J Phytopathol 161:1–10 (2013) doi: 10.1111/jph.

12036
© 2012 Blackwell Verlag GmbH

Review Article
Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya

Fusarium langsethiae – a HT-2 and T-2 Toxins Producer that Needs More
Attention
Samuel M. Imathiu1, Simon G. Edwards2, Rumiana V. Ray3 and Matthew A. Back2
Authors addresses: 1Jomo Kenyatta University of Agriculture and Technology, P.O. Box 62000-00200, Nairobi, Kenya;
2
Harper Adams University College, TF10 8NB, Newport, Shropshire, UK; 3University of Nottingham, LE12 5RD,
Nottingham, UK (correspondence to S. Imathiu. E-mail: smutembei@yahoo.com)
Received May 9, 2012; accepted September 10, 2012

Keywords: Fusarium langsethiae, HT-2 and T-2 toxins, mycotoxins, cereals, food safety

Abstract (Bottalico and Perrone 2002). Among the most impor-

Fusarium langsethiae is a toxigenic fungus that was
formally described as a new species in 2004. This fun-
gus was first detailed in the 1990s but was initially
referred to as ‘powdery Fusarium poae’ having a spore
morphology similar to F. poae but a mycotoxin profile
like that of Fusarium sporotrichioides. The species has
been isolated from infected oat, wheat and barley
grains but has been reported as more problematic in
the former crop rather than the latter two. Whilst the
epidemiology of F. langsethiae remains unclear, the
fungus has been shown to produce high levels of type-
A trichothecenes HT-2 and T-2 toxins in small-grain
cereals. HT-2 and T-2 toxins are two of the most
potent trichothecenes capable of inhibiting protein
synthesis in eukaryotes. In this regard, mycotoxin con-
tamination caused by F. langsethiae is clearly a food
and feed safety hazard. With the European Commis-
sion considering legislation of HT-2 and T-2 toxins,
more information is required not only on the producer
and conditions favouring mycotoxin production, but
also on reliable methods of pathogen detection and
reduction of cereal contamination. This review
describes recent research concerning the known epide-
miology of F. langsethiae and suggestions of what
needs to be known about the fungus in order to be
able to understand and employ measures for prevent-
ing its infection and contamination of cereals with
HT-2 and T-2 toxins.
Introduction
Fungi of the genus Fusarium are among the most
destructive pathogens of small-grain cereals and maize
worldwide, where more than one species is frequently
encountered in a single crop. Several species of this
genus are well-known infectious agents of a number of
cereal diseases causing root, stem and ear infections
that result in significant losses to the cereal industry
tant diseases caused by Fusarium species is fusarium
head blight (FHB; Parry et al. 1995), which is also
referred to as fusarium ear blight (FEB), scab or head
fusariosis, and describes a disease of small-grain cere-
als such as oats, wheat and barley. Some of the major
Fusarium species known to cause FHB are F. avenace-
um, F. culmorum, F. graminearum, Microdochium
nivale and M. majus (Parry et al. 1995; Xu et al.
2005). Infection by Fusarium species on cereal heads
may result in reduced overall crop yields (Goswami
and Kistler 2004), reduced grain quality (McMullen
et al. 1997; Nightingale et al. 1999; Snijders 2004),
reduced seed quality (Gilbert and Tekauz 1995; Win-
son et al. 2001) and of greatest health concern, con-
tamination of grain with mycotoxins (Desjardins
2006). These negative effects have a huge economic
impact on food safety, security and trade in both the
developed and the developing countries (FAO 2004;
Nganje et al. 2004), with the former being affected sig-
nificantly. For example, in the 1990s, wheat producers
in regions affected by FHB in the USA suffered cumu-
lative losses of $1.3 billion (Johansson et al. 2003).
Although monetary losses caused by mycotoxins hav-
ing a direct effect on human health is difficult to quan-
tify, it is thought to be significant (Pohland 1993).
Fusarium mycotoxins are produced in the field, and
the amount produced is heavily influenced by environ-
mental factors that cannot be controlled. For this
reason, complete elimination from agricultural com-
modities is unachievable. According to the Food and
Agriculture Organisation (FAO), exposure to some
level of mycotoxins cannot be avoided and has to be
tolerated (FAO 2004). A key goal in the production of
food is, therefore, to develop and/or adopt practices
that reduce the extent of contamination by these toxins
to levels that are considered to have no significant
impact on health (Desjardins 2006). Some of the
2 Imathiu et al.
recommended practices for the general reduction of
Fusarium mycotoxins in products include crop rotation
(Schaafsma et al. 2001; Champeil et al. 2004a; Koch
et al. 2006), ploughing (Schaafsma et al. 2005; Maior-
ano et al. 2008), planting of less susceptible varieties
of crops (Diamond and Cooke 1999) and control of
weeds and insects in the field (Jenkinson and Parry
1994; Miller et al. 1998; Inch and Gilbert 2003).
As the research in cereal diseases and pathogens
intensifies, more information is generated regarding
previously unidentified and less understood potential
phytopathogenic fungi that are capable of directly
influencing the cereal quality and safety, and thus,
indirectly affecting human and animal well-being. Just
over a decade ago, an unknown fungus was reported
in Norway that was suspected to be a potent producer
of HT-2 and T-2 toxins in oats (Torp and Langseth
1999). As part of COST Action 835, this fungus and
related fungi within the Sporotrichiella family were
intensively studied using a polyphasic approach (Torp
and Adler 2004), resulting in the description of the
new species named Fusarium langsethiae (Torp and
Nirenberg 2004). Reports on Fusarium langsethiae were
relatively scant up until 2004 when more detailed
information began to emerge. For instance, high levels
of unexplained HT-2 and T-2 toxins in the UK’s oat
and wheat crops around 2004 prompted investigations
to identify the causative agent (Imathiu 2008a; Baxter
et al. 2009). Fusarium langsethiae has been reported in
oats, wheat and barley in Central and Northern Eur-
ope including England, Norway, Austria, Germany,
Czech Republic and Denmark (Torp and Adler 2004;
Torp and Nirenberg 2004). Accounts on the detection,
isolation and identification of this fungus, mainly in
European countries continue to be reported. Most
recently, F. langsethiae has been isolated from Italian
and Russian cereals (Infantino et al. 2007; Yli-Mattila
et al. 2011). The known distribution of Fusarium
langsethiae is largely limited to Europe with one isolate
found in East Siberia (Gavrilova et al. 2010). It has
not been reported worldwide possibly because its
known distribution may be limited due to the fact that
it was only recently identified. As a result of its unique
colony morphology, it may be easily disregarded dur-
ing isolation of Fusarium species from suspect cereal
grains as a fungal contaminant because it is not
described in the current identification manual (Leslie
and Summerell 2006). The species was also previously
misidentified as other Fusarium species. For example,
there was an erroneous identification of two isolates
each from Poland and Italy, which were originally
classed as F. sporotrichioides, when in fact, they were
F. langsethiae, as confirmed diagnostically, on the basis
of ITS and Tri5 sequences as well as on amplification
with F. langsethiae-specific primer pair designed for
the species by Wilson et al. (2004).
As a result of the association of F. langsethiae with
HT-2 and T-2 mycotoxin production, this fungal spe-
cies has in recent times received improved attention.
The natural occurrence of T-2 toxin has been of
particular interest in Europe because of the association
of T-2 toxin-producing Fusarium species, which caused
an outbreak of alimentary toxic aleukia (ATA) that
was responsible for the death of thousands of people
in Russia during World War II in the 1940s (Joffe
1986; Desjardins 2006). However, there is no sufficient
information available with regard to the conditions
under which these toxins are formed in cereal grains
during crop growth and/or storage. The European
Commission (EC) has been considering setting maxi-
mum levels of HT-2 and T-2 toxins in cereals and cer-
eal products, particularly in oats and oat products,
which seem to be most affected (Edwards et al. 2009),
taking into consideration, the progress of the scientific
knowledge on these toxins in foods, which is currently
limited.
Legislative limits for the sum of HT-2 and T-2 tox-
ins may be set by the EC after the generation of more
occurrence data, development of sensitive analytical
methods and after more research has been carried out
on the factors involved in the presence of these toxins
in cereal and cereal-based products (EC 2006).
Recently, the European Food Safety Authority
(EFSA) Panel on Contaminants in the Food Chain
established a group TDI of 100 ng/kg body weight for
the sum of HT-2 and T-2 toxins. The report included
occurrence results on HT-2 and T-2 toxins obtained
from 22 European countries, which showed that the
highest mean concentrations for the sum of these tox-
ins were observed in grains and grain milling products,
especially in oats and oat products (EFSA 2011).
Grains and grain-based products including bread, fine
bakery wares, grain milling products and breakfast
cereals made the largest contribution to the sum of
HT-2 and T-2 toxins exposure for humans. It is appar-
ent that continued monitoring of these toxins will
remain high priority.
Occurrence and Morphological Description
of Fusarium langsethiae
Fusarium langsethiae was formally described as a new
species in 2004 (Torp and Nirenberg 2004). This spe-
cies is mainly found in infected oats, wheat and barley
but is more of a problem in the former than the latter
two (Edwards et al. 2009). Fusarium langsethiae was
initially referred to as ‘powdery F. poae’ due to its
abundant production of small napiform to globose
conidia, giving the colony a powdery-like appearance
(Fig. 1; Torp and Langseth 1999). It has spore mor-
phology similar to F. poae (Fig. 2) but with a myco-
toxin profile similar to that of F. sporotrichioides
(Thrane et al. 2004). In this regard, it is likely that
many potent T-2 toxin-producing strains of F. poae
reported earlier were F. langsethiae (Torp and
Langseth 1999; Knutsen et al. 2004), some have
recently been reidentified as F. sibiricum, a close relative
of F. langsethiae and F. sporotrichioides (Yli-Mattila
et al. 2011). Fusarium langsethiae differs from F. poae
by its slower growth, production of fewer aerial
mycelia and lack of peach-like odour on synthetic
Fusarium langsethiae, a HT-2 and T-2 Toxins Producer
media such as potato dextrose agar (PDA; Torp and
Nirenberg 2004; Mylona and Magan 2011). The ‘pow-
dery’ appearance on the colony surface is an attribute,
which is obvious and morphologically, one of the
characters that can be used to easily and quickly dif-
ferentiate F. langsethiae from all other Fusarium spe-
cies (Torp and Langseth 1999; Torp and Nirenberg
2004; Imathiu 2008a). The ease with which it is possi-
ble to identify F. langsethiae due to its profuse produc-
tion of spores, which gives the colonies their distinctive
powdery appearance, is of utmost importance to
researchers, particularly in laboratories that lack facili-
ties for molecular validation of the species identity.
The fungal colonies colour on synthetic solid media
range from whitish, yellowish white, pinkish white,
pale red and/or pastel red (Torp and Nirenberg 2004;
Imathiu 2008a; Lukanowski and Sadowski 2008;
Fig. 1). Colony pigmentation is known to be uniform
within some Fusarium species, in others, it is a variable
character (Burgess et al. 1988). Fusarium langsethiae
appears to be one of those species that may naturally
produce different colony colour shades irrespective of
the type of small-grain cereal the isolates are recovered
from (Imathiu 2008a). The different shades of colour
in F. langsethiae cultures can be explained by the fact
that some of the strains of this fungus can produce a
pigment called aurofusarin (Thrane et al. 2004), which
is produced by nearly all strains of F. poae and
F. sporotrichioides and influences colony colour devel-
opment. Fusarium langsethiae isolates have been
reported to either have an entire or lobed colony mar-
gins, which may or may not be stable for the same iso-
late, indicating that this secondary attribute is not
useful in the characterisation of the F. langsethiae iso-
lates (Imathiu 2008a). Fusarium langsethiae has a slow
growth rate and sparse aerial mycelia and is, therefore,
easily overgrown by other more rapidly growing fungi
such as F. culmorum and F. poae (Torp and Nirenberg
2004; Imathiu 2008a; Mylona and Magan 2011),
meaning that its isolation and identification can be
problematic. Recovery of F. langsethiae from infected
cereal grain in terms of isolation has been demon-
strated to be low. From the UK oats and wheat sam-
ples with high HT-2 and T-2 toxins of >500 and
>50 lg/kg, respectively, F. langsethiae was isolated
from just 5–10% of the grain and none from oat
Fig. 1 Fusarium langsethiae colony characteristics on potato dextrose agar after incubation at room temperature for 7 days. Colony colour
range from white, orange to purple, while margin shape is either entire or lobed. Adapted from Imathiu 2008a
3
F.poae
F. sporotrichioides
F. langsethiae
Fig. 2 Comparison of Fusarium poae, Fusarium sporotrichioides and
Fusarium langsethiae conidia morphology. Fusarium langsethiae has
napiform to globose-shaped conidia. Adapted from Knutsen et al.
2004
samples containing <10 lg/kg HT-2 and T-2 toxins
(Imathiu 2008a). A study carried out in Poland also
resulted in low recovery of F. langsethiae isolates from
winter wheat kernels (Lukanowski and Sadowski
2008). These results are in agreement with previous
studies that stated that F. langsethiae was difficult to
isolate from infected seed (Torp and Nirenberg 2004;
Yli-Mattila et al. 2004). The reason behind this is not
clear and warrants further attention by researchers.
Growth Conditions of Fusarium langsethiae
Fusarium langsethiae has been reported to have an
optimum growth temperature in the range of 20–30°C
(Torp and Nirenberg 2004; Lukanowski and Sadowski
2008; Medina and Magan 2010, 2011; Mylona and
Magan 2011), which is common to most Fusarium spe-
cies including F. poae, F. culmorum and F. graminea-
rum (Brennan et al. 2003; Doohan et al. 2003; Hope
et al. 2005). Most of these findings have been obtained
from experiments carried out under controlled envi-
ronment conditions in laboratories, glasshouses and a
few from field experiments. In the only study of its
kind investigating how storage environment influences
4 Imathiu et al.
dry matter losses and HT-2 and T-2 toxin contamina-
tion of oats by F. langsethiae, Mylona and Magan
(2011) reported that optimum conditions for colonisa-
tion of harvested oats and HT-2 and T-2 toxins pro-
duction by F. langsethiae were observed at a water
activity (aw) of 0.97 and a temperature of 25°C. These
conditions are typical for mycotoxin production by
most Fusarium species.
Mycotoxins Produced by Fusarium langsethiae
Mycotoxins are fungal toxins produced by many phy-
topathogenic and food spoilage fungi of the genera
Fusarium, Aspergillus, Penicillium and Alternalia (Moss
1992; Sweeney and Dobson 1998). While Aspergillus
and Penicillium species are mostly found as contami-
nants in food during drying and storage, Fusarium and
Alternaria species can produce mycotoxins before or
immediately after harvesting (Sweeney and Dobson
1998). Mycotoxins are secondary metabolites because
their biosynthesis is not required for the primary func-
tions of growth and reproduction (Desjardins 2006).
They are considered to be the most significant natural
food contaminants with regard to their negative
impact on public health, food security and the national
economy of many countries. Fusarium langsethiae
mycotoxins are no exception. Fusarium langsethiae
produces T-2 toxin and HT-2 toxin (a deacetylated
form of T-2 toxin), diacetoxyscirpenol and neosolaniol
(Eriksen and Alexander 1998; Visconti 2001; Thrane
et al. 2004; Kokkonen et al. 2010) that are all type-A
trichothecenes (Smith et al. 1994). Among these, HT-2
and T-2 toxins are the most common and produced in
large amounts by F. langsethiae (Langseth and Rundb-
erget 1999; Torp and Langseth 1999; Thrane et al.
2004) and are usually found together in contaminated
cereal grains and their products. These toxins are two
of the most toxic trichothecenes. They are powerful
inhibitors of protein synthesis, majorly cytotoxic, caus-
ing skin and mucosa erosions and reduction of lym-
phocytes, immune defence and growth in exposed
animals (Pettersson et al. 2010). In European cereal
production, F. langsethiae has been implicated as the
main producer of HT-2 and T-2 trichothecenes
(Edwards et al. 2009, 2012).
The first account implicating F. langsethiae in the
production of HT-2 and T-2 toxins was reported
when a survey carried out in Norway on oats estab-
lished that these toxins regularly occurred in high
concentrations (Langseth and Rundberget 1999). Such
high levels of the toxins could not be accounted for
by F. sporotrichioides which was then, the only known
producer of large amounts of these toxins (Marasas
et al. 1984; Kokkonen et al. 2010) as its incidence
and isolation was limited during that crop year.
Edwards et al. (2012) and Imathiu (2008a) have inves-
tigated and reported high levels of these toxins in
symptomless oats both in field and harvested grains
from which F. sporotrichioides was not detected.
Other recent reports indicating that F. langsethiae is a
potent producer of HT-2 and T-2 toxins include those
of Kokkonen et al. (2010) and Medina and Magan
(2011).
Environmental Conditions Favouring Production of
HT-2 and T-2 Toxins
Environmental conditions favourable for the produc-
tion of HT-2 and T-2 mycotoxins in vivo in small-grain
cereal crops are not well understood. Hietaniemi et al.
(2004) reported reduced concentrations of HT-2 and
T-2 toxins in Finnish oats in 1 of the 3 years moni-
tored when a wet summer occurred, a condition that
could have been conducive for the formation of large
amounts of other Fusarium mycotoxins such as deoxy-
nivalenol (DON) and nivalenol (NIV). The authors
did not implicate any specific Fusarium species in the
production of HT-2 and T-2 toxins in that study.
However, it is likely that they were produced by
F. langsethiae, which is considered to be the main pro-
ducer of these toxins in European cereals (Edwards
et al. 2009). The fact that the levels were low may indi-
cate that F. langsethiae was outcompeted by other
fast-growing Fusarium species or that wet weather con-
ditions, to some extent, discouraged its growth and
consequently diminished production of HT-2 and T-2
toxins contrary to what is known for most fungi in the
same genera. This finding is also in agreement with
those of Edwards (2007a,b) who reported lower mean
HT-2 and T-2 toxin concentrations in cereals after wet
summers and those of Langseth and Rundberget
(1999) who reported high levels of these trichothecenes
during warm and dry summers in Norway. In Norway,
highest levels were detected in oats, followed by barley
and lowest in wheat samples (Langseth and Rundber-
get 1999). In Europe, oats are generally more affected
than any other small-grain cereal crop, irrespective of
the environmental conditions. Survey data from Nor-
dic countries indicate that these mycotoxins have
increased in recent years where in some oat samples
concentrations >1000 lg/kg of combined HT-2 and
T-2 toxins have been reported (Edwards et al. 2009).
In this regard, it appears that these toxins are pro-
duced in the field under contrasting conditions to
other Fusarium toxins such as DON and NIV, which
increase during warm and wet conditions from anthe-
sis onwards (Parry et al. 1995; Lacey et al. 1999; Xu
2003). However, further research is required to clearly
identify what climatic factors and at what crop growth
stages they impact on HT-2 and T-2 toxin concentra-
tions in each cereal.
Because F. langsethiae has been reported as the pri-
mary HT-2 and T-2 toxins producer in UK cereals
(Edwards et al. 2012), it is of paramount importance
that more knowledge is gained regarding the toxin-
producing characteristics of this fungus (Kokkonen
et al. 2010). An understanding of the environmental
conditions associated with toxin production by
F. langsethiae in vitro is vital in order to generate infor-
mation relevant in the prediction of mycotoxin profiles
that might occur in the field or during storage. Little
information is currently available regarding the in vitro
Fusarium langsethiae, a HT-2 and T-2 Toxins Producer
production of HT-2 and T-2 toxins by F. langsethiae.
Medina and Magan (2010) reported that the optimum
aw and temperature conditions for HT-2 and T-2 toxins
production was between 0.980–0.995 and 20–30°C,
respectively. This result is in agreement with other
recent studies by Kokkonen et al. (2010) and Strub
et al. (2010). Kokkonen et al. (2010) showed that an aw
of 0.994 and a temperature of 15°C favoured the type-
A trichothecene production by F. langsethiae and
F. sporotrichioides, while Strub et al. (2010) reported an
optimal temperature and aw for the fungus toxinogene-
sis as 28°C and 0.997, respectively. These observations
imply that high levels of HT-2 and T-2 toxins are pro-
duced by F. langsethiae in the presence of high moisture
on the crop, levels of which are influenced by ambient
temperature in turn affecting fungal colonisation. These
findings also demonstrate the potential ability of
F. langsethiae to colonise and contaminate cereals with
HT-2 and T-2 toxins preharvest as these conditions are
often present in the field before harvest. As these condi-
tions also favour most of the other Fusarium species, it
is likely that preventative methods employed for com-
mon Fusarium species could be used to counter
F. langsethiae mycotoxins.
Pathogenicity of Fusarium langsethiae
Currently, the greatest challenge in the study of the
pathogenic capability of F. langsethiae is the inability
to artificially inoculate cereals with the fungus to
mimic the natural infection as is documented for other
Fusarium species such as F. graminearum and F. cul-
morum. Several experiments involving artificial inocu-
lation of the fungus on oats have been carried out,
both in glasshouse and in the field with little or no
significant infection as determined by quantitative
polymerase chain reaction (Q-PCR) assay (Imathiu
2008a). More recently, Divon et al. (2011) have
achieved artificial infection of oats using F. langsethiae,
which resulted in typical FHB symptoms in glasshouse
studies. However, for field experiments where fungal
detection and quantification was confirmed by PCR;
there was a lack of visual symptoms on the infected
cereal heads making it impossible to employ visual
assessment as a tool for monitoring F. langsethiae inci-
dence and severity of infection. In a UK-based epide-
miological study investigating the occurrence of
fusarium panicle blight of oats, F. langsethiae infection
and HT-2 and T-2 mycotoxins, no disease symptoms
were observed, but the fungus was isolated in symp-
tomless spikelets and high levels of HT-2 and T-2 tox-
ins were quantified from the same (Imathiu 2008a).
Symptomless infections on oats caused by F. langse-
thiae as was demonstrated in these limited studies calls
for novel measures of infection monitoring to be
designed and implemented if timely correct diagnosis is
to be made in the field. In doing so, this can help to
curb the use of cereals highly contaminated with HT-2
and T-2 toxins in food and feed production. One such
tool for monitoring fungal biomass is the use of molec-
ular techniques such as PCR assays.
5
The reason for F. langsethiae not being able to cause
head blight of oats is not known but it is possible that
it is a weak pathogen and as such unable to cause
severe disease symptoms on cereals, particularly in
oats, which is reported to be more resistant to FHB
compared with wheat and barley (Langseth and Stabb-
etorp 1996; Liu et al. 1997 and Tekauz et al. 2004).
Apparently, F. langsethiae may be behaving as a symp-
tomless endophyte upon infection. In a study investi-
gating the possible pathogenicity and aggressiveness of
F. langsethiae on oats and wheat seedlings, Imathiu
et al. (2010) demonstrated that the fungus is not a
seedling blight pathogen of these cereals as there was
no significant difference in the disease development
between the fungus inoculated and the control seed-
lings. The authors’ conclusion was that F. langsethiae
is unlikely to affect crop establishment, crop stand or
yield if there is no subsequent foot-rot and/or head
blight where infected seeds are sown. The results also
identified that seedling blight may not be a part of the
disease cycle for F. langsethiae. However, if F. langse-
thiae is a symptomless pathogen, this could present
problems later in the crop development as a potential
reservoir, which can act as a primary inoculum source
for subsequent ear or panicle infection. Further inves-
tigations are justified to establish whether F. langse-
thiae is a systemic endophyte.
In a rather interesting separate study, F. langsethiae
was found to be a pathogen in detached leaf assays
(Imathiu et al. 2009). The fungus was found to be
more pathogenic to wounded oat than wheat leaves as
well as to unwounded detached leaves of oats but not
those of wheat (Imathiu et al. 2009). These results,
according to the authors, indicated some form of pref-
erence of the species towards oats than wheat, which
can explain why oats are infected and accumulate
more HT-2 and T-2 toxins than other cereals.
Although there were no significant differences in lesion
lengths observed between the three oats varieties used
in this study, a clear trend was observed consistent
with their reported susceptibility to HT-2 and T-2 tox-
ins accumulation, which may suggest a correlation
between susceptibility to F. langsethiae in the in vitro
assay and HT-2 and T-2 toxins contamination. These
assays may be of potential use in evaluating the sus-
ceptibility of different oat varieties to F. langsethiae. If
so, this would allow a rapid screening of potential
breeding material and progeny of oats, which would
reduce incidences of HT-2 and T-2 toxins and possibly
other mycotoxins in the raw and processed oats. The
ability of F. langsethiae to cause disease symptoms on
detached leaves in contrast to live seedlings and adult
plants in previous glasshouse and field studies suggest
that F. langsethiae may lack certain pathogenicity
genes or proteins to overcome the general defence
mechanisms in live functional plant systems. Further-
more, cereal leaves, heads and seedling stems are three
very different plant structures whose reaction to infec-
tion by F. langsethiae is expected to differ; symptom-
atic in the former in vitro and asymptomatic in the
6 Imathiu et al.
latter two in vivo. In addition to this, both cereal heads
and seedling stems are on a naturally growing and
functioning plant whose defence mechanism to infec-
tion will be different from those of detached leaves.
Impact of Agronomy on Fusarium langsethiae and
HT-2 and T-2 Toxins Production in Cereals
A limited number of studies have been conducted in
Europe on the impact of agronomic practices on
F. langsethiae and HT-2 and T-2 toxins contamination
of cereals, particularly in oats. Although the impact of
agronomy on F. langsethiae and the concentration of
HT-2 and T-2 toxins in cereals have not yet been
clearly identified, it is evident that it could be different
from the impact of agronomy on DON-producing spe-
cies such as F. graminearum and F. culmorum (Imathiu
2008a; Edwards et al. 2009). Recent surveys have iden-
tified F. langsethiae and high concentrations of HT-2
and T-2 toxins in barley in France and in oats in UK
and Nordic countries including Finland (Pettersson
et al. 2008; Yli-Mattila et al. 2008; Edwards et al.
2009). The occurrence of F. langsethiae and distribu-
tion of HT-2 and T-2 toxins in other crops other than
oats is difficult to conclude on as there is less data
available for them, although in recent years, more
cereals have been included within national surveys. As
previously mentioned, oats seem to accumulate the
greatest amounts of these toxins compared with wheat
and barley irrespective of the country in which the
crop was grown.
A summary of the main findings of the effect of
agronomy practice on HT-2 and T-2 toxins contami-
nation as provided from national surveys carried out
on barley in France (Gautier 2007; Barrier-Guillot
2008), and wheat, barley and oats in the UK (Edwards
2007a,b,c) is presented in Table 1.
It is clear that the influence of most of the agro-
nomic factors are similar for HT-2 and T-2 toxins
analysed in both oats and barley. The differences in
levels of HT-2 and T-2 toxins in France’s spring barley
and UK’s winter wheat where the concentration in the
former was higher than in the latter may be genetically
linked or may be based on prevailing weather condi-
tions when the different crops are in flower (Edwards
et al. 2009). In a survey investigating the distribution
Table 1
Impact of agronomy on HT-2 and T-2 toxins in French barley and UK oats
HT-2 + T-2 toxins in French
Agronomic practice Barley
Previous crop High after cerealsa
Low after maize
Low after non-cereals
Cultivation Ploughing beneficial after non-cereal
Variety Higher in Spring barleys (difference between varieties
unknown)
Irrigation (misting) at Increases mycotoxins
flowering
a
Cereals refers to small-grain cereals – wheat, barley and oats.
Adapted from Edwards et al. 2009.
of trichothecene and zearalenone producing Fusarium
species in grain of different cereal species and cultivars
grown under organic farming conditions in Lithuania,
F. langsethiae was more frequent in spring than winter
cereals, especially in oats and barley (Suproniene et al.
2010), an observation reported also by Yli-Mattila
et al. (2008) on Finnish oats. Anthesis has been shown
to be the most susceptible growth stage for infection
to Fusarium species (Lacey et al. 1999; Xu 2003) and
winter and spring varieties flower at different times.
Lower levels of HT-2 and T-2 toxins have been
reported in UK’s organically produced oats compared
with conventionally grown oats (Edwards 2009).
Although the reason for this is not apparent, the result
could be explained by the fact that organic farmers
often grow oats after a non-cereal, plough before oats,
grow less susceptible varieties including more spring
oats and follow less intense cereal rotations (Edwards
2007b) all of which may reduce infection and toxin
build-up by F. langsethiae.
Many authors have reported on the importance of
cultivation methods and the contribution of crop resi-
dues to various plant diseases including FHB (Parry
et al. 1995; Champeil et al. 2004a,b). Presence of crop
debris on the soil surface has been shown to increase
the incidence and severity of FHB and mycotoxin con-
centration in wheat, the disease intensity and toxin
level depending on the type of crop debris, the patho-
gen involved, whether or not the field was ploughed
and the climatic conditions. Fusarium langsethiae infec-
tion and HT-2 and T-2 toxins production were found
to be influenced in the same way by these cultural
practices. Oat grains harvested from minimum-tilled
plots with straw incorporated were infected more by
F. langsethiae than from ploughed plots. The accumu-
lation of HT-2 and T-2 toxins followed the same trend
(Imathiu 2008a). These results are in agreement with
those of Parikka et al. (2007) who reported high levels
of F. langsethiae infection in oats in direct-drilled plots
compared with ploughed plots in Finland. These find-
ings are also in support of those of Edwards (2007a)
who reported higher HT-2 and T-2 toxins in oat sam-
ples from non-ploughed fields than those, which were
ploughed in a UK study. In an isolated case in
Finland, which is difficult to explain, F. langsethiae/
HT-2 + T-2 toxins in UK Oats
High after cereals
Low after maize
Low after non-cereals
Ploughing beneficial after non-cereal
Higher in Winter oats (large differences between
varieties)
Higher in dryer summers
Fusarium langsethiae, a HT-2 and T-2 Toxins Producer
F. sporotrichioides DNA and HT-2 and T-2 toxin lev-
els were found in plots with tillage including ploughing
as compared with direct drilling in spring oats and
barley. In general, these results suggest that crop deb-
ris is important in the epidemiology of F. langsethiae
and HT-2 and T-2 toxin production. In these studies,
ploughing served to bury the residue, significantly
reducing the amount of inoculum available for causing
an infection. Minimum tillage and direct drilling, on
the other hand, would result in a considerable amount
of debris lying on the soil, which, if contaminated with
inoculum, may cause greater infection. The results
reported from these studies support those of Maiorano
et al. (2008) who reported in general, increased infec-
tion by FHB pathogens as a result of direct drilling or
minimum tillage in a wheat field. Miller et al. (1998)
and Pirgozliev et al. (2003) also found that ploughing
is one of the most effective previous crop residue man-
agement strategies, as it removes plant debris from the
soil surface and buries it reducing the amount of inoc-
ulum available for FHB infection and subsequent
mycotoxin contamination.
Effects of fungicide use in the control of F. langse-
thiae and HT-2 and T-2 toxins are lacking except for a
single report. A recent study on the activity of fungi-
cides to reduce HT-2 and T-2 toxins in oats by Petters-
son et al. (2008) reported little or no reduction. It is
worth noting that it would be difficult to develop
methods of control of an organism whose epidemiol-
ogy has not been well understood. The biology of
F. langsethiae and its interaction with the plant
remains poorly understood to date, partly hindered by
difficulties in reproducing a natural level of infection
under controlled conditions (Divon et al. 2011).
Detection and Quantification of Fusarium
langsethiae
Physical identification of Fusarium species is difficult
due to the great variations in morphological and cul-
tural characteristics such as colony morphology, pig-
mentation, growth rate, presence or absence of macro
and/or microconidia and their shape (Nelson et al.
1983; Windels 1991). Several quantitative PCR assays
for FHB pathogens have been developed (Nicholson
et al. 2003; Waalwijk et al. 2004; Nicolaisen et al.
2009; Fredlund et al. 2010). These PCR-based methods
are fast as there is no need for culturing and identify-
ing the pathogen before quantification, as this can be
determined directly from plant tissue extracts. Quanti-
tative PCR assays are highly specific because identifi-
cation of species implicated in a given infection,
disease or mycotoxin occurrence is based on genotypic
differences rather than variable phenotypic attributes.
PCR-based assays are sensitive as they can detect and
quantify target DNA molecules in complex mixtures
even when the mycelia and spores are no longer viable
offering an alternative to microbiological traditional
procedures in fungal diagnostics and quantification.
These types of assays are particularly important for
the diagnosis and quantification of a species such as
7
F. langsethiae that has been shown to be relatively
difficult to isolate from plant material and present
asymptomatic reactions on cereals upon infection.
Quantification of biomass of F. langsethiae is essen-
tial in the understanding of the interaction between the
fungus and the susceptible crop(s). In recent times,
many authors have developed assays for the early and
specific detection of F. langsethiae in plant material.
The assays have been successful in discriminating
between F. langsethiae from other Fusarium species
including those closely related to it such as F. poae,
F. sporotrichioides and a recently identified species,
F. sibiricum isolated predominantly in Northern Asia
(Yli-Mattila et al. 2011). Wilson et al. (2004) devel-
oped the first species-specific PCR assay for the detec-
tion of F. langsethiae based on differentially amplified
RAPD-PCR products. These primers were successfully
used in SybrGreen real-time PCR assays for the quan-
tification of F. langsethiae in cereals (Fredlund et al.
2010; Edwards et al. 2012). Other assays developed
include a TaqMan assay that quantifies both F. langse-
thiae and F. sporotrichioides based on the ITS region
(Yli-Mattila et al. 2008), and an F. langsethiae-specific
SybrGreen assay based on the elongation factor 1
alpha gene (Nicolaisen et al. 2009).
Many of these assays have been very useful in dem-
onstrating the relationships between pathogen(s) bio-
mass in the form of DNA and mycotoxin
concentration. This has greatly facilitated researchers
to make useful predictions based on the trends from
the results obtained for forecasting mycotoxin risk.
Strong relationships between F. langsethiae DNA and
HT-2 and T-2 toxins have been demonstrated in a
number of published studies. Halstensen et al. (2006a,
b) investigating toxigenic Fusarium species as determi-
nants of trichothecenes in settled grain dust from Nor-
wegian farm grain stores reported coefficient of
determination (r2) of 0.59 and 0.50 for HT-2 and 0.59
and 0.48 for T-2 and F. langsethiae DNA. An r2 of
0.41 and 0.84 was found between F. langsethiae/
F. sporotrichioides DNA levels and T-2 and HT-2 tox-
ins in Finnish oats samples (Yli-Mattila et al. 2008).
Similarly, a study of mycotoxins in Danish cereals
identified a strong correlation between F. langsethiae
and HT-2 toxin (Nielsen et al. 2011) while Fredlund
et al. (2010) reported a relationship between F. langse-
thiae DNA and HT-2 and T-2 toxins in 62 Swedish
oat samples accounting for 72% of the variance.
Recently, the real-time PCR assay developed by
Edwards et al. (2012) also showed a strong correlation
between F. langsethiae DNA and HT-2 and T-2 toxins
in UK oat grain flour samples (r2 = 0.60) and individ-
ual oat grains from a single field sample (r2 = 0.77).
These findings clearly show that F. langsethiae is the
main, if not, sole producer of HT-2 and T-2 toxins in
many European cereals.
Conclusions
Fusarium langsethiae has been identified as the main
producer of large quantities of HT-2 and T-2 toxins in
8 Imathiu et al.
European small-grain cereal crops. Oat has been
shown to be more affected by HT-2 and T-2 mycotox-
in accumulation compared with wheat and barley irre-
spective of the agronomy practised in their production.
It is, therefore, likely that F. langsethiae has a prefer-
ence for oats as opposed to the other two. The known
distribution of Fusarium langsethiae is currently limited
to Europe. It may not have been detected in other
parts of the world because it has only recently been
described and its description is absent from the current
Fusarium identification manual and therefore it may be
overlooked. Fusarium langsethiae is readily overgrown
by other fast-growing species making its isolation from
plant material difficult. Even from inoculated infected
material, as confirmed by PCR diagnosis, it is difficult
to recover a large number of F. langsethiae isolates.
The challenges encountered in the study of this fungus
that require urgent attention include inability to artifi-
cially inoculate cereals to provide infections in experi-
mental material that are comparable to natural
infections, elucidation of its status as an endophyte or
as a pathogen due to the lack of clear disease symp-
toms, and gap in our knowledge of the infection
process and the biology of the fungus.
HT-2 and T-2 toxins are acute and potentially
chronic mycotoxins. Given that F. langsethiae pro-
duces high concentrations of HT-2 and T-2 toxins in
symptomless grains, this is a significant threat to
future food safety and security. It is, therefore, of par-
amount importance that more research is carried out
to understand the biology and epidemiology of this
fungus in order to develop measures directed towards
minimising the infection and subsequent contamina-
tion of cereals with these mycotoxins.
References
Barrier-Guillot B. (2008) T-2 and HT-2 in cereals grown in France.
In: Proceedings of the Fifth Fusarium Toxin Forum, 10-11 January.
European Commission, Brussels, Belgium. http://www.micotossine.
it/public/pag_542.pdf (verified Apr 15, 2012).
Baxter ED, Byrd N, Slaiding IR. (2009) Food safety review of UK
cereal grain for use in malting, milling and animal feed. HGCA
Report No. 464.
Bottalico A, Perrone G. (2002) Toxigenic Fusarium species and
mycotoxins associated with head blight in small-grain cereals in
Europe. Eur J Plant Pathol 108:611–624.
Brennan JM, Fagan B, van Maanen A, Cooke BM, Doohan FM.
(2003) Studies on in vitro growth and pathogenicity of European
Fusarium fungi. Eur J Plant Pathol 109:577–587.
Burgess LW, Liddell CM, Summerell BA. (1988) Laboratory Manual
for Fusarium Research. Sydney, University of Sydney.
Champeil A, Dore T, Fourbet JF. (2004a) Fusarium head blight: epi-
demiological origin of the effects of cultural practices on head
blight attacks and the production of mycotoxins by Fusarium in
wheat grains. Plant Sci 166:1389–1415.
Champeil A, Fourbet JF, Dore T, Rossignol L. (2004b) Influence of
cropping system on fusarium head blight and mycotoxin levels in
winter wheat. Plant Prot Sci 23:531–537.
Desjardins AE. (2006) Fusarium Mycotoxin Chemistry: Genetics and
Biology. St. Paul, MN, USA, American phytopathological society.
Diamond H, Cooke BM. (1999) Towards the development of a novel
in vitro strategy for early screening of fusarium ear blight resis-
tance in adult winter wheat plants. Eur J Plant Pathol 105:363
–372.
Divon HH, Razzaghian J, Udnes-Aamot H, Klemsdal SS. (2011)
Fusarium langsethiae (Torp and Nirenberg), investigation of alter-
native infection routes in oats. Eur J Plant Pathol 132:147–161.
Doohan FM, Brennan J, Cooke BM. (2003) Influence of climatic
factors on Fusarium species pathogenic to cereals. J Plant Pathol
109:755–768.
EC. (2006) Commission regulation (EC) No 1881/2006 of 19 Decem-
ber 2006 setting maximum levels of certain contaminants in food-
stuffs. Off J Eur Communities: Legis. http://eur-lex.europa.eu/
LexUriServ/LexUriServ.do?uri=OJ:L:2006:364:0005:0024:EN:PDF
(verified Apr 15, 2012).
Edwards SG. (2007a) Investigation of Fusarium Mycotoxins in UK
Barley and Oat Production. HGCA Report No. 415. London,
HGCA.
Edwards SG. (2007b) Investigation of Fusarium Mycotoxins in UK
Wheat Production. HGCA Report No. 413. London, HGCA.
Edwards SG. (2007c) Impact of agronomy on mycotoxin contamina-
tion of wheat and oats. Fusarium diseases in cereals-potential
impact for sustainable cropping systems. In: Vogelsang S, Jalli M,
Kovacs G, Vida G (eds) Proceedings of the COST SUSVAR Fusa-
rium Workshop, 1-2 June 2007. Valence, Hungary, pp 12–14.
Edwards SG. (2009) Fusarium mycotoxin content in UK organic and
conventional oats. Food Addit Contam Part A Chem Anal Control
Expo Risk Assess 26:1063–1069.
Edwards S, Barrier-Guillot B, Clasen PE, Hietaniemi V, Pettersson
H. (2009) Emerging issues of HT-2 and T-2 toxins in European
cereal production. World Mycotoxin J 2:173–179.
Edwards SG, Imathiu SM, Ray RV, Back M, Hare MC. (2012)
Molecular studies to identify the Fusarium species responsible for
HT-2 and T-2 mycotoxins in UK oats. Int J Food Microbiol
156:168–175.
EFSA. (2011) Scientific opinion on the risks for animal and public
health related to the presence of T-2 and HT-2 toxin in food and
feed. EFSA J 9:2481.
Eriksen GS, Alexander J (eds) (1998) Fusarium Toxins in Cereals – A
Risk Assessment. Nordic Council of Ministers, Tema Nord,
Copenhagen, 502, pp 7–44.
FAO. (2004) Worldwide Regulations for Mycotoxins in Food and Feed
in 2003. FAO Food and Nutrition Paper 81. Rome, FAO.
Fredlund E, Gidlund A, Pettersson H, Olsen M, Borjesson T. (2010)
Real-time PCR detection of Fusarium species in Swedish oats and
correlation to T-2 and HT-2 toxin content. World Mycotoxin
J 3:77–88.
Gautier P. (2007) Les 1ers enseignements des enquetes parcellaires
pluri annuelles en orges, 4eme Colloque Qualites de Cereales. Ver-
sailles, Syngenta Agro.
Gavrilova O, Gagkaeva T, Burkin A, Kononenk G (2010) Charac-
terisation of Fusarium langsethiae isolates originated from different
regions of Russia and North Europe. Fusarium – mycotoxins, tax-
onomy, pathogenicity and host resistance. In: Arseniuk E, Czem-
bor E, Goral T. (eds) 11th European Fusarium Seminar. Poland,
IHAR Radzików, pp 129–130.
Gilbert J, Tekauz A. (1995) Effects of fusarium head blight and seed
treatment on germination, emergence and seedling vigour of spring
wheat. Can J Plant Pathol 17:252–259.
Goswami RS, Kistler HC. (2004) Heading for disaster: Fusarium
graminearum on cereal crops. Mol Plant Pathol 5:515–525.
Halstensen AS, Nordby K, Eduard W, Klemsdal SS. (2006a) Real-
time PCR detection of toxigenic Fusarium in airborne and settled
grain dust and associations with trichothecene mycotoxins. J Envi-
ron Monit 8:1235–1241.
Halstensen AS, Nordby KC, Klemsdal SS, Elen O, Clasen PE,
Eduard W. (2006b) Toxigenic Fusarium spp. as determinants of
trichothecene mycotoxins in settled grain dust. J Occup Environ
Hyg 3:651–659.
Hietaniemi V, Kontturi M, Eurola M, Ramo S, Niskanen M, Kan-
gas A, Saastamoinen M. (2004) Content of trichothecenes in oats
during official variety, organic cultivation and nitrogen fertiliza-
tion trials in Finland. Agric Food Sci 13:54–67.
Hope R, Aldred D, Magan N. (2005) Comparison of environmental
profiles for growth and deoxynivalenol production by Fusarium
Fusarium langsethiae, a HT-2 and T-2 Toxins Producer
culmorum and F. graminearum on wheat grains. Lett Appl Micro-
biol 40:295–300.
Imathiu SM. (2008a) Fusarium langsethiae Infection and Mycotoxin
Production in Oats. Newport, UK, Harper Adams University
College, PhD Thesis.
Imathiu SM, Ray RV, Back M, Hare MC, Edwards SG. (2009)
Fusarium langsethiae pathogenicity and aggressiveness towards
oats and wheat in wounded and unwounded in vitro detached leaf
assays. Eur J Plant Pathol 124:117–126.
Imathiu SM, Hare MC, Ray RV, Back M, Edwards SG. (2010)
Evaluation of pathogenicity and aggressiveness of F. langsethiae
on oats and wheat seedlings relative to known seedling blight
pathogens. Eur J Plant Pathol 126:203–216.
Inch S, Gilbert J. (2003) The incidence of Fusarium species recovered
from inflorescences of wild grasses in southern Manitoba. Can
J Plant Pathol 25:379–383.
Infantino A, Pucci N, Conca G, Santori A. (2007) First report of
Fusarium langsethiae on durum wheat kernels in Italy. Plant Dis
91:1362.
Jenkinson P, Parry DW. (1994) Isolation of Fusarium species from
common broad-leaved weeds and their pathogenicity to winter
wheat. Mycol Res 98:776–780.
Joffe AZ. (1986) Fusarium Species: Their Biology and Toxicology.
New York, USA, J. Wiley & Sons, pp 588.
Johansson PM, Johansson L, Gerhardson B. (2003) Suppression of
wheat-seedling diseases caused by Fusarium culmorum and
Microdochium nivale using bacterial seed treatment. Plant Pathol
52:219–227.
Knutsen AK, Torp M, Holst-Jensen A. (2004) Phylogenetic analyses
of the Fusarium poae, Fusarium sporotrichioides and Fusarium
langsethiae species complex based on partial sequences of the
translation of elongation factor-1 alpha gene. Int J Food Microbiol
95:287–295.
Koch HJ, Pringas C, Maerlaender B. (2006) Evaluation of environ-
mental and management effects of fusarium head blight infection
and deoxynivalenol concentration in the grain of winter wheat.
Eur J Agron 24:357–366.
Kokkonen M, Ojala L, Parikka P, Jestoi M. (2010) Mycotoxin pro-
duction of selected Fusarium species at different culture conditions.
Int J Food Microbiol 143:17–25.
Lacey J, Bateman GL, Mirocha CJ. (1999) Effects of infection time
and moisture on the development of ear blight and deoxynivalenol
production by Fusarium species in wheat. Ann Appl Biol 134:
277–283.
Langseth W, Rundberget T. (1999) The occurrence of HT-2 toxin
and other trichothecenes in Norwegian cereals. Mycopathologia
147:157–165.
Langseth W, Stabbetorp H. (1996) The effect of lodging and time of
harvest on deoxynivalenol contamination in barley and oats.
J Phytopathol 144:241–245.
Leslie JF, Summerell BA. (2006) The Fusarium Laboratory Manual,
1st edn. USA, Blackwell publishing professional.
Liu WZ, Langseth W, Skinnes H, Elen ON, Sundheim L. (1997)
Comparison of visual head blight ratings, seed infection levels and
deoxynivalenol production for assessment of resistance in cereals
inoculated with Fusarium culmorum. Eur J Plant Pathol 103:
589–595.
Lukanowski A, Sadowski C. (2008) Fusarium langsethiae on kernels
of winter wheat in Poland – occurrence and mycotoxigenic
abilities. Cereal Res Commun 36(Suppl. B):453–457.
Maiorano A, Blandino M, Reyneri A, Vanara F. (2008) Effect of
maize residues on the Fusarium spp. Infection and deoxynivale-
nol (DON) contamination of wheat grain. Crop Prot 27:182–
188.
Marasas WFO, Nelson PE, Toussoun TA. (1984) Toxigenic Fusari-
um Species: Identity and Mycotoxicology. London, UK, The Penn-
sylvania State University Press.
McMullen M, Jones R, Gallenburg D. (1997) Scab of wheat and
barley: a re-emerging disease of devastating impact. Plant Dis
81:1340–1348.
Medina A, Magan N. (2010) Comparisons of water activity and tem-
perature impacts on growth of Fusarium langsethiae strains from
9
northern Europe on oat-based media. Int J Food Microbiol
142:365–369.
Medina A, Magan N. (2011) Temperature and water activity
effects on production of T-2 and HT-2 by Fusarium langsethiae
strains from north European countries. Food Microbiol 28:
392–398.
Miller JD, Culley J, Fraser K, Hubbard S, Meloche F, Ouellet T,
Seaman WL, Seifert KS, Turkington K, Voldeng H. (1998) Effect
of tillage practice on fusarium head blight of wheat. Can J Plant
Pathol 20:95–103.
Moss MO. (1992) Secondary metabolism and food intoxication-
moulds. J Appl Bacteriol Symp Suppl 73:80–88.
Mylona K, Magan N. (2011) Fusarium langsethiae: storage environ-
ment influences dry matter losses and T2 and HT-2 toxin contami-
nation of oats. J Stored Prod Res 47:321–327.
Nelson PE, Toussoun TA, Marasas WFO. (1983) Fusarium Species:
An Illustrated Manual for Identification. University Park, PA,
USA, Pennsylvania State University Press.
Nganje W, Bangsund D, Leistritz F, Wilson W, Tiapo N. (2004)
Regional economic impacts of fusarium head blight in wheat and
barley. Rev Agric Econ 26:332–347.
Nicholson P, Chandler E, Draeger RC, Gosman NE, Simpson DR,
Thomsett M, Wilson AH. (2003) Molecular tools to study epide-
miology and toxicology of fusarium head blight of cereals. Eur
J Plant Pathol 109:691–703.
Nicolaisen M, Suproniene S, Nielsen LK, Lazzaro I, Spliid NH,
Justese AF. (2009) Real-time PCR for quantification of eleven
individual Fusarium species in cereals. J Microbiol Methods 76:234
–240.
Nielsen LK, Jensen JD, Nielsen GC, Jensen JE, Spliid NH, Thomsen
IK, Justesen AF, Collinge DB, Jorgensen LN. (2011) Fusarium
head blight of cereals in Denmark: species complex and related
mycotoxins. Phytopathology 101:960–969.
Nightingale MJ, Marchylo BA, Clear RM, Dexter JE, Preston KR.
(1999) Fusarium head blight: effect of fungal proteases on wheat
storage proteins. Cereal Chem 76:150–158.
Parikka P, Hietaniemi V, Ramo S, Jalli H (2007) The effect of culti-
vation practices on Fusarium langsethiae infection of oats and bar-
ley. Fusarium diseases in cereals – potential impact from
sustainable cropping systems. In: Vogelsang S, Jalli M, Kovacs G,
Vida G. (eds) Proceedings of the COST SUSVAR Fusarium Work-
shop, 1-2 June 2007. Valence, Hungary, pp 15–18.
Parry DW, Jenkinson P, McLead L. (1995) Fusarium ear blight
(scab) in small grain cereals-a review. Plant Pathol 44:207–238.
Pettersson H, Borjesson T, Persson L, Lerenius C, Berg G, Gustafs-
son G. (2008) T-2 and HT-2 toxins in oats grown in northern
Europe. Cereal Res Commun 36(Suppl. B):591–592.
Pettersson H, Brown C, Hauk J, Hoth S, Meyer J, Wessels D.
(2010) Survey of T-2 and HT-2 toxins by LC–MS/MS in oats and
oat products from European oat mills in 2005–2009. Food Addit
Contam Part B Surveill 4:110–115.
Pirgozliev SR, Edwards SG, Hare MC, Jenkinson P. (2003) Strate-
gies for the control of fusarium head blight in cereals. Eur J Plant
Pathol 109:731–742.
Pohland AE. (1993) Mycotoxins in review. Food Addit Contam 10:
17–28.
Schaafsma AW, Tamburic-llinic L, Miller JD, Hooker DC. (2001)
Agronomic considerations for reducing deoxynivalenol in wheat
grain. Can J Plant Pathol 23:279–285.
Schaafsma AW, Tamburic-llinic L, Hooker DC. (2005) Effect of pre-
vious crop, tillage, field size, adjacent crop and sampling direction
on airborne propagules of Gibberella zeae/Fusarium graminearum,
fusarium head blight severity and deoxynivalenol accumulation in
winter wheat. Can J Plant Pathol 27:217–224.
Smith JE, Lewis CW, Anderson JG, Solomons GL. (1994) Mycotox-
ins in Human Nutrition and Health. Luxembourg, EEC.
Snijders CHA. (2004) Resistance in wheat to Fusarium infection and
trichothecene formation. Toxicol Lett 153:37–46.
Strub C, Pocaznoi D, Lebrihi A, Fournier R, Mathieu F. (2010)
Influence of barley malting operating parameters on T-2 and HT-2
toxinogenesis of Fusarium langsethiae, a worrying contaminant of
malting barley in Europe. Food Addit Contam 27:1247–1252.
10
Suproniene S, Justesen AF, Nicolaisen M, Mankeviciene A, Dabkev-
icius Z, Semaskiene R, Leistrumaite A. (2010) Distribution of
trichothecene and zearalenone producing Fusarium species in grain
of different cereal species and cultivars grown under organic farm-
ing conditions in Lithuania. Ann Agric Environ Med 17:79–86.
Sweeney MJ, Dobson ADW. (1998) Mycotoxin production by
Aspergillus, Fusarium and Penicillium species. Int J Food Microbiol
43:141–158.
Tekauz A, McCallum B, Ames N, Fetch JM. (2004) Fusarium head
blight of oats-current status in western Canada. Can J Plant
Pathol 26:473–479.
Thrane U, Adler A, Clasen P, Galvano F, Langseth W, Lew H,
Logrieco A, Nielen KF, Ritieni A. (2004) Diversity in metabolite
production by Fusarium langsethiae, Fusarium poae and Fusarium
sporotrichioides. Int J Food Microbiol 95:257–266.
Torp M, Adler A. (2004) The European Sporotrichiella Project: a
polyphasic approach to the biology of new Fusarium species. Int
J Food Microbiol 95:257–266.
Torp M, Langseth W. (1999) Production of T-2 toxin by a Fusarium
resembling Fusarium poae. Mycopathologia 147:89–96.
Torp M, Nirenberg HI. (2004) Fusarium langsethiae sp. nov. on cere-
als in Europe. Int J Food Microbiol 95:247–256.
Visconti A. (2001) Problem associated with Fusarium mycotoxins in
cereals. Bull Inst Compr Agric Sci, Kinki Univ 9:39–55.
Waalwijk C, van der Heide R, de Vries I et al. (2004) Quantitative
detection of Fusarium species in wheat using TaqMan. Eur J Plant
Pathol 110:481–494.
Wilson A, Simpson D, Chandler E, Jennings P, Nicholson P. (2004)
Development of PCR assays for the detection and differentiation
of Fusarium sporotrichioides and Fusarium langsethiae. FEMS
Microbiol Lett 233:69–76.
Imathiu et al.
Windels CE. (1991) Current status of Fusarium taxonomy. Phytopa-
thology 81:1048–1051.
Winson SJ, Hare MC, Jenkinson P. (2001) The interaction between
ear sprays and seed treatment for the control of Fusarium seedling
blight in wheat. In: Biddle AJ. (ed.) Seed Treatment-Challenges
and Opportunities. Farnham, UK, British Crop Protection Council,
pp 251–256.
Xu X. (2003) Effects of environmental conditions on the develop-
ment of fusarium ear blight. Eur J Plant Pathol 109:683–689.
Xu XM, Parry DW, Nicholson P et al. (2005) Predominance and
association of pathogenic fungi causing fusarium ear blight in
wheat in four European countries. Eur J Plant Pathol 112:143
–154.
Yli-Mattila T, Paavanen-Huhtala S, Parikka P, Konstantinova P,
Gagkaeva TY. (2004) Molecular and morphological diversity of
Fusarium species in Finland and north-western Russia. Eur J Plant
Pathol 110:573–585.
Yli-Mattila T, Paavanen-Huhtala S, Jestoi M, Parikka P, Hietaniemi
V, Gagkaeva T, Sarlin T, Haikara A, Laaksonen S, Rizzo A.
(2008) Real-time PCR detection and quantification of Fusarium
poae, F. graminearum, F. sporotrichioides and F. langsethiae in cer-
eal grains in Finland and Russia. Arch Phytopath Plant Protect
41:243–260.
Yli-Mattila T, Ward TJ, O’Donnell K, Proctor RH, Burkin AA,
Kononenko GP, Gavrilova OP, Aoki T, McCormick SP,
Gagkaeva TY. (2011) Fusarium sibiricum sp. nov, a novel type A
trichothecene-producing Fusarium from northern Asia closely
related to F. sporotrichioides and F. langsethiae. Int J Food Micro-
biol 147:58–68.