1

Tropical Plant Pathology 39 (1) January - February 2014

Tropical Plant Pathology, vol. 39(1):001-018, 2014
Copyright by the Brazilian Phytopathological Society.
www.sbfto.com.br
REVIEW ARTICLE
Interactions between foliar diseases: Concepts and
epidemiological approaches
Waldir C. Jesus Junior
1
, Trazilbo J. Paula Jnior
2
, Miller S. Lehner
3
& Bernhard Hau
4
1
Departamento de Produo Vegetal, Universidade Federal do Esprito Santo, 29500-000, Alegre, ES, Brazil;
2
EPAMIG,
Vila Gianetti 47, 36570-900, Viosa, MG, Brazil;
3
Programa de Ps-graduao em Gentica e Melhoramento, Universidade
Federal de Viosa, 36570-900, Viosa, MG, Brazil;
4
Institut fr Pfanzenkrankheiten und Pfanzenschutz, Leibniz Universitt
Hannover, Herrenhuser Str. 2, 30419, Hannover, Germany
Author for correspondence: Waldir C. Jesus Junior, e-mail: wcintra@cca.ufes.br
ABSTRACT
This review deals with the phenomenon of plant disease interactions. The epidemiological implications of foliar diseases occurring
simultaneously on the same crop are important because the establishment of disease management strategies depends on the knowledge of
disease interactions. We discuss some concepts and the terminology related to the interaction studies and present related examples with
special emphasis on interacting wheat diseases.
Key words: crop loss, disease dynamics, multiple diseases.
INTRODUCTION
The occurrence of two or more pathogens
simultaneously on the same host is frequent in many
production systems (Zadoks & Schein, 1979; Kranz & Jrg,
1989). This situation may be even more recurrent in many
tropical areas, where environmental conditions are mostly
favourable to the occurrence of diseases during all periods
of the year. Little is known about the combined effects
of diseases on crop yield and only a few epidemiological
studies on this subject have been carried out. Estimates of
disease effects on yield are usually made assuming that
each disease acts independently. Interactions of diseases
can increase crop damage and complicate the identifcation
of primary causes of diseases and their control. The
interactions may alter the occurrence and speed of
epidemics. Weber et al. (1994), for instance, concluded for
the two wheat pathogens Septoria nodorum and Erysiphe
graminis that wherever the two pathogens occur together,
neither their dynamics, nor the infuence of external factors
could be understood, if interspecifc interactions are
neglected. Interactions may have signifcant implications
for assessing crop losses, diagnosing the causes of these
losses and for selecting appropriate management strategies,
as well as for forecasting, modelling and simulations of
epidemics (Waller & Bridge, 1984; Bassanezi et al., 1998).
Estimates of yield losses caused by several diseases made
by adding of single disease yield-loss models are likely
to be inaccurate if interactions are occurring (Zhou et al.,
2000). Interactions may be important because the expected
beneft from the control of one pathogen depends on the
level of the other pathogens (Johnson et al., 1986) and
therefore multiple diseases can signifcantly alter economic
decision criteria in comparison to single disease occurrence
(Pinnschmidt, 1991). According to Newton et al., (2010),
new approaches in agronomy, crop protection and breeding
could be achieved by understanding the population dynamic
balance between the organisms of the phyllosphere as an
ecological system.
The objectives of studies in multiple-disease
situations usually can be divided into understanding (i)
the population dynamics of interacting diseases and (ii)
the combined effect on crop yield or yield loss. Once the
specifc effects of combined pathogens are understood,
the question shifts towards how to manage a crop grown
under combined infection conditions (Johnson, 1990). The
examples of interactions presented in literature are mainly
dealing with their effects on yield. Epidemiological aspects
of these interactions in terms of changes in the component
analysis have rarely been studied (Zadoks & Schein, 1979;
Weber et al., 1994). Here some aspects related to the
dynamics and to crop losses of the interactions between
diseases caused by aerial pathogens are discussed. The
discussion will be restricted to the relationships between
two or more aerial pathogens on the same host. Cross-
protection and biological control will be not emphasized,
although in these cases some kind of interactions can occur
between the organisms involved.
TERMINOLOGY
Terms like interaction, association, interference and
interrelationship have been used to describe relationships
among diseases. In many cases these terms are used in an
Tropical Plant Pathology 39 (1) January - February 2014 2
W.C. Jesus Junior et al.
improper manner (Wallace, 1983; Sikora & Carter, 1987).
According to Wallace (1983), the various etiological agents
can infuence each other in their effects on the plant; that is,
they interact. Consequently, the effect of the contribution
of different pathogens on the same host may not be purely
additive. As diseases can interact in their dynamics and/
or in their effects on crop loss, it is necessary to classify
the interactions for both aspects. Sometimes there is no
signifcant interaction between two diseases with respect to
yield, although one disease affects the development of the
other (Simkin & Wheeler, 1974). For a given combination
of pathogens, the type of interaction may change under
different conditions or during successive stages in their
life histories. Mixtures of synergistic and antagonistic
interactions, creating usually unpredictable biological and
epidemiological consequences, are likely to occur in plants,
as Syller (2012) observed for interacting viruses.
Interactions concerning the disease dynamics
Several terms have been proposed to qualitatively
describe interactions while quantitative methods seem to
be used scarcely. The interactions between two and more
diseases on a common host may produce antagonistic or
protective, mutually exclusive, additive, or synergistic
effects in the host (Damsteegt et al., 1993). An interaction
between different pathogens can be antagonistic or protective
when one inhibits or reduces the development of another
(Latch & Potter, 1977). A mutually exclusive interaction
occurs when the development of all involved pathogens
is reduced (Jedlinski & Brown, 1965). An interaction is
additive when the development of one pathogen is not
altered in the presence of another and vice versa (Gordon &
Schmitthenner, 1969). When there is some enhancement in
the development of one or more interacting pathogens, the
interaction is called synergistic (Beute, 1973).
In ecology, one population can infuence a second
one in different ways, whereby the effect can be positive
(+), negative (-) or neutral (0). On the other hand, the second
population can also affect the frst one. Odum (1953) defned
in an ecological sense that populations of two species may
interact theoretically in six basic ways, corresponding to the
six combinations of 0, +, and -, as follows: 00 (neutralism),
-- (competition), ++ (mutualism or protocooperation), +0
(commensalism), -0 (amensalism), and +- (parasitism or
predation). Although many types of direct effects of an
organism on another can occur, indirect effects through the
host plants seem to explain most of the cases of interacting
diseases (Waller & Bridge, 1984). Sometimes it is even
not clear whether there are any antagonistic or synergistic
effects of interacting pathogens, like with Alternaria porri
and Stemphylium vesicarium which often occur together
in the same purple leaf blotch lesion on Allium species
(Suheri & Price, 2000). In some cases the interactions
between two diseases may not be detectable due to clear
differences in time of disease onset or low disease levels,
like for anthracnose (Colletotrichum sublineolum) and leaf
blight (Exserohilum turcicum) on sorghum in Kenya (Ngugi
et al., 2000).
In situations involving the simultaneous occurrence
of aerial pathogens on the same plant, terms interactions
between diseases and interactions between pathogens
are practically similar. However, approaches involving this
subject should focus on the interactions between diseases,
since, in many cases, there are indirect effects mediated by
the host.
Interactions concerning crop losses
Similar to the defnition of interactions with respect
to disease dynamics, the interactions related to yield or
yield loss are termed in different ways although the terms
seem to be clearer. There are three outcomes of combined
effects of diseases on crop loss (Waller & Bridge, 1984):
the combined loss is equal to (no interaction, additive),
more than (greater-than-additive, synergistic, positive
interaction), or less than (less-than-additive, antagonistic,
negative interaction) the sum of yield losses from individual
diseases alone. According to the literature survey of Johnson
(1990), studies of the effects of multiple pest and diseases
on crop yield mostly report antagonistic interactions, which
may result from competition between pathogen populations
or from stimulation of active defence mechanisms in the
host. Reports of synergistic interactions are relatively
rare (Johnson, 1990). The synergistic interactions seem
to operate through effects on host resistance permitting
a pathological succession rather than by direct mutual
synergism of pathogens (Waller & Bridge, 1984).
EXAMPLES OF DISEASE INTERACTIONS
Some data concerning interactions between
aerial diseases are presented in the Tables 1, 2 and 3. In
some pathosystems, the determination of the type of
interaction concerning dynamics aspects and/or crop loss
is demonstrated. Criteria utilized to classify the interactions
in terms of dynamics and crop loss were made considering
three categories antagonistic, synergistic and additive
interactions.
It is important to emphasized that two plant
pathogens can interact as antagonists in vitro, however
the diseases as a result of their infections on the same host
can present an additive effect. Thus, it is not appropriate to
do generalizations.
CASE STUDY: RESULTS OBTAINED FROM
PUBLISHED STUDIES ON WHEAT DISEASES
Most of the cases of interaction between foliar diseases
reported in the literature is related to wheat. This crop can
be infected by many pathogens singly or simultaneously.
Although wheat is a crop of temperate regions, it has been
cultivated in many tropical areas, which may contribute to
increase the frequency of interaction cases. In Brazil, for
3
Tropical Plant Pathology 39 (1) January - February 2014
Interactions between foliar diseases: Concepts and epidemiological approaches
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9
Tropical Plant Pathology 39 (1) January - February 2014
Interactions between foliar diseases: Concepts and epidemiological approaches
example, wheat is being introduced gradually in the cerrado
areas usually under irrigation, which may be favourable to
the infection by foliar pathogens.
Different parts of the wheat plant can be infected
by different pathogens at the same time (Bonfg-Picard &
Kranz, 1984). These pathogens can naturally interact with
each other. Interactions between diseases caused by aerial
pathogens on wheat have frequently been demonstrated,
mainly with respect to the dynamics of the pathogens.
However, even for wheat, the crop that receives the most
attention regarding interactions among diseases, there
are little multi-disease studies concerning management
or epidemiological approaches. Moreover, the observed
effects of reported interactions (for instance synergism,
antagonism or additive effect) are highly dependent on
inoculum concentration, disease levels (Jrg, 1987; Weber et
al., 1994), pre-infection by one of the interacting pathogens
(Donchev et al., 1980), and climatic conditions (Weber et
al., 1994). Cox et al. (2004) have demonstrated the potential
of cultivar mixtures for the simultaneous management of
tan spot (Pyrenophora tritici-repentis) and leaf rust of
wheat (Puccinia triticina).
Johnston (1934) observed that uredospores of
Puccinia recondita f. sp. tritici could develop on normally
resistant varieties of wheat when the leaves were infected
with Erysiphe graminis f. sp. tritici before the rust
inoculation. Similarly, Manners & Gandy (1954) reported
higher susceptibility to P. recondita of some wheat varieties
infected with mildew. However, when mildew severity was
high, the rust development was limited. On the other hand,
the severity of mildew was signifcantly reduced on wheat
plants previously inoculated with P. recondita, maybe due to
biochemical changes in the plants (Donchev et al., 1980).
In many studies, it has been demonstrated that one
pathogen is promoted by another. Plants infected with
Tilletia caries are more susceptible to P. striiformis (Straib,
1938). In the presence of Ustilago nuda, the damage by P.
graminis f. sp. tritici is higher (Hart, 1931 cited by Straib,
1938, Thomas & Chatarth, 1976). Raju et al. (1969) found
that the number of pustules of P. recondita was increased
in the presence of wheat streak mosaic virus (WSMV). In
the same way, the number and the size of lesions caused
by Helminthosporium sativum was higher when the plants
were infected by WSMV (Adlakha & Raychaudhuri, 1975).
Wainwright et al., (1986) observed that S. nodorum caused
more damage than T. caries. According to Willingale &
Mantle (1987) it was evident in the interaction involving
Claviceps purpurea and T. caries that invasion by C.
purpurea was essentially a displacement phenomenon,
which characterize C. purpurea parasitism of healthy
ovaries. The establishment of the sphacelium and subsequent
differentiation to sclerotial tissue was more rapid in bunted
rather than non-bunted ovaries.
One pathogen can also inhibit the development of
another. Damage caused by Urocystis agropyri is reduced
in the presence of T. controversa (Holton & Jackson, 1951).
The severity of Helminthosporium blight (H. sativum) was
lower in plants infected with U. nuda (Thomas & Chatarth,
1976). Jones & Roane (1982) found that Xanthomonas
campestris pv. undulosa reduced germination and the
length of germinative tube of spores of S. nodorum. Potter
(1982) observed that, in plants infected with barley yellow
dwarf virus (BYDV), the severity of P. recondita was lower,
although the latent period was not affected. When infected
with both BYDV and rust, yield was reduced by 63%.
Erasmus & Von Wechmar (1983) observed that wheat plants
with brome mosaic virus (BMV) were found less susceptible
to P. graminis f. sp. tritici infection than virus-free plants.
Adee et al. (1990) found that competition occurred between
Pyrenophora tritici-repentis and S. nodorum. Sporulation by
Puccinia triticina was reduced substantially by the presence
of Pyrenophora tritici-repentis; in contrast, the presence
of Puccinia triticina sometimes increased sporulation of
Pyrenophora tritici-repentis (Al-Naimi, 2003).
No interaction was observed for the combinations
P. striiformis x U. agropyri (Purdy & Holton, 1963) and S.
nodorum x S. tritici (Jenkins & Jones, 1981). Hyde (1981)
observed no interaction for the combination S. nodorum x P.
striiformis regarding seed weights, although the proportion
of diseased leaves for the combination was less than the
sum of effects of each pathogen occurring alone. Jones et al.
(1981) observed that the apparent photosynthetic rate and
transpiration rate of fag leaves did not differ statistically in
the X. translucens f. sp. undulosa + S. nodorum treatment
compared with S. nodorum alone. At lower incubation
temperatures, combined inoculation had no effect compared
with inoculation with either organism alone.
Van der Wal et al. (1970) and Van der Wal & Cowan
(1974) observed synergistic effect on crop losses when they
studied the combination P. recondita x S. nodorum. Van der
Wal et al. (1970) observed also that on plants infected by P.
recondita, the intensity of glume blotch symptoms caused
by S. nodorum was greater than on not inoculated plants.
They observed also that, in the presence of S. nodorum,
the production of uredospores of P. recondita was reduced
while the production of teliospores was stimulated. The
loss caused by the interacting fungi is signifcantly larger
than the calculated sum of the losses caused by each
fungus alone. Wheat plants infected by P. recondita were
predisposed to infection by S. nodorum (Van der Wal &
Cowan, 1974). According to these authors the effect of
both pathogens together on the dry weight of the heads was
greater than the sum of the effects of each of the pathogen
separately. However, no interaction was observed when
the infection by S. nodorum occurred before P. recondita
infection (Hyde, 1978). Spadafora & Cole (1987) found an
inverse relationship between the severities of P. recondita
and S. nodorum.
Broscious et al. (1982) and Bonfg-Picard & Kranz
(1984) have observed a competition between populations
of S. nodorum and E. graminis f. sp. tritici. Geuting (1984)
found that in the presence of S. nodorum the number of
Tropical Plant Pathology 39 (1) January - February 2014 10
W.C. Jesus Junior et al.
mildew colonies was lower and the colonies were smaller
compared to the control plants. The number of conidia/
colony was also lower. The latent period of S. nodorum
was shortened in the presence of E. graminis f. sp. tritici.
Jrg (1987) confrmed under feld conditions the results
of Geuting (1984), although he found no infuence of E.
graminis on S. nodorum. The development of mildew was
inhibited in the presence of S. nodorum and the effect was
more pronounced at high severity of the diseases. Similarly
to Geuting (1984), Brokenshire (1974) observed reduced
latency duration of S. tritici in the presence of E. graminis.
Resistant plants were susceptible to S. tritici in the presence
of mildew. There was an inverse relationship, based on
individual replicate values, between the pre-inoculation
mildew treatments and the latent period of S. tritici, but a
signifcant positive correlation for the sporulation index. For
this combination, Madariaga & Scharen (1984) observed
that in the presence of S. tritici, the effect of P. striiformis
was always reduced by the presence of M. graminicola. The
two pathogens could colonize the same leaf simultaneously,
and the diseased area was similar or smaller than the area
affected by each pathogen separately. A smaller amount
of leaf tissue was colonized by P. striiformis when M.
graminicola was present. M. graminicola acted as a
hypostatic parasite.
Weber et al. (1994) observed that, in greenhouse,
S. nodorum reduced the severity of mildew. On the other
hand, under feld conditions, E. graminis increased the
fnal intensity of S. nodorum. The apparent contradiction
was explained as a result of different climatic conditions,
which allowed secondary infections of S. nodorum in the
feld. Based on the studies of Brokenshire (1974), Geuting
(1984) and Jrg (1987), Weber et al. (1994) concluded
that these pathogens couldnt strictly be described as
competitors sensu Odum (1953). The relation between E.
graminis and S. nodorum is better described, sensu Powell
(1979), as predisposition with dominance of the secondary
pathogen, with E. graminis as primary, and S. nodorum as
secondary pathogen (Jrg, 1987; Weber et al., 1994).
Tatineni et al. (2010) studied the double infection of
wheat cultivars with Triticum mosaic virus (TriMV), the type
member of the Poacevirus genus, and Wheat streak mosaic
virus (WSMV), the type member of the Tritimovirus genus,
both of the family Potyviridae. They found that double
infections in wheat cvs. Arapahoe and Tomahawk induced
disease synergism with severe leaf deformation, bleaching,
and stunting, with an increase in accumulation of both
viruses over single infections at 14 days post inoculation.
QUANTIFYING INTERACTIONS
Interactions in disease dynamics
As mentioned above, the interactions between
pathogens or diseases can be of various natures, for instance
characterised as competition, symbiosis, parasitism, etc.
Independent of the kind of interactions, the effect is refected
in changes of the disease progress curves compared to the
situation in which each disease is occurring alone. Some
research has been published showing the effect of the pre-
infection of one disease on a second disease. A detailed study
for this approach to interactions was presented by Bassanezi
et al. (1998) who investigated the effect of pre-infection
with Bean line pattern mosaic virus (BLPMV) on some
elements of Uromyces appendiculatus and Phaeoisariopsis
griseola over a wide range of temperatures. Other studies
have applied the de Wit replacement series technique to
investigate the outcome of competitive interactions between
two plant pathogens using the conidial production (Adee et
al., 1990; Nolan et al., 1999). In order to compare epidemics
of interacting diseases, the area under the disease progress
curve have been calculated and analysed using analyses of
variance (Savary & Zadoks, 1992a).
In many publications the disease dynamics of single
diseases is modelled, but only a few examples have been
published in which the progress of epidemics in a multiple
disease situation has been quantifed and modelled.
This approach will be discussed in more detail, starting
with the classical Lotka-Volterra competition model.
Madden et al. (1987) applied the classical Lotka-Volterra
competition equations to model the disease progress curves
of the disease incidence of tobacco etch virus (TEV) and
tobacco vein mottling virus (TVMV). The model is based
on the assumption that the disease progress curves are
logistic functions if one disease would be there alone. The
competition model is given by the following system of
differential equations for the disease severity or incidence
of two diseases y
1
and y
2
given as proportions with values
between 0 and 1:
dy
1
/dt = r
1
y
1
(1 - [y
1
+ a
12
y
2
] / K
1
)
(1)
dy
2
/dt = r
2
y
2
(1 - [y
2
+ a
21
y
1
] / K
2
)
The parameters r
1
and r
2
are the apparent infection
rates and K
1
and K
2
the maximum disease levels of both
diseases in absence of the other disease. The two parameters
a
12
and a
21
are the coeffcients of competition. The
coeffcient a
12
indicates the competitive effect of disease
2 on disease 1. The system of differential equations (eq. 1)
can be re-arranged to point out the mutual effects of the
diseases on each other:
dy
1
/dt = r
1
(1 - a
12
y
2
/ K
1
) y
1
(1 - y
1
/ [K
1
(1 - a
12
y
2
/ K
1
)])
(2)
dy
2
/dt = r
2
(1 - a
21
y
1
/ K
2
) y
2
(1 - y
2
/ [K
2
(1 - a
21
y
1
/ K
2
)])
The new system (eq. 2) clearly shows that the actual
apparent infection rate and the actual maximum disease
level of each disease are linearly decreasing with increasing
severity of the other disease. Moreover, the reducing effect
is identical to the rate and the capacity.
In the example of Madden et al. (1987) the dynamics
of two tobacco virus diseases TEV (Tobacco etch virus =
1) and TVMV (Tobacco vein mottling virus = 2) occurring
11
Tropical Plant Pathology 39 (1) January - February 2014
Interactions between foliar diseases: Concepts and epidemiological approaches
at the same time in tobacco felds were modelled. Disease
incidence progression was quantifed by ftting the Lotka-
Volterra equations (eq. 1), resulting in the following
parameters values for the data set in 1984 B without
insecticide usage: r
1
= 0.223/day, r
2
= 0.261/day, K
1
= 0.175,
K
2
= 1.00, a
12
= 0.06 and a
21
=1.67. From eq. 2 it can
be concluded that the actual rate and the maximum disease
level of TEV are reduced by 0.34% when the disease
incidence of TVMV increases 1%. The reduction of TVMV
is 1.67% per 1% increase of TEV. Due to the interaction
modelled as competition, the maximum disease levels of
both diseases are reduced.
Ngugi et al. (2001) used the Lotka-Volterra equations
(eq. 1) to simultaneously describe the disease progress
curves of sorghum anthracnose (caused by Colletotrichum
sublineolum) and leaf blight (caused by Exserohilum
turcicum). In most cases the competition coeffcients were
not signifcantly different from 0 so they concluded that
interactions between both diseases did not occur.
Although the Lotka-Volterra competition equations
have been successfully applied in these examples, the
general disease progression resulting from the model
may not refect interacting plant disease epidemics in a
real situation. The equations allow a decrease in disease
intensities, which is not possible without regarding changes
of the host plant. Even under adverse conditions to the
pathogen and the disease, the leaf area covered by disease
symptoms cannot decrease and thus the disease levels in the
worst case remain constant. Thus it is logical to demand that
in the Lotka-Volterra equations the changes of the disease
severity must be equal or greater than 0 (dy
1
/dt 0 and dy
2
/
dt 0). This can be achieved by introducing the maximum
function max(0; x) which is zero if x is below 0. The Lotka-
Volterra equations can then be replaced by the following
model:
dy
1
/dt = max(0; r
1
y
1
(1 - [y
1
+ a
12
y
2
] / K
1
))
(3)
dy
2
/dt = max(0; r
2
y
2
(1 - [y
2
+ a
21
y
1
] / K
2
))
It must be pointed out that this more biological
approach has a disadvantage as the equilibrium values of
the interacting diseases are not fxed, like in the original
Lotka-Volterra model, but depend on the initial disease
values.
Weber (1996) used this approach to describe disease
progress curves of wheat powdery mildew (E. graminis f.
sp. tritici) and leaf blotch disease (S. nodorum) and their
interactions. In addition to this change of the Lotka-Volterra
equations, he included a promoting effect as possible
interaction between diseases, thus going beyond a competition
model. For the interactions between E. graminis, a biotrophic
pathogen, and S. nodorum, a perthotrophic fungus (which
initiates infection as a biotroph but spends most of its life
cycle as a necrotroph), he assumed an inhibiting effect of S.
nodorum on E. graminis and a disease-promoting effect of
E. graminis on S. nodorum. This led to the following model
for the interactions between the diseases whereby y
M
and y
S

represent the disease severities (as proportions) of powdery
mildew and Septoria leaf blotch, respectively:
dy
M
/dt = max [0; r
M
y
M
(1 - y
M
/ K
M
- a
s
y
S
)] (4)
dy
S
/dt = r
S
y
S
(1 - y
S
/ K
S
+ a
M
y
M
)
Again, r
M
and r
S
are infection rates, K
M
and K
S
the
maximum severity levels of mildew and Septoria leaf blotch,
respectively, without mutual infuences. The interaction
term a
M
(> 0) gives the infuence of mildew on Septoria
disease, and the coeffcient a
s
(> 0) the infuence of Septoria
leaf blotch on mildew. Here the Septoria disease is modelled
adversely to mildew, as a competitor for infection places.
However, the effect of mildew is incorporated as a factor
delaying the density regulation of Septoria disease by the
positive of sign. The function max prevents a decline of the
mildew growth rate which can be biologically interpreted
as the exclusion of the overgrowing of mildew lesions by
Septoria leaf blotch.
To show the similarity to the Lotka-Volterra
equations, Webers system (eq. 4) can be re-arranged
resulting in the following equations (eq. 5):
dy
M
/dt = max {0; r
M
(1 - a
s
y
S
) y
M
(1 - y
M
/ [K
M
(1 - a
s
y
S
)])}
(5)
dy
S
/dt = r
S
(1 + a
M
y
M
) y
S
(1 - y
S
/ [K
S
(1 + a
M
y
M
)])
The effect of Septoria leaf blotch on mildew is
refected in the reduced infection rate as well as in the
decreased maximum disease level of mildew. On the other
side, increasing mildew severity raises the actual infection
rate and the maximum disease level of Septoria disease.
The relative changes of the rate and capacity parameter
values as a result of the interaction are identical, negative
for mildew, but positive for Septoria leaf blotch.
For data of disease progression in 1991, the following
parameter values were estimated by Weber (1996): r
M
= 0.2
/ day, r
S
= 0.19 / day, K
M
= 0.07, K
S
= 0.334, a
M
= 17.13
and a
S
= 4.32. Thus, an increase of Septoria disease by 1%
reduces the mildew parameter values by 4.32%, while a 1%
increase of mildew raises the Septoria parameter values by
17.13%. Simulated disease progress curves of both diseases
in 1991 are calculated according to the modifed Lotka-
Volterra equations (eq. 5) and under the assumption of no
disease interaction.
In a second model, Weber (1996) assumed that
mildew is not changing the maximum disease level of
Septoria leaf blotch so that the model can be written as:
dy
M
/dt = max {0; r
M
(1 - a
s
y
S
) y
M
(1 - y
M
/ [K
M
(1 - a
s
y
S
)])} (6)
dy
S
/dt = r
S
(1 + a
M
y
M
) y
S
(1 - y
S
/ K
S
)
In contrast to the previous interaction models, the
rate and capacity parameters are now not affected in the
same way, as the capacity of Septoria leaf blotch remains
unchanged in presence of powdery mildew. Weber (1996)
Tropical Plant Pathology 39 (1) January - February 2014 12
W.C. Jesus Junior et al.
also ftted this model to the data of disease progression in
1991 and determined the following parameter values: r
M
=
0.29 / day, r
S
= 0.14 / day, K
M
= 0.066, K
S
= 0.40, a
M
= 57.83
and a
S
= 3.29. When the disease incidence of Septoria leaf
blotch increases by 1%, the actual rate and the maximum
disease level of mildew are reduced by 3.29%. A 1%
increase of mildew increases the rate of Septoria disease by
57.83%, however, without changing the maximum disease
level of Septoria leaf blotch.
Following Webers approach by assuming that in an
interaction the rate and the capacity parameters are affected
in the same direction but to a different extent, a general
interaction model can be constructed:
dy
1
/dt = r
1
(1 - a
12
y
2
/ K
1
) y
1
(1 - y
1
/ [K
1
(1 - b
12
y
2
/ K
1
)]
(7)
dy
2
/dt = r
2
(1 - a
21
y
1
/ K
2
) y
2
(1 - y
2
/ [K
2
(1 - b
21
y
1
/ K
2
])
The model would be more fexible because of
additional parameters. The coeffcients a
ij
describe the
mutual effects on the rates and the b
ij
on the maximum
values. However, to our knowledge this approach has never
been tested in explaining disease dynamics.
The models discussed so far describe the
interactions of plant disease epidemics without taking into
consideration the host plant. Host growth, however, can
change the dynamic of diseases, leading for instance to a
decrease in disease severity if the host is growing faster
than the disease is progressing. Thus the host infuences
the disease dynamics. On the other hand, a disease
can affect host growth in different ways, as classifed
by Boote et al. (1983). The mutual effects of host and
diseases form another important interaction demanding
an additional equation in interaction models to account
for changes of the host plant. Waggoner (1986) and Jeger
(1986) have dealt with analytical models to describe the
dynamics of interacting host and disease. Hau & Meier
(1998) included the host dynamics when modelling the
progression of different leaf diseases (U. appendiculatus,
P. griseola and C. lindemuthianum) on Phaseolus beans.
The coupling of pest and disease models with crop growth
models forms an essential element in understanding the
interactions among diseases and between diseases and host
plants, especially with respect to the combined yield losses
caused by several diseases (Boote et al., 1983; Rouse, 1988;
Basse et al., 2000).
Interactions of diseases on yield or yield loss
Compared to the quantifcation of interactions on
the epidemic level, more information is available on the
combined effect of multiple attacks on yield loss. A good
example is the study of Johnson et al. (1986, 1987), in
which the yield reduction in potato caused by early blight
(A. solani), Verticillium wilt (Verticillium dahliae) and
potato leafhopper (Empoasca fabae) was investigated.
The principal conclusion from the feld studies was
that combined infestations resulted in yield and foliage
losses that were less than the sum of losses from solitary
infestations of each organism. In another study, Savary &
Zadoks (1992a, b, c) analysed the crop losses of groundnut
due to a combined attack of rust (P. arachidis) and late
leaf spot (Cercosporidium personatum). The overall result
indicated that the effects of the two diseases on damage
were less than additive. Similarly, injuries caused by rice
pathogens, insects and weeds were less than additive in
their yield-reducing effects (Savary et al., 2000).
The effects of interacting pathogens on yield loss
have been modelled using multiple regression equations
(Savary & Zakoks, 1992a; b), analysis of variance of
factorial designs (Johnson et al., 1986; 1987), discriminant
analysis (Francl et al., 1987), principal component analysis
(Savary et al., 2000) or correspondence analysis (Savary &
Zadoks, 1992c; Savary et al., 2000).
Empirical yield-loss equations for a complex
of diseases are often obtained via multiple regression
analyses with yield or yield loss as the dependent
variable. Disease parameters, used directly or after a
transformation, serve as independent variables. For two
diseases, the general equation for the total yield loss (YL)
predicted is given as:
YL = b
1
f
1
(y
1
) + b
2
f
2
(y
2
) + b
12
g(y
1
,y
2
)
The two disease parameters, y
1
and y
2
, could be disease
severities which can be transformed with the functions f
1

and f
2
. The coeffcients b
1
and b
2
are the respective damage
coeffcients for the transformed values of y
1
and y
2
. The
third term is the interaction term of the model depending on
the function g of both disease severities. If the coeffcient
b
12
is equal 0, the diseases reduce yield independent from
each other. For b
12
> 0 the total yield loss is higher than the
sum of the individual yield losses, for b
12
< 0 the effects of
y
1
and y
2
are less than additive.
If the disease parameters represent disease incidence
or disease severity at one time in the season, this equation
refects a so-called single point or critical point model.
The disease parameters could also be the areas under disease
progress curves (AUDPC). A special case of this equation
would be the well-known linear regression equation with an
interaction term involving the multiplication of the disease
parameters:
YL = b
1
y
1
+ b
2
y
2
+ b
12
y
1
y
2
For the application of this model as a critical point
model, the disease severities of both diseases at a certain
point in time of the season must be known. These disease
levels are a result of the dynamics of epidemics of the two
interacting diseases. Thus the understanding of interactions
of diseases with respect to their dynamics is a prerequisite
to understand their combined effect on yield loss.
For some diseases it has been shown that yield
or yield loss are not related to disease parameters, like
13
Tropical Plant Pathology 39 (1) January - February 2014
Interactions between foliar diseases: Concepts and epidemiological approaches
the disease severity in a critical stage or the area under
disease progress curve, for instance for angular leaf spot (P.
griseola) on Phaseolus beans (Bergamin Filho et al., 1997).
Therefore, it can be expected that an equation involving an
interaction term by multiplying disease severities may also
not be useful in predicting yield loss. Disease severity is
a relative measure, which doesnt contain information on
the total amount of leaf area. The latter, however, or other
host parameters like the area under leaf area progress curve
(AULAPC), may be strongly related to yield (Waggoner
& Berger, 1987). In such a case, useful predictions of
yield loss can only be achieved by realistic estimations
of the available leaf area. The dynamics of the leaf area
is infuenced by the disease progress, which in turn is
affected by the leaf area available for infection. Thus
without understanding the interactions between host
dynamics and progression of epidemics, no appropriate
yield loss prediction can be achieved. Consequently, crop
growth simulation models, coupled with disease models
have been applied to estimate crop losses (e.g. Johnson,
1992; Batchelor et al., 1993; Pinnschmidt & Teng, 1994;
Pinnschmidt, 1997) by identifying coupling points
as described by Boote et al. (1983). Teng & Johnson
(1988) pointed out that crop-pest models may be the
only realistic way to understand or predict the effects
of multiple pests on yield, but the application of this
approach is rather limited still today.
Zhang et al. (2006) analyzed the relationship
between winter wheat cultivar susceptibility to four main
fungal diseases (Septoria tritici blotch, brown rust, yellow
rust and powdery mildew), multiple disease systems,
and yield loss (YL) levels. According to authors fve
potential disease profles (PDP) were obtained. For all
fve PDP, cultivar susceptibility profles (CP) 1 and CP3
(susceptible to Septoria tritici blotch and brown rust)
consistently made a major contribution to YL, whereas
CP8 (most resistant to diseases) consistently contributed
little to YL. The impact of CP5 (high susceptibility to
Septoria tritici blotch and medium to high susceptibility
to yellow rust) on YL is higher among the cultivar
profles for PDP5 (with the occurrence of yellow rust and
Septoria tritici blotch) and also for PDP3 and PDP4 (no
yellow rust but high intensity of Septoria tritici blotch),
but is comparatively lower in the case of PDP1 and PDP2
(no yellow rust and nil to medium intensity of Septoria
tritici blotch). Authors concluded that these results could
be used to improve the disease module of an agronomic
model for wheat aimed at designing cultivar-crop
management combinations for a given environment and
cost/price ratio.
In a previous review (Paula Jnior et al. 2010), it
was discussed some aspects related to the epidemiology of
interactions among diseases and concluded that there are
only few studies that emphasize epidemiological aspects
and they are not merely descriptive. We also assumed
that although studies involving interactions between
diseases still remain quite new, it is obvious for many
pathosystems that signifcant progress in recommending
the implementation of appropriate strategies of disease
management can only be achieved by careful consideration
of all implications related to the interactions.
FINAL REMARKS
It is evident that the interactions of different
diseases occurring on one host are a very complex
phenomenon. Although effects of some disease
combinations on specifc hosts, like Septoria disease and
mildew on wheat, are known and intensively studied,
effects of interactions in general cannot be anticipated.
Nevertheless, it has been reported that combinations
involving obligate pathogens and viruses frequently result
in antagonism (Blumer et al., 1955; Wilson, 1958; Latch
& Potter, 1977; Potter, 1982; Erasmus & Von Wechmar,
1983; Omar et al., 1986; Conti et al., 1990; Zaiter et al.,
1990; Kutzner et al., 1993; Marte et al., 1993; Dalla Pria,
1994; Bassanezi et al., 1998). Conversely, combinations
involving non-obligate pathogens and viruses often
result in synergism (Hedges, 1944; 1946a; b; Panzer &
Nickeson, 1959; Crane & Calpouzos, 1969; Beute, 1973;
Beniwal & Gudauskas, 1974; Adlakha & Raychaudhuri,
1975; Stevens & Gudauskas, 1982; 1983; Omar et al.,
1986). For most combinations that may occur in the
nature, results will depend on several factors. Methods
of experimentation and assessment are important factors
in interpreting results in interactions studies (Hyde,
1981; Sikora & Carter, 1987), since sites and timing
of inoculations, level of infection, host age, and many
other host and pathogen characters may affect the disease
outcome (Hyde, 1981).
Disease development under glasshouse conditions
where environmental conditions may differ from those
prevalent in the feld can produce artifcial or forced
interactions. Normally the inoculum concentration,
temperature, nutrition, relative humidity, wetness and
others variables used in glasshouse experiments may not
occur in the feld or, if they occur, other interactions could
make the interpretation of the data diffcult. This review
emphasizes the necessity of studies at feld conditions to
understand possible interactions.
Interaction between foliar diseases is a subject
that should be not neglected in breeding programs,
especially in tropical regions. Investigations should
include inoculations of mixtures of inoculum from
different pathogens and incorporation of genes that
confer resistance to multiple pathogens.
ACKNOWLEDGEMENTS
W.C. Jesus Junior, T.J. Paula Jnior and M.S. Lehner
are supported by Conselho Nacional de Desenvolvimento
Cientfco e Tecnolgico - CNPq.
Tropical Plant Pathology 39 (1) January - February 2014 14
W.C. Jesus Junior et al.
REFERENCES
Adee SR, Pfender WF, Hartnett DC (1990) Competition between
Pyrenophora tritici-repentis and Septoria nodorum in the wheat leaf
as measured with the de Wit Replacement series. Phytopathology
80:1177-1182.
Adlakha KL, Raychaudhuri SP (1975) Interaction between
Helminthosporium sativum and mosaic streak virus. Zeitschrift fr
Pfazenkrankheiten und Pfanzenschutz 82:201-206.
Ahrens W (1981) Schadwirkung eines kombinierten Befalls des
echten Rbenmehltaus (Erysiphe betae) und der Virusvergilbung
an Zuckerrben bei unterschiedlicher Mehltauanflligkeit.
Zeitschrift fr Pfazenkrankheiten und Pfanzenschutz 88:221-
227.
Alves-Jnior M, Alfenas-Zerbini P, Andrade EC, Esposito DA,
Silva FN, Cruz ACF, Ventrella MC, Otoni WC, Zerbini FM (2009)
Synergism and negative interference during co-infection of tomato
and Nicotiana benthamiana with two bipartite begomoviruses.
Virology 387:257-266.
Al-Naimi FA (2003) The competitive interaction between
Pyrenophora tritici-repentis and Puccinia triticina. MS Thesis,
Kansas State University. Manhattan KS, USA.
Anjos JR, Jarlfors U, Ghabrial SA (1992) Soybean mosaic
potyvirus enhances the titer of two comoviruses in dually infected
soybean plants. Phytopathology 82:1022-1027.
Ataga AE, Epton HAS, Frost RR (1999) Interaction of virus-
infected celery and Septoria apiicola. Plant Pathology 48:620-
626.
Bassanezi RB, Amorim L, Bergamin Filho A, Hau B (1998)
Effects of bean line pattern mosaic virus on the monocyclic
components of rust and angular leaf spot of Phaseolus bean at
different temperatures. Plant Pathology 47:289-298.
Basu PK, Butter G (1988) Assessment of brown spot (Septoria
glycines) alone and in combination with bacterial blight
(Pseudomonas syringae pv. glycinea) on soybeans in a short-
season area. Canadian Journal of Plant Pathology 10:78-82.
Batchelor WD, Jones JW, Boote KJ, Pinnschmidt H (1993)
Extending the use of crop models to study pest damage. Transaction
of ASAE 36:1-8.
Basse C, Ney B, Tivoli B (2000) A simple model of pea (Pisum
sativum) growth affected by Mycosphaerella pinodes. Plant
Pathology 49:187-200.
Benival SPS, Gudauskas RT (1974) Maize dwarf mosaic virus
increases susceptibility of sorghum and corn to Helminthosporium
maydis race T. Phytopathology 64:1197-1201.
Bergamin Filho A, Carneiro SMTPG, Godoy CV, Amorim L,
Berger RD, Hau B (1997) Angular leaf spot of Phaseolus beans:
Relationships between disease, healthy leaf area, and yield.
Phytopathology 87:5056-515.
Bergstrom GC, Knavel DE, Kuc J (1982) Role of insect injury and
powdery mildew in the epidemiology of the gummy stem blight
disease of cucurbits. Plant Disease 66:683-686.
Beute MK (1973) Increased leaf exudation enhances Curvularia
leaf spot severity in virus-infected Gladiolus. Phytopathology
63:1204-1205.
Blaszczak W, Milchert M (1980) Pea reaction to cucumber mosaic
virus and bean yellow mosaic virus in greenhouse conditions.
Journal of Phytopathology 99:310-317.
Blumer S, Stalder L, Harder A (1955) ber die gegenseitigen
Beziehungen zwischen Gurkenmosaik und Gurkenmehltau.
Phytopathologische Zeitschrift 25:39-54.
Bonfg-Picard G, Kranz J (1984) Untersuchung ber
Wechselwirkungen von Schadorganismen im Agro-kosystem
Weizen. Journal of Plant Diseases and Protection 91:619-628.
Boote KJ, Jones JW, Mishoe JW, Berger RD (1983) Coupling
pests to crop growth simulators to predict yield reductions.
Phytopathology 73:1581-1587.
Brokenshire T (1974) Predisposition of wheat to Septoria
infection following attack by Erysiphe. Transactions of the British
Mycological Society 63:393-397.
Broscious SC, Frank JA, Cole Jr H (1982) Control of powdery
mildew on wheat and its subsequent effect on Septoria severity
and yield. Phytopathology 72:258.
Carneiro SMTPG (2000) Efeito da infeco conjunta de
Phaeoisariopsis griseola e Colletotrichum lindemuthianum
nos componentes de produo e nas variveis de rea foliar do
feijoeiro. PhD Thesis, Universidade de So Paulo. Piracicaba SP,
Brazil.
Catherall PL (1987) Effects of barley yellow dwarf and ryegrass
mosaic viruses alone and in combination on the productivity of
perennial and Italian ryegrasses. Plant Pathology 36:73-78.
Castillo-Urquiza GP, Maia FGM, Carvalho MG, Pinto CMF,
Zerbini FM (2006) Caracterizao de um isolado do Bean rugose
mosaic virus (BRMV) de Minas Gerais e estimativa de perdas
em feijoeiro em infeco simples ou em conjunto com o BCMV.
Fitopatologia Brasileira 31:455-461.
Cherif M, Rezgui S, Devaux P, Harrabi M (2007) Interaction
between Rhynchosporium secalis and Pyrenophora teres in the
feld and identifcation of genotypes with double resistance in a
doubled-haploid barley population. Journal of Phytopathology
155:90-96.
Cohen J, Loebenstein G, Spiegel S (1988) Infection of sweet
potato by cucumber mosaic virus depends on the presence of
sweet potato feathery mottle virus. Plant Disease 72:583-585.
Cole DL (1982) Interactions between Cercospora arachidicola
and Phoma arachidicola, and their effects on defoliation and
kernel yield of groundnut. Plant Pathology 31:355-362.
Conti GG, Bassi M, Carminucci D, Gatti L, Bocci AM (1990)
Preinoculation with tobacco necrosis virus enhances peroxidase
activity and lignifcation in cucumber, as a resistance response to
Sphaerotheca fuliginea. Journal of Phytopathology 128:191-202.
Cox CM, Garret KA, Bowden RL, Fritz AK, Dendy SP, Herr WF
(2004) Cultivar mixtures for the simultaneous management of
multiple diseases: Tan spot and leaf rust of wheat. Phytopathology
94:961-969.
Crane GL, Calpouzos L (1969) Synergism of Cercospora beticola
and beet yellows virus in killing sugar beet leaves. Phytopathology
59:1338-1339.
Dalla Pria M, Bianchini A, Souza EA (1994) Avaliao da resistncia
de dez cultivares de feijoeiro ao vrus do mosaico-em-desenho. In: 5
o

Seminrio sobre Pragas, Doenas e Plantas Daninhas do Feijoeiro,
Resumos... Piracicaba SP, Brazil. FEALQ. p. 22.
15
Tropical Plant Pathology 39 (1) January - February 2014
Interactions between foliar diseases: Concepts and epidemiological approaches
Damsteegt VD, Bonde MR, Hewings AD (1993) Interactions
between maize streak virus and downy mildew fungi in susceptible
maize cultivars. Plant Disease 77:390-392.
Donchev N, Mallinsky I, Iliev I (1980) Effect of leaf rust (Puccinia
recondita f. sp. tritici) on the development of powdery mildew
(Erysiphe graminis f. sp. tritici) on wheat. Cereal Rust Bulletin
7:11-15.
Erasmus DS, Von Wechmar MB (1983) Reduction of susceptibility
of wheat to stem rust (Puccinia graminis f. sp. tritici) by brome
mosaic virus. Plant Disease 67:1196-1198.
Faria JC, Hagedorn DJ (1986) A multiple inoculation technique
for selection of bean seedlings with resistance to three pathogens.
Fitopatologia Brasileira 11:535-542.
Finke ML, Coyne DP, Steadman JR (1986) The inheritance and
association of resistance to rust, common blight, plant habit and
foliar abnormalities in Phaseolus vulgaris L. Euphytica 35:969-
982.
Francl LJ, Madden LV, Rowe RC, Riedel RM (1987) Potato yield
loss prediction and discrimination using preplant population
densities of Verticillium dahliae and Pratylenchus penetrans.
Phytopathology 77:579-584.
Garca-Cano E, Resende RO, Fernndez-Muoz R, Moriones E
(2006) Synergistic interaction between Tomato chlorosis virus and
Tomato spotted wilt virus results in breakdown of resistance in tomato.
Phytopathology 96:1263-1269.
Geuting G (1984) Wechselwirkungen zwischen Septoria nodorum
und Erysiphe graminis f. sp. tritici auf Weizen. Mitteilungen aus der
Biologischen Bundesanstalt fr Land- und Forstwirtschaft. Berlin-
Dahlem 223:96.
Gil-Salas FM, Peters J, Boonham N, Cuadrado IM, Janssen D (2012)
Co-infection with Cucumber vein yellowing virus and Cucurbit
yellow stunting disorder virus leading to synergism in cucumber.
Plant Pathology 61:468-478.
Goodman RM, Ross F (1974) Enhancement by potato virus Y of
potato virus X synthesis in doubly infected tobacco depends of the
timing of invasion by the viruses. Virology 58:263-271.
Gordon DT, Schmitthenner AF (1969) Association of soybean
mosaic virus with tobacco ringspot virus in soybean bud blight.
Phytopathology 59:1028.
Graham JH, Devine TE, Hanson CH (1976) Occurrence and
interaction of three species of Colletotrichum on alfalfa in the mid-
Atlantic United States. Phytopathology 66:538-541.
Hamilton RI, Nichols C (1977) The infuence of bromegrass mosaic
virus on the replication of tobacco mosaic virus in Hordeum vulgare.
Phytopathology 67:484-489.
Harrison AL (1973) Control of peanut leaf rust alone or in combination
with Cercospora leaf spot. Phytopathology 63:668-673.
Hau B, Meier F (1998) Modelling the dynamics of simultaneously
occurring fungal leaf diseases and their interactions with host growth
and defoliation of Phaseolus beans. In: 7
th
International Congress of
Plant Pathology, Proceedings... Edinburgh Scotland. British Society
for Plant Pathology. p. 2.8.11.
Hedges F (1944) Association of Xanthomonas phaseoli and
the common bean mosaic virus, Marmor phaseoli: I. Effect on
pathogenicity of the seedborne infective agents. Phytopathology
34:662-693.
Hedges F (1946a) Association of Xanthomonas phaseoli and the
common bean mosaic virus, Marmor phaseoli: II. Dissociation studies
of X. phaseoli. Phytopathology 36:589-612.
Hedges F (1946b) Association of Xanthomonas phaseoli and the
common bean mosaic virus, Marmor phaseoli: III. The effect of
varying amounts of nitrogen on pathogenicity. Phytopathology
36:613-623.
Hobbs HA, Hartman GL, Wang Y, Hill CB, Bernard RL, Pedersen
WL, Domier LL (2003) Occurrence of seed coat mottling in soybean
plants inoculated with Bean pod mottle virus and Soybean mosaic
virus. Plant Disease 87:1333-1336.
Hoffmann K, Geske SM, Moyer JW (1998) Pathogenesis of tomato
spotted wilt virus in peanut plants dually infected with peanut mottle
virus. Plant Disease 82:610-614.
Hoffman-Wolf U, Mayee CD, Sarkar S (1990) Synergismus zwischen
Kartoffelvirus X und Kartoffelvirus Y: Mgliche Bedeutung der
Virusstmme. Zeitschrift fr Pfazenkrankheiten und Pfanzenschutz
97:168-186.
Holton CS, Jackson TL (1951) Varietal reaction to dwarf bunt and
fag smut, and the occurrence of both in the same wheat plant.
Phytopathology 41:1035-1037.
Hwang I, Lim SM (1992) Effects of individual and multiple infections
with three bacterial pathogens on disease severity and yield of
soybeans. Plant Disease 76:195-198.
Hyde PM (1978) A study of the effects on wheat of inoculation with
Puccinia recondita and Leptosphaeria nodorum, with respect to
possible interactions. Journal of Phytopathology 92:12-24.
Hyde PM (1981) The effects on wheat of inoculation with Puccinia
striiformis and Septoria nodorum with respect to possible interactions.
Journal of Phytopathology 100:111-120.
Jedlinski H, Brown CM (1965) Cross-protection and mutual exclusion
by three strains of barley yellow dwarf virus in Avena sativa. Virology
26:613-621.
Jeger MJ (1986) The potential of analytic compared with simulation
approaches to modelling in plant disease epidemiology. In: Leonard
KJ, Fry WE (Eds.) Plant Disease Epidemiology. Vol. 1. Population
Dynamics and Management. New York NY, USA. Macmillan
Publishing Co.
Jenkins PD, Jones DG (1981) The effects of dual inoculation of
wheat cultivars with Septoria tritici and Septoria nodorum. Journal of
Phytopathology 101:210-221.
Jesus Junior WC, Vale FXR, Coelho RR, Hau B, Zambolim L, Costa
LC, Bergamin Filho A (2001) Effects of angular leaf spot and rust on
yield loss of Phaseolus vulgaris. Phytopathology 91:1045-1053.
Johnson KB, Radcliffe EB, Teng PS (1986) Effect of interacting
populations of Alternaria solani, Verticillium dahliae, and the potato
leafhopper (Empoasca fabae) on potato yield. Phytopathology
76:1046-1052.
Johnson KB, Teng PS, Radcliffe EB (1987) Analysis of potato foliage
losses caused by interacting infestations of early blight, Verticillium
wilt, and the potato leafhopper; and the relationships to yield. Journal
of Plant Diseases and Protection 94:22-33.
Johnson KB (1990) Assessing multiple pest populations and their
effects on crop yield. In: IRRI. Crop Loss Assessment in Rice. Los
Banos The Philippines. IRRI. pp. 203-214.
Johnson KB (1992) Evaluation of a mechanistic model that describes
Tropical Plant Pathology 39 (1) January - February 2014 16
W.C. Jesus Junior et al.
potato crop losses caused by multiple pests. Phytopathology 82:363-
369.
Johnston CO (1934) The effect of mildew infection on the response
of wheat leaf tissues normally resistant to leaf rust. Phytopathology
24:1045-1046.
Jones JB, Roane CW, Wolf DD (1981) The effects of Septoria nodorum
and Xanthomonas translucens f. sp. undulosa on photosynthesis and
transpiration of wheat fag leaves. Phytopathology 71:1173-1177.
Jones JB, Roane CW (1982) Interaction of Xanthomonas campestris
pv. undulosa or Psedomonas cepacia with Septoria nodorum in vitro
and in vivo. Canadian Journal of Microbiology 28:205-210.
Jrg E (1987) Synkologische Untersuchungen ber Wechselwirkungen
im Agokosystemen Winterweizen. Ph.D. Dissertation, Universitt
Giessen. Giessen Germany.
Kiel K, Hau B (2000) Wechselwirkungen zwischen Blattpathogenen
(Uromyces appendiculatus und Colletotrichum lindemuthianum) an
der Phaseolus-Bohne. Mitteilung aus der Biologische Bundesanstalt
fr Land- und Forstwirtschaft 376:403.
Kiessling U, Hoffmann GM (1985a) Interaktionswirkungen zwischen
Erysiphe graminis f. sp. hordei und Puccinia hordei an Gerste unter
Bercksichtigung epidemiologischer Aspekte. Journal of Plant
Diseases and Protection 92:396-406.
Kiessling U, Hoffmann GM (1985b) Physiologische Effekte bei
Interaktionen zwischen Echtem Mehltau (Erysiphe graminis f. sp.
hordei) und Zwergrost (Puccinia hordei) an Gerste. Journal of Plant
Diseases and Protection 92:407-416.
Koning G, TeKrony DM, Ghabrial SA (2003) Soybean seedcoat
mottling: Association with Soybean mosaic virus and Phomopsis spp.
seed infection. Plant Disease 87:413-417.
Koning G, TeKrony DM, Pfeiffer TW, Ghabrial SA (2001) Infection
of soybean with Soybean mosaic virus increases susceptibility to
Phomopsis spp. seed infection. Crop Science 41:1850-1856.
Kranz J, Jrg E (1989) The synecological approach in plant disease
epidemiology. Review of Tropical Plant Pathology 6:27-38.
Kunwar IK, Singh T, Sinclair JB (1985) Histopathology of mixed
infections by Colletotrichum truncatum and Phomopsis spp. or
Cercospora sojina in soybean seeds. Phytopathology 75:489-492.
Kutzner B, Hellwald KH, Buchenauer H (1993) Systemic induction
of resistance in Phaseolus vulgaris L. to tobacco necrosis virus (TNV)
by Uromyces phaseoli (Pers.) Wint. Journal of Phytopathology 138:9-
20.
Latch GCM, Potter LR (1977) Interaction between crown rust
(Puccinia coronata) and two viruses of ryegrass. Annals of Applied
Biology 87:139-145.
Le May C, Potage G, Andrivon D, Tivoli B, Outreman Y (2009) Plant
disease complex: Antagonism and synergism between pathogens of
the Ascochyta blight complex on pea. Journal of Phytopathology
157:715-721.
Lim LG, Gaunt RE (1986a) The effect of powdery mildew (Erysiphe
graminis f. sp. hordei) and leaf rust (Puccinia hordei) on spring barley
in New Zealand. I. Apical development and yield potential. Plant
Pathology 35:54-60.
Lim LG, Gaunt RE (1986b) The effect of powdery mildew (Erysiphe
graminis f. sp. hordei) and leaf rust (Puccinia hordei) on spring barley
in New Zealand. II. Epidemic development, green leaf area and yield.
Plant Pathology 35:44-53.
Lopes DB, Berger RD (2001) The effects of rust and anthracnose on the
photosynthetic competence of diseased bean leaves. Phytopathology
91:212-220.
Madariaga RB, Scharen AL (1984) Interactions of Mycosphaerella
graminicola and Puccinia striiformis on wheat. Phytopathology
74:820.
Madden LV, Pirone TP, Raccah B (1987) Temporal analysis of two
viruses increasing in the same tobacco felds. Phytopathology 77:974-
980.
Madeira AC, Fryett KP, Rossall S, Clark JA (1993) Interaction
between Ascochyta fabae and Botrytis fabae. Mycological Research
97:1217-122.
Maino AL, Schroth MN, Vitanza VB (1974) Synergy between
Achromobacter sp. and Pseudomonas phaseolicola resulting in
increased disease. Phytopathology 64:277-283.
Manners JG, Gandy DG (1954) A study of the effect of mildew
infection on the reaction of wheat varieties to brown rust. Annals of
Applied Biology 23:271-301.
Marchoux G, Delecolle B, Selassie KG (1993) Systemic infection
of tobacco by pepper veinal mottle potyvirus (PVMV) depends on
the presence of potato virus Y (PVY). Journal of Phytopathology
137:283-292.
Marte M, Buonauro R, Della Torre G (1993) Induction of systemic
resistance to tobacco powdery mildew by tobacco mosaic virus,
tobacco necrosis virus or ethephon. Journal of Phytopathology
138:137-144.
Mascia T, Cillo F, Fanelli V, Finetti-Sialer MM, De Stradis A, Palukaitis
P, Gallitelli1 D (2010) Characterization of the interactions between
Cucumber mosaic virus and Potato virus Y in mixed infections in
tomato. Molecular Plant-Microbe Interactions 23:1514-1524.
Mndez-Lozano J, Torres-Pacheco I, Fauque CM, Rivera-Bustamante
RF (2003) Interactions between geminiviruses in a natural occurring
mixture: Pepper huasteco virus and Pepper golden mosaic virus.
Phytopathology 93:270-273.
Morris SC (1982) Synergism of Geotrichum candidum and Penicillium
digitatum in infected citrus fruit. Phytopathology 72:1336-1339.
Murphy JF, Kyle MM (1995) Alleviation of restricted systemic
spread of pepper mottle potyvirus in Capsicum annum cv. Avelar by
coinfection with a cucumovirus. Phytopathology 85:561-566.
Ngugi HK, Julian AM, King SB, Peacocke BJ (2000) Epidemiology
of sorghum anthracnose (Colletotrichum sublineolum) and leaf blight
(Exserohilum turcicum) in Kenya. Plant Pathology 49:129-140.
Ngugi HK, King SB, Holt J, Julian AM (2001) Simultaneous temporal
progress of sorghum anthracnose and leaf blight in crop mixtures with
disparate patterns. Phytopathology 91:720-729.
Nolan S, Cooke BM, Monahan FJ (1999) Studies on the interaction
between Septoria tritici and Stagonospora nodorum in wheat.
European Journal of Plant Pathology 105:917-925.
Odum EP (1953) Fundamentals of Ecology. Philadelphia PA, USA.
W. B. Saunders Co.
Omar SAM, Bailiss KW, Chapman GP, Mansfeld JW (1986) Effects
of virus infection of faba bean on subsequent infection by Uromyces
viciae-faba. Plant Pathology 35:535-543.
Pacheco R, Garca-Marcos A, Barajas D, Martiez J, Tenllado
F (2012) PVX-potyvirus synergistic infections differentially alter
17
Tropical Plant Pathology 39 (1) January - February 2014
Interactions between foliar diseases: Concepts and epidemiological approaches
microRNA accumulation in Nicotiana benthamiana. Virus Research
165:231-235.
Panzer JD, Nickeson RL (1959) Delayed synergism of bacterial blight
and bean mosaic on Phaseolus vulgaris L. Plant Disease Reporter
43:133-136.
Paula Jnior TJ, Jesus Junior WC, Morandi MAB, Bettiol W,
Vieira RF, Hau B (2010) Interactions between aerial and soil-borne
pathogens: mechanisms and epidemiological considerations. Pest
Technology 4:19-28.
Pearson MN, Cole JS (1991) Further observations on the effects of
Cymbidium mosaic virus and Odontoglossum ringspot virus on the
growth of Cymbidium orchids. Journal of Phytopathology 131:193-
198.
Pearson MN, Cole JS (1986) The effects of Cymbidium mosaic virus
and Odontoglossum ringspot virus on the growth of Cymbidium
orchids. Journal of Phytopathology 117:193-197.
Pinnschmidt HO, Teng PS (1994) Advances in modeling multiple
insect-disease-weed effects on rice and implications for research.
In: Teng PS, Heong KL, Moody K (Eds.) Rice Pest Science and
Management. Los Banos The Philippines. IRRI. pp. 101-128.
Pinnschmidt HO (1991) Effects of multiple pests on crop growth and
yield. Philippine Phytopathology 21:1-11.
Pinnschmidt HO (1997) Simulation of host-parasite dynamics, crop
loss, and effects of fungicide applications. In: Francl LJ, Neher DA
(Eds.) Exercises in Plant Disease Epidemiology. St. Paul MN, USA.
APS Press. pp. 166-174.
Pio-Ribeiro G, Wyatt SD, Kuhn CW (1978) Cowpea stunt: A disease
caused by a synergistic interaction of two viruses. Phytopathology
68:1260-1265.
Pohl D, Wege C (2007) Synergistic pathogenicity of a phloem-limited
begomovirus and tobamoviruses, despite negative interference.
Journal of General Virology 88:1034-1040.
Potter LR (1980) The effects of barley yellow dwarf virus and
powdery mildew in oats and barley with single and dual infections.
Annals of Applied Biology 94:11-17.
Potter LR (1982) Interaction between barley dwarf virus and rust
in wheat, barley and oats, and the effects on grain yield and quality.
Annals of Applied Biology 100:321-329.
Potter LR, Jones IT (1981) Interaction between barley yellow dwarf
virus and powdery mildew in four barley genotypes. Plant Pathology
30:133-139.
Powell NT (1979) Internal synergisms among organisms inducing
disease. In: Horsfall JG, Cowling EB (Eds.) Plant Disease. Vol. 4.
New York NY, USA. Academic Press. pp. 113-133.
Purdy LH, Holton CS (1963) Flag smut of wheat, its distribution
and existence with stripe rust in the Pacifc Northwest. Plant Disease
Reporter 47:516-518.
Quinones SS, Dunleavy JM, Fisher JW (1971) Performance of three
soybean varieties inoculated with soybean mosaic virus and bean pod
mottle virus. Crop Science 11:662-664.
Raju DG, Sill WH, Browder LE (1969) The combined effects of
two viral diseases and leaf rust on wheat. Phytopathology 59:1488-
1492.
Rodriguez-Alvarado G, Kurath G, Dodds JA (1994) Symptom
modifcation by satellite tobacco mosaic virus in pepper types
and cultivars infected with helper tobamoviruses. Phytopathology
84:617-621.
Ross JP (1968) Effect of single and double infections of soybean
mosaic and bean pod mottle viruses on soybean yield and seed
characters. Plant Disease Reporter 52:344-348.
Ross JP (1969) Effect of time and sequence of inoculation of soybeans
with soybean mosaic and bean pod mottle viruses on yield and seed
characters. Phytopathology 59:1404-1408.
Savary S, Zadoks JC (1992a) Analysis of crop loss in the multiple
pathosystem groundnut-rust-late leaf spot. I: Six experiments. Crop
Protection 11:99-109.
Savary S, Zadoks JC (1992b) Analysis of crop loss in the multiple
pathosystem groundnut-rust-late leaf spot. II: Study of the interactions
between diseases and crop intensifcation in factorial experiments.
Crop Protection 11:110-120.
Savary S, Zadoks JC (1992c) Analysis of crop loss in the multiple
pathosystem groundnut-rust-late leaf spot. III: Correspondence
analyses. Crop Protection 11:229-239.
Savary S, Willocquet L, Elazegui FA, Castilla NP, Teng PS (2000)
Rice pest constraints in tropical Asia: Quantifcation of yield losses
due to rice pests in a range of production situations. Plant Disease
84:357-369.
Shearer BL, Wilcoxson RD, Skovmand B, Anderson WH (1978)
Infection of barley by Septoria avenae f. sp. triticea enhanced by
Puccinia hordei. Journal of Plant Diseases and Protection 85:461-
470.
Sherwood JL, Reddick BB, Conway KE (1988) Reactions of
Bahamian hot chile to single and double infections with tobacco
mosaic virus and potato virus Y. Plant Disese 72:14-16.
Sikora RA, Carter WW (1987) Nematode interaction with fungal
and bacterial plant pathogens - fact or fantasy. In: Veech JA, Dickson
DW (Eds.) Vistas on Nematology. Hyattsville MD, USA. Society of
Nematologists Inc. pp. 307-312.
Simkin MB, Wheeler BEJ (1974) Effects of dual infections of
Puccinia hordei and Erysiphe graminis on barley, cv. Zephyr. Annals
of Applied Biology 78:237-250.
Sommerfeld ML, Gildow FE, Frank JA (1993) Effects of single or
double infections with Helminthosporium avenae and barley yellow
dwarf virus on yield components of oats. Plant Disease 77:741-744.
Spadafora VJ, Cole Jr H (1987) Interactions between Septoria nodorum
leaf blotch and leaf rust on soft red winter wheat. Phytopathology
77:1308-1310.
Stevens C, Gudauskas RT (1983) Effects of maize dwarf mosaic virus
infection of corn on inoculum potential of Helminthosporium maydis
race 0. Phytopathology 73:439-441.
Stevens C, Gudauskas RT (1982) Relation of maize dwarf mosaic
virus infection to increased susceptibility of corn to Helminthosporium
maydis race 0. Phytopathology 72:1500-1502.
Straib W (1938) ber den Einfu der Steinbrandinfektion auf das
Gelbrostverhalten des Weizens. Phytopathologische Zeitschrift
11:571-587.
Suheri H, Price TV (2000) Infection of onion leaves by Alternaria
porri and Stemphylium vesicarium and disease development in
controlled environments. Plant Pathology 49:375-382.
Teng PS, Johnson KB (1988) Analysis of epidemiological components
Tropical Plant Pathology 39 (1) January - February 2014 18
W.C. Jesus Junior et al.
in yield loss assessment. In: Kranz J, Rotem J (Eds.) Experimental
Techniques in Plant Disease Epidemiology. Berlin West Germany.
Springer. pp. 179-189.
Thomas NR, Chatarth MS (1976) On the relationship between
susceptibility of loose smut infected plants to black rust and
Helminthosporium blight. Indian Phytopathology 28:572-573.
Uyemoto JK, Clafin LE, Wilson DL (1981) Maize chlorotic
mottle and maize dwarf mosaic viruses: effect of single and double
inoculations on symptomatology and yield. Plant Disease 65:39-41.
Valverde RA, Heick JA, Dodds JA (1991) Interactions between
satellite tobacco mosaic virus, helper tobamoviruses and their hosts.
Phytopathology 81:99-104.
Van Der Wal AF, Shearer JC, Zadoks JC (1970) Interaction between
Puccinia recondita f. sp. triticina and Septoria nodorum on wheat,
and its effects on yield. Netherlands Journal of Plant Pathology
76:261-263.
Van Der Wal AF, Cowan MC (1974) An ecophysiological approach
to crop loss exemplifed in the system wheat, leaf rust and glume
blotch. II. Development, growth, and transpiration of uninfected
plants and plants infected with Puccinia recondita f .sp. triticina
and/or Septoria nodorum in a climate chamber experiment.
Netherlands Journal of Plant Pathology 80:192-214.
Varughese J, Griffths E (1983) Effect of barley yellow dwarf virus on
susceptibility of barley cultivars to net blotch (Pyrenophora teres) and
leaf blotch (Rhynchosporium secalis). Plant Pathology 32:435-440.
Waggoner PE, Berger RD (1987) Defoliation, disease, and growth.
Phytopathology 77:93-398.
Waggoner PE (1986) Progress curves of foliar diseases: Their
interpretation and use. In: Leonard KJ, Fry WE (Eds.) Plant Disease
Epidemiology. Vol. 1. Population Dynamics and Management. New
York NY, USA. Macmillan Publishing Co. pp. 3-37.
Wainwright A, Kenny MA, Yarham DJ (1986) Increased susceptibility
to Septoria nodorum in winter wheat infected by Tilletia caries. Plant
Pathology 35:582-584.
Walkey DGA, Payne CJ (1990) The reaction of two lettuce cultivars
to mixed infection by beet western yellows virus, lettuce mosaic virus
and cucumber mosaic virus. Plant Pathology 39:156-160.
Wallace HR (1983) Interactions between nematodes and other factors
on plants. Journal of Nematology 15:221-227.
Waller JM, Bridge J (1984) Effects of pathogen interactions on
tropical crop production. In: Wood RHS, Jellis GJ (Eds.) Plant
Diseases: Infection, Damage and Loss. Oxford UK. Blackwell
Scientifc Publications. pp. 311-320.
Wang Y, Gaba V, Yang J, Palukaitis P, Gal-On A (2002)
Characterization of synergy between Cucumber mosaic virus and
potyviruses in cucurbit hosts. Virology 92:51-58.
Weber GE, Glec S, Kranz J (1994) Interactions between
Erysiphe graminis and Septoria nodorum on wheat. Plant
Pathology 45:158-163.
Weber GE (1996) Modelling interactions between epidemics of
Erysiphe graminis and Septoria nodorum on wheat. Journal of
Plant Diseases and Protection 103:364-376.
Williams DJ, Nyvall RF (1980) Leaf infection and yield losses
caused by brown spot and bacterial blight diseases of soybean.
Phytopathology 70:900-902.
Willingale J, Mantle PG (1987) Interactions between Claviceps
purpurea and Tilletia caries in wheat. Transactions of the British
Mycological Society 89:145-153.
Wilson EM (1958) Rust-TMV cross protection and necrotic ring
reaction in bean. Phytopathology 48:228-231.
Wintermantel WM (2005) Co-infection of Beet mosaic virus with
beet yellowing viruses leads to increased symptom expression on
sugar beet. Plant Disease 89:325-331.
Wisler GC, Lewellen RT, Sears JL, Wasson JW, Liu HY,
Wintermantel WM (2003) Interactions between Beet necrotic
yellow vein virus and Beet soilborne mosaic virus in sugar beet.
Plant Disease 87:1170-1175.
Xi D, Feng H, Lan L, Du J, Wang J, Zhang Z, Xue L, Xu W, Lin
H (2007) Characterization of synergy between Cucumber mosaic
virus and Tobacco necrosis virus in Nicotiana benthamiana.
Journal of Phytopathology 155:570-573.
Xi D, Yang H, Jiang Y, M Xu, Shang J, Zhang Z, Cheng S, Sang
L, Lin H (2010) Interference between Tobacco necrosis virus
and Turnip crinkle virus in Nicotiana benthamiana. Journal of
Phytopathology 158:263-269.
Yang H, Wang S, Xi D, Yuan S, Wang J, Xu M, Lin H (2010)
Interaction between Cucumber mosaic virus and Turnip crinkle
virus in Arabidopsis thaliana. Journal of Phytopathology 158:833-
836.
Yarwood CE (1977) Pseudoperonospora cubensis in rust-infected
bean. Phytopathology 67:1021-1022.
Zadoks JC, Schein RD (1979) Epidemiology and Plant Disease
Management. Oxford UK. Oxford University Press.
Zaiter HZ, Coyne DP, Steadman JR (1990) Coinoculation effects
of the pathogens causing common bacterial blight, rust, and bean
common mosaic in Phaseolus vulgaris. Journal of the American
Society for Horticultural Science 115:319-323.
Zhang XY, Loyce C, Meynard JM, Savary S (2006) Characterization
of multiple disease systems and cultivar susceptibilities for the
analysis of yield losses in winter wheat. Crop Protection 25:1013-
1023.
Zhou Y, Fitt BDL, Wleham SJ, Evans N, Gladders P (2000)
Effects of stem canker (Leptoshaeria maculans) and light leaf spot
(Pyrenopeziza brassicae) on yield of winter oilseed rape (Brassica
napus) in southern England. Plant Pathology 49:487-497.
TPP-2013-0080
Submitted: 16 May 2013
Revisions requested: 19 August 2013
Accepted: 21 October 2013
Section Editor: Renato B. Bassanezi