocytolysis on the malt flavour, mycelium
from both stages was disrupted for the GC–MS analysis. Gas
chromatograms of F. graminearum obtained at different
physiological stages are shown in Fig. 1.
The GC approach allowed the identification of 36 peaks in
both conditions including sporulated and unsporulated myce-
lium, as listed in Table 1, including aldehydes, alcohols, ketones,
organic acids and aromatic compounds, based on the retention
times and data from MS libraries. Among them, 17 and 31 of
these were detected in the unsporulated and sporulated myce-
lium, respectively. This suggests that the majority of volatile
compounds emitted from F. graminearum were synthesized
after the mycelium sporulated. The main differences between
these two physiological periods came from the composition of
the volatile aldehydes and ketones, with 2-methyl-propanal,
2-methyl-butanal, pentanal, hexanal, (E)-2-octenal, nonanal, (E)-
2-nonenal, decanal, 3-pentanone, 2-heptanone, and 6-methyl-5-
hepten-2-one only being found in the sporulated mycelium.
Further it was noted that there were more volatiles detected
in the disrupted mycelium compared with that undisrupted.
Comprehensive evaluation of the volatile metabolites
changes contaminated by F. graminearum during malting
As list in Table 1, including aldehydes, alcohols, ketones, organic
acids, aromatic compounds and furans, a total number of 46 vola-
tile compounds were identified during the malting process
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Figure 1. Total ion current chromatogram in the analysis of volatiles from
unsporulated and sporulated Fusarium graminearum by solid-phase microextraction/
gas chromatography–mass spectrometry. (a) Unsporulated mycelium cultured for
3 days; (b) disrupted unsporulated mycelium cultured for 3 days; (c) sporulated myce-
lium cultured for 5 days; and (d) disrupted sporulated mycelium cultured for 5 days.
The peak numbers are consistent with the data in Table 1.
wileyonlinelibrary.com/journal/jib Copyright © 2017 The Institute of Brewing & Distilling
Y. Chen et al.
contaminated by F. graminearum. The standardized data were
assessed via multivariate analysis. To comprehensively evaluate
the volatile metabolite changes with contamination by F.
graminearum during malting, multivariate analysis was conducted
using PCA for each single fraction (aldehydes, alcohols, ketones, or-
ganic acids, aromatic compounds), as well as for the combined
fractions. The score plots obtained for the barley at different stages
of the malting process are shown in Fig. 2(a–f ). In order to assess
the major drivers for the time-dependent separation of the con-
taminated malting barley samples, the PCA loading scores were
also analyzed (Fig. 3a–f ). Additionally, the changes in all of the vol-
atile compounds were illustrated by means of a heatmap (Fig. 4).
The increases and decreases in the volatile metabolites caused
the separation of the contaminated samples in the PCA.
For the combined fractions, the first two principal components,
PC1 and PC2, accounted for 42.1% of the total variation seen in the
control and F. graminearum-contaminated malting procedures
(Fig. 2a). As shown in Fig. 2(a), most of the contaminated malting
samples, which were in the negative region of PC1, were clearly
differentiated from the six control samples, except for the samples
at 24 h. Taking into account the data of all volatile compounds
identified in the six fractions, analysis of the PCA loadings resulted
in the loadings plot shown in Fig. 3(a). This figure demonstrates
that 18 volatile compounds were major contributors to the
separation along the first principal components, including six
aldehydes 2-methyl-propanal, 2-methyl-butanal, pentanal,
2-hexenal, (E)-2-octenal and (E)-2-nonenal two alcohols
[1-penten-3-ol and (Z)-2-nonen-1-ol] and five ketones (acetone,
2,3-pentanedione, 3-hydroxy-2-butanone, 6-methyl-5-hepten-
2- one and 3,5-octadien-2-one), two aromatic compounds
ethylbenzene and benzeneacetaldehyde and three other kinds
of compounds methacrolein, 2-pentyl-furan and 3-ethyl-2-
methyl-1,3-hexadiene. This result reflects the more pronounced
influence of the volatile aldehydes and ketones on the
separation of germinating barley during the malting procedure
shown for the score plot containing the data from both control
and contaminated grains.
To better determine which volatile aldehydes contributed most
to the differences induced by F. graminearum, PCA was applied to
all volatile aldehydes identified. As shown in Fig. 2(b), the contam-
inated samples (48, 96, 120, 144 h) were separated in the fourth di-
mension. The corresponding loading plots of the volatile
aldehydes were 2-methyl-butanal, pentanal, 2-hexenal and (E)-2-
nonenal (Fig. 3b). This observation is in agreement with the results
obtained above. As shown in Fig. 4(a), the levels of these four
aldehydes increased at the end of the germination period in
the contaminated samples. Two reasons were considered to
be the major contributors to this phenomenon. One was the
perturbation to the volatile aldehyde metabolism of the malt.
The other was the volatile aldehydes emitted from the
mycelium based on the result that 2-methyl-butanal, pentanal
and (E)-2-nonenal were also detected in the sporulated
mycelium (Table 1). Volatile aldehydes are considered as the
major component of flavour in both barley and malt with the
fresh and slightly green notes (18,19,25). Most of the key odorants
in barley and malt were composed of aldehydes (18,19). As a result,
a possible conclusion could be that F. graminearum influences
the malt flavour during malting.
The PCA results of the alcohols fraction are shown in Fig. 2(c).
Nearly all of the contaminated samples were separated by PC1 ex-
cept the sample at 120 h. The most variable volatile alcohol
compounds were 2-methyl-1-propanol, 1-penten-3-ol, 3-methyl-
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Comprehensive evaluation of malt volatile compounds contaminated by Fusarium graminearum during malting
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Table 1. Compounds identified in the unsporulated and sporulated Fusarium graminearum

No. Compound name KIa Barley Malt Unsporulated Disrupted unsporulated Sporulated Disrupted sporulated
mycelium myceliumc mycelium mycelium
1 Acetaldehyde 400 +b + + + + +
c
2 2-Methyl-propanal 571 + + + + +
3 3-Methyl-butanal 667 + + + + + +
4 2-Methyl-butanal 678 + + + +
5 Pentanal 711 + + + +
6 Hexanal 809 + + + +
7 2-Hexenal 876
8 Heptanal 906 + +
9 (Z)-2-Heptenal 967 + +
10 Octanal 1004 + +
11 (E)-2-Octenal 1072 + + + +
12 Nonanal 1116 + + + +
13 (E)-2-Nonenal 1175 + + + +
14 Decanal 1203 + +
15 Ethanol 477 + + + + + +
16 2-Methyl-1-propanol 650 + + + + +
17 1-Penten-3-ol 693 + + +
18 Cyclopentanol 718 + +
19 3-Methyl-1-butanol 756 + + + + +
20 1-Pentanol 759 + +
21 1-Hexanol 886 + +
22 1-Octen-3-ol 996 + + + + + +
23 3-Octanol 1007 + + + +
24 (Z)-2-Nonen-1-ol 1046 +
25 Acetone 515 +
26 2,3-Butanedione 602 +
27 2,3-Pentanedione 708
28 3-Hydroxy-2-butanone 732
29 3-Pentanone 715 + +
30 2-Heptanone 905 + + + +
31 3-Octanone 997 + + + +
32 6-Methyl-5-Hepten-2-one 1005 + +
33 5-Methyl-5-hepten-3-one 1002 + + + +
34 3,5-Octadien-2-one 1090 +
35 Acetic acid 618 + +
36 Hexanoic acid 1018
37 Heptanoic acid 1020 +
38 Toluene 775 + + + + + +
39 Ethylbenzene 858 + + + +
40 ρ-Xylene 869 + +
41 Benzaldehyde 974 + + + +
42 1,4-Dichloro-benzene 1019
43 Benzeneacetaldehyde 1048 + + + + +
44 1,3-Dimethyl-benzene 866 + + + +
45 Phenyethyl alcohol 1125 + + + +
46 Dimethyl sulfide 567 +
47 Methacrolein 584 +
48 2-Methyl-furan 623 + + + + +
49 Ethyl acetate 634 + + + +
50 Limonene 1033 + + + +
51 2-Pentyl-furan 1000 +
52 Hexanoic acid Ethyl ester 1017
53 3-Ethyl-2-methyl-1,3- 1045 + +
hexadiene
54 Naphthalene 1194 + + + +
a
KI, Kovats retention indices.
b
‘+’, detected;
c
‘ ’, not detected.

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 Y. Chen et al.
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Figure 2. Principal component analysis of standardized volatile metabolite profiling data of the combined fractions and of aldehydes, alcohols, ketones, aromatic compounds
fractions and other identified volatile fractions separately over the course of control and contaminated malting. (a) The combined fractions; (b) aldehydes; (c) alcohols; (d) ketones;
(e) aromatic compounds fractions; and (f ) other identified volatile fractions.

1-butanol, 1-hexanol and 1-octen-3-ol. The heatmap showed a
slight drop in these compounds after F. graminearum infection at
the later stage of malting (Fig. 4b). Meanwhile, these volatile
alcohols were also detected in the sporulated mycelium except
for 1-hexanol (Table 1).
The PCA results of the ketone fractions are shown in Fig. 2(d).
The contaminated samples (72, 96, 120 and 144 h) were located
in the second dimension. The contaminated samples were
separated owing to the contributions of 2,3-pentanedione and
6-methyl-5-hepten-2-one. As shown in Fig. 4(c), the levels of
6-methyl-5-hepten-2-one increased dramatically at the end of
the contaminated malting process. Further, the levels of 2,3-
pentanedione peaked at 96 h, then decreased slightly towards
the end of the process; however, its concentration was still higher
in the contaminated samples than in the controls. In addition, only
6-methyl-5-hepten-2-one was detected in the sporulated
mycelium (Table 1).
An effect of contamination was observed during the PCA for the
aromatic compounds, with the samples diverging from the
controls in the positive region of PC1 (Fig. 2e). The later stages of
contaminated germination (96, 120 and 144 h) showed larger
changes located in the fourth dimension separately, with
ethylbenzene being the most variable compound. The heatmap
shows that contamination mostly decreased its quantities (Fig. 4e),
and it was also detected in the sporulated mycelium (Table 1).
Generally, aromatic compounds are a potential key odorant owing

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Comprehensive evaluation of malt volatile compounds contaminated by Fusarium graminearum during malting
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Figure 3. Principal component analysis loading plots of standardized volatile metabolite profiling data of combined fractions and of aldehydes, alcohols, ketones, aromatic com-
pounds fractions and other identified volatile fractions separately. (a) The combined fractions; (b) aldehydes; (c) alcohols; (d) ketones; (e) aromatic compounds fractions; and (f )
other identified volatile fractions. The peak numbers were consistent with the data in Table 1. [Colour figure can be viewed at wileyonlinelibrary.com]

to their low odor threshold with the sweet, flowery and green
grass notes (25), and the origin of these compounds isstill unclear.
The PCA of the other identified volatile metabolites resulted in a
similar clustering, as observed in Fig. 2(f ). The contaminated
samples (96, 120 and 144 h) were clearly differentiated from the
other samples, and were in the third dimension of the PCA. The
contaminated samples separated owing to the contribution of
methacrolein alone. The heatmap shows that the levels of this
compound in the contaminated samples slightly increased at the
end of the malting. Moreover, it was only detected in the
unsporulated and disrupted mycelium.
This experiment showed high similarity in F. graminearum myce-
lium to barley or malt in terms of the volatile compositions. Nearly
all of the volatiles from the barley or malt could be detected in
those emitted from the mycelium. One conclusion might be drawn
that the levels of each volatile compounds in the green malt were
influenced to an extent by contaminating F. graminearum fungi,
especially for the volatile aldehydes, alcohols and aromatic
compounds. This variation may directly change the malt flavour.
The influence of F. graminearum on malt flavour was mainly
reflected by the increased and decreased volatile levels rather than
bringing new volatile compounds to the malt. Generally, volatile

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Figure 4. Heatmaps of volatile metabolite profiling data of combined fractions and
of aldehydes, alcohols, ketones, aromatic compounds, organic acids, and and other
identified volatile fractions separately over the course of control and contaminated
4
malting (24–144 h), peak area counts × 10 . [Colour figure can be viewed at
wileyonlinelibrary.com]
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Y. Chen et al.
emissions from fungal-infected cereal grains have been used as
contamination markers for filamentous fungi such as Fusarium
sporotrichioides, Penicillium verrucosum, and Fusarium culmorum
(26). The production of odorous metabolites is considered to be
a consequence of spoilage fungi growth (26). In agreement with
our findings, most of the volatile compounds emitted from the
mycelium were detected in the unsporulated or disrupted ones.
This means that some malt or barley flavour volatiles probably
came from the mycelium or mycelium cytolysis.
Moreover, one consideration requiring more attention was that
the levels of the effected volatiles by F. graminearum might be
increased. Some volatiles increased, some were stable and yet
others decreased significantly when the malt was contaminated
by F. graminearum. This suggests that the volatile concentration
was modulated by the multi-metabolism of green malt and F.
graminearum. The malting environment was considered as a
complex ecosystem involving two metabolically active components:
the germinating grains and the microbial communities
colonizing the grains (27). Our findings offered strong evidence
for this conclusion.
In our previous work, we investigated volatile metabolic
changes over the course of a malting process contaminated by F.
poae to assess its influence on malt flavour. The results showed
that volatile metabolites from green malt were influenced by
contamination with F. poae fungi during malting to an extent,
especially for the volatile aldehyde fractions. A similar result was
also found in this work. Accordingly, the Fusarium fungi not only
produced mycotoxins (28,29), premature yeast flocculation and
gushing factors, but also had an impact on the malt flavour.
Moreover, this impact was not simply judged as positive or
negative, because some key odorants were probably generated
by these fungi.
It was considered that aromatic and furan compounds are
potential key odorants of malt, but the origin of these compounds
was still unclear (20). However, changes in aromatic compounds
are associated with cereal grain spoilage. For instance p-xylene
has been reported in Aspergillus niger, Aspergillus flavus, Aspergillus
versicolor and Aspergillus candidus infections (29,30). 2-Methylfuran
and 2-penthylfuran have been associated with Penicillium
aurantiogriseum and Penicillium verrucosum contamination of
barley grains (31). In this work, most of the aromatic and furan
compounds were detected in the volatiles emitted from mycelium.
This suggests that these compounds could be generated by
Fusarium fungi too (data for F. poae is not shown). In conclusion,
volatile compounds from green malt were influenced by F.
graminearum fungi contamination during malting. These
compounds can be modulated by the metabolism of the green
malt and F. graminearum.
Conclusions
Analysis of volatile composition described in the present research
is a valid alternative for comprehensive evaluation of the influence
of F. graminearum on malt flavour during the malting process. A to-
tal of 36 volatiles were identified from the mycelium, including a
broad spectrum of aldehydes, ketones, alcohols, organic acids
and aromatic compounds, with high similarity to barley and malt
flavour compositions. The data analysis showed that volatile con-
centration was modulated by the -metabolism of the green
malt and F. graminearum. The major contributors to the time-
dependent dynamic changes in the volatiles were the volatile al-
dehyde, alcohol and aromatic fractions. Volatile compounds from
J. Inst. Brew. 2017
Comprehensive evaluation of malt volatile compounds contaminated by Fusarium graminearum during malting
green malt were influenced by F. graminearum fungi contamina-
tion during malting.
Acknowledgments
We thank the support of Basic Research Fund of Education Depart-
ment of Liaoning Province (2016 J020) and the Science Foundation
of Dalian Polytechnic University (QNJJ201403).
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