14 breeding for resistance to ear rots caused by

Bạn đang xem bản rút gọn của tài liệu. Xem và tải ngay bản đầy đủ của tài liệu tại đây (468.5 KB, 19 trang )

Plant Breeding 131, 1—19 (2012)
Ó 2011 Blackwell Verlag GmbH

doi:10.1111/j.1439-0523.2011.01936.x

Review
Breeding for resistance to ear rots caused by Fusarium spp. in maize – a review
´ K O S M E S T E R H A´ Z Y 1 , M A R C L E M M E N S 2 and L A N A M . R E I D 3
A
1

Cereal Research Non-profit Company, PO Box 391, H-6701 Szeged, Hungary, E-mail: ;
Department for Agrobiotechnology, University for Natural Resources and Life Sciences, A-3430 Tulln, Konrad Lorenz Street
20, Vienna, Austria; 3 Eastern Cereal and Oilseed Research Centre, Agriculture and Agri-Food Canada, Ottawa, ON K1A0C6,
Canada
2

With 2 tables
Received February 17, 2011/Accepted November 7, 2011
Communicated by T. Miedaner

Abstract
Ear rots caused by diﬀerent Fusarium spp. are one of the most
dangerous food and feed safety challenges in maize production. At
present, the majority of the inbreds and hybrids are susceptible.
Gibberella and Fusarium ear rots (caused by Fusarium graminearum
and Fusarium verticillioides, respectively) are the two main diseases, but
more than 10 further Fusarium spp. cause ear rots. Natural infection is
initiated by a mixture of the local Fusarium spp., but usually one species
predominates. Many maize breeders rely on natural infection to create
suﬃcient levels of disease severity for selection-resistant genotypes;

however, there are few locations where the natural infection is
suﬃciently uniform to make this selection eﬃcient and successful.
Thus, an artiﬁcial inoculation method normally performed with one
fungal species is now used by more breeders. Most published papers on
breeding for ear rot resistance are focused on either F. graminearum or
F. verticillioides, and reports involving both or more Fusarium spp. are
rare. Several reports support the hypothesis that resistance to multiple
species especially F. graminearum, F. culmorum and F. verticillioides
may be common. Signiﬁcant diﬀerences in genotypic resistance after
inoculation exist. Resistance to the two major modes of fungal entry
into the ear, via the silk or through kernel wounds, is not correlated in
all genotypes. The reason is not clear. When silk channel resistance was
assessed, the data from natural and artiﬁcial inoculation trials
correlated well. Analogous data relating to kernel resistance have not
been published. Both native and exotic sources of resistance are
important, but surprisingly little information is available. Few papers
report on the use of artiﬁcial inoculation during inbred development.
Most of the publications on inoculation are concerned with testing at
later stages when combining ability is tested. Inbreds diﬀer in general
and speciﬁc combining ability for ear rot resistance. The expression of
resistance to disease severity and resistance to toxins is often used as
synonyms, but in fact they are not. Higher resistance to visual disease
severities mostly results in lower toxin contamination, and the
resistance level seems to be the most important factor regulating the
toxin content. The mode of inheritance of resistance appears to diﬀer:
additive, possibly non-additive eﬀects, digenic (dominant) and polygenic patterns have been identiﬁed. Improved phenotyping methods
that take into account the inﬂuence of stalk rot and the use of several
independent isolates are available. The QTLs mostly exhibit small
eﬀects and some are validated; however, marker-assisted selection in
breeding cannot yet be foreseen. As the severity of natural infections

tends to correlate with the artiﬁcial inoculation results, the incorporation of artiﬁcial inoculation methods in breeding programmes is now
the most important task. As genotypic resistance diﬀerences between
hybrids are high, the registration of hybrids should consider the use of
the inoculation tests to choose most resistant hybrids for commercial
production. This is the most rapid way to increase feed safety.

Key words: Fusarium graminearum — Fusarium verticillioides
— Fusarium — inoculation methods — resistance — inheritance of resistance — mycotoxins — breeding — corn — maize
— Zea mays — ear rot
Ear rot diseases of maize, or corn, caused by Fusarium spp. have
long been known. One of the ﬁrst scientiﬁc reports was that of
Bisby and Bailey (1923) in Canada. In contrast to Fusarium
stalk rots that often result in direct yield losses, ear rots rarely
do so; however, occasional high yield losses have been reported
(Vigier et al. 2001). As a consequence, only sporadic breeding
eﬀorts have been undertaken to increase resistance to ear rots.
It was not until the discovery of Fusarium mycotoxins that the
full impact of the indirect economic loss from an ear rot
outbreak became known. New regulations for the allowable
mycotoxin limits in food and feed have been put in place in
most countries. Today, more and more maize breeding
programmes at both public and private institutions are initiating and expanding breeding programmes to develop resistant
inbreds and hybrids for both human and animal consumption.
In the 1920s and 1930s, hybrid breeding of maize was
developed in the USA. By the late 1950s, hybrid varieties of
maize dominated the maize acreage (Sprague 1977). This
resulted in two signiﬁcant changes in maize breeding: (i) the
use of open pollinated landraces and varieties with their broader
genetic diversity decreased and (ii) inbreeding for line and hybrid
development was carried out in the same location, and owing to

a lack of continuous epidemics, selection for ear rot resistance
was not possible and susceptibility levels increased. As a result,
sporadic resistance breeding programmes were initiated in
North America and elsewhere. Initial studies were mostly on
Gibberella ear rot (GER) caused by Fusarium graminearum
Schwabe [teleomorph = Gibberella zeae (Schwein.) Petch].
Gibberella ear rot is not to be confused with Fusarium ear rot
(FER) that is caused by a diﬀerent Fusarium species, Fusarium
moniliforme, which was recently reclassiﬁed by Seifert et al.
(2004) as Fusarium verticillioides [=F. moniliforme J. Sheld.
(sexual stage: G. moniliformis Wineland)]. Early on, it was
reported that resistance to both diseases is inherited in a
quantitative manner (Boling and Grogan 1965, Ullstrup 1977).
Interest in increasing ear rot resistance spiked with the
detection of Fusarium mycotoxins in the grain. Zearalenone

wileyonlinelibrary.com

´ . M e s t e r h a´ z y , M . L e m m e n s and L . M . R e i d
A

2

Table 1. Fusarium spp. found in naturally infected maize grains in several maize-producing countries
Country
Canada
Canada
China
Europe

France
Germany
Germany
Germany
Hungary
Mexico
Switzerland
USA
USA
USA
USA
USA
Zambia

Fac Fant Fav Fc Fcer Fcr Feq Fg Fm Fo Fp Fpro Fsg Fsp Ftr Fv Fven Other
x
x
x

x

x
x
x
x

x

x
x

x
x
x

x

x

x

x
x

x

x

x
x
x
x
x
x
x
x
x
x
x
x

x

x

x

x

x
x
x
x
x
x
x
x

x
x

x

x
x

x
x
x

x

x
x
x

x

x
x
x

x

x

x

x
x
x
x

x
x
x

x
x

x

x
x

5
1
x
8

x
x
x
x
x
x

Author
Sutton and Baliko (1981), Sutton (1982)
Martens et al. (1984)
Tanaka et al. (1988)
Logrieco et al. (2002)
Folcher et al. (2009)
Focke (1966), Focke and Kuăhnel (1964)
Sass et al. (2007)
Goertz (2009), Goertz et al. (2008, 2010)
Mesterha´zy and Vojtovics (1977)
Garcia-Aguirre and Martinez-Flores (2010)
Dorn et al. (2009)
Koehler (1959)
Koehler (1950)

Ullstrup (1953)
Jugenheimer (1976)
Munkvold (2003b)
Schjoth et al. (2009)

Fac, F. acuminatum, Fant, F. anthophilum, Fc, F. culmorum, Feq, F. equiseti, Fg, F. graminearum, Fm, F. moniliforme, Fo, F. oxysporum, Fp,
F. poae, Fpro, F. proliferatum, Fsg, F. subglutinans, Fsp, F. sporotrichioides, Ftr, F. tricinctum, Fv, F. verticillioides, Fven, F. venenatum.

(ZEA) was the ﬁrst toxin to be identiﬁed followed by deoxynivalenol (DON) (Mirocha 1974, Vesonder et al. 1979), both
produced by F. graminearum. The F. verticillioides mycotoxin,
fumonisin B1, was discovered in 1988 (Gelderblom et al. 1988).
The main goal of breeding eﬀorts was to develop either toxin
resistance or disease resistance; however, the relationship
between these two types of resistance was not clearly deﬁned
and they were often used as synonyms (Clements and White
2004, Menkir et al. 2006, Williams 2006). Knowledge relating to
mycotoxins grew rapidly from many diﬀerent laboratories. The
metabolic synthesis and physiological eﬀects on humans and
livestock are now known for most of the toxins. This resulted in
the establishment of legally allowable limits for many toxins in
all important grain-producing regions of the world. Unfortunately, it did not result in the development of commercial
hybrids with improved resistance as most are susceptible or very
susceptible (Munkvold 2003b, Reinprecht et al. 2008).
As an alternative to or in addition to resistance breeding,
breeding transgenic maize for increased insect resistance and
better agronomic practices are suggested for ear rot control.
Insect wounds, especially to the ear, from pests such as
Ostrinia nubilalis, Diatraea grandiosella, Diabrotica virgifera
virgifera, Heliocoverpa zeae and Frankliniella spp., increase the
levels of Fusarium infection by creating new points of entry for

the fungus to enter the plant (Archer et al. 2001, Parsons and
Munkvold 2010a). Numerous recent articles have indicated
that transgenic plants modiﬁed by Bt genes (genes from
Bacillus thuringiensis with insecticidal properties) have significantly decreased DON and other toxins levels (Munkvold
et al. 1997a, Dowd 2001, Munkvold 2003a, de la Campa et al.
2005, Papst et al. 2005, Wu 2006). No fungicide control has yet
to be released until just recently in Europe (Loăer et al.
2010a). Folcher et al. (2009) reported a 90% reduction in
Fusarium mycoﬂora with some fungicides; however, further
analysis is required.
Resistance to ear rots is important for both grain and silage
maize. Stalk rot resistance in silage maize is a crucial trait, as
mycotoxins can be found in stalks, but a detailed evaluation of
stalk resistance is beyond the scope of this paper. For more
information, the reader is referred to Christensen and Wilcoxson (1966) who published an excellent review of the early
literature. More recent partial reviews can be found in Afolabi

et al. (2008), Barrie`re et al. (1997), Nagy and Cabulea (1996),
and Pappelis (1984); however, a comprehensive review of the
past 50 yearsÕ research has yet to be written.
The more recent binding EU regulations on toxin contamination for human consumption and recommendations for
animal feeding (Anonymous 2005, 2006, 2007) have forced a
renewed interest in breeding eﬀorts for ear rot resistance as the
preferred method of control. As the growing knowledge on
resistance has not been reviewed in detail in the last few
decades and numerous papers on resistance have been
published since the two partial reviews by Munkvold (2003b)
and Clements and White (2004), we decided to summarize the
novel results and concepts developed and discuss several
important conclusions for the future.

The Pathogens and Associated Mycotoxins
The pathogens
One of the ﬁrst reports on ear rots caused by Fusarium spp.
originated from Canada by Bisby and Bailey (1923). The ear
rot caused by F. graminearum was later called GER and is
widespread in Canada, the USA and many other countries,
Table 1 (Koehler 1957, 1959, Sutton and Baliko 1981, Reid
et al. 1996a). Fusarium verticilliodes (referred to as F. moniliforme in papers published prior to the reclassiﬁcation by
Seifert et al. (2004) as F. verticillioides) was identiﬁed as a
weak ear rot pathogen in the earlier reports (Ullstrup 1953,
cited by Jugenheimer 1976) but has since been shown to be
more of an endophyte fungi that tends to have lower visible
symptoms of infection in the kernels and can be systemic in the
maize plant (Munkvold et al. 1997a,b). This pathogen is the
causal agent of FER. Other members of the Liseola Section
like Fusarium proliferatum are also understood to be pathogens
responsible for FER. Many diﬀerent species occur in maize
grain besides these three (Table 1), and in many cases, they
play an important role in causing GER and FER. Folcher
et al. (2009) identiﬁed 12 Fusarium spp. in France. In the
southern regions, mainly F. verticillioides and F. proliferatum
were present, and in the northern part, mainly F. graminearum
and Fusarium culmorum. Hungary is similar; Mesterha´zy and
Vojtovics (1977) found that in dry years the distribution of the
Fusarium spp. is closer to the distribution of Fusarium spp. in

Breeding for resistance to ear rots

3

Table 2: Mycotoxigenic Fusarium species associated with cereal crops and their mycotoxins (Logrieco et al. 2002)
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium
Fusarium

species1
acuminatum
anthophilum
avenaceum
cerealis
chlamydosporum

culmorum
equiseti
graminearum
heterosporum
nygamai
oxysporum
poae
proliferatum
sambucinum
semitectum
sporotrichioides
subglutinans
tricinctum
verticillioides

Mycotoxins2
T2, MON, HT2, DAS, MAS, NEO, BEA
BEA
MON, BEA
NIV, FUS, ZEN, ZOH
MON
DON, ZEN, NIV, FUS, ZOH, AcDON
ZEN, ZOH, MAS, DAS, NIV, DAcNIV, FUS, FUC, BEA
DON, ZEN, NIV, FUS, AcDON, DAcDON, DAcNIV
ZEN, ZOH
BEA, FB1, FB2
MON, BEA
DAS, NIV, FUS, MAS, T2, HT2, NEO, BEA
FB1, BEA, MON, FUP, FB2,
DAS, T2, NEO, ZEN, MAS, BEA

ZEN, BEA
T2, HT2, NEO, MAS, DAS
BEA, MON, FUP
MON, BEA
FB1, FB2, FB3

1

Fusarium nomenclature according to Nelson et al. (1983).
Bold letters indicate the important mycotoxins.
AcDON, monoacetyldeoxynivalenols (3-AcDON, 15-AcDON); AcNIV, monoacetylnivalenol (15-AcNIV); BEA, Beauvericin; DiAcDON,
Diacetyldeoxynivalenol (3,15-AcDON); DAcNIV, diacetylnivalenol (4,15-AcNIV); DAS, diacetoxyscirpenol; DON, deoxynivalenol (vomitoxin);
FB1, fumonisin B1; FB2, fumonisin B2; FB3, fumonisin B3; FUP, fusaproliferin; FUS, fusarenone-X (4-acetyl-NIV); FUC, fusarochromanone;
HT2, HT-2 toxin; MAS, monoacetoxyscirpenol; MON, moniliformin; NEO, neosolaniol; NIV, nivalenol; T2, T-2 toxin; ZEN, zearalenone;
ZOH, zearalenols (a and b isomers).
2

the south, and in wetter years the Fusarium spp. of the
northern regions predominated. Other Hungarian results
(Be´ke´si and Hinfner 1970, Bı´ ro´ne´ 1975) support this complexity of the pathogen population. Similar species distributions
are found in North America with GER predominantly found
in the northern regions and FER in the southern regions or in
dryer years in a northern area (Reid et al. 1999). A single ear
or grain can occasionally be infected by diﬀerent Fusarium spp.
depending on the conditions of a growing season in a region
(Logrieco et al. 2002). Identiﬁcation of Fusarium spp. is easier
than it used to be. The most important species have speciesspeciﬁc markers and can be quantiﬁed by PCR analysis (Reid
et al. 1999, Pauls et al. 2001, Waalwijk et al. 2004, Xu et al.
2008, Nicolaisen et al. 2009).
Pathogenicity between Fusarium spp. and aggressiveness

within a species is quite variable. Isolates of F. graminearum
and F. culmorum are commonly highly aggressive with a
considerable proportion of the isolates considered very
aggressive. Fusarium verticillioides and the other Fusarium
spp. tend to display lower aggressiveness. Careful screening of
isolates is necessary to select the more aggressive ones for
artiﬁcial inoculation in a breeding programme (Mesterha´zy
1978, Reid et al. 2002, Iglesias et al. 2010, Miedaner et al.
2010). For F. graminearum and F. culmorum from wheat,
Mesterha´zy (1983, 1995, 2002) and Mesterha´zy et al. (1999)
found large variation in aggressiveness and DON production
between isolates and years. Considerable diﬀerences in aggressiveness and toxin production were observed also when inocula
from the same test tube were tested, and this did not correlate
with the conidium concentrations measured. Similar data were
obtained for maize (A´. Mesterha´zy, unpublished). Garcia et al.
(2009) concluded that it would be diﬃcult to predict mycotoxin levels because these levels are highly associated with the
contaminating fungal strain not just the environmental conditions. Marı´ n et al. (2008) also reported high variability in
mycotoxin production between diﬀerent fungal strains and on
diﬀerent substrates. Therefore, complicating prediction models

based on visible symptoms and mycotoxin formation may be
diﬃcult to create. From the same isolate, inocula with diﬀerent
aggressiveness can be produced (Kova´cs et al. 1994). For this
reason, a change of inoculum, even though originating from
one and the same isolate, within an experiment is not
recommended as the two levels of aggressiveness of the
diﬀerent inocula can vary and inﬂuence infection levels.
Therefore, each experiment is so planned that a change of
inoculum should not occur. Further research on aggressiveness, fungal mass and conidium concentration is necessary.
Fusarium graminearum possesses diﬀerent pathogenesisrelated (PR) genes (Dufresne et al. 2008), but these are not

necessarily virulence genes and they cannot be used in a
breeding programme. It is certain that Fusarium spp. have
virulence factors, but it is not known whether the diﬀerent
Fusarium spp. possess common and/or diﬀerent virulence
factors. Mesterha´zy et al. (1999) reported that DON production is a virulence factor of F. graminearum in wheat. Harris
et al. (2005) also proved this for F. graminearum in maize; its
role, however, is not known. Another risk factor may be the
change in pathogenic population structure when more resistant
hybrids are grown. No reliable information is available on this
topic, but it will presumably signiﬁcantly inﬂuence breeding
programmes.
Although no data exist for maize, in wheat there is no
evidence of race-speciﬁc specialization within Fusarium spp.
(Snijders and van Eeuwijk 1991, Mesterha´zy 1995). The same
QTLs gave protection to all Fusarium spp. tested (Mesterha´zy
et al. 2007). Research in this ﬁeld for maize should be
undertaken. For resistance breeding, the appreciable number
of Fusarium spp. creates a serious challenge.
Mycotoxins
Fusarium spp. produce a large number of chemically very
diﬀerent mycotoxins (Table 2) (Logrieco et al. 2002). The high
diversity of these toxins and those detected recently (Barto´k

4

et al. 2006, 2010) excludes the possibility of selecting for
general toxin resistance. The two toxins of most importance to
GER are DON and ZEA. If contaminated grain is fed to
livestock, especially swine, the trichothecene DON results in

vomiting, feed refusal, decreased weight gain and reproductive
problems (Vesonder et al. 1981, Prelusky et al. 1994). Storage
workers might also be exposed to toxins, mainly through
powder of infected grains in the air through inhalation, but
this problem was not mentioned in the monograph of
Christensen (1982). In the authorized Hungarian regulation,
there is no word on this problem. We think that this research
branch will be important in the future to see clear and make
the necessary regulations. This toxin is also an immunosuppressant and thus predisposes animals to other diseases and
masks underlying toxicoses (Pestka and Bondy 1994). Zearalenone causes reproductive problems including reduced litter
size, swine oestrogenic syndrome and male infertility (Prelusky
et al. 1994). Human relations are also important, immunsuppression of trichethecenes was proved (Berek et al. 2001), and
ZEA inﬂuences also children hormone household causing
telarche (Szuăts et al. 1997). Therefore toxin contaminated
grains may cause human health problems. FER results in the
contamination of the grain with the polyketide fumonisin
mycotoxins such as FB1, which causes equine leukoencephalomalacia (Kellerman et al. 1990), porcine pulmonary oedema
(Harrison et al. 1990), liver cancer in rats (Gelderblom et al.
1988) and neural tube defects in mice (Voss et al. 2006).
Fumonisins have also been associated with human oesophageal cancer (IARC 1993). Besides causing direct and indirect
economic losses, these fungi can also aﬀect the health of grain
handlers and processors. Throughout the literature, resistance
to these toxins and resistance to disease symptoms have been
treated as two diﬀerent types of resistance.
Some Fusarium spp. with apparent lower aggressiveness, as
measured by visible disease symptoms, pose an additional
challenge as these pathogens may be excellent toxin producers
like F. verticillioides with its many fumonisin toxins and
Fusarium sporotrichioides with its T-2 toxin. Resistance to
these pathogens should therefore not be neglected. Resistance

to one species may not be correlated to resistance to other
species (Reid et al. 2002, 2009). Also, selection for resistance to
a pure isolate of one species may not result in resistance to a
multi-Fusarium population in commercial maize ﬁelds.

Infection Pathways, Disease Symptoms and Evaluation of
Resistance
There are three main modes of fungal entry or infection
pathways, by which Fusarium spp. enter maize ears: (i) by
fungal spores landing on the silks, germinating and then the
fungal mycelia grow down the silks to infect the kernels and
cob (rachis) (Koehler 1942); (ii) wounds created by insects
feeding on the ear or from bird or hail damage oﬀer a point of
entry for fungi (Sutton 1982); and (iii) some Fusarium spp. are
systemic, such as F. verticilliodes, and can enter the ear from
infected stalks (Foley 1959, Munkvold et al. 1997b). Which
infection pathway is more important depends on the Fusarium
spp. that is predominant and insect pressures in a given
geographical location. In some locations, ear rot outbreaks are
mainly associated with infection through the silk while in other
locations where maize boring insects are a problem and are not
controlled by other measures, infection through the kernels is
predominant.

´ . M e s t e r h a´ z y , M . L e m m e n s and L . M . R e i d
A

Gibberella ear rot
The symptoms of GER, caused mainly by F. graminearum, are
characterized by a pinkish coloured mould (White 1999). Similar

symptoms are found with F. culmorum infections; this species is
a pathogen also associated with GER, but it lacks a Gibberella
teleomorph. Infection of the ear commonly begins as white
mycelium moving down from the ear tip. This mycelium later
turns reddish-pink on infected kernels. In some cases, pinkish
fungal growth can be found on the exterior husk leaves, and in
severe infections, it is impossible to separate the husks from the
kernels as the entire ear becomes a tightly bound mass of fungal
and plant tissue that appears ÔmummiﬁedÕ. If infection occurred
through kernel wounds, similar fungal growth is seen but it starts
from the initial wound site and tends to spread to the tip of the
ear faster than to the butt of the ear. The latter occurs because
silks from the butt kernels emerge from the ear earlier than
kernels from the tip of the ear and are hence pollinated earlier
and dry earlier (Reid and Sinha 1998) Once the kernels reach 22–
23% moisture, it is diﬃcult for the fungus to further infect
(Christensen and Kaufmann 1969); however cob (rachis) moisture can be 15–25% higher than kernel moisture, so the infection
may spread in the cobs and can enter younger kernels via the
pedicel. In some cases, only the cob is infected; the ear may
appear to be symptomless but when squeezed by hand, it will be
quite spongy feeling and the cob will be wet and often pink/red in
colour. How fast symptoms develop in a given year is highly
dependent on the environment that inﬂuences not only ear
development and subsequent kernel drydown but also fungal
growth. The optimum temperature for GER development is 26–
28°C, while FER rot has broader range extending to higher
temperatures (Reid et al. 1999). GER also requires a much
longer period of precipitation after infection usually around the
time of plant (Reid et al. 1996a). Infection through the silks
cannot proceed once the silks have dried out (Reid et al. 1992a,

Reid and Sinha 1998). Recently, Xiang et al. (2010a) reported
that there is a direct relationship between kernel drydown rates
of a given maize genotype and the extent of ear rot severity
symptoms. Husk tightness (Koehler 1959), ear declination and
physiological resistance mechanisms all inﬂuence the spread of
infection. Stalk rot and ear rot are strongly interrelated
(Mesterha´zy 1983, Mesterha´zy and Kova´cs 1988, Mesterha´zy
et al. 2000) as stalk rot interrupts the water supply to the ears
and speeds up development and drying of the ear. This can
reduce ear rot by 50% or more. Thus, it is important that in ear
rot breeding nurseries, like all disease nurseries, the plants be as
healthy as possible prior to ear rot inoculation; stalk rot should
be controlled and only ear rot data on healthy stalks should be
accepted to estimate resistance levels (Mesterha´zy 1979, Kova´cs
et al. 1994).
Fusarium ear rot
In contrast to GER, symptoms of FER from F. verticillioides
infection occur mainly on individual kernels or on limited
areas of the ear (White 1999). In some ears, many independent
infection sites may develop. Infected kernels develop a cottony
growth or may develop white streaks on the pericarp and
fungal growth on the cob. Ears infested by earworms are
usually infected with F. verticillioides. Eller et al. (2008a) state
that the disease is prevalent in warm, dry conditions, like those
common to the southern United States, and F. verticillioides is
found in grain or crop residue of virtually all mature maize

Breeding for resistance to ear rots

ﬁelds in the United States. However, F. proliferatum and
F. subglutinans are also minor causal agents of FER, as are
probably other members of the Liseola Section of Fusaria.
(Iglesias et al. 2010). Reid et al. (1996a) adds that rainy
weather or irrigation at silking thereafter signiﬁcantly increases
disease severity for FER and especially for GER. Duncan and
Howard (2010) studied the initial phases of the infection
process by F. verticillioides and described in detail how the
hyphae spread and colonize host cells and how the macroscopic symptoms develop. In many cases, the extent of toxin
contamination is proportional to the visual severity of infection; however, asymptomatic kernels may also be infected and
may contain toxins, usually trace amounts (Reid et al. 2009).
Bacon and Hinton (1996) reported on the endophytic colonization of maize plants by F. moniliforme (F. verticillioides) and
presumed that this can contribute to toxin contamination of
the plants. Murillo-Williams and Munkvold (2008) reported
that systemic infections from the stalk to the ear leading to
more asymptomatic infections and toxin accumulation may be
a problem predominantly in hot regions but not in the cooler
areas. As global warming seems to be durable, this problem
may become more serious in the currently cooler regions like
central Europe and Canada.
Other ear rots
For the remaining Fusarium spp., a clear demonstration of the
signiﬁcance of a given species, its symptoms and epidemiological conditions is poorly documented. White (1999) does not
even mention them. Their toxins, however, play a signiﬁcant
role; thus, their neglect is by no means justiﬁed. For example,
T-2 toxin is produced by Fusarium sporotrichioides (Table 1)
and others. As we have only FER and GER to describe these
ear rots, a new term should be found for ear rots caused by
other Fusarium spp. Perhaps, they can be grouped under the
term ÔOther Fusarium Ear RotÕ (OFER). It is unpractical to

assign a new term to each of the species unless it is found that
the incidence of a given species increases because of environmental or agronomic changes.
Reid et al. (1996a, 1999) stress that the two main Fusarium
spp. may produce mixed infections. Some species will dominate in a ﬁeld (Table 1) because of environmental conditions,
but natural infection is almost always mixed. This makes
breeding for resistance complicated as minor species should
also be considered. Visual identiﬁcation of a pathogen is often
not possible: with mixed infections, atypical symptoms can
occur. In inoculated trials, the breeder is determining which
species is the predominant one; in trials where multiple species
are inoculated at the same time, the environmental conditions
after inoculation determine which species will predominate
(Reid et al. 2001a,b). When natural infections are evaluated,
general ear rot values based on visual symptoms are given
without species identiﬁcation. Most breeders follow this
procedure, and Variety Oﬃces like that in Hungary similarly
report disease severity (percentage or rating of diseased area
on the ear) and incidence (percentage of the number of visually
infected ears) because of Fusarium spp. without species
identiﬁcation (Gergely et al. 2010).
Seedling blight
A greenhouse method was evaluated to check seedling stage
resistance (Mesterha´zy 1982). Commercial garden perlite (a

5

very light-heated volcanic stone) is used, and this makes
possible the washing of the whole plant and checking of plant
damage and root rot more precisely. The method is used also
for testing seed dresser against Fusarium seedling blight

(Mesterha´zy 1982).
Evaluation of disease
Disease incidence is measured as the number or percentage of
visually infected ears. Disease severity is often rated visually on
scales ranging from 1 to 5, 1 to 7 and 0 to 9 or as percentage of
the ear surface with symptomatic kernels. For breeding
purposes, the rating scales are commonly used, but for
scientiﬁc studies the percentage of infected kernels may give
more precise data. In addition to disease incidence and
severity, it is important to assess other natural infections
(e.g. Aspergillus) as well as the occurrence of insect, bird, wind
or hail damage on the ear because all of these factors will
inﬂuence infection levels. As wounds are often points of fungal
entry, extensive damage may inﬂuence resistance measurements. In silk resistance evaluations, only ears without insect
or other wound-mediated infection should be considered for
evaluation and toxin analyses.
Reid and Sinha (1998) found that visual symptoms of GER
stabilized and reached a maximum 6–8 weeks after inoculation
of the silk channels. The rate of fungal spread after inoculation
is quite variable and highly related to genotypic resistance.
Mesterha´zy et al. (2000) measured a fungal spread of 0.1–0.3%
of the ear surface per day in highly resistant genotypes
compared to 2–3% per day for the most susceptible genotypes
measured after inoculation and until kernel moisture reached
28%. Similar to GER, working with FER Bush et al. (2004)
found that fumonisin content is at a maximum at 20% kernel
moisture and cannot be detected earlier than 35–40% moisture
content. All of these studies indicate that for both GER and
FER, symptoms reach a maximum 7 weeks after pollination
and that toxin levels reach a maximum at 9 weeks. The later is

therefore an optimum harvest time for ear rot evaluations;
however, it should be noted that a wet fall and/or wet
conditions in the grain after harvest can lead to more toxin
development.
Considerable debate exists whether or not toxin evaluations
should also be used to evaluate disease resistance. Without a
doubt, the level of mycotoxins is an extremely important trait
to record; however, mycotoxin analyses can be cost-prohibitive
in some breeding programmes. Many breeders rely on visual
ratings of disease severity for most of the inbred development
and use toxin analysis for parent selection, testcross evaluation
and the ﬁnal developmental stages of inbreds and hybrids. It
must be recognized that although there are published reports
on high correlations between disease symptoms and toxin
levels (Reid et al. 1996b) for F. graminearum, it seems to be
necessary for F. verticillioides where signiﬁcant diﬀerences in
amount of toxins can be detected at the same visual severity
rating (Butron et al. 2006). In their review relating to the
prediction of mycotoxins in food, Garcia et al. (2009) state
that not all fungal growth results in mycotoxin formation and
the detection of mycotoxic fungi may or may not imply the
presence of mycotoxins. Strains of mycotoxigenic species are
able to synthesize mycotoxins in diﬀerent amounts, and
conditions conducive to fungal growth may not be conducive
to mycotoxin production. For this reason, special attention
must be paid to the relationship between visual symptoms and

6

the level of toxin contamination, the NIRS may provide a
cheap and eﬃcient way to check toxin content.

Resistance Components and Artiﬁcial Inoculation
As the severity of natural infection is not consistent from year
to year, maize researchers must use artiﬁcial inoculation
methods to inoculate the plant material with fungal spores
(Schaafsma et al. 1997). Currently, the only way to screen for
resistance to GER is in the ﬁeld. Satisfactory levels of infection
and reliable genotypic diﬀerentiation have not been achieved
under greenhouse conditions, and there is no laboratory
technique or seedling test that can be used to screen for
resistance that is exhibited in a fully grown plant (Reid et al.
1996a).
At present, the literature highlights the silk channel method
of inoculation rather than the kernel wound inoculation by
colonized toothpicks or injection of a fungal spore suspension.
Both techniques result in the spread of infection from infected
kernels to neighbouring kernels; however, with the silk channel
inoculation, the infection must ﬁrst proceed down the silks to
the kernels. Whichever technique is used, the research is
cautioned to ﬁrst determine the major mode of fungal entry for
the Fusarium spp. of interest in a given geographical area. The
methods used for artiﬁcial inoculation and the evaluation of
resistance are similar for both GER and FER as well as other
Fusarium spp. Researchers working with two or more Fusarium spp. used the same methodology for all (Reid et al. 2002,
2009, Loăer et al. 2010a).
Methods of inoculation
A number of artiﬁcial inoculation methods and their variants
have been developed. They were ﬁrst assessed by Ullstrup

(1970). The oldest is the toothpick method of Young (1943).
Working with this method, several improvements were made
(Mesterha´zy 1982, 1983). The toothpicks are boiled in deionized water three times to wash out tannins and other fungal
growth–inhibiting compounds from the wood. Thereafter, they
are air-dried and submerged into a suitable liquid medium (e.g.
Czapek-Dox) for 1 h in an Erlenmeyer ﬂask. Most of the
medium is then removed leaving only 5–10 mm depth of media
in the ﬂask to ensure high humidity; the ﬂask is then
autoclaved for 1 h at 120°C. A small amount of mycelium is
transferred to the sterilized ﬂask, and after 3 weeks the fungus
grows through the toothpicks that are now ready to use
(Mesterha´zy 1982, 1983). The toothpicks are generally used for
the inoculation of ears in two ways: insertion into the centre of
the ear or into the silk channel representing kernel resistance or
silk channel (silk) resistance, respectively (Reid et al. 1996a,
Plienegger and Lemmens 2002). After 7–9 weeks, disease
severity is estimated by the percentage of visually infected
kernels directly or by using a rating scale as discussed earlier
(Mesterha´zy 1978, Enerson and Hunter 1980, Reid et al.
1996a). One of the disadvantages of this technique for silk
channel resistance evaluation is with maize genotypes where
the cob outgrows the husk leaves, causing the toothpick to fall
out thus reducing infection severity. Another criticism of the
toothpick technique is that infection levels can be too high
because of the fact that the toothpick itself is a substrate for
fungal growth and kernel inoculations result in severe
wounding of several kernels and the cob (rachis).

´ . M e s t e r h a´ z y , M . L e m m e n s and L . M . R e i d
A

It is important to choose an inoculation technique that
results in a suﬃcient level of infection to diﬀerentiate genotypic
diﬀerences in resistance but not so severe of an inoculation
that these diﬀerences are hard to observe. It is rare that natural
inoculations are as severe as artiﬁcial inoculations. As a
consequence, several other methods of inoculation have been
developed since the toothpick technique; however, it should be
noted that for some researchers, the toothpick technique is
necessary to achieve the best genotypic diﬀerentiation. Many
researchers produce Fusarium suspensions in liquid media with
or without aeration with sterile air, or the Fusarium conidia
are washed from solid media poured into Petri dishes. The
production methods are very variable (Mesterha´zy 1978, Reid
et al. 1996a, Plienegger and Lemmens 2002). Mesterha´zy
(1983) used the bubble breeding method that allowed the
facile production of large quantities. If a researcher desires to
inoculate with a mix of isolates or species, to avoid competition in the media, the isolates/species are grown separately
and then just prior to inoculation mixed (Reid et al. 1996a,
Presello et al. 2006). Loăer et al. (2010a) used this method,
but the isolates were not mixed to avoid isolate x isolate
interactions. Conidia have been shown to be as good infection
materials as mycelium (Takegami and Sasai 1970) and in fact,
in natural infections, conidia are often the source of infection.
The developed conidial suspension can be used in diﬀerent
ways (Papst et al. 2007): the silks can be sprayed with the
suspension, or the cob tip can be immersed into the suspension. The resistance type observed after this type of inoculation
is termed silk resistance. After spraying, the silks can be
covered with polyethylene bags to achieve higher humidity and
consequently higher disease severity. However, the toothpick

method gave more than double level of GER and FER severity
than these methods (A´. Mesterha´zy and E. Toldi, unpublished)
and covering the ear with a polyethylene bag also serves to
increase the development of other fungi and bacteria, which
may complicate resistance evaluations (L. M. Reid, unpublished). A more common use of the suspension is to inject it
into the silk channel (silk channel resistance) or the centre of
the ear (kernel resistance) using syringes or vaccinators (Reid
et al. 1996a). The amount of inoculum injected can vary from
several ll to 5 ml, with the larger volumes used for silk or silk
channel resistance. Reid et al. (1996a, 2009) and Presello et al.
(2008), for example, used 2 ml. Loăer et al. (2010a) utilized
only 1 ml. The conidium concentration varies: Presello et al.
(2008) and Loăer et al. (2010a) used 1 Ã 106 conidia/ml for
FER, while Loăer et al. (2010a) used 1 · 105 for GER.
Clements et al. (2003) compared several inoculation methods
for FER: injection of inoculum through the ear husk leaves at
the R2 developmental stage; spray inoculation with diﬀerent
variants (coverage of silks with shoot bags, and re-inoculation
after 1 week), and insertion of six Fusarium-colonized toothpicks into the silk channel. Only the injection through the husk
leaves signiﬁcantly increased fumonisin concentration and
infection severity. Eller et al. (2008a) developed a methodology
to identify resistance against F. verticillioides and identiﬁed
superior genotypes. They preferred silk inoculation, which
appears to be more important for the entrance of F. verticillioides. Furthermore, they compared four inoculation methods
and found that the highest infection severity and largest
genotypic diﬀerentiation were found when inoculum was
inserted through the husks. Bush et al. (2004) compared ﬁve
inoculation methods and concluded the most useful to be

Breeding for resistance to ear rots

penetrating husks with pin bars and injecting inoculum down
the silk channel.
Comparatively few data are available on the relationship
between kernel and silk channel resistance. Lemmens (1999,
2010) found low correlation (r = 0.12), whereas Loăer et al.
(2010a) reported a much closer relationship (rP = 0.66) for a
wider genetic stock. Chungu et al. (1996b) also found a
correlation between the two traits (r = 0.77–0.89). Few
genotypes exist with good resistance to both modes of fungal
entry (Reid et al. 2003). The relationship between silk vs.
kernel resistance is very important as two parallel methodologies would be cost-prohibitive in a breeding programme.
Loăer et al. 2010b has reported signiﬁcant genotypic variances for kernel and silk channel resistance. The correlations
between silk and kernel resistance were moderate (r = 0.66),
but there were genotypes with very diﬀerent resistance level
with both methods. Therefore, authors suggest the use of both
inoculation methods. There are arguments on the use of both
inoculation techniques and on the number of isolates to be
used, including whether to use a pure or mixed conidial
suspension. The breeder is cautioned to carefully determine
which mode of fungal entry is predominant at their research
station and how heterogeneous is the Fusarium population at
the station before making decisions on inoculation methods. In
addition, the genotypic resistance that the breeder initially has
to work with will inﬂuence this decision as sources of resistance
to one mode of fungal entry may not be available in adapted
material. For example, Presello et al. (2005) found kernel
resistance for FER useful, but the sources for this resistance
are very limited compared to sources for silk resistance. On the

other hand, the breeders need the assistance of the research to
answer better the questions they have.
Timing of inoculation
In a summary report, Jugenheimer (1976) cited Andrew (1954),
who initiated GER by placing infected barley grains under the
husk leaves 5–10 days after silking, that is, a very early form of
silk channel inoculation, and further applied by spraying silks
at silking to promote FER. In both cases, symptoms appeared
after 1 month. This study can possibly be considered the ﬁrst
of many silk resistance tests. Since that time, many other
researchers have performed silk and kernel inoculations at
various stages of ear development. For GER, Papst et al.
(2007) sprayed the silks 4–7 days after mid-silking and applied
inoculum with wounding (toothpicks) 10–15 days after midsilking. For kernel resistance, later inoculation times result in a
general decrease in disease severity for all species; though, it
was not as strong as that reported with silk inoculations (Reid
and Hamilton 1996, Reid et al. 2002). The best diﬀerentiation
of genotypes was achieved when the kernel inoculation was
performed 15 days after mid-silking (Reid and Hamilton 1996,
Reid et al. 2002). Silva et al. (2007) used 14 days in regular
tests; later inoculations (19, 21 and 23 days after mid-silking)
resulted in signiﬁcantly less disease severity. Reid et al. (1996a)
used 2 ml of suspension inoculated 4–6 days after mid-silking
for both GER and FER; earlier inoculations (2–3 days after
mid-silking) led to very high infection severities, and later
inoculations (10 days or more) resulted in little or no infection
(Reid et al. 1992a, 2002). Schaafsma et al. (1997) concluded
that the beginning of silk browning is the ideal time for the silk
channel inoculation. They found irrigation useful for the initial
stages of infection for both inoculation methods; this supports

7

the data of Reid et al. (1996a). Silva et al. (2007) compared
diﬀerent inoculation methods. Robertson et al. (2006) and
Eller et al. (2008a) used silk and direct ear inoculations at
10 days after mid-silking and 7 days later, respectively. Both
methods gave replicable results for several superior lines.
Disease levels between cultivars ranged from 20 to 50%.
Interestingly, inoculation of the husk leaves resulted in
signiﬁcantly more severe infection of the grains.
Miller et al. (2007) found that silk-mediated F. graminearum
infection reached the kernels in 7–9 days in susceptible
genotypes, and 12–15 days in more resistant genotypes. These
diﬀerences are of great importance in our goal of understanding disease severity and consequently resistance diﬀerences.
This explains the roughly 1 week diﬀerence in timing of
inoculation between the two inoculation methods. Adding
1 week to the 5–7 days postsilking of the silk channel
inoculations, we achieve the optimum time for inoculating
the kernels at the same stage in which the fungus growing
down the silk would reach the kernels.
It should be mentioned that there are diﬀerences in the
optimum timing of inoculation depending on the level of
resistance. For early-maturing genotypes, the kernel development is more rapid than it is in later-maturing genotypes.
Thus, a 10-day delay after mid-silking for kernel inoculations
may be too late for some early genotypes. In large-scale
breeding or screening programmes, the researcher should not
rely just on chronological time for determining inoculation
time; genotype maturity and growth stage must be taken into
consideration as well as the eﬀect of the environment in

inﬂuencing growth and development of the ear. Control
genotypes with known resistance levels in diﬀerent maturity
groups can be used to monitor this in large screenings such as a
mapping population with very diverse silking and maturity
rates.

Natural vs. Artiﬁcial Inoculation of Maize Ears
Disease severity after natural infection varies strongly from
year to year, from location to location and with the length of
the vegetation period; earlier hybrids normally show less ear
rot infection and less toxin contamination (Papst et al. 2007).
Late-sown or later hybrids tend to be more infected by
F. graminearum and contaminated by DON than early ones
(Manninger 1978, Blandino et al. 2009a). Good agronomy
practices can also decrease the risk of fumonisin contamination (Blandino et al. 2009b). Weather conditions aﬀect diﬀerent Fusarium spp. in diﬀerent ways (Reid et al. 1999), and the
types and levels of physiological resistance strongly inﬂuence
the severity observed. The many Fusarium spp. that are present
in the ﬁelds cannot be controlled, and this complicates the
comparison of natural and articial inoculation results (Loăer
et al. 2010b). Ear tips that are fully covered by the husk leaves
tend to be subject to more infection than those with early cob
outgrowth as the humid period is longer in the former case
(Butron et al. 2006). The optimum time for natural infection to
occur is similar to that for artiﬁcial inoculation, about 10–
14 days after silking after which the infection severity sharply
decreases. Natural infection is moderate to low in most years,
and it is absent in some years and does not allow an eﬃcient
selection of genotypes with high resistance. These restrictions
also explain the high ratio of susceptible inbreds and
commercial hybrids bred under natural infection pressure. In

2010, an unusual strong epidemic caused by diﬀerent FERs

´ . M e s t e r h a´ z y , M . L e m m e n s and L . M . R e i d
A

8

was observed in Hungary. Disease incidence vas very high, and
severity was on average 20%. No genotype could be rated as
resistant; rather, diﬀerences in susceptibility could be observed.
In the most severely infected location, the incidence was
between 28 and 87%, and the severity was between 8.5 and
29.4%. Most of the hybrids were susceptible or very susceptible, indicating the need for a more successful breeding against
ear rots (Anonymous 2010).
Artiﬁcial inoculation methods have several advantages over
relying on natural infection to create an outbreak of ear rot.
The Fusarium spp. isolate, inoculation times and mode of
entrance/infection pathway are known. The disease severity is
normally much higher and results in more uniform ratings that
make genotypic comparisons easier and reproducible especially when phenotyping for QTLs. Genotype diﬀerences are
normally much larger for artiﬁcial inoculation regimes than for
natural ones (Oberforster and Felder 2010). Silva et al. (2007)
compared natural and artiﬁcial inoculation results and concluded that when only the husks were wounded, the sterile
water control resulted in higher disease severity than the
natural control. As the ranking order of the cultivars after
wounding only and after inoculation did not seem to diﬀer
from that of the natural control, it was suggested to wounding
only and to allow natural infection to proceed through the
wounds in areas with high inoculum pressures as that found in

the Andes where the study was conducted. Geographical areas
such as these with reliable levels of natural infection are rare,
especially in most maize-growing regions of the world.
In spite of all the concerns, both artiﬁcial and natural
infections are of great signiﬁcance. The genotypes selected
under artiﬁcial infection pressure must demonstrate their
superior resistance under natural infection pressures. For this
reason, research that clariﬁes the relationships between artiﬁcial and natural infection results is of high priority. Lemmens
(2010) observed a close correlation between the results of the
silk channel method and natural infection (r = 0.75–0.96). In
2004, 2005 and 2006, Palaversˇ ic´ et al. (2010) found medium to
close (r = 0.66, 0.61, 0.84) correlations between the silk
channel and natural infection severity data. The data support
the view that artiﬁcial and natural infection data tend to be
closely correlated. This could mean that some form of complex
resistance to diﬀerent Fusarium spp. exists. The data suggest
that this hypothesis may hold true.
Some maize breeders oppose the use of artiﬁcial inoculation
methods. The reasons listed include the opinions that the
natural infection severity is suﬃcient for eﬃcient selection and
that wounding at inoculation is far from the natural mode of
infection and introduces instability in the system. However, in
tests on commercial hybrids, these views cannot be fully
justiﬁed as many hybrids from these programmes display
considerable susceptibility. The eﬀect of wounding seems to be
overemphasized. In susceptible genotypes, the infection
spreads rapidly to the unwounded, healthy kernels, whereas
in resistant genotypes, the spread is very limited or does not
occur at all. Some companies in many countries facing the
food and feed safety problems have started intensive selection

work with artiﬁcial inoculation methods.

Inheritance, Genotypic Diﬀerences and Sources of
Resistance
Boling and Grogan (1965) estimated several additive, dominant and additive x dominant digenic epistatic gene eﬀects.

They estimated an average dominance of approximately 0.5,
and the number of participating genes was estimated at 1.47, a
relatively low number. Hart et al. (1984) reported that GER
resistance is governed by genetic factors. Symptomatic and
asymptomatic kernel infections have been studied in sweet
corn hybrids between inbreds with diﬀerent susceptibility levels
(Nankam and Pataky 1996); a broad range of heritabilities for
the two symptom groups were recorded, and resistance was
determined to be controlled by several genes. In two maize
populations, Robertson et al. (2006) found genotypic and
phenotypic correlations between fumonisin and FER data of
0.96 and 0.40, and 0.86 and 0.64, respectively; heritability
estimates for fumonisin were 0.75 and 0.86, and for ear rot
resistance, 0.88 and 0.47, respectively. These high genetic
correlations suggested that it is highly possible to reduce
fumonisin contamination indirectly by increasing FER resistance levels. Using a silk channel inoculation method, Headrick and Pataky (1991) observed a signiﬁcant maternal eﬀect
on hybrid performance. Eller et al. (2008a) concluded that the
US hybrid maize crop was based on crosses between
proprietary inbred lines, and many of them were developed
from older, publicly developed inbreds representing a rather
narrow gene pool. As the resistance level is seemingly
unsatisfactory, they suggested a search for germplasms with
higher resistance not closely related to this group.
Natural ear rot

There are many surveys for natural infection; in Europe,
several Variety Oﬃces regularly use the data for decisionmaking (Hertelendy et al. 2010, Oberforster and Felder 2010,
Palaversˇ ic´ et al. 2010, Pastircˇa´k et al. 2010). In most years, the
infection severities are low. In Hungary in 2010, the strongest
epidemic was recorded for at least 20 years: the severity of
maize ear rot across eight sites (the best-yielding hybrids were
tested from many leading companies) was 35% with hybrid
reactions ranging between 27 and 48%, the severity (coverage)
by ear rot was 10.2% (range, 7–14%). The most infected site
had an average disease incidence of 63% (range, 28–87%) and
mean severity of 20% (range, 8–29%). This underlines two
facts: (i) we cannot be satisﬁed with the results of breeding
under natural infection regimes and (ii) a signiﬁcant improvement in hybrid resistance is necessary. Similar outbreaks occur
in other countries, and when this happens the result is high
levels of localized disease incidence and severity.
Gibberella ear rot
The inheritance of resistance to Fusarium spp. is complex. Reid
et al. (1992b) carried out a complete diallel analysis with 12
inbreds representing highly resistant to highly susceptible
selected from a screening of 37 inbreds after silk channel
inoculation. Both general (GCA) and speciﬁc combining
ability (SCA) were signiﬁcant. The GCA values were correlated to disease severity data; however, the performance of the
hybrids could not be predicted based on the GCA of the
parents. Four inbreds exhibited signiﬁcant GCA for resistance
to F. graminearum. Chungu et al. (1996a) tested the inheritance of kernel resistance by injecting a small amount of liquid
inoculum into the centre of the ears. Generation mean analysis
indicated that resistance to F. graminearum was under both
simple (additive and dominance) and digenic (dominance x
dominance) eﬀects. Estimates of the number of factors

Breeding for resistance to ear rots

aﬀecting kernel resistance ranged from 4.6 to 13.7. Lemmens
(1999) described a similar phenomenon – maize hybrids seem
to possess diﬀerent resistance levels as regards kernel and silk
channel resistance. In some hybrids, Kova´cs et al. (1994)
found maternal eﬀects, and in others, a paternal eﬀect; kernel
resistance to F. graminearum and F. culmorum in hybrids
could be predicted only when both parents were solidly
resistant.
Inbreds A632 and WP9 and their relatives exhibited GER
resistance that was far above the average (Kova´cs et al. 1994).
Reid et al. (2000) observed resistance diﬀerences in sweet
maize F. graminearum after silk channel inoculation, but the
diﬀerences were relatively small and overall all genotypes were
quite susceptible. In this study, DON levels increased rapidly
such that by 2 weeks after silking concentrations were above
1 mg/kg. Reid et al. (2001a,b, 2003) have released eight maize
inbreds (CO387, CO388, CO389, CO430, CO431, CO432,
CO433, CO441) speciﬁcally bred for increased resistance to
GER using both silk channel and kernel inoculation techniques. The latest release, CO441, has the highest published
inbred resistance and possesses both silk and kernel resistance
as well as acceptable grain yields when tested in combining
ability trials (Reid et al. 2003). This it is feasible to develop
resistant inbreds and high-yielding hybrids, thus breaking the
Ôresistance-yieldÕ barrier so often found when breeding for
disease resistance. Inbreds developed with selection for GER
also exhibited high levels of resistance to FER and common
smut (Ustilago zeae) in inoculated trials (Reid et al. 2009),

indicating that it may be possible to develop hybrids with
resistance to multiple Fusarium spp. Schaafsma et al. (1997)
tested 61 commercial hybrids for GER by silk channel and
kernel inoculation methods and concluded that only two
ranked highly resistant with both inoculation methods. de
Oliveira et al. (2009) found some resistant sources among
landraces with higher grain hardiness. Mesterha´zy (1978, 1982,
1983) and Mesterha´zy et al. (2000) tested maize hybrids
against four isolates (two F. graminearum and two F. culmorum) with the toothpick method. The severity data on
F. graminearum and F. culmorum correlated very closely, but
the correlations with the less-pathogenic F. verticillioides and
F. avenaceum were not convincing.
Research was initiated to ﬁnd an indirect way for selecting
to ear rot resistance. However, resistance to ear rot, stalk rot
and seedling blight did not correlate, indicating that a
preliminary selection at the seedling stage will not automatically result in higher ear or stalk rot resistance (Mesterha´zy
1982). The data clearly showed (Mesterha´zy and Kova´cs 1988)
that although the traits do not interrelate genetically, they may
inﬂuence each other physiologically.
In most maize-growing regions, with the exception of
developing countries, commercial varieties are hybrids; thus,
it is critical that inbreds developed for improved GER carry
this resistance into the hybrid. Kova´cs et al. (1994) tested 18
hybrids with their respective inbred parents for GER. The
mean for the maternal lines on scale 0–10 was 1.23, and that
for the paternal lines was 2.40. Their calculated mean was 1.82,
but the actual value was 1.08. This means that the hybrids had
41% less ear rot than the calculated mean. In six cases (33%),
the hybrid was more resistant than the more resistant parental
line. These data indicate that selection for resistant inbreds will

result in resistant hybrids. Correlation between mother and
hybrid performance was r = 0.65 (P = 0.01), and between
father and hybrid performance, r = 0.85 (P = 0.001),

9

indicating a stronger father inﬂuence. Recently, researchers
in Germany conducted more formal studies to compare the
relationship between inbred line resistance and toxin
contamination (Bolduan et al. 2010, Loăer et al. 2010b). It
was concluded that eﬀective line selection is possible, and toxin
contamination follows closely the severity (rg = 0.88 between
GER and FER, and rg = 0.77 for DON and FUM), indicating that the resistance to the diﬀerent pathogens seems to be
closely related. Toxin contamination is proportional to symptom severity when inoculation is performed with the same
isolate. It seems that both proper line and testcross evaluations
for ear rot resistance are equally important.
Some researchers have sought relations between seedling
blight, ear rot and stalk rot (Mesterha´zy and Kova´cs 1988,
Reid et al. 1996a), but failed to demonstrate any. Direct
measurement of the resistance in the given organ is therefore
necessary.
It is not clear what the mechanism of resistance to GER is in
the resistant maize genotypes. Changes in silk ﬂavone content
and resistance to GER have been reported (Reid et al.
1992a,b). Assabgui et al. (1993) found a correlation of
r = 0.70 between the (E)-ferulic acid content and resistance
to F. graminearum. Bily et al. (2003) identiﬁed dehydrodimers
of ferulic acid as a resistance component to F. graminearum ear
rot. 4-Acetylbenzoxazolin-2-one (4-ABOA) was also reported
to lead to a higher resistance level to GER (Miller et al. (1997).

Recently, Cao et al. (2011) researched the role of hydoxycinnamic acids in resistance to GER and concluded that several
changes in cell wall-bound compounds of silk tissues were
observed after inoculation. Further studies are required in this
research area.
Fusarium ear rot
Pascale et al. (2002) tested the resistance of 29 hybrids against
F. verticillioides and F. proliferatum. The hybrid ÔMonaÕ was
the most resistant. For fumonisin B1 + B2, Mona contained
an average of 1.9 mg/kg for the 3 years, whereas a more
susceptible hybrid Milpa had levels that reached 108 mg/kg.
Fusarium proliferatum was more pathogenic, resulting in
higher disease severities and smaller diﬀerences between the
hybrids. Mona had a total fumonisin content of about 70 mg/
kg, while that of Milpa was about 50% less. Visibly infected
grains had a high toxin concentration, indicating that separation of these grains from less-infected grain could signiﬁcantly
decrease the level of contamination. Presello et al. (2008)
detected signiﬁcant hybrid diﬀerences using silk channel
inoculations with one isolate of F. verticillioides; the more
susceptible hybrids also had higher natural infection levels.
However, in symptomless grains, fumonisin could be measured
in quantities exceeding the recommended limits. Diseased
grains may be smaller, resulting yield losses up to 58%
(Jovicevic and Sultan 1979, Warﬁeld and Davis 1996) although
F. verticillioides is thought to have no or only minimal impact
on the yield. Sweet corn is generally considered to be a
susceptible crop. Du Toit and Pataky (1999) observed highly
signiﬁcant resistance diﬀerences, but none of the hybrids was
highly resistant. The silk channel injection method led to
higher variation and was more laborious as compared with the
toothpick method. Schjoth et al. (2008) found very good

diﬀerences in resistance when medium disease pressure was
applied, but these diﬀerences were less apparent when high
pressure was applied. Clements et al. (2004) screened 1589

10

inbreds and a B73-type inbred for resistance to FER. On the
basis of the fumonisin concentration, only 11 inbreds (A188,
A682, B8, B66, C127, CK31, CM5, CQ201, H117, M14 and
ND211) were superior and stable in the two trials conducted.
Pericarp thickness has been considered to play a role in FER
resistance. The results of Ivic et al. (2008) clearly showed that
no correlation between pericarp thickness and resistance exists
in Croatian genotypes, so that breeding for this trait would not
increase resistance. In contrast, Sampietro et al. (2009) identiﬁed various properties of the pericarp and its wax layer as
resistance factors to F. verticillioides. These traits were consistent over 2 years under very diﬀering ecological conditions.
When the wax was removed, infection severity increased
signiﬁcantly. Waxy hybrids exhibit a higher average contamination of fumonisins (+440% in 2000 and +234% in 2001)
than normal hybrids (Blandino and Reyneri 2007). Hoenisch
and Davis (1994) observed a correlation between higher
pericarp thickness and resistance. They considered that the
thicker pericarp inhibits the fungus and may also act as a
barrier to insect feeding. These studies may explain why sweet
corn is so susceptible to both GER and FER; sweet corn
varieties, a food crop, are intentionally bred to have thinner
pericarps to improve texture upon eating. Long-chain alkanes
on the surface of maize silks have also been implicated in
resistance to GER (Miller et al. 2003).
The An2 gene encodes an ent-copalyl synthase gene that has

a role in gibberellin synthesis. This gene was strongly upregulated after Fusarium infection of the silk (Harris et al. 2005).
It was postulated that the gene might play a role in silk
resistance. Haptoglobin-related protein (HRP) (Harris et al.
2005) genes have also been reported to play a potential role in
resistance. Several ﬂavonoids have been identiﬁed that have a
possible role in resistance (Sekhon et al. 2006). Choi and Xu
(2010) reported the cAMP signalizing pathway in F. verticillioides, which is important for conidiation and infection, may
play a role in the infection process.
Farrar and Davis (1991) and Parsons and Munkvold
(2010b) detected diﬀerent thrips species on ears that increased
the severity of FER infection. Husk looseness correlated with
FER at the brown silk stage and also with the size of the thrips
population. It was concluded that husk tightness plays an
important part in epidemiology and disease development. Eller
et al. (2008b) reported that the kernel moisture content
inﬂuences the degree of ear rot. This concurs with studies on
stalk rot causing pathological drydown and thus inﬂuencing
GER (Mesterha´zy 1983) as well as FER. Eller et al. (2008b)
did not ﬁnd a relation between ear rot resistance and yield
performance. This would support the hypothesis that high
resistance and high yield are not mutually exclusive for FER as
well as GER.
Relationships between diﬀerent ear rots
Many researchers work with more than one Fusarium spp. in
their tests. Presello et al. (2004, 2006) found highly signiﬁcant
genotypic diﬀerences to diﬀerent Fusarium spp. Resistance
tests in both Canada and Argentina demonstrated correlations
between F. graminearum and F. verticillioides resistance. Six
populations (mostly being Andean landraces ARZM 01107,
ARZM 07138, ARZM 10041, ARZM 13031, ARZM 16002

and Pora INTA) were identiﬁed that had very high levels of
resistance to both pathogens and could be used as sources of
high and stable resistance. Czembor and Ochodzki (2009)

´ . M e s t e r h a´ z y , M . L e m m e n s and L . M . R e i d
A

found higher ear rot resistance in int genotypes than in dent
ones. Loăer et al. (2010a) reported the opposite experience.
As the tested sets of genotypes were not the same in both
studies, the data are not necessarily contradictory. Loăer et al.
(2010a) observed good phenotypic and genotypic correlations
in the ﬂint and dent groups between F. graminearum and
F. verticillioides. Negative correlations emerged between the
silking date and ear rot severity for both Fusarium spp.
(F. graminearum, rP = )0.28; F. verticillioides, rP = )0.26).
So the lower severities for the later genotypes were conﬁrmed.
In the cited literature, there are several indications that
resistance to F. graminearum and F. culmorum may be closely
related (Mesterha´zy 1982, 1983). As both cause GER, this is
not surprising. For other Fusarium spp., however, the picture is
not clear. In wheat, resistance protects all Fusarium spp. tested
(Mesterha´zy 2002, Mesterha´zy et al. 2005). In maize, this
remains to be clariﬁed.
There is no clear evidence of resistance to speciﬁc toxins
produced by the diﬀerent Fusarium spp.; however, many
studies (Reid et al. 1996a, Pascale et al. 1997, Perkowski
et al. 1997, Reid and Sinha 1998) clearly indicate that
severity of infection is highly correlated to toxin contamination, thus indicating a role of resistance in toxin regulation. Bolduan et al. (2009) found a high correlation between
toxin contamination and the severity of the disease in

response to F. graminearum with r = 0.94. Visual scoring
can therefore be suﬃcient in selection work for GER
resistance. For F. verticillioides, the infection severities are
often signiﬁcantly less and not as highly correlated to toxin
levels (Miedaner et al. 2008); however, it was concluded that
toxin analysis for both GER and FER are not necessary at
all stages of breeding. Loăer et al. (2011) found that the
heritabilities for mycotoxin values were similar or higher
than those found for ear rot data (both F. graminearum and
F. verticillioides).
However, as the close correlation was not characteristic for
all genotypes, they recommended separate testing of F. graminearum and F. verticillioides and corresponding mycotoxins.
Henry et al. (2009) identiﬁed genotypes with good resistance to
both F. verticillioides and Aspergillus ﬂavus. Correlations
between ear rot severities of the two pathogens (r = 0.72)
and between aﬂatoxin and fumonisin concentrations
(r = 0.61) led to the conclusion that good resistance to both
species in the same genotype is attainable. Robertson-Hoyt
et al. (2007b) came to the same conclusion.
It is interesting that the available literature does not
concentrate on sources of resistance, the use of alien species
for this purpose and the selection of inbred lines. Reid et al.
(2009) identiﬁed inbreds with diﬀering silk and kernel resistance types. In their study, silk channel resistance was
investigated using one F. verticillioides and one F. graminearum isolate. It appeared that both additive and non-additive
eﬀects contributed to the resistance, and similarities in reaction
to these pathogens were found. In tests in Szeged in Hungary,
the correlation between the mean ear rot severity and DON
contamination was r = 0.67, and for fumonisin B1-4, a total
r = 0.68 was calculated, both signiﬁcant at P = 0.1% (Toldi
et al. 2008 and not published data). Presello et al. (2011)

described resistance of inbreds selected from F2 populations
and their hybrids inoculated with F. proliferatum. The populations were also inoculated by F. verticillioides and F. graminearum.
Selection
was
similarly
eﬀective
against
F. graminearum and F. verticillioides.

Breeding for resistance to ear rots

Henry et al. (2009) tested 20 inbreds for F. verticillioides and
A. ﬂavus resistance. The ear rot values correlated for the two
pathogens (r = 0.72, at P = 0.0002), as did the aﬂatoxin and
fumonisin concentrations (r = 0.61, P = 0.0004), indicating
that inbreds with aﬂatoxin resistance may be good sources for
breeding for fumonisin resistance. Williams and Windham
(2009) analysed fumonisin accumulation in a diallel analysis
using A. ﬂavus-resistant and A. ﬂavus-susceptible inbreds inoculated with F. verticillioides and A. ﬂavus. The inbreds Mp715
and MP 717 revealed high aﬂatoxin and fumonisin resistance;
however, inbred Mp313E revealed resistance only against
fumonisins, not aﬂatoxin. Farrar and Davis (1991) concluded
that maize genotypes behaved very similarly to A. ﬂavus and
F. moniliforme (syn. F. verticillioides). Their data clearly show
that resistance can be eﬀective to diﬀerent Fusarium spp., but
also against other pathogens from diﬀerent genera, for
example A. ﬂavus. There also appears to be a connection with
common smut caused by Ustilago maydis (Reid et al. 2009).
Eight GER-resistant inbreds were also resistant to Ustilago

maydis. It should be further investigated whether this is caused
by linkage or pleiotropy.
The lesson is clear. The literature indicates that toxin and
ear rot severity data are correlated more often than not for
FER and GER. Artiﬁcial inoculation followed by selection on
the basis of disease severity is suﬃcient during the inbred
selection process. Toxin evaluations should be made with
initial parental selection for new populations, in the ﬁnal stages
of inbred development and in the second and third year of the
oﬃcial registration tests (in countries where this is applicable)
to demonstrate the low toxin-producing capacity of the given
hybrid. The close similarities in resistance to Fusarium,
Gibberella and Aspergillus ear rots that have been described
indicate with high probability that the resistance to these
diseases may be common. However, exceptions have also been
found. It is not known, however, whether the same resistance
genes are responsible for this in a given maize genotype, or
what is the interaction between the environment and diﬀerent
pathogen-speciﬁc genes. This will be an important research
ﬁeld in the future.

Molecular Genetics and QTL Mapping
QTL mapping for GER resistance
In an F5 RIL population, Ali et al. (2005) found 11 QTLs
for ear rot following silk inoculation and 18 QTLs after
kernel inoculation (explaining 6–35% of the phenotypic
variation). However, only two QTLs could be detected that
were active across environments for silk resistance and only
one for kernel resistance, indicating a strong inﬂuence of the
environment. The majority of the favourable alleles came

from the resistant parent CO387. Reinprecht et al. (2008) set
out to identify the genes behind QTLs. About 100 genes
were identiﬁed, among them chitinase and protein kinase
were similar to previous gene-based markers that cosegregated with Fusarium resistance QTLs. Recently, Martin
et al. (2011a,b) identiﬁed co-localized QTL for both GER
resistance and reduced levels of DON in diﬀerent mapping
populations; they suggested that it may now be possible to
conduct marker-assisted selection to improve GER resistance
in the oﬀ-season but that classical phenotypic selection with
ﬁeld inoculations continue to be used during the cropping
season.

11

QTL mapping for Fusarium ear rot resistance
Eller et al. (2008b) established that resistance to FER is
determined by polygenes. Robertson-Hoyt et al. (2006c) tested
two populations for resistance to F. verticillioides. In the FER
population, seven QTLs were identiﬁed, explaining 47% of the
phenotypic variation for FER, and nine were found for
fumonisin content, explaining 67% of the variation. In the
NCB population, ﬁve QTLs explained 31% of the FER
variation and six QTLs with three epistatic interactions
explained 81% of the phenotypic variation. Of the QTLs in
the two populations, three QTLs for FER and two for
fumonisin were mapped in similar positions. Two QTLs,
localized on chromosome 4 and 5, appeared to be consistent in
both populations. Ding et al. (2008) tested a RIL population
of 187 genotypes for F. verticillioides resistance. Phenotyping
was performed in four environments (location–year combinations). Two QTLs on chromosome 3 were identiﬁed with

stability across environments. The major QTL explained 13–
22% of the phenotypic variation for FER. Perez-Brito et al.
(2001) identiﬁed nine and seven QTLs in two populations,
three of which were co-located. Kozhukhova et al. (2007)
found a codominant marker RGA11 on the short arm of
chromosome 1 for FER at 18.3 cM to the resistance locus in
an F2 mapping population. For the SSR locus, the phi001
polymorphic amplicon 180 bp was identiﬁed. R2 or heritability
values were not given.
Relationship of QTL to Fusarium ear rot resistance to other ear
rots and agronomic traits
Robertson-Hoyt et al. (2007a) found that QTLs for F. verticillioides resistance were also eﬀective against A. ﬂavus. The
genotypic correlations between ear rot data of the two
pathogens (rG = 0.99) were very close. On chromosome 5, a
large eﬀect QTL was identiﬁed. The resistance QTLs against
A. ﬂavus and F. verticillioides were occasionally clustered on
the same chromosomes. However, it was considered that a
ﬁne-scale genetic mapping will be necessary to distinguish
linked QTLs, such as those in a resistance cluster from
pleiotropic QTLs that inﬂuence resistance. This supports the
view of common resistance to diﬀerent Fusarium spp. (Robertson-Hoyt et al. 2007b). Robertson-Hoyt et al. (2007b)
mapped two fumonisin QTLs to similar positions as that for
grain yield, but the two QTLs were mapped to distinct
genomic positions. Generally, close relations were not found
between resistance and agronomic traits, and selection for
higher resistance should therefore not unduly aﬀect agronomic
performance. A new attempt is the meta-analysis of QTLs
associated with ear rot resistance (Xiang et al. 2010a,b). The
data of 14 studies representing F. graminearum, F. verticillioides and A. ﬂavus QTL studies were analysed; resistance QTLs
against the three fungi were clustered on the same chromosomes. These data seem to support the idea of common

resistance on QTL level. Of the 87 individual QTLs, 29 metaQTLs were identiﬁed with 2–6 individual QTLs within a
cluster. One resistance source can contribute to diﬀerent
clusters, for example CO387 inﬂuenced 18 of the 29 metaQTLs. At present, it is not clear whether the QTLs in a cluster
are individually eﬀective to all three fungal pathogens or
whether they are specialized to diﬀerent fungal species and the
cluster eﬀect secures the broad sense resistance. We think

12

based on wheat studies; the former is more likely (Mesterha´zy
et al. 2007).
Molecular genetics of Gibberella ear rot and mycotoxin
accumulation
Yuan et al. (2008) found a guanylyl cyclase-like gene (Zmgc1)
that ensures resistance to G. zeae; it is nearly identical to one
resistance gene of the G. zeae-resistant line CO387. Jenczmionka and Schaefer (2005) described Gpmk1 MAP kinase
disruption mutants and concluded that the infection process
depends on the secretion of cell wall-degrading enzymes,
especially during the early infection stages. Igawa et al. (2007)
tested a ZEA-detoxifying enzyme in transgenic plants. It was
expressed in the vegetation period and was also active up to
16 weeks during storage. The problem is that the disease was
not or only moderately inhibited and other toxins may
contaminate maize. Boutigny et al. (2008) surveyed naturally
occurring mechanisms to the reduction of trichothecene toxins.
They identiﬁed Class 1 mechanisms for detoxifying these
toxins. Class 2 comprises mechanisms that result in reduced
mycotoxin accumulation through inhibition of their biosynthesis. Some might work in practice, but their cost will
certainly be considerable.

Molecular genetics of Fusarium ear rot and mycotoxin
accumulation
Alexander et al. (2009) compared the biosyntheses of trichothecenes and fumonisins and concluded that the genes participating in these processes could possibly be used to enhance
resistance to disease and reduce toxin contamination. Lanubile
et al. (2010) found that in a resistant line, the assayed defencerelated genes (b-tubulin 2 and FUM21 genes of F. verticillioides) were transcribed at high levels before infection and
provided basic defence against the fungus. In the susceptible
line, the same genes are qualitatively induced from a basal level
and respond speciﬁcally to pathogen infection. Zhang et al.
(2011) identiﬁed the FvMK1 mitogen-activated protein kinase
gene in F. verticillioides, which regulates conidiation, pathogenesis and also lowers the activity of the FUM1 and FUM8
genes.
Use of QTL mapping in practical breeding
The existence of meta-QTLs does not change the fact that most
of the QTLs found are not validated and have only small
eﬀects (Robertson-Hoyt et al. 2006c, 2007a, Eller et al.
2008a,b). The 19 meta-QTLs (Xiang et al. 2010b) explain
much of the resistance, but the individual QTLs are of small
eﬀect. Only one or two QTLs can be considered to have
medium to large eﬀects (Robertson-Hoyt et al. 2007a). Their
additive (in some cases epistatic) eﬀect seems to be proved.
Therefore, their use for marker-assisted selection is limited at
this time. Further complexity arises from the fact that in some
hybrids, a maternal or paternal eﬀect was dominant. The
hybrid eﬀect can be explained to some extent, but the
resistance level in hybrids cannot be predicted with utmost
certainty. This is similar to the situation in wheat (Buerstmayr
et al. 2009). The results of Wilde et al. (2007) on wheat
indicated that marker-assisted selection resulted in a twofold
higher susceptibility in the progeny than in the phenotypically
selected variant. We consider that a strong selection for

´ . M e s t e r h a´ z y , M . L e m m e n s and L . M . R e i d
A

increased resistance may give novel material for the development of new mapping populations that will allow the determination of new QTLs with higher eﬀects, or identiﬁcation of
QTLs that ensure transgressive segregation. Other attempts
with new genes may be of importance especially when the
given enzymes can be identiﬁed in the QTL regions (Reinprecht et al. 2008).

Breeding Aspects
The development of genetic resistance to F. graminearum,
F. verticillioides and other Fusarium spp. in maize should be a
high priority in light of the toxins these species contaminate
maize grain with (Reid et al. 1996a, Munkvold 2003b). Duvick
(2001) suggested three theoretical approaches to decrease
fumonisin contamination. Resistance is mentioned ﬁrst, but
resources may be limited. Molecular markers can also be
applied to identify QTLs, but validated and eﬀective markers
are rare. A possibility in the future is to transfer resistance
genes into maize and ensure higher resistance in this way, but
at present no resistance genes are available. Presello et al.
(2005) suggested pedigree selection to improve F. graminearum
resistance. Both silk channel and kernel resistance were
investigated: the selection for kernel resistance was more
eﬀective, and the resistance was more stable. Reid et al.
(2001a,b, 2003) used modiﬁed pedigree selection to develop
eight inbreds with improved GER resistance, some with high
levels of both silk and kernel resistance. Researchers in
Germany are using double haploid technology to develop
GER-resistant inbreds (Martin et al. 2011b). Robertson-Hoyt

et al. (2007a) did not ﬁnd a close correlation between FER
resistance and other traits such as yield; therefore, they hope
that a strong selection for resistance will not result in lower
yield and other unwanted consequences. This would question
the yield penalty we mentioned regarding the high resistance in
this paper. Reid et al. (2003) did develop an inbred, CO441,
with high resistance to GER and excellent combining ability
for yield. Mesterha´zy et al. (2000) reported that resistant
hybrids will be bred when both parents have good or excellent
resistance; otherwise, the amount of resistance in the hybrid
cannot be predicted with certainty. Ali et al. (2005) and
Robertson et al. (2006) found transgressive segregation in
maize; this could be utilized in maize breeding as was the case
in wheat where the best F. graminearum-resistant source
(Sumai-3) was bred from two medium-resistant lines.
Breeding for ear rot resistance involves two important steps.
Munkvold (2003a) stresses the identiﬁcation and use of native
resistant sources. Breeding programmes could be based on
these sources, because they are adapted and already available
in the breeding nurseries. Nearly every paper cited reported
signiﬁcant diﬀerences in ear rot resistance; breeders need only
start with the more resistant genotypes in their programme. de
Oliveira et al. (2009) added that valuable breeding material
can be identiﬁed among landraces; however, breeding with
landraces can be time-consuming as many unwanted traits
may have to be bred out of the populations ﬁrst. Breeding can
be started from hybrids made from crossing involving one or
more lines with good resistance or from existing hybrids with
proven superior resistance, providing no proprietary issues are
involved that may restrict the use of the hybrids in a breeding

programme. There is not much in the literature about when
resistance selection should be performed in segregating generations. In most inbred breeding programmes, testing of the

Breeding for resistance to ear rots

combining ability occurs in the S3, S4, or later generations;
thus, the ﬁrst resistance evaluation of testcrosses can be made
at this time. However, as Loăer et al. (2010a) has reported,
many inbreds are susceptible as the infection pressure during
inbreeding was not strong enough. Reid (1999) collected
germplasms from around the world (adapted and unadapted)
with moderate to high resistance to various ear pathogens, but
no mention was made of how the inbreds were produced.
However, as indicated in Reid et al. (2001a,b, 2003), inbreds
were inoculated every generation in their development with the
exception of few generation advances that were performed in
oﬀ-season winter nurseries. Some of these inbreds resulted
from crosses between a resistant inbred and an inbred with
good agronomic performance, and other inbreds were selfed
out of reciprocal recurrent selection populations that were
subject to intense selection with artiﬁcial inoculations and
toxin evaluations. Eller et al. (2010) also reported on inoculation during inbreeding; they concluded that the backcross
method, that is normally used to transfer single major genes,
was also successful in improving FER resistance. This might
work for major QTLs, but for the normally polygenic trait it is
less suitable as QTLs might be lost. In this case, the reciprocal
recurrent selection suggested by Boling and Grogan (1965)
might work better. Bolduan et al. (2010) suggested that the
focus should be more on testing of hybrids and less on inbreds.

We think both are important, as inbreds having superior
resistance we can bred with to produce more resistant hybrids
after several years. It is more important to start breeding of
new resistant inbreds from materials with good or superior
resistance. These sources with superior resistance should also
be adapted to the target environment, otherwise commercially
competitive inbreds are hard to achieve. If possible, both
inbreds of a single cross should have good or excellent
resistance to allow the breeding of commercial hybrids with
maximum resistance.
Artiﬁcial inoculation methods must be extensively used in
the testing of the new hybrids and their parents. Currently,
most breeders use conidial suspensions, but toothpicks are also
used by some. The interest in artiﬁcial inoculation is growing.
It is interesting that fumonisin content has proven to be a more
reliable trait than visual scores (Eller et al. 2008a). However,
ﬁeld evaluation of symptoms is rapid and can extend to
thousands of genotypes, whereas any toxin analysis demands
more time and is money-consuming. For both ear rots, the
correlations between visual symptoms and toxin contamination are generally close (with a few exceptions). Accordingly,
visual symptoms are suggested for screening. To verify the low
toxin response of the new hybrids, at the end of the breeding
process toxins should be evaluated (Bolduan et al. 2009).
Many breeders screen either for GER or for FER only, and
few screen for both. Loăer et al. (2010a) and Miedaner et al.
(2008) stress the testing of inbreds and hybrids in several
locations with a single isolate or a mixture of isolates. As no
specialization is known, theoretically no diﬀerence exists
between single isolates and mixtures of isolates of the same
Fusarium spp. Therefore, the isolates may be used separately,

and so (in the case of four isolates), the amount of resistance
can be evaluated more precisely as with one single epidemic
situation. Even so, resistance evaluation is made 2–3 years
(Mesterha´zy 1983, Kova´cs et al. 1988). Some prefer isolate
mixtures to avoid the possibility of a single isolate being less
aggressive in a given ﬁeld season, resulting in levels of disease
too low to make accurate evaluations of resistance in 2–3 years

13

(Reid et al. 1993). A mixture of isolates will decrease the
environmental interaction. The resistance level will be the
mean of those of several isolates used, so the extent of
resistance can therefore be estimated better. A preselection of
the isolates for aggressiveness is very important (Miedaner
et al. 2010). As the aggressiveness varies (Mesterha´zy 1985),
the use of more isolates increases the reliability of the
evaluations. As there are diﬀerent ideas in these respects and
solid scientiﬁc material is scare, further research is needed to
give better suggestions for breeders.
Many studies have been published on the diﬀering resistance
mechanisms that may play a role in GER and FER resistance,
and QTLs and genes have been found responsible for higher
resistance. It is probable that some of these results will be used
in breeding programmes. However, a well-working, methodical, phenotyping system must be used; otherwise, the gene
expression cannot be checked at a practical level.
Regarding the two types of resistance, resistance to kernel
infection is more stable and can be reproduced better than silk
or silk channel resistance as the latter may be under more
environmental inﬂuence and the window for fungal invasion is

smaller as the fungus must grow down the silk channel before
the silk dries out (Reid et al. 1992a, Reid and Hamilton 1996,
Reid and Sinha 1998). Breeders must choose for themselves
which mode of fungal entry is more important in their growing
region. Some breeders separate their nurseries into silk channel
and kernel resistance sections based on the sources of
resistance used. Evaluation for both modes should be made
during parental selection for new inbred development programmes and during the hybrid testing and evaluation of lines.
In some cases where the major source of kernel infection is
attributed to boring insects but these are controlled by Bt
hybrids in commercial ﬁelds, it may be more practical to focus
breeding eﬀorts on silk channel resistance. However, it is
important to remember that several reports indicate that the
diﬀerence between these two modes may be less pronounced
than normally anticipated.

Conclusions and Outlook
The maize–Fusarium system is complicated, but several conclusions can be drawn that are useful for resistance breeding
programmes and resistance research. Breeding is a decisive
part of the integrated production process from farm to fork
(van der Fels-Klerx and Booij 2010). In all important maizegrowing regions, many Fusarium spp. occur at the same time,
and their species structure depends on the region and the local
weather conditions. Fusarium graminearum and F. verticillioides, the two most important species, and their close relatives
have very diverging ecosystem requirements for their successful infection of a host plant. The available data indicate that
common resistance may exist to both species in maize,
consequently simplifying the breeding process. It is highly
important that several authors have found correlations
between the resistances to Aspergillus, Fusarium and Gibberella ear rots. This can lead to the hypothesis that resistance
may be much wider than previously believed. This point is very
important as hybrids are developed for global needs, and their

resistance to all local Fusarium and other fungal populations
should therefore be ensured whenever possible. Research on
this complex resistance is needed to determine the cause of the
high correlation between the natural and artiﬁcial inoculation
results.

14

The data are clear in the respect that visual symptom
severity and toxin contamination correlate closely for most
species. Highly resistant genotypes demonstrate low disease
severity and low toxin contamination. Speciﬁc toxin resistance is at present problematic. For example, in GER, DON
may play virulence-increasing role, and glycosyl transferases
(Lemmens et al. 2005) can also decrease the DON content in
maize, but the signiﬁcance of this for breeding is not yet
known.
The registration process of new maize hybrids (in countries
where this is applicable) should contain results from an
artiﬁcial inoculation survey of the variety candidates. In this
way, the susceptible and very susceptible hybrids could be
banned from registration. This is the most eﬀective way to
improve food and feed safety worldwide. Unfortunately, as
very few resistant hybrids currently exist, such a regulation
would mean few if any hybrids get registered in some
countries. With new regulations on allowable mycotoxin limits
in several countries, breeding programmes to develop ear rot
resistance are being initiated or strengthened with more
resources. As a consequence, future hybrids may possess more
resistance. Until this time comes, it is still paramount that

farmers have access to ear rot rating data on hybrids that they
may grow. This will allow farmers to choose hybrids with more
resistance if ear rot is a signiﬁcant threat on their farm.
Countries need to organize an unbiased evaluation of all
registered hybrids each year and make this information
available to farmers until the time that enough resistant
sources exist for resistant hybrids to be available.
The important fundamental steps of breeding for higher
resistance have already been taken. These steps allow the
breeding of inbreds and hybrids with a higher level of
resistance than it was previously possible. However, many
important questions are not yet answered. Additionally, more
eﬀective selection methods should be developed and existing
methodology should be improved and standardized. The
relationships between natural and artiﬁcial infection should
also be clariﬁed.
Food and feed safety requires more healthy grain (also
silage); the investment in this sector of breeding and science
may be expected to increase. We hope that this paper will
contribute to the initiation of this process.

Acknowledgements
The authors express their thanks to the following projects: Hungarian
Grant Agency NKTH: GAK (OMFB-01286/2004, OMFB 00313/
2006), NAP-2-2007-0001 and the FP7 MYCORED KBBE-2007-2-5-05
and Deak Zrt Szeged, Hungary, Ontario Corn ProducersÕ Association,
Ontario Pork, Agriculture and Agri-Food Canada and the Canadian
Field Crop Research Alliance.

References

Afolabi, C. G., P. S. Ojiambo, E. J. A. Ekpo, A. Menkir, and
R. Bandyopadhyay, 2008: Novel sources of resistance to fusarium
stalk rot of maize in tropical Africa. Plant Dis., 92, 772—780.
Alexander, N. J., R. H. Proctor, and S. P. McCormick, 2009: Genes,
gene clusters, and biosynthesis of trichothecenes and fumonisins in
Fusarium. Toxin Rev. 28, 198—215.
Ali, M. L., J. H. Taylor, L. Jie, G. Sun, M. William, K. J. Kasha,
L. M. Reid, and K. P. Pauls, 2005: Molecular mapping of QTLs for
resistance to Gibberella ear rot, in corn, caused by Fusarium
graminearum. Genome 48, 521—533.

´ . M e s t e r h a´ z y , M . L e m m e n s and L . M . R e i d
A
Andrew, R. H., 1954: Disease of maize. Seventh FAO Hybrid Maize
Meeting Report. FAO and UN.
Anonymous, 2005: Commission Regulation (EC) No 856/2005 of 6
June 2005: amending Regulation (EC) No 466/2001 as regards
Fusarium toxins. Oﬀ. J. Eur. Union. 7.6.2005, L 143/3-8
Anonymous, 2006: Commission Recommendation of 17 August 2006
on the prevention and reduction of Fusarium toxins in cereals and
cereal products (Text with EEA relevance). (2006/583/EC), 234/3540.
Anonymous, 2007: Commission Regulation (EC) No 1126/2007 of 28
September 2007 amending Regulation (EC) No 1881/2006 setting
maximum levels for certain contaminants in foodstuffs as regards
Fusarium toxins in maize and maize products. Oﬀ. J. Eur. Union
29.09.2007, L 255/14-17.
Anonymous, 2010: GOSZ-VSZT Kukorica Posztregisztra´cio´s
Fajtakı´ se´rlet Ko´rtani eredme´nyek, 2010 (Post registration variety test
for maize by the Association of Cereal Producers and the National
Seed Committee, Pathology results). Available at: t.

hu/hu/gosz-vszt+kukorica+posztregisztr%C3%A1ci%C3%B3s+
k%C3%ADs%C3%A9rlet+2010+1.html (last accessed on May 27,
2011, 14:25:17).
Archer, T. L., C. Patrick, G. Schuster, G. Cronholm, E. D. Jr Bynum,
and W. P. Morrison, 2001: Ear and shank damage by corn borers
and corn earworms to four events of Bacillus thuringiensis transgenic
maize. Crop Prot. 20, 139—144.
Assabgui, R. A., L. M. Reid, R. I. Hamilton, and J. T. Arnason, 1993:
Correlation of kernel (e)-ferulic acid content of maize with resistance
to Fusarium-graminearum. Phytopathology 83, 949—953.
Bacon, C. W., and D. M. Hinton, 1996: Symptomless endophytic
colonization of maize by Fusarium moniliforme. Can. J. Bot. 74,
1195—1202.
Barrie`re, Y., O. Argillier, B. Michalet-Doreau, Y. He´bert, E. Guingo,
C. Giauﬀret, and J. C. Mile, 1997: Relevant traits, genetic variation
and breeding strategies in early silage maize. Agronomie 17,
395—411.
Barto´k, T., A´. Sze´csi, A. Szekeres, A´. Mesterha´zy, and M. Barto´k,
2006: Detection of new fumonisin mycotoxins and fumonisin-like
compounds by reversed phase – high-performance liquid chromatography/electrospray ionization – ion-trap mass spectrometry.
Rapid Commun. Mass Spectrom. 20, 117.
Bartok, T., L. Toălgyesi, A. Szekeres, M. Varga, R. Bartha, A´. Sze´csi,
M. Barto´k, and A´. Mesterha´zy, 2010: Detection and characterization of twenty-eight isomers of fumonisin B1 (FB1) mycotoxin in a
solid rice culture infected with Fusarium verticillioides by reserved
phase high-performance liquid chromatography/electro spray ionization time-of-ﬂight and ion trap mass spectrometry. Rapid Commun. Mass Spectrom. 24, 35—42.
Be´ke´si, P., and K. Hinfner, 1970: Adatok a kukorica fuza´riumos
megbetegede´se´nek ismerete´hez (Data on the Fusarium spp. in
maize). Noăvenyvedelem 6, 1318. (in Hungarian, English summary)
Berek, L., I. B. Perti, A´. Mesterha´zy, J. Te´ren, and J. Molna´r, 2001:
Effect of mycotoxins on human immune functions in vitro. Toxicol.

In Vitro 15, 25—30.
Bily, A. C., L. M. Reid, J. H. Taylor, D. Johnston, C. Malouin,
A. J. Burt, B. Bakan, C. Regnault-Roger, K. P. Pauls, J. T. Arnason,
and B. J. R. Philogene, 2003: Dehydrodimers of ferulic acid in maize
grain pericarp and aleurone: resistance factors to Fusarium graminearum. Phytopathology 93, 712—719.
Bı´ ro´ne´, G. M., 1975: Kukorica´n ka´rosı´ to´ Fusarium fajok elterjede´se e´s
toxikolo´giai vizsga´lata (Prevalence of Fusarium spp. in corn and
their toxicity) (in Hungarian). PhD thesis, Goădoăll}
o. (Availability:
Library of Hung. Acad. Sci., Budapest)
Bisby, G. R., and D. L. Bailey, 1923: Ear and root rots. Fourth Annual
Report of the Survey of the Prevalence of Plant Diseases in the
Dominion of Canada. 33 pp.
Blandino, M., and A. Reyneri, 2007: Comparison between normal and
waxy maize hybrids for Fusarium-toxin contamination in NW Italy.
Maydica 52, 127—134.

Breeding for resistance to ear rots
Blandino, M., A. Reyneri, and F. Vanara, 2009a: Effect of sowing time
on toxigenic fungal infection and mycotoxin contamination of maize
kernels. J. Phytopathol. 157, 7—14.
Blandino, M., A. Reyneri, G. Colombari, and A. Pietri, 2009b:
Comparison of integrated ﬁeld programmes for the reduction of
fumonisin contamination in maize kernels. Field Crops Res. 111,
284—289.
Bolduan, C., T. Miedaner, W. Schipprack, B. S. Dhillon, and A. E.
Melchinger, 2009: Genetic variation for resistance to ear rots and
mycotoxins contamination in early European maize inbred lines.
Crop Sci. 49, 2019—2028.

Bolduan, C., T. Miedaner, H. F. Utz, B. S. Dhillon, and A. E.
Melchinger, 2010: Genetic variation in testcrosses and relationship
between line per se and testcross performance for resistance to
Gibberella ear rot in maize. Crop Sci. 50, 1691—1696.
Boling, M. B., and C. O. Grogan, 1965: Gene action affecting host
resistance to Fusarium ear rot of maize. Crop Sci. 5, 305—307.
Boutigny, A. L., F. Richard-Forget, and C. Barreau, 2008: Natural
mechanisms for cereal resistance to the accumulation of Fusarium
trichothecenes. Eur. J. Plant Pathol. 121, 411—423.
Buerstmayr, H., T. Ban, and J. A. Anderson, 2009: QTL mapping and
marker-assisted selection for Fusarium head blight resistance in
wheat: a review. Plant Breed. 128, 1—26.
Bush, B. J., L. M. Carson, M. A. Cubeta, W. M. Hagler, and G. A.
Payne, 2004: Infection and fumonisin production by Fusarium
verticillioides in developing maize kernels. Phytopathology 94,
88—93.
Butron, A., Santiago, R., P. Mansilla, C. Pintos-Varela, A. Ordas, and
R. A. Malvar, 2006: Maize (Zea mays L.) genetic factors for
preventing fumonisin contamination. J. Agric. Food. Chem. 54,
6113—6117.
de la Campa, R., Hooker, D. C., J. D. Miller, A. W. Schaafsma, and
B. G. Hammond, 2005: Modeling effects of environment, insect
damage, and Bt genotypes on fumonisin accumulation in maize in
Argentina and the Philippines. Mycopathologia 159, 539—552.
Cao, A., L. M. Reid, A. Butro´n, R. A. Malvar, X. C. Souto, and
R. Santiago, 2011: Role of hydroxycinnamic acids in the infection of
maize silks by Fusarium graminearum Schwabe. Mol. Plant Microbe
Interact. 24, 1020—1026.
Choi, Y. E., and J. R. Xu, 2010: The cAMP signaling pathway in
Fusarium verticillioides is important for conidiation, plant infection,

and stress responses but not fumonisin production. Mol. Plant
Microbe Interact. 23, 522—533.
Christensen, C. M. (ed.). 1982: Storage of Cereal Grains and their
Products. American Association of Cereal Chemists, Inc., St. Paul,
MN, 544 pp. ISBN: 0-913250-23-6.
Christensen, C. M., and H. H. Kaufmann, 1969: Grain Storage. The
University of Minnesota Press, Minneapolis, 153 pp.
Christensen, J. J., and R. D. Wilcoxson, 1966: Stalk rot of corn.
American Phytopathological Society, Monograph No.3. 59 pp.
Chungu, C., D. E. Mather, L. M. Reid, and R. I. Hamilton, 1996a:
Inheritance of kernel resistance to Fusarium graminearum in maize.
J. Hered. 87, 382—385.
Chungu, C., D. E. Mather, L. M. Reid, and R. I. Hamilton, 1996b:
Comparison of techniques for inoculating maize silk, kernel and cob
tissues with Fusarium graminearum. Plant Dis., 80, 81—84.
Clements, M. J., and D. G. White, 2004: Identifying sources of
resistance to aﬂatoxin and fumonisin contamination in corn grain. J.
Toxicol. Toxin Rev. 23, 381—396.
Clements, M. J., C. E. Kleinschmidt, C. M. Maragos, J. K. Pataky,
and D. G. White, 2003: Evaluation of inoculation techniques for
Fusarium ear rot and fumonisin contamination of corn. Plant Dis.
87, 147—153.
Clements, M. J., C. A. Maragos, J. K. Pataky, and D. G. White, 2004:
Sources of resistance to fumonisin accumulation in grain and
Fusarium ear and kernel rot of corn. Phytopathology 94, 251—260.
Czembor, E., and P. Ochodzki, 2009: Resistance of ﬂint and dent
maize forms for colonization by Fusarium spp. and mycotoxins
contamination. Maydica 54, 263—267.

15

Ding, J. Q., X. M. Wang, S. Chander, J. B. Yan, and J. S. Li, 2008:
QTL mapping of resistance to Fusarium ear rot using a RIL
population in maize. Mol. Breed. 22, 395403.
Dorn, B., H.-R. Forrer, S. Schuărch, and S. Vogelsang, 2009: Fusarium
species complex on maize in Switzerland: occurrence, prevalence,
impact and mycotoxins in commercial hybrids under natural
infection. Eur. J. Plant Pathol. 125, 51—61.
Dowd, P. F., 2001: Biotic and abiotic factors limiting efﬁcacy of Bt
corn in indirectly reducing mycotoxin levels in commercial ﬁelds.
J. Econ. Entomol. 94, 1067—1074.
Du Toit, L. J., and J. K. Pataky, 1999: Reactions of processing sweet
corn hybrids to Gibberella ear rot. Plant Dis. 83, 176—180.
Dufresne, M., T. van der Lee, S. B. MÕBarek, X. Xu, X. Zhang, T. Liu,
C. Waalwijk, W. Zhang, G. H. J. Kema, and M.–. J. Daboussi,
2008: Transposon-tagging identiﬁes novel pathogenicity genes in
Fusarium graminearum. Fungal Genet. Biol. 45, 1552—1561.
Duncan, K. E., and R. J. Howard, 2010: Biology of maize kernel
infection by Fusarium verticillioides. Mol. Plant Microbe Interact.
23, 6—16.
Duvick, J., 2001: Prospects for reducing fumonisin contamination of
maize through genetic modiﬁcation. Environ. Health Perspect. 109,
337—342.
Eller, M., J. Holland, and G. Payne, 2008a: Breeding for improved
resistance to fumonisin contamination in maize. Toxin Rev. 27,
371—389.
Eller, M. S., L. A. Robertson-Hoyt, G. A. Payne, and J. B. Holland,
2008b: Grain yield and Fusarium ear rot of maize hybrids developed
from lines with varying levels of resistance. Maydica 53, 231—237.
Eller, M. S., G. A. Payne, and J. B. Holland, 2010: Selection for
reduced Fusarium ear rot and fumonisin content in advanced

backcross maize lines and their topcross hybrids. Crop Sci. 50,
2249—2260.
Enerson, P. M., and R. B. Hunter, 1980: A technique for screening
maize (Zea mays L.) for resistance to ear mould incited by Gibberella
zeae (Schw.). Petch. Can. J. Plant Sci. 60, 1123—1128.
Farrar, J. J., and R. M. Davis, 1991: Relationship among ear
morphology, western ﬂower thrips, and Fusarium ear rot of corn.
Phytopathology 81, 661—666.
van der Fels-Klerx, H. J., and C. H. J. Booij, 2010: Perspectives for
geographically oriented management of Fusarium mycotoxins in the
cereal supply chain. J. Food Prot. 73, 1153—1159.
Focke, I., 1966: Fusarium culmorum/W.G.Sm.) und F. moniliforme
Sheld. als Erreger von Kolbenfaulen des Maises (Zea mays L.) im
mitteldeutschem Raum. Wissenschaftliche Zeitschrift der WilhelmPieck-Universitaăt Rostock. Naturwissenschaftliche Reihe. WilhelmPieck-Universitaăt Rostock, Rostock. Wiss. Z. Univ. Rostock, Nat.
Wiss. Reihe 15, 219—227.
Focke, I., and W. Kuăhnel, 1964: Die Weissfaule der Maiskolben
(Fusarium poae PK/Wr.). Nachrichtenblatt fuăr Deutschen Panzenschutzdienst (Berlin) 18, 18.
Folcher, L., M. Jarry, A. Weissenberger, F. Gerault, N. Eychenne,
M. Delos, M. Delos, and C. Regnault-Roger, 2009: Comparative
activity of agrochemical treatments on mycotoxin levels with regard
to corn borers and Fusarium mycoﬂora in maize (Zea mays L.)
ﬁelds. Crop Prot. 28, 302—308.
Foley, D. C., 1959: Systemic infection of corn by Fusarium moniliforme. Phytopathology 49, 538.
Garcia, D., Ramos, A. J., V. Sanchis, and S. Marı´ n, 2009: Predicting
mycotoxins in foods: a review. Food Microbiol. 26, 757—769.
Garcia-Aguirre, G., and R. Martinez-Flores, 2010: Fusarium species
from corn kernels recently harvested and shelled in the ﬁelds in the
Ciudad Serdan Region, Puebla. Rev. Mex. Biodivers. 81, 15—20.
Gelderblom, W. C. A., K. Jaskiewicz, W. F. O. Marasas, P. G. Thiel,
R. M. Horak, R. Vleggaar, and N. P. J. Kriek, 1988: Fumonisins –

novel mycotoxins with cancer-promoting activity produced by
Fusarium moniliforme. Appl. Environ. Microbiol. 54, 1806—1811.
Gergely, L., P. Hertelendy, Z. Birta-Vas, Sz. Szla´vik, L. La´za´r, and J.
Csapo´, 2010: The evaluation of the diseases caused by Fusarium
fungi at the Central Agricultural Ofﬁce. In: A´. Mesterha´zy (ed.),

16
Workshop for Variety Registration in Cereals for Fusarium Resistance, 27—28. March 2324, 2010, Szeged, Hungary.
Goertz, A. 2009: Auftreten der Fusarium-Kolbenfaăule im Maisanbau
in Deutschland und Maßnahmen zur Vermeidung der Mykotoxinbelastung in Maiskoărnern. Inaugural Dissertation, University of
Bonn, 138 pp.
Goertz, A., E.-C. Oerke, U. Steiner, C. Waalwijk, I. Vries, and H.-W.
Dehne, 2008: Biodiversity of Fusarium species causing ear rot of
maize in Germany. Cereal Res. Commun. 36, 617—622.
Goertz, A., S. Zuehlke, M. Spiteller, U. Steiner, H. W. Dehne, C.
Waalwijk, I. de Vries, and E. C. Oerke, 2010: Fusarium species and
mycotoxin proﬁles on commercial maize hybrids in Germany. Eur.
J. Plant Pathol. 128, 101—111.
Harris, L. J., A. Saparno, A. Johnston, S. Prisic, M. Xu, S. Allard, A.
Kathiresan, T. Ouellet, and R. J. Peters, 2005: The maize An2 gene is
induced by Fusarium attack and encodes an ent-copalyl diphosphate
synthase. Plant Mol. Biol. 59, 881—894.
Harrison, L. R., B. N. Colvin, J. T. Greene, L. E. Newman, and R. J.
Cole, 1990: Pulmonary edema and hydrothorax in swine produced
by fumonisin B1, a toxic metabolite of Fusarium moniliforme. J.
Vet. Diagn. Invest. 2, 217—221.
Hart, L. P., E. Gendloﬀ, and E. C. Rossman, 1984: Effect of corn
genotypes on ear rot infection by Gibberella zeae. Plant Dis. 68,
296—298.

Headrick, J. M., and J. K. Pataky, 1991: Maternal inﬂuence on the
resistance of sweet corn lines to kernel infection by Fusarium
moniliforme. Phytopathology 81, 268—274.
Henry, W. B., W. P. Williams, G. L. Windham, and L. K. Hawkins,
2009: Evaluation of maize inbred lines for resistance to Aspergillus
and Fusarium ear rot and mycotoxin accumulation. Agron. J. 101,
1219—1226.
Hertelendy, P., Z. Birta-Vas, and S. Szla´vik, 2010: Evaluation methods
of Fusarium stalk rot and Fusarium ear rot for the registration
process in Hungary. In: A´. Mesterha´zy (ed.), Workshop for Variety
Registration in Cereals for Fusarium Resistance, 21—22. March 23–
24, 2010, Szeged, Hungary.
Hoenisch, R. W., and R. M. Davis, 1994: Relationship between kernel
pericarp thickness and susceptibility to Fusarium ear rot in ﬁeld
corn. Plant Dis. 78, 517—519.
Igawa, T., N. Takahashi-Ando, N. Ochiai, S. Ohsato, T. Shimizu, T.
Kudo, I. Yamaguchi, and M. Kimura, 2007: Reduced contamination by the Fusarium mycotoxin zearalenone in maize kernels
through genetic modiﬁcation with a detoxiﬁcation gene. Appl.
Environ. Microbiol. 73, 1622—1629.
Iglesias, J., D. A. Presello, G. Botta, G. A. Lori, and C. M. Fauguel,
2010: Aggressiveness of Fusarium Section Liseola isolates causing
maize ear rot in Argentina. J. Plant Pathol. 92, 205—211.
International Agency for Research on Cancer (IARC), 1993: Monograph 56: Some Naturally Occurring Substances: Some Food Items
and Constituents Heterocyclic Amines and Mycotoxins. IARC,
Lyon, France.
Ivic, D., M. Cabric, B. Palaversic, and B. Cvjetkovic, 2008: No correlation
between pericarp thickness and Fusarium ear rot (Fusarium verticillioides) in Croatian maize hybrids and lines. Maydica 53, 297—301.
Jenczmionka, N. J., and C´. W. Schaefer, 2005: The Gpmk1 MAP
kinase of Fusarium graminearum regulates the induction of speciﬁc
secreted enzymes. Curr. Genet. 47, 29—36.

Jovicevic, B., and M. Sultan, 1979: Effect of Fusarium ear rot on corn
yields. Zastita Bilja 30, 223—228.
Jugenheimer, R. W., 1976: Corn Improvement, Seed Production and
Uses. John Wiley and Sons, New York, London, Sydney, Toronto,
670 pp.
Kellerman, T. S., W. F. O. Marasas, P. G. Thiel, W. C. A.
Gelderblom, M. Cawood, and J. A. W. Coetzer, 1990: Leukoencephalomalacia in two horses induced by oral dosing of fumonisin
B1. Onderstepoort J. Vet. Res. 57, 269—275.
Koehler, B., 1942: Natural mode of entrance of fungi into corn ears
and some symptoms that indicate infection. J. Agric. Res. 64,
421—442.

´ . M e s t e r h a´ z y , M . L e m m e n s and L . M . R e i d
A
Koehler, B., 1950: Corn stalk rot and ear studies. Proceeding of 5th
Corn Research Conference. 33—45. American Seed Trade Association.
Koehler, B., 1957: Pericarp injuries in seed corn. Prevalence in dent
corn and relation to seedling blights. Univ. Ill. Agric. Exp. Sta.
Bulletin 617, 72.
Koehler, B., 1959: Corn ear rots in Illinois. Ill. Agric. Exp. Sta.
Bulletin 639, 87.
Kova´cs, G., Jr, G.-ne´. Kova´cs, and A´. Mesterha´zy, 1988: Kukoricahibridek cs}
o- e´s sza´rfuza´riummal szembeni ellena´llo´sa´ga e´s
mechanikai szila´rdsa´ga. (Resistance of corn hybrids to fusarial stalk
rot and ear rot and their mechanical stalk characteristics).
Noăvenytermeles 37, 112.
Kovacs, K., G. Jr Kovacs, and A. Mesterhazy, 1994: Expression of
resistance to fusarial ear blight in corn inbreds and their hybrids.
Maydica 39, 187—190.
Kozhukhova, N. E., M. Syvolap Yu, B. F. Varenyk, and V. M.

Sokolov, 2007: Marking of the loci encoding maize resistance to
Fusarium. Cytol. Genet. 41, 37—41.
Lanubile, A., P. Luca, and M. Adriano, 2010: Differential gene
expression in kernels and silks of maize lines with contrasting levels
of ear rot resistance after Fusarium verticillioides infection. J. Plant
Physiol. 167, 1398—1406.
Lemmens, M., 1999: Anwendung kuănstlicher Inokulationsmethoden
zur Kolbenfusariose-Resistenzbestimmung bei Mais. 50. Tagung der
Vereinigung Oăsterreichischer Panzenzuăchter, BAL Gumpenstein,
6368.
Lemmens, M., 2010: Fusarium ear rot resistance testing in maize:
natural infection versus artiﬁcial inoculation. In: A´. Mesterha´zy
(ed.), Workshop for Variety Registration in Cereals for Fusarium
Resistance, 18—20. March 23–24, 2010, Szeged, Hungary.
Lemmens, M., U. Scholz, F. Berthiller, C. DallÕAsta, A. Koutnik, R.
Schuhmacher, G. Adam, H. Buerstmayr, A´. Mesterhazy, R. Krska,
and P. Ruckenbauer, 2005: The ability to detoxify the mycotoxin
deoxynivalenol co-localizes with a major QTL for Fusarium head
blight resistance in wheat. Mol. Plant Microbe Interact. 18,
13181324.
Loăer, M., B. Kessel, M. Ouzunova, and T. Miedaner, 2010a:
Population parameters for resistance to Fusarium graminearum and
Fusarium verticillioides ear rot among large sets of early, mid-late
and late maturing European maize (Zea mays L.) inbred lines.
Theor. Appl. Genet. 120, 10531062.
Loăer, M., T. Miedaner, B. Kessel, and M. Ouzunova, 2010b:
Mycotoxin accumulation and corresponding ear rot rating in three
maturity groups of European maize inoculated by two Fusarium
species. Euphytica 174, 153164.
Loăer, M., B. Kessel, M. Ouzunova, and T. Miedaner, 2011:

Covariation between line and testcross performance for reduced
mycotoxin concentrations in European maize after silk channel
inoculation of two Fusarium species. Theor. Appl. Genet. 121,
925—934.
Logrieco, A., G. Mule, A. Moretti, and A. Bottalico, 2002: Toxigenic
Fusarium species and mycotoxins associated with maize ear rot in
Europe. Eur. J. Plant Pathol. 108, 597—609.
Manninger, I., 1978: Evaluation of corn diseases in breeding for
resistance and the qualiﬁcation of wheat varieties (in Hungarian
with English captions and abstract). Noăvenytermeles 27, 710.
Mar n, S., I. Hodzic, A. J. Ramos, and V. Sanchis, 2008: Predicting the
growth/nogrowth boundary and ochratoxin A production by
Aspergillus carbonarius in pistachio nuts. Food Microbiol. 25,
683—689.
Martens, J. W., W. L. Seaman, and T. G. Atkinson, 1984: Diseases of
Field Crops in Canada. An Illustrated Compendium. Canadian
Phytopathological Society, Harrow, Ontario, Canada.
Martin, M., T. Miedaner, B. S. Dhillon, U. Ufermann, B. Kessel, M.
Ouzunova, W. Schipprack, and A. E. Melchinger, 2011a: Colocalization of QTL for Gibberella ear rot resistance and low mycotoxin
contamination in early European maize. Crop Sci. 51, 1935—1945.

Breeding for resistance to ear rots
Martin, M., D. D. Miedaner, B. Schwegler, M. Kessel, B. S.
Ouzunova, W. Dhillon, and H. F. Schipprack, 2011b: Comparative
QTL mapping for Gibberella ear rot resistance and reduced
deoxynivalenol contamination across connected maize populations.
Crop Sci. 57, 1935—1945.
Menkir, A., R. L. Brown, R. Bandyopadhyay, Z.-Y. Chen, and
T. Cleveland, 2006: A USA-Africa collaborative strategy for identifying, characterizing, and developing maize germplasm with resistance

to aﬂatoxin contamination. Mycopathologia 162, 225—232.
Mesterha´zy, A´., 1978: Kukoricahibridek cs}
o- e´s sza´rfuza´riummal
szembeni ellena´llo´sa´ga e´s mechanikai szila´rdsa´ga (Resistance of corn
hybrids to stalk rot and ear rot and the mechanical strength of the
stalk). Noăvenytermeles 37, 111.
Mesterhazy, A., 1979: Stalk splitting as a method for evaluating stalk
rot of corn. Plant Dis. Reporter 63, 227—231.
Mesterha´zy, A´., 1982: Resistance of corn to Fusarium ear rot and its
relation to seedling resistance. Phytopathologische Zeitschrift 103,
218—231.
Mesterha´zy, A´., 1983: Relationship between resistance to stalk rot and
ear rot of corn inﬂuenced by rind resistance, premature death and
the rate of drying of the ear. Maydica 28, 425—437.
Mesterha´zy, A´., 1985: Effect of seed production area on the seedling
resistance of wheat to Fusarium seedling blight. Agronomie (Paris),
5, 491—497.
Mesterha´zy, A´., 1995: Types and components of resistance against
Fusarium head blight of wheat. Plant Breed. 114, 377—386.
Mesterha´zy, A´., 2002: Role of deoxynivalenol in aggressiveness of
Fusarium graminearum and F. culmorum and in resistance to
Fusarium head blight. Eur. J. Plant Pathol. 108, 675—684.
Mesterha´zy, A´., and K. Kova´cs, 1988: Breeding corn against fusarial
stalk rot, ear rot and seedling blight. Acta Phytopathol. Acad. Sci.
Hung. 21, 231—249.
Mesterha´zy, A´., and M. Vojtovics, 1977: A kukorica Fusarium okozta
fertozoăttsegenek vizsgalata 1972-1975-ben. (Investigation of Fusarium infection in corn 19721975). Noăvenytermeles 26, 367378.
Mesterhazy, A´., T. Barto´k, C. M. Mirocha, and R. Komoro´czy, 1999:
Nature of resistance of wheat to Fusarium head blight and
deoxynivalenol contamination and their consequences for breeding.

Plant Breed. 118, 97—110.
Mesterha´zy, A´., G. Jr Kova´cs, and K. Kova´cs, 2000: Breeding
resistance for Fusarium ear rot (FER) in corn. Genetika 32,
495—505.
Mesterha´zy, A´., T. Barto´k, G. Ka´szonyi, M. Varga, B. To´th, and J.
Varga, 2005: Common resistance to different Fusarium spp. causing
Fusarium head blight in wheat. Eur. J. Plant Pathol. 112, 267—281.
Mesterha´zy, A´., H. Buerstmayr, B. To´th, Sz. Lehoczki-Krsjak, A´.
Szabo´-Heve´r, and M. Lemmens, 2007: An improved strategy for
breeding FHB resistant wheat must include Type I resistance. In: R.
Clear (ed.), Proceedings of the 5th Canadian Workshop on
Fusarium Head Blight, 5166. November 2730, 2007, Delta
Winnipeg.
Miedaner, T., M. Loăer, C. Bolduan, B. Kessel, M. Ouzunova,
V. Mirdita, and A. E. Melchinger, 2008: Genetic variation for
resistance and mycotoxin content of European maize inoculated
with Fusarium graminearum and F. verticillioides. Cereal Res.
Commun. 36(Suppl B), 45—48.
Miedaner, T., C. Bolduan, and A. E. Melchinger, 2010: Aggressiveness
and mycotoxin production of eight isolates each of Fusarium
graminearum and Fusarium verticillioides for ear rot on susceptible
and resistant early maize inbred lines. Eur. J. Plant Pathol. 127,
113—123.
Miller, J. D., M. Miles, and D. A. Fielder, 1997: Kernel concentrations
of 4-acetylbenzoxazolin-2-one and diferuloylputrescine in maize
genotypes and Gibberella ear rot. J. Agric. Food Chem. 45,
4456—4459.
Miller, S. S., L. M. Reid, G. Butler, S. P. Winter, and N. J.
McGoldrick, 2003: Long chain alkanes in silk extracts of maize
genotypes with varying resistance to Fusarium graminearum. J.

Agric. Food. Chem. 51, 6702—6708.

17
Miller, S. S., L. M. Reid, and L. J. Harris, 2007: Colonization of maize
silks by Fusarium graminearum, the causative organism of Gibberella ear rot. Can. J. Bot. 85, 369—376.
Mirocha, C. J., 1974: Isolation, detection, and quantization of
zearalenone in maize and barley. J. Assoc. Oﬀ. Anal. Chem. 57,
1104—1974.
Munkvold, G. P., 2003a: Epidemiology of Fusarium diseases and their
mycotoxins in maize ears. Eur. J. Plant Pathol. 109, 705—713.
Munkvold, G. P., 2003b: Cultural and genetic approaches to managing
mycotoxins in maize. Annu. Rev. Phytopathol. 41, 99—116.
Munkvold, G. P., R. L. Hellmich, and W. B. Showers, 1997a: Reduced
Fusarium ear rot and symptomless infection in kernels of maize
genetically engineered for European corn borer resistance. Phytopathology 87, 1071—1077.
Munkvold, G. P., D. C. McGee, and W. M. Carleton, 1997b:
Importance of different pathways for maize kernel infection by
Fusarium moniliforme. Phytopathology 87, 209—217.
Murillo-Williams, A., and G. P. Munkvold, 2008: Systemic infection
by Fusarium verticilliodes in maize plants grown under three
temperature regimes. Plant Dis. 92, 1695—1700.
Nagy, E., and I. Cabulea, 1996: Breeding maize for tolerance to
Fusarium stalk rot and ear rot stress. Romanian Agr. Res. –
INCDA Fundulea. 5–6, 43—58.
Nankam, C., and J. K. Pataky, 1996: Resistance to kernel infection by
Fusarium moniliforme in the sweet corn inbred IL125b. Plant Dis. 80,
593—598.
Nelson, P. E., T. A. Tousson, and W. F. O. Marasas, 1983: Fusarium
species. An illustrated manual for identiﬁcation. The Pennsylvania
State University Press, University Park and London, 193 pp.

Nicolaisen, M., S. Suproniene, L. K. Nielsen, I. Lazzaro, N. H. Spliid,
and A. F. Justesen, 2009: Real-time PCR for quantiﬁcation of eleven
individual Fusarium species in cereals. J. Microbiol. Meth., 76,
234—240.
Oberforster, M., and H. Felder, 2010: Systems for evaluating the
susceptibility of cereal and maize cultivars to Fusarium in Austria.
In: A´. Mesterha´zy (ed.), Workshop for Variety Registration in
Cereals for Fusarium Resistance, 31—33. March 23–24 2010,
Szeged, Hungary.
de Oliveira, T. R., D. D. Jaccoud, L. Henneberg, M. D. Michel,
I. M. Demiate, A. T. B. Pinto, M. Machinski, and A. C. Barana,
2009: Maize (Zea mays L.) landraces from the Southern Region of
Brazil: contamination by Fusarium spp., zearalenone, physical and
mechanical characteristics of the kernels. Braz. Arch. Biol. Technol.
52, 11—16.
Palaversˇ ic´, B., M. Jukic´, I. Buhinicˇek, A. Vragolovic´, and Z. Kozic´,
2010: Several years of testing maize hybrids for resistance to
Gibberella ear rot. In: A´. Mesterha´zy (ed.), Workshop for Variety
Registration in Cereals for Fusarium Resistance, 20—21. March 23–
24, 2010, Szeged, Hungary.
Pappelis, A. J. 1984: The maize root rot, stalk rot. In: Sorghum Root
and Stalk Rots, A Critical Review. Proceedings of the Consultative
Group Discussion on Research Needs and Strategies for Control of
Sorghum Root and Stalk Rot Diseases, 155—172. 27 November–2
December 1983, ICRISAT, Bellagio, Italy.
Papst, C., H. F. Utz, A. E. Melchinger, J. Eder, T. Magg, D. Klein,
and M. Bohn, 2005: Mycotoxins produced by Fusarium spp. in
isogenic Bt vs. non-Bt maize hybrids under European corn borer
pressure. Agron. J. 97, 219—224.
Papst, C., J. Zellner, S. Venkataratnam, and J. Eder, 2007: Fusarium

Problematik bei Koărnermais (Zea mais L.). Gesunde Pﬂanzen 59,
7—16.
Parsons, M. W., and G. P. Munkvold, 2010a: Associations of planting
date, drought stress, and insects with Fusarium ear rot and
fumonisin B1 contamination in California maize. Food Addit.
Contam. Part A 27, 591—607.
Parsons, M. W., and G. P. Munkvold, 2010b: Relationships of
immature and adult thrips with silk-cut, Fusarium ear rot and
fumonisin B-1 contamination of maize in California and Hawaii.
Plant. Pathol. 59, 1099—1106.

18
Pascale, M., A. Visconti, M. Pronczuk, H. Wisniewska, and
J. Chelkowski, 1997: Accumulation of fumonisins in maize hybrids
inoculated under ﬁeld conditions with Fusarium moniliforme Sheldon. J. Sci. Food Agric. 74, 1—6.
Pascale, M., A. Visconti, and J. Chelkowski, 2002: Ear rot susceptibility and mycotoxin contamination of maize hybrids inoculated
with Fusarium species under ﬁeld conditions. Eur. J. Plant Pathol.
108, 645—651.
Pastircˇa´k, M., M. Lemmens, and A. Sˇroba´rova´, 2010: Resistance of
maize hybrids to ear rot. In: A´. Mesterha´zy (ed.), Workshop for
Variety Registration in Cereals for Fusarium Resistance, 34—35.
March 23–24, 2010, Szeged, Hungary.
Pauls, P., J. Taylor, G. Sun, M. William, J. Liu, K. Kasha, and L. M.
Reid, 2001: Identiﬁcation of molecular markers for resistance to
Fusarium graminearum in maize. Canadian Workshop on Fusarium
Head Blight, 4—6. Ottawa.
Perez-Brito, D., D. Jeﬀers, D. Gonzalez-de-Leon, M. Khairallah, and
M. Cortes-Cruz, 2001: QTL mapping of Fusarium moniliforme earrot resistance in highland maize, Mexico. Agrosciencia 35, 181—196.
Perkowski, J., M. Pronczuk, and J. Chelkowski, 1997: Deoxynivalenol

and acetyldeoxyniva-lenol accumulation in ﬁeld maize inoculated by
F. graminearum. J. Phytopathol. 145, 113—116.
Pestka, J. J., and G. S. Bondy, 1994: Immunotoxic effects of
mycotoxins. In: J. D. Miller, and H. L. Trenholm (eds), Mycotoxins
in Grain: Compounds other than Aﬂatoxin, 339—358. The American Phytopathological Society, St. Paul, MN.
Plienegger, J., and M. Lemmens, 2002: Kolbenfaăule Gibt es
Sortenunterschiede? Mais 30, 9597.
Prelusky, D. B., B. A. Rotter, and R. G. Rotter, 1994: Toxicology of
mycotoxins. In: J. D. Miller, and H. L. Trenholm (eds), Mycotoxins
in Grain: Compounds other than Aﬂatoxin, 359—403. The American Phytopathological Society, St. Paul, MN.
Presello, D. A., L. M. Reid, and D. E. Mather, 2004: Resistance of
Argentine maize germplasm to Gibberella and Fusarium ear rots.
Maydica 49, 73—81.
Presello, D. A., L. M. Reid, G. Butler, and D. E. Mather, 2005:
Pedigree selection for Gibberella ear rot resistance in maize
populations. Euphytica 143, 1—8.
Presello, D. A., J. Iglesias, G. Botta, L. M. Reid, G. A. Lori, and G. H.
Eyherabide, 2006: Stability of maize resistance to the ear rots caused
by Fusarium graminearum and F. verticillioides in Argentinean and
Canadian environments. Euphytica 147, 403—407.
Presello, D. A., G. Botta, J. Iglesias, and G. H. Eyherabide, 2008:
Effect of disease severity on yield and grain fumonisin concentration
of maize hybrids inoculated with Fusarium verticillioides. Crop Prot.
27, 572—576.
Presello, D. A., A. O., Pereyra., J. Iglesias, C. M. Fauguel, D. A.
Sampietro, and G. H. Eyhe´rabide, 2011: Responses to selection of
S5 inbreds for broad-based resistance to ear rots and grain
mycotoxin contamination caused by Fusarium spp. in maize.
Euphytica, 178, 23—29.
Reid, L. M. 1999: Breeding for resistance to ear rot in corn. Canadian

Workshop on Fusarium Head Blight (Colloque Canadien Sur La
Fusariose), 66–68. November 28–30, 1999, Holiday Inn Crown
Plaza Winnipeg, Manitoba.
Reid, L. M., and R. I. Hamilton, 1996: Effects of inoculation position,
timing, macroconidial concentration, and irrigation on resistance of
maize to Fusarium graminearum infection through kernels. Can. J.
Plant Pathol. 18, 279—285.
Reid, L. M., and R. C. Sinha, 1998: Maize maturity and the
development of Gibberella ear rot symptoms and deoxynivalenol
after inoculation. Eur. J. Plant Pathol. 104, 147—154.
Reid, L. M., A. T. Bolton, R. I. Hamilton, T. Woldemariam, and D. E.
Mather, 1992a: Effect of silk age on resistance of maize to Fusarium
graminearum. Can. J. Plant Pathol. 14, 293—298.
Reid, L. M., R. I. Hamilton, and A. T. Bolton, 1992b: Diallel analysis
of resistance in maize to Fusarium graminearum infection via the silk.
Can. J. Plant Sci. 2, 915—923.

´ . M e s t e r h a´ z y , M . L e m m e n s and L . M . R e i d
A
Reid, L. M., D. Spaner, D. E. Mather, A. T. Bolton, and R. I.
Hamilton, 1993: Resistance of maize hybrids and inbreds following
silk inoculation with three isolates of Fusarium graminearum. Plant
Dis. 77, 1248—1251.
Reid, L. M., R. E. Hamilton, and D. E. Mather, 1996a: Screening
Maize for Resistance to Gibberella Ear Rot. Publication 1996–5E,
Agriculture and Agri-Food Canada, Technical Bulletin, Ottawa,
ON, Canada, 62 pp.
Reid, L. M., D. W. Stewart, and R. I. Hamilton, 1996b: A 4-year study
of the association between Gibberella ear rot severity and deoxynivalenol concentration. J. Phytopathol. – Phytopathologische
Zeitschrift 144, 431—436.

Reid, L. M., R. W. Nicol, T. Ouellet, M. Savard, J. D. Miller, J. C.
Young, D. W. Stewart, and A. W. Schaafsma, 1999: Interaction of
Fusarium graminearum and F. moniliforme in maize ears: disease
progress, fungal biomass, and mycotoxin accumulation. Phytopathology 89, 1028—1037.
Reid, L. M., X. Zhu, M. E. Savard, R. C. Sinha, and B. Vigier, 2000: Preharvest accumulation of deoxynivalenol in sweet corn ears inoculated
with Fusarium graminearum. Food Addit. Contam. A 17, 689—701.
Reid, L. M., G. McDiarmid, A. J. Parker, T. Woldemariam, and R. I.
Hamilton, 2001a: CO388 and CO389 corn inbred lines. Can. J. Plant
Sci. 81, 457—459.
Reid, L. M., G. McDiarmid, A. J. Parker, T. Woldemariam, and R. I.
Hamilton, 2001b: CO430, CO431 and CO432 corn inbred lines. Can.
J. Plant Sci. 81, 283—284.
Reid, L. M., T. Woldemariam, X. Zhu, D. W. Stewart, and A. W.
Schaafsma, 2002: Effect of inoculation time and point of entry on
disease severity in Fusarium graminearum, Fusarium verticillioides, or
Fusarium subglutinans inoculated maize ears. Can. J. Plant Pathol.
24, 162—167.
Reid, L. M., G. McDiarmid, A. J. Parker, and T. Woldemariam, 2003:
CO441 corn inbred line. Can. J. Plant Sci. 83, 79—80.
Reid, L. M., C. X. Zhu, C. A. Parker, and C. W. Yan, 2009: Increased
resistance to Ustilago zeae and Fusarium verticillioides in maize
inbred lines bred for Fusarium graminearum resistance. Euphytica
165, 567—578.
Reinprecht, Y., X. G. Wu, S. Yan, L. Labey, E. Dasilva, J. C. Martin,
and K. P. Pauls, 2008: A microarray-based approach for identifying
genes for resistance to Fusarium graminearum in maize (Zea mays
L.). Cereal Res. Commun. 36(Suppl B), 253—259.
Robertson, L. A., C. E. Kleinschmidt, D. G. White, G. A. Payne, C.
M. Maragos, and J. B. Holland, 2006: Heritabilities and correlations
of Fusarium ear rot resistance and fumonisin contamination

resistance in two maize populations. Crop Sci. 46, 353—361. and
Erratum, 1420.
Robertson-Hoyt, L. A., M. P. Jines, P. J. Balint-Kurti, C. E.
Kleinschmidt, D. G. White, G. A. Payne, C. M. Maragos, T. L.
Molnar, and J. B. Holland, 2006c: QTL mapping for Fusarium ear
rot and fumonisin contamination resistance in two maize populations. Crop Sci. 46, 1734—1743.
Robertson-Hoyt, L. A., C. E. Kleinschmidt, D. G. White, G. A.
Payne, C. M. Maragos, and J. B. Holland, 2007a: Relationships of
resistance to Fusarium ear rot and fumonisin contamination with
agronomic performance of maize. Crop Sci. 47, 1770—1778.
Robertson-Hoyt, L. A., J. Betra´n, G. A. Payne, D. G. White, T.
Isakeit, C. M. Maragos, T. L. Molna´r, and J. B. Holland, 2007b:
Relationships among resistances to Fusarium and Aspergillus ear
rots and contamination by fumonisin and aﬂatoxin in maize.
Phytopathology 97, 311—317.
Sampietro, D. A., M. A. Vattuone, D. A. Presello, C. M. Fauguel, and
C. A. N. Catalan, 2009: The pericarp and its surface wax layer in
maize kernels as resistance factors to fumonisin accumulation by
Fusarium verticillioides. Crop Prot., 28, 196—200.
Sass, V., J. Milles, J. Kramer, and A. Prange, 2007: Competitive
interactions of Fusarium graminearum and Alternaria alternata in
vitro in relation to deoxynivalenol and zearalenone production. J.
Food Agric. Environ. 5, 257—261.

Breeding for resistance to ear rots
Schaafsma, A. W., R. W. Nicol, and L. M. Reid, 1997: Evaluating
commercial maize hybrids for resistance to Gibberella ear rot. Eur.
J. Plant Pathol. 103, 737—746.
Schjoth, J. E., A. M. Tronsmo, and L. Sundheim, 2008: Resistance

to Fusarium verticillioides in 20 Zambian maize hybrids.
J. Phytopathol. 156, 470—479.
Schjoth, J. E., A. Visconti, and L. Sundheim, 2009: Fumonisins in
maize in relation to climate, planting time and hybrids in two
agroecological zones in Zambia. Mycopathologia 167, 209—219.
Seifert, K. A., T. Auki, R. Baayen, D. Brayford, L. W. Burgess, S.
Chulze, A. Gams, D. Geiser, J. de Gruyter, J. Leslie, A. Logrieco,
W. F. O. Marasas, H. Nirenberg, K. OÕDonnell, J. Rheeder, G. J.
Samuels, B. A. Summerell, U. Thrane, and C. Waalwijk, 2004: The
name Fusarium moniliforme should no longer be used. Mycol. Res.
107, 643—644.
Sekhon, R. S., G. Kuldau, M. Mansﬁeld, and S. Chopra, 2006:
Characterization of Fusarium-induced expression of ﬂavonoids and
PR genes in maize. Physiol. Mol. Plant Pathol. 69, 109—117.
Silva, E., E. A. Mora, A. Medina, J. Vasquez, D. Valdez, D. L. Danial,
and J. E. Parlevliet, 2007: Fusarium ear rot and how to screen for
resistance in open pollinated maize in the Andean regions. Euphytica 153, 329—337.
Snijders, C. H. A., and F. A. van Eeuwijk, 1991: Genotype-strain
interactions for resistance to Fusarium head blight caused by Fusarium
culmorum in winter wheat. Theor. Appl. Genet. 81, 239—244.
Sprague, G. F., 1977: Corn and Corn Improvement. No. 18. in the
series Agronomy, American Society of Agronomy, Inc. Publisher,
Madison, WI, USA, 774 pp.
Sutton, J. C., 1982: Epidemiology of wheat head blight and maize ear
rot caused by Fusarium graminearum. Can. J. Plant Pathol. 4,
195—209.
Sutton, J. C., and W. Baliko, 1981: Methods for quantifying resistance
to Gibberella zeae in maize ears. Can. J. Plant Pathol. 3, 26—32.
Szu
}ts, P., A´. Mesterha´zy, G. Falkay, and T. Barto´k, 1997: Early

telarche symptoms in children and their relations to zearalenone
contamination in foodstuffs. Cereal Res. Commun. 25, 429—436.
Takegami, S., and K. Sasai, 1970: Investigations on resistance of wheat
varieties to Gibberella zeae after particular inoculation techniques.
X. Experiments on improved inoculation methods involving conidiospores and hyphae. Proc. Crop. Sci. Soc. Jpn., 39, 1—6.
Tanaka, T., A. Hasegawa, S. Yamamoto, U.-S. Lee, Y. Surgiura, and
Y. Ueno, 1988: Worldwide contamination of cereals by the
Fusarium mycotoxins nivalenol, deoxynivalenol, and zearalenone.
1. Survey of 19 countries. J. Agric. Food. Chem. 36, 979—983.
Toldi, E., T. Barto´k, M. Varga, A. Szekeres, B. To´th, and
A´. Mesterha´zy, 2008: The role of breeding in reducing mycotoxin
contamination in corn. Cereal Res. Commun. 36(Suppl B), 175—177.
Ullstrup, A. J., 1953: Several Ear Rots of Corn. U.S. Department of
Agriculture Y. B., the headquarter of USDA research center,
Beltsville, USDA. 390—392.
Ullstrup, A. J., 1970: Methods of inoculating corn ears with Gibberella
zeae and Diplodia maydis. Plant Dis. Reporter 54, 658—662.
Ullstrup, A. J., 1977: Corn diseases. In: G. F. Sprague (ed.), Corn and
Corn Improvement, 391—500. No. 18. in the series AGRONOMY.
American Society of Agronomy, Inc. Publisher, Madison, WI, USA.
774 pp.
Vesonder, R. F., A. Ciegler, H. R. Burmeister, and A. H. Jensen, 1979:
Acceptance by swine and rats of corn amended with trichothecenes.
Appl. Environ. Microbiol. 38, 344—346.

19
Vesonder, R. F., J. Ellis, and W. K. Rohwedder, 1981: Elaboration of
vomitoxin and zearalenone by Fusarium isolates and the biological
activity of Fusarium-produced toxins. Appl. Environ. Microbiol. 42,
1132—1134.

Vigier, B., L. M. Reid, L. M. Dwyer, D. W. Stewart, R. C. Sinha, J. T.
Arnason, and G. Butler, 2001: Maize resistance to Gibberella ear
rot: symptoms, deoxynivalenol, and yield. Can. J. Plant Pathol. 23,
99—105.
Voss, K. A., J. B. Gelineau-van Waes, and R. T. Riley, 2006:
Fumonisins: current research trends in developmental toxicology.
Mycotoxin Res. 22, 61—69.
Waalwijk, C., R. van der Heide, I. de Vries, T. van der Lee, C. Schoen,
G. Costrel-de Corainville, I. Hauser-Hahn, P. Kastelein, J. Kohl, P.
Lonnet, T. Demarquet, and G. H. J. Kema, 2004: Quantitative
detection of Fusarium species in wheat using TaqMan. Eur. J. Plant
Pathol. 110, 481—494.
Warﬁeld, C. Y., and R. M. Davis, 1996: Importance of husk covering
on the susceptibility of corn hybrids to Fusarium ear rot. Plant Dis.,
80, 208—210.
White, D. G., 1999: Compendium of Corn Diseases, 3rd edn. APS
Press, St. Paul, MN, ISBN 978-0-89054-234-7, 128 pages.
Wilde, F., V. Korzun, E. Ebmeyer, H. H. Geiger, and T. Miedaner,
2007: Comparison of phenotypic and marker-based selection for
Fusarium head blight resistance and DON content in spring wheat.
Mol. Breed. 19, 357—370.
Williams, W. P., 2006: Breeding for resistance to aﬂatoxin accumulation in maize. Mycotoxin Res. 22, 27—32.
Williams, W. P., and G. L. Windham, 2009: Diallel analysis of
fumonisin accumulation in maize. Field Crops Res. 114, 324—326.
Wu, F., 2006: Mycotoxin reduction in Bt corn: potential economic,
health, and regulatory impacts. Transgenic Res. 15, 277—289.
Xiang, K., L. M. Reid, and X. Zhu. 2010a: Relationship among kernel
drydown rates, environmental factors and resistance to Gibberella
ear rot, Fusarium ear rot and common smut of corn. Joint Annual
Meeting of the Canadian Phytopathological Society and the Paciﬁc

Division of the American Phytopathological Society, June 19–23,
Vancouver, BC.
Xiang, K., Z. M. Zhang, L. M. Reid, X. Y. Zhu, G. S. Yuan, and G. T.
Pan, 2010b: A meta-analysis of QTL associated with ear rot
resistance in maize. Maydica 55, 281—290.
Xu, X.-M., D. W., Parry., P. Nicholson, M. A. Thomsett, D. Simpson,
S. G. Edwards, B. M. Cooke, F. M. Doohan, S. Monaghan, A.
Moretti, G. Tocco, G. Mule, L. Hornok, E. Be´ki, J. Tatnell, and A.
Ritieni, 2008: Within-ﬁeld variability of Fusarium head blight
pathogens and their associated mycotoxins. Eur. J. Plant Pathol.
120, 21—34.
Young, H. C., Jr, 1943: The toothpick method of inoculating corn for
ear and stalk rots. Phytopathology 33, 16. (Abstr.)
Yuan, J., M. Liakat Ali, J. Taylor, J. Liu, G. Sun, W. Liu, P.
Masilimany, A. Gulati-Sakhuja, and K. P. Pauls, 2008: A guanylyl
cyclase-like gene is associated with Gibberella ear rot resistance in
maize (Zea mays L.). Theor. Appl. Genet. 116, 465—479.
Zhang, Y., Y.-E. Choi, X. Zou, and J.-R. Xu, 2011: The FvMK1
mitogen-activated protein kinase gene regulates conidiation, pathogenesis, and fumonisin production in Fusarium verticillioides.
Fungal Genet. Biol. 48, 71—79.

14 breeding for resistance to ear rots caused by

Tài liệu liên quan

Tài liệu bạn tìm kiếm đã sẵn sàng tải về