Plant Pathology (2009) 58, 409–424 Doi: 10.1111/j.1365-3059.2009.02039.

REVIEW
Blackwell Publishing Ltd

Aggressiveness and its role in the adaptation of plant

pathogens

B. Pariauda*, V. Ravignéb, F. Halkettc, H. Goyeaua, J. Carlierb and C. Lannoua

a
INRA, UMR 1290, 78850 Thiverval Grignon; bCIRAD, UMR 385, Campus de Baillarguet, 34398 Montpellier; and cINRA UMR 1136, 54280
Champenoux, France

Aggressiveness, the quantitative component of pathogenicity, and its role in the adaptation of plant pathogens are
still insufficiently investigated. Using mainly examples of biotrophic and necrotrophic fungal pathogens of cereals and
Phytophthora infestans on potato, the empirical knowledge on the nature of aggressiveness components and their
evolution in response to host and environment is reviewed. Means of measuring aggressiveness components are considered,
as well as the sources of environmental variance in these traits. The adaptive potential of aggressiveness components is
evaluated by reviewing evidence for their heritability, as well as for constraints on their evolution, including differential
interactions between host and pathogen genotypes and trade-offs between components of pathogenicity. Adaptations of
pathogen aggressiveness components to host and environment are analysed, showing that: (i) selection for aggressiveness
in pathogen populations can be mediated by climatic parameters; (ii) global population changes or remarkable population
structures may be explained by variation in aggressiveness; and (iii) selection for quantitative traits can influence pathogen
evolution in agricultural pathosystems and can result in differential adaptation to host cultivars, sometimes leading to
erosion of quantitative resistance. Possible links with concepts in evolutionary ecology are suggested.

Keywords: environmental sources of variation, fitness, heritable reproductive variation, quantitative host resistance,
virulence

host–pathogen interactions and their consequences for

Introduction
Understanding why and how pathogens harm their hosts
is a central focus in plant pathology and is of particular
importance in the context of cultivated host plants. Upon
encountering a potential host, a pathogen may be able to
cause infection or not. This compatibility relationship
has so far largely monopolized the attention of plant
pathologists and shaped the discipline (Barrett, 1985;
Thrall & Burdon, 2003). One good reason for this may
be that compatibility relationships are relatively easy to
investigate empirically. In addition, a convincing genetic
mechanism was proposed early on [the ‘gene-for-gene’
model (Flor, 1955)] and was rapidly supported by empirical
evidence (Flor, 1971). Finally, plant epidemiology has
repeatedly proved the dramatic importance of these
compatibility relationships for disease dynamics in crop
systems (e.g. Hovmøller et al., 1993). In contrast, relatively
few studies have examined the quantitative aspects of
*E-mail: bpariaud@grignon.inra.fr
Published online 5 April 2009
the dynamics and evolution of pathogen populations.
Most studies on the quantitative aspects of the host–
pathogen interaction make reference to pathogen ‘aggres-
siveness’. Defining aggressiveness may not be simple,
however, as the practical (and often implicit) definition in
use in many papers often differs from both the original
and the ‘official’ definitions.
Originally, Van der Plank (1963) defined aggressiveness
as the non-specific component of pathogenicity. Later,
Van der Plank (1968) illustrated this definition with data
from an experiment (Paxman, 1963) in which isolates
of Phytophthora infestans were grown for successive
generations on a potato cultivar with no major resistance
R-genes (i.e. all isolates were virulent, according to the
gene-for-gene model). Van der Plank (1968) summarized the
results of Paxman’s experiment in an anova table in which
the isolate effect (main effect) represented aggressiveness.
The absence of isolate × cultivar interaction supported
Van der Plank’s concept of pathogenicity, according to
which differential interactions always relate to ‘virulence’
(which is linked to the presence or absence of R-genes),
whereas ‘aggressiveness’ describes a quantitative component

© 2009 The Authors

Journal compilation © 2009 BSPP 409
410 B. Pariaud et al.
of pathogenicity that is, by definition, non-specific relative
to host genotypes. In the same book, Van der Plank (1968)
distinguished the effects of ‘vertical’ and ‘horizontal’ resistance
(counterparts in the host of ‘virulence’ and ‘aggressiveness’
in the pathogen): ‘vertical’ (qualitative) resistance, determined
by the presence of R-genes, only reduces the amount of
initial inoculum (by removing avirulent spores), whereas
‘horizontal’ (quantitative) resistance reduces the epidemic
rate by altering spore infection efficiency, lesion development
rate, time from infection to sporulation and the abundance
of spores produced. Thus, Van der Plank clearly related
‘virulence’ to the presence or absence of R-genes and con-
sidered that ‘aggressiveness’, determined by quantitative
traits of the pathogen cycle, cannot lead to differential
adaptation to susceptible host genotypes. However, this
paradigm was challenged by Caten (1974), who presented
a diagram clearly contradicting Van der Plank’s definition
and concluded that ‘the criterion of the presence or
absence of a differential interaction used by Van der Plank
for the classification of ... pathogenic variation is of
limited use’. Indeed, in the phytopathological literature,
‘aggressiveness’ is often used as an equivalent for ‘quantitative
traits related to pathogenicity’ (referred to as the ‘practical
definition’ in this paper) and many papers present significant
interactions for such traits among isolates and cultivars
that are not accounted for by R-genes (see section: Adaptive
potential of aggressiveness components).
The last definition in use is that of specialized dic-
tionaries. It departs from the two others and either rejects
the term ‘aggressiveness’ or defines it as the relative ability
of a plant pathogen to colonize and cause damage to
plants, without distinguishing between quantitative
and qualitative aspects (FBPP, 1973; Shurtleff & Averre,
1997; Holliday 1998; http://www.apsnet.org/education/
IllustratedGlossary/default.htm). This review is not an
attempt to redefine the term, but will simply follow the most
general definition, compatible with most cited papers.
‘Aggressiveness’ will therefore refer to the quantitative
variation of pathogenicity on susceptible hosts, without
any restriction related to specificity.
In practice, aggressiveness may be measured on different
scales. For authors dealing with the epidemic level (field
and landscape scales), aggressiveness is usually evaluated by
directly measuring epidemic rates (Cumagun & Miedaner,
2003). In another context, authors interested in the inter-
action between plant and pathogen genotypes at the
host-plant scale measure aggressiveness through a variety
of quantitative traits expressed during the host–pathogen
interaction. These traits, referred to as aggressiveness
components, are: infection efficiency, latent period, spore
production rate, infectious period and lesion size. Neither
scale is exclusive: aggressiveness components measured
on the scale of a given plant largely determine the rate of
epidemic development (Sackett & Mundt, 2005).
Aggressiveness is traditionally assumed to be poly-
genically determined (as are most quantitative traits; see
below for a detailed discussion of this point). Therefore,
quantitative adaptation to the host is theoretically
expected to be slower than the acquisition of additional
qualitative virulence factors, and quantitative plant
resistances are generally expected to be more durable
than qualitative resistances. However, both experimental
evidence and theory remain scarce, and much work is still
to be done to investigate the existence and to evaluate the
modalities of adaptation of pathogens to their hosts for
quantitative traits. It is therefore necessary to gather
empirical knowledge on the nature of aggressiveness (which
traits are significantly involved), as well as its genetic
and environmental determinants, and on the ability of
pathogens to respond to the selection pressures imposed
by quantitative host resistances. In this paper, adaptation
is defined as the result of selection for heritable traits that
confers an increase in reproductive performance.
This paper reviews the literature on quantitative aspects
of the host–pathogen interaction and their evolution in
response to host and environment. Most published papers
on aggressiveness concern fungi and oomycetes, but
data from other plant pathogens will be presented when
available. First, this review describes (i) how aggressiveness
components are measured, (ii) the sources of environmental
variance on these traits, and (iii) what is known about
their genetic basis. Secondly, the potential for quantitative
traits to evolve in response to environmental or host-related
selection pressures is evaluated. Finally, published data on
responses of pathogen aggressiveness components to host
and environment are presented.
Measuring quantitative components of the
host–pathogen interaction
Aggressiveness is often separated into elementary
quantitative traits of the pathogen life cycle, such as infection
efficiency, latent period, sporulation rate, infectious
period or lesion size. For some pathogens, the capacity
for toxin production is also sometimes evaluated.
Infection efficiency is defined as the probability that a
spore deposited on a receptive host surface produces a
lesion in the absence of competitive interactions. It is
usually measured as a percentage of successful infections
resulting from a controlled number of deposited spores
(Mehta & Zadoks, 1970; Sache, 1997). For practical
reasons, infection efficiency may be indirectly measured
by the observed numbers of lesions or chlorotic flecks per
unit of leaf area (Clifford & Clothier, 1974; Milus & Line,
1980; Knott & Mundt, 1991). This trait is difficult to
precisely estimate because it depends on the number of
spores deposited as well as on microclimatic conditions,
which are difficult to control (Milus & Line, 1980; Lehman
& Shaner, 1997).
The latent period is the time interval between infection
and the onset of sporulation from that infection. It deter-
mines the duration of epidemic cycles and thus largely
controls the rate of epidemic development. The definition
of latent period is clear when applied to a single lesion. In
most experimental studies, however, artificial inoculations
result in a large number of infections per leaf, and the
variation in observed latent period among infection sites
on a leaf may be considerable (Shaner, 1980). To cope
Plant Pathology (2009) 58, 409–424
 Aggressiveness of plant pathogens
with this difficulty, several criteria are used to estimate
latent periods, such as the time from inoculation to first
sporulation (Jeffrey et al., 1962; Jinks & Grindle, 1963;
Knott & Mundt, 1991; Miller et al., 1998) or the time
needed for half of the final number of lesions (T50) to
sporulate (Knott & Mundt, 1991; Flier & Turkensteen,
1999) or to show apparent sporulation structures (Johnson,
1980; Tomerlin et al., 1983). The most precise method for
estimating T50 was proposed by Shaner (1980) and is based
on an adjustment of the dynamics of lesion emergence to
a sigmoid curve. Since latent period is highly dependent
on temperature, it is recommended to express the time
in degree-days to allow comparisons between different
experiments (Lovell et al., 2004). It has been observed
that using different methods to measure latent period
(e.g. T50 vs. the time to first sporulation) could lead to
differences in its estimation [see Knott & Mundt (1991)
for Puccinia triticina on wheat and Flier & Turkensteen
(1999) for P. infestans on potato]. Such differences might,
of course, result from uncontrolled environmental effects.
A more interesting alternative is that variability in latent
period among pathogen genotypes could reveal heter-
ogeneity in both the time at which the first sporulation
occurs and the dynamics of lesion maturation, as discussed
by Shaw (1990).
Sporulation rate is the amount of spores produced
per lesion and per unit of time (Clifford & Clothier, 1974;
Sache, 1997). In practice, spores are either weighed
(Imhoff et al., 1982; Kardin & Groth, 1989) or counted
(Leonard, 1969; Rouse et al., 1980). Sporulation is
sometimes expressed in spore production per unit area of
diseased leaf (Clifford & Clothier, 1974) or relative to
lesion size (Miller et al., 1998). It has repeatedly been
shown that spore production per lesion is highly density-
dependent (Kardin & Groth, 1989). It can be useful to
consider the spore production per unit area of sporulating
tissue (Hamid et al., 1982a; Subrahmanyam et al., 1983;
Dowkiw et al., 2003), which is considerably less density-
dependent (Robert et al., 2004).
The infectious period is the time from the beginning to
the end of sporulation. This component is difficult to
precisely estimate since sporulation often shows an early
peak followed by an asymptotic decrease (Leonard, 1969;
Robert et al., 2004), but more irregular patterns may be
obtained (Imhoff et al., 1982). For cereal rusts, sporulation
can last for more than 40 days under controlled conditions
on adult plants (Leonard, 1969; Mehta & Zadoks, 1970;
Imhoff et al., 1982; Robert et al., 2004).
Since many pathogen species have two or more forms
of propagule related to sexual or asexual reproduction
(Pringle & Taylor, 2002), infection efficiency, sporulation
rate, latent period and infectious period may, in principle,
be measured for each type of spore (e.g. Gilles et al., 2001;
Karolewski et al., 2002). Nevertheless, a given parameter
may not have the same meaning when measured on sexual
and asexual spores. For example, the latent period
associated with sexual spores is very different from that
of asexual spores because it depends on the fortuitous
encounter and merger of two sexually compatible lesions.
Plant Pathology (2009) 58, 409 – 424
411
Therefore, while there seems to be room for adaptive
adjustment of asexual latency, sexual latency is expected
to be highly dependent on environmental stochasticity.
Moreover, organs resulting from sexual reproduction
often ensure inter-season survival, as in Blumeria graminis
or in Leptosphaeria maculans, and the latent period, as
defined above, has no meaning in such cases.
Lesion size is another quantitative trait that is measured
as an aggressiveness component (Kolmer & Leonard,
1986; Mundt et al., 2002b). It is generally defined as the
surface area that produces spores. For some pathogens,
such as P. triticina, lesion size remains limited, but it can
dramatically increase in some species such as P. infestans
or Puccinia striiformis, for which lesion growth is
semisystemic (Emge et al., 1975). In this case, lesion size
accounts for a large part of the quantitative development
of epidemics and lesion growth rate is a key factor in
pathogen competition for available host tissue. Lesion size
is not easy to precisely determine for pathogens such as
Mycosphaerella graminicola that induce necrosis on the
host leaf (Cowger et al., 2000). Moreover, such pathogens
often indirectly cause apical necrosis on the leaves that can
be confused with a diseased area.
Aggressiveness is sometimes estimated through disease
severity, measured as the percentage of the infected plant
organ (root, leaf or spike) covered by pathogen lesions
(Krupinsky, 1989; Ahmed et al., 1995, 1996; Gilbert et al.,
2001; Cowger & Mundt, 2002; Zhan et al., 2002;
Cumagun & Miedaner, 2003). Disease severity here is a
composite variable resulting from the integrated effect of
infection efficiency and lesion size, but also, when assessed
at the crop scale, sporulation and dispersal.
The production of mycotoxins (inducing host necrosis)
is generally considered an aggressiveness component, but
the relationship between disease severity and mycotoxin
production is not straightforward. In fusarium head
blight of wheat, some studies did not show any relationship
between aggressiveness (measured as disease severity) and
toxin production (Gilbert et al., 2001), whereas other
authors found that DON-toxin concentrations in grains
were closely correlated with disease severity (Cumagun &
Miedaner, 2004). Deciphering the exact function of
toxin production is important to determine its role in
aggressiveness. In necrotrophic species, where toxin
production is only used to kill plant cells and convert them
into resources for growth, toxin production may indeed
be correlated with within-host multiplication. In contrast,
in species where toxin production is needed to allow spore
release (e.g. by accelerating host death), it is not expected
to directly correlate with other measurements of within-
host multiplication (Day, 2002).
Effects of environment on expression of
aggressiveness components
The effects of climatic parameters (mainly temperature
and relative humidity) on the expression of disease have
been extensively described in the literature. In addition, it
is known that host physiological status (e.g. nitrogen
412 B. Pariaud et al.
content, tissue age) affects disease development, particularly
for biotrophic pathogens (Eversmeyer et al., 1980; Tomerlin
et al., 1983; Turechek & Stevenson, 1998; Robert et al.,
2004). Finally, some components of the pathogen life cycle
(e.g. spore production per lesion) are strongly influenced by
lesion density (Katsuya & Green, 1967; Mehta & Zadoks,
1970; Rouse et al., 1980; Kardin & Groth, 1989; Robert
et al., 2004). These sources of variation are generally
considered unwanted effects in aggressiveness measure-
ments, but may account for a large portion of variability.
For instance, in a study of the adaptation of P. triticina
to wheat cultivars (Knott & Mundt, 1991), most of the
variability was accounted for by the growth chamber
for two out of three parameters measured. Similarly,
ranking by disease severity of isolates of M. graminicola,
as well as cultivar-by-isolate interaction, were found to
vary between a greenhouse and a growth-chamber
experiment (Krenz et al., 2008).
Effect of climatic conditions
Variation among years in field experiments can be con-
siderable, underlining the strong sensitivity of aggressive-
ness measurements to climatic conditions. For instance, in
a field study with Fusarium graminearum, Cumagun &
Miedaner (2004) calculated that the isolate-by-environ-
ment interaction accounted for 29% of the variance for
aggressiveness (measured by disease severity) and 19% of
the variance for mycotoxin production.
Most studies linking aggressiveness and climate are
limited to the effect of temperature. It is well known that
temperature influences pathogen development as well as
the expression of host resistance. The effect of temperature
on aggressiveness components has been established for
many pathogen species and presents an optimum for
spore germination, lesion development and sporulation.
However, the response to temperature may differ among
individuals (Milus et al., 2006). For instance, Milus &
Line (1980) showed that the spore production rate of two
leaf rust isolates (P. triticina) was identical at 2–18°C but
different at 10–30°C.
Interestingly, differences in aggressiveness among
pathogen isolates have sometimes been reported to be
greater under non-optimal conditions: differences in the
latent period among isolates were more effectively observed
at suboptimal temperatures for pathogen development in
P. triticina and P. striiformis f.sp. tritici (Eversmeyer et al.,
1980; Johnson, 1980; Milus et al., 2006). This result sug-
gests that differential responses in terms of aggressiveness
may be less detectable under optimal environmental
conditions (Eversmeyer et al., 1980; Johnson, 1980).
Effect of host physiological status
For several biotrophic parasites, high nitrogen content in
host tissues results in increased infection efficiency and
spore production (Tiedemann, 1996; Jensen & Munk, 1997;
Robert et al., 2004). Spore production of biotrophic
parasites was also reported to increase when host photo-
synthesis was stimulated (Cohen & Rotem, 1970). More-
over, the response to infection may depend on host growth
stage (Eversmeyer et al., 1980; Johnson, 1980; Milus &
Line, 1980; Tomerlin et al., 1983) or on the type or age of
host tissues (Turechek & Stevenson, 1998). Changes in the
quantitative expression of disease with host development
stage were reviewed by Develey-Rivière & Galiana (2007)
and probably largely relate to differences in the expression
of resistance factors. Host status may affect the quantitative
host–pathogen interaction through the amount of available
resources or through the expression of resistance genes
(the latter is not considered further).
Milus & Line (1980) observed that the relative spore
production of two P. triticina cultures changed with host
growth stage (seedling or adult plant) on some cultivars.
Turechek & Stevenson (1998) showed that the age of host
tissues can have a strong effect on a tree disease such as
pecan scab (caused by Cladosporium caryigenum) for
aggressiveness components such as infection efficiency,
incubation period, lesion size and sporulation. Knott &
Mundt (1991) found a significant difference between upper
and lower leaves for latent period and infection efficiency
when measuring the aggressiveness of field populations
of P. triticina on wheat. On average, spore populations
exhibited 25% higher infection efficiency and a 3 –4%
shorter latent period on the upper leaves than on the lower
leaves. This was attributed either to greater susceptibility
of the upper leaves or to physiological effects. Katsuya &
Green (1967) even found significant differences in the
latent period of wheat stem rust, depending on the position
of the lesions along the leaves: latent period was about
1 day shorter at the leaf base than toward the tip.
Measurements performed on detached leaves, although
generally considered reliable, may sometimes alter the
differences observed: Miller et al. (1998) compared the
responses of three to five P. infestans isolates on two potato
cultivars, either on detached leaflets or whole plants. They
found that one isolate (537) had a significantly greater
sporulation capacity on whole plants than two others
(367 and 416), whereas no significant differences were
found among isolates on detached leaflets, regardless of
cultivar.
Effect of lesion density
For many biotrophic pathogens, lesion size and spore
production are highly density-dependent (e.g. Robert et al.,
2004), probably because of increased competition among
lesions for host resources and available tissues. This density
effect may have major consequences for experimental
measurements of aggressiveness components such as spore
production and lesion size, particularly when differences
in infection efficiency among isolates result in different
lesion densities. In such cases, observed differences in
spore production may result from a density effect rather
than from genetic differences among isolates. For instance,
in a study by Clifford & Clothier (1974) on barley leaf
rust (Puccinia hordei), the greater sporulation capacity
observed on moderately resistant cultivars than on the
Plant Pathology (2009) 58, 409–424
 Aggressiveness of plant pathogens
susceptible control could have partly resulted from a
density effect generated by differences in infection
efficiencies.
Pathogen genotypes may respond differently to this
competition effect, however, and some individuals seem to
be less affected than others by lesion density (Katsuya &
Green, 1967; Kardin & Groth, 1989). Katsuya & Green
(1967) observed the competition between two isolates
belonging to two different pathotypes of Puccinia graminis
during 14 generations on wheat seedlings in a greenhouse.
One isolate was predominant at low densities (less than
10 lesions per leaf) on both cultivars, whereas the other
isolate became predominant on one of the cultivars at
high densities (> 100 lesions per leaf). Additional evidence
of genotype-by-density interaction was found by Kardin
& Groth (1989) with bean leaf rust (caused by Uromyces
appendiculatus). They observed that the relative lesion
size of several isolates changed when lesion density was
increased: isolates with the largest lesions at low lesion
density presented the smallest lesions at high density. The
authors concluded that a reproductive advantage found
at low densities might be obviated at higher densities.
However, the consequences of these differential responses
to competition might be weak on an epidemic scale (see
Lannou & Mundt, 1997).
Effect of pathogen physiological status
Variability in aggressiveness measurements may also result
from the physiological state of the pathogen. In particular,
storage or multiplication conditions may alter pathogen
aggressiveness. This was clearly shown for P. infestans by
Day & Shattock (1997) in which isolates collected in
different years and stored in liquid nitrogen were
compared with ‘standard’ reference isolates. Jeffrey et al.
(1962) and Jinks & Grindle (1963) observed a decrease in
aggressiveness of P. infestans strains after repeated transfers
on chickpea medium, and reported that different strains
underwent these changes to varying extents and at differing
rates. Nonetheless, Jinks & Grindle (1963) observed that
cycling on potato tubers could enable P. infestans to recover
its initial aggressiveness level, suggesting that the observed
changes resulted from phenotypic plasticity. Mundt et al.
(2002b), using the bacterial pathosystem Xanthomonas
oryzae pv. oryzae on rice, tested two cultures resulting
from separate maintenance of the same initial material.
The difference between cultures approached significance
(P = 0.06) in one trial out of two, and variance compo-
nent analysis indicated that the culture environment of the
pathogen accounted for 14% of the total variation in
lesion length. The authors concluded that culture varia-
bility should be considered more often in aggressiveness
measurements.
The great sensitivity of the quantitative host–pathogen
interaction to environmental variations (including climatic
effects, lesion density, host physiological status, isolate
maintenance and culture conditions) has at least two con-
sequences. First, it constitutes a constraint for empirical
studies of aggressiveness, since it appears to be of primary
Plant Pathology (2009) 58, 409 – 424
413
importance to perform aggressiveness measurements
under well-defined and controlled conditions and with
standardized host and pathogen material. Secondly, it is
questionable from an evolutionary perspective whether
aggressiveness components, variable as they are with
environment, may respond to selection. The genetic basis
of aggressiveness traits and their adaptive potential are
discussed below.
Genetic basis of aggressiveness components
Compared with studies on the genetics of quantitative
resistance, investigations of the genetic bases of aggres-
siveness components in fungi are scarce. An example of
the former is the meta-analysis of the genetic support
of quantitative and qualitative resistance of rice to
Magnaporthe grisea by Ballini et al. (2008). Generally,
the number of effective genetic factors for quantitative
resistance tends to range from two to 10 or more, but it is
commonly determined by three to five loci (Parlevliet,
1993; Young, 1996; Singh et al., 2005). Moreover, it has
been suggested that quantitative loci could be allelic
versions of qualitative resistance genes with intermediate
phenotypes (Young, 1996, Ballini et al., 2008). It thus
appears that the genetic determination of quantitative
resistance is both complex and diversified in terms of the
number and nature of genes involved. As a consequence,
the genetic control of aggressiveness is likely to be complex
and variable, and is probably of polygenic determination
in most cases.
Several studies have suggested that aggressiveness
components are polygenically determined (Blanch et al.,
1981; Caten et al., 1984; Hawthorne et al., 1994; Cumagun
& Miedaner, 2004). This was shown, for instance, with
segregation for wheat leaf necrosis and production of
pycnidia in Phaeosphaeria nodorum, by tetrad analysis
(Halama et al., 1999).
The genetic architecture of quantitative traits can be
further studied through quantitative trait loci (QTL)
mapping. Only a few QTL were detected for components
such as lesion length or fungal growth in Gibberella zeae
(Cumagun et al., 2004) and Heterobasidion annosum (Lind
et al., 2007). However, several obstacles make this approach
generally difficult for plant pathogenic fungi. First, the
number of loci detected in QTL analysis depends on
several factors, including the genetic properties of the
QTL that control the traits studied, environmental effects,
population size and experimental error (Collard et al.,
2005). Secondly, QTL analysis cannot be applied to
asexually reproducing species and thus to a large number
of pathogenic fungi. Lastly, QTL analysis requires phe-
notypic evaluation and, as mentioned above, quantitative
measurements in plant pathogens are time-consuming
and subject to high variability, which limits the number of
progeny and components analysed.
Molecular genetic and genomic approaches have also
been used to identify the genes involved in pathogenicity,
either qualitatively or quantitatively (aggressiveness-related
genes) (Xu et al., 2006). The pathogenicity-related genes
414 B. Pariaud et al.
identified in the rice blast model M. grisea were recently
reviewed (Ebbole, 2007). The vast majority of these genes
were involved in the ability to infect the host, but some
were found to control quantitative variations of aggres-
siveness components.
As a conclusion on this point, empirical evidence
for genetic control has been found for at least some
aggressiveness components. In all cases, this genetic
support implies that several genes are involved, even if the
precise number of genes and their interactions are still to
be determined. An alternative approach to elucidate the
genetic basis of adaptation involves genome scans of DNA
polymorphism (Schlötterer, 2003; Storz, 2005), based on
the identification of neutral markers with deviant
behaviour in natural populations. This population-based
approach makes it possible to identify loci undergoing
selection without having to evaluate the phenotypes
themselves, but is again limited to sexually reproducing
fungi. Although promising, it has not yet been applied to
fungal pathogens.
Adaptive potential of aggressiveness
components
The fact that aggressiveness components have a genetic
basis opens up opportunities for pathogen adaptation.
Such adaptation is only possible, however, if heritable
genetic variations exist in pathogen populations for these
traits. Assuming that heritable genetic variation on aggre-
ssiveness components exists in pathogen populations,
evolution of aggressiveness will be shaped by genetic
constraints such as (i) differential interactions between
hosts and pathogen isolates for quantitative traits, (ii) trade-
offs between qualitative virulence and aggressiveness (‘cost
of qualitative virulence’) and (iii) trade-offs between
aggressiveness components or between aggressiveness and
survival capacity.
Variability for aggressiveness within pathogen
populations
Within-population variation for quantitative traits is a
basic prerequisite for adaptation. However, it is important
to note that potential genetic diversity in aggressiveness
has often been underestimated. In fact, pathotypes have
sometimes been considered as homogeneous genetic
units and compared on the basis of a single isolate per
pathotype (Katsuya & Green, 1967). Nevertheless, apparent
uniformity within a pathogen population studied on the
basis of qualitative indicators does not exclude the possi-
bility of a certain level of variability in aggressiveness:
many studies have documented differences in aggressiveness
among isolates belonging to the same pathotype or
sharing similar genotypes as defined by neutral markers
(Jeffrey et al., 1962; Hamid et al., 1982b; Miller et al.,
1998; Carlisle et al., 2002; Mundt et al., 2002b; Milus
et al., 2006). Hamid et al. (1982b) found significant intra-
pathotype variations for infection efficiency, lesion length
and sporulation capacity among isolates of the same
pathotype of Cochliobolus carbonum, with differences
between the least and the most aggressive isolate of up
to 91%. Milus et al. (2006) found that two isolates of
P. striiformis f.sp. tritici belonging to the same pathotype
not only had different latent periods at 18°C on wheat
seedlings, but also presented different optimal temperatures
for this trait, one isolate developing faster at 12°C and the
other at 18°C. Significant differences in aggressiveness
(lesion expansion rate, latent period, sporulation and
infection efficiency) were found among 17 P. infestans
individuals collected from a Northern Ireland population
and sharing an identical multilocus genotype (allozyme
profiles and mtDNA haplotypes), the same mating type,
the same capacity to overcome the specific R1 resistance
gene and the same sensitivity to a fungicide (Carlisle et al.,
2002). Mundt et al. (2002b) investigated the potential
association of aggressiveness variation among isolates and
phylogenetic classification in the bacterial pathogen
X. oryzae pv. oryzae, and found significant differences in
aggressiveness between isolates of the same clonal lineage,
and even between isolates of the same RFLP haplotype
within a clonal lineage, suggesting that mutations leading
to increased aggressiveness had rapidly accumulated
within the phylogenetic lineages.
Heritability of aggressiveness components
Heritability is defined as the proportion of phenotypic
variance attributable to genetic variance and can be
estimated by different methods (Hamid et al., 1982a; Hill
& Nelson, 1982; Kolmer & Leonard, 1986; Lehman &
Shaner, 1996, 2007). Lehman & Shaner (1996) estimated
the heritability of the latent period in P. triticina from
variance analysis involving all possible combinations of
seven single-uredinial isolates on four wheat cultivars
expressing different levels of quantitative resistance.
Except on the most susceptible cultivar, on which all
isolates responded equally, heritability values for the
latent period ranged from 0.28 to 0.76, depending on the
cultivar tested. The greatest part (42–49%) of the variation
among isolates attributed to genetic factors was found on
cultivar CI-13227. This result was later confirmed
(Lehman & Shaner, 2007) by a selection experiment:
heritability of the latent period was then about 0.70 on
cultivar CI-13227 and 0.20 on another partially resistant
cultivar. This suggests that heritability of aggressiveness
strongly depends on the genetics of the host–pathogen
interaction. Hill & Nelson (1982) estimated heritability of
several aggressiveness components in progeny populations
obtained from different crosses between five isolates of
Cochliobolus heterostrophus race T on one maize line.
Their estimates ranged between 0 and 0.6 for lesion length,
0.23 and 0.52 for sporulation capacity and 0.21 and 0.58
for infection efficiency. According to the authors, the
low heritability value for lesion length confirmed the low
genetic variation within race T for this aggressiveness
component. In C. carbonum race 3, Hamid et al. (1982a)
estimated lesion length heritability at 0.87, based on an
analysis of variance of crossed responses of 22 isolates on
Plant Pathology (2009) 58, 409–424
 Aggressiveness of plant pathogens
two corn inbred lines. However, Kolmer & Leonard
(1986) commented that heritability values determined
from genetic responses in multiple environments were
more realistic than values determined by analysis of
variance and based on restricted environmental variation
and a limited number of phenotypes. They estimated
heritability of lesion length in C. heterostrophus race O in
an artificial selection experiment on a single corn line:
starting with a set of bulk isolates, the largest lesions
were selected to constitute the following generation and
the rate of increase of mean lesion length throughout
generations was calculated by regression. On the basis of
this method, a heritability value of 0.27 was estimated
for lesion length.
Other authors evaluated the variability explained by
genotype vs. environment without formally calculating
heritability. In a study on P. infestans on artificial medium,
Caten (1974) found that 83% of the total variation
between isolates was of genetic origin. In a greenhouse
trial with the bacterial pathogen X. oryzae pv. oryzae on
rice, Mundt et al. (2002b) recorded 47–55% of the total
variation in aggressiveness measurements was accounted
for by genetic factors.
Differential interactions between isolates and cultivars
for aggressiveness components
According to the original definition of aggressiveness
(Van der Plank, 1963), variation for quantitative traits
was considered to occur among isolates, but without
interactions with the host genotypes (see Introduction).
Nevertheless, many studies have shown that these kinds
of interactions can be observed. Most of these studies
were undertaken to evaluate quantitative resistance in
host plants, but indirectly revealed differential interactions
between host and pathogen genotypes for quantitative
traits.
Using the pathosystem Hordeum vulgare–P. hordei,
Parlevliet (1977) compared the latent period and infection
efficiency of five isolates on adult plants of three cultivars,
both under controlled conditions and in the field. The
cultivar-by-isolate interaction was significant for the
latent period in both trials. With P. infestans on potato,
Carlisle et al. (2002) found cultivar-by-isolate interactions
for latent period, lesion expansion and sporulation capacity.
Cultivar-by-isolate interactions were also found for infection
efficiency, latent period and sporulation capacity with
P. triticina (Kuhn et al., 1978; Milus & Line, 1980;
Lehman & Shaner, 1996), for infection efficiency and
sporulation capacity with B. graminis f.sp. tritici (Rouse
et al., 1980), for infection efficiency with P. nodorum
(Scharen & Eyal, 1983), and for lesion expansion with
Septoria musiva on poplar (Krupinsky, 1989). It should
be mentioned, however, that such interactions are not
always found: Van Ginkel & Scharen (1988) analysed
the responses of 14 wheat cultivars to 34 Septoria tritici
(M. graminicola) isolates for lesion size (necrotic area) on
seedlings. Significant differences were found among cultivars
and isolates, but with no significant interactions.
Plant Pathology (2009) 58, 409 – 424
415
Cost of virulence: a trade-off between qualitative
virulence and aggressiveness
The cost of qualitative virulence is the reduction in
pathogen fitness induced by a mutation from avirulence
to qualitative virulence. This concept was originally
developed by Van der Plank (1963) and has since been
widely discussed in the literature (see below). With this
concept, changes in pathogen aggressiveness result directly
from the loss of avirulence gene function.
Estimating this fitness cost may be challenging because
(i) fitness varies with experimental conditions (Weltz et al.,
1990) and (ii) the effect of genetic background has to be
eliminated (Østergård, 1987). When comparing aggres-
siveness components of B. graminis f.sp. tritici isolates
differing in number of qualitative virulence genes,
Menzies & MacNeill (1987) did not clearly distinguish
which part of the reduction in fitness could be attributed
to qualitative virulence genes or to isolate genetic back-
grounds. Bronson & Ellingboe (1986) even showed by
a progeny study that reduced fitness segregated inde-
pendently of the qualitative virulence loci.
Some attempts to evaluate the cost of qualitative
virulence have remained inconclusive. In an artificial
selection experiment with P. infestans on potato, a single-
virulence pathotype was shown to predominate in a
pathotype mixture after two to nine successive generations
(Thurston, 1961). However, in the field, this pathotype
was not always the most aggressive, and more complex
pathotypes could be more frequent on a susceptible
cultivar. In a similar experiment with P. triticina on wheat,
Kolmer (1993) found that even though pathogen fitness
seemed to sometimes be associated or dissociated with
certain individual qualitative virulences, no general
relationship could be established between the number
of unnecessary qualitative virulence factors and pathogen
fitness.
Several authors, however, obtained fitness differences
between avirulent races and races carrying unnecessary
virulence factors that could be clearly attributed to the
cost of qualitative virulence. Because the effect of genetic
background cannot be easily separated from the effect
of the avirulence gene itself, these studies were based on
indirect measurements. Measured values for virulence
cost (reduction in aggressiveness) ranged between 14 and
39% for P. graminis f.sp. avenae (Leonard, 1969), 12 and
30% for C. heterostrophus, depending on the experimental
procedure used (Leonard, 1977), 4 and 5.2% for P. graminis
f.sp. tritici (Grant & Archer, 1983), and 5.4 and 6.1% for
B. graminis f.sp. hordei (Grant & Archer, 1983). The first
direct evidence of a cost of virulence was obtained in the
causal agent of bacterial blight on rice (X. oryzae pv.
oryzae) by comparing virulent and avirulent isogenic lines
(Vera Cruz et al., 2000). Since then, the same result was
obtained with other cloned avirulence genes (Leach
et al., 2001).
Recent progress in plant pathogen genomics has shown
that mutations from avirulence to qualitative virulence
may stem from very different events, ranging from a
416 B. Pariaud et al.
single-base mutation to a large chromosome deletion
(e.g. Gout et al., 2007). Depending on the function of the
qualitative virulence gene, its redundancy in the genome
and the nature of the mutation, the cost for qualitative
virulence might vary from neutral to nearly lethal, the
latter obviously being not selected in field populations.
Moreover, it has been shown with other biological systems
that fitness costs resulting from the acquisition of resistance
to antibiotics or insecticides (Levin et al., 2000; Schoustra
et al., 2006; Labbé et al., 2007) can be progressively
compensated for by subsequent mutations. Similar
mechanisms could reduce the cost of virulence in plant
pathogen populations, possibly explaining why pathotypes
carrying multiple virulence genes can be present at high
frequencies and over long periods of time (e.g. Goyeau
et al., 2006).
This link between qualitative virulence and aggre-
ssiveness probably has considerable consequences on
pathogen evolution, since genotypes which accumulate a
large number of qualitative virulence genes might never
be the most aggressive on a given host (Thrall & Burdon,
2003).
Genetic correlations between quantitative traits
Genetic correlations between traits, either positive or
negative (trade-offs), should constrain quantitative trait
evolution. Trade-offs between aggressiveness components
or between aggressiveness and other life-history traits
should therefore be of the utmost importance for pathogen
adaptation. Nevertheless, there are surprisingly few datasets
available to show the existence of such trade-offs in fungal
plant pathogens.
Trade-offs between aggressiveness and survival were
suggested in a study by Leonard et al. (1988) which showed
that C. carbonum presented a low aggressiveness level on
maize but a great survival ability, whereas C. heterostrophus
expressed high aggressiveness levels but a low survival
ability. At the intra-species level, Carson (1998) found
evidence of a trade-off between C. heterostrophus lesion
length and survival rate on the soil surface during winter.
In a recent study on P. infestans, Montarry et al. (2007)
found no trade-off between aggressiveness (measured by
combining lesion size, sporulation and latent period) and
overwinter survival on potato tubers.
Correlations between aggressiveness components have
rarely been investigated in fungal plant pathogens. Leonard
et al. (1988) found that B. maydis race T, which produces
a host-specific toxin, quickly disappeared from the
pathogen population when the host genotypes susceptible
to the toxin were removed from the host population,
suggesting the existence of a trade-off between toxin
production and fitness of the fungus. Authors often
consider that components of the pathogen life cycle related
to aggressiveness are positively correlated, and sometimes
suggest that they are under pleiotropic control (Ohm &
Shaner, 1975; Milus & Line, 1980). For instance, Milus &
Line (1980) found that long latent periods were associated
with small lesion sizes in wheat leaf rust.
Adaptation for quantitative traits in pathogen
populations
Most population studies on pathogen adaptation for
quantitative traits deal with agricultural systems, but
interesting results have also been obtained with wild path-
osystems. Four points are examined here: (i) selection for
aggressiveness mediated by climatic parameters; (ii) global
population changes related to aggressiveness; (iii) adaptation
to host cultivars for quantitative traits; and (iv) adaptation
to identified quantitative resistances.
Adaptation to environmental conditions
Most studies linking aggressiveness components to the
environment have aimed to understand quantitative
epidemic development in a range of environmental
situations, only considering the species level. In some
cases, however, it has been demonstrated that the relative
fitness of different genotypes within the same pathogen
species can vary according to environmental effects
(Eversmeyer et al., 1980; Johnson, 1980; Milus & Line,
1980; Milus et al., 2006) and a few studies have attempted
to link pathogen population structures and climate.
Milus et al. (2006) demonstrated that better adaptation
to warmer temperatures might explain the observed
changes in P. striiformis f.sp. tritici populations in the south-
central USA around the year 2000. Under a controlled
conditions trial, ‘new’ and ‘old’ isolates had similar
aggressiveness levels at 12°C, whereas at 18°C the latent
period was shortened by about 2 days for isolates from
the ‘new’ population and germination rates were doubled
compared to the ‘old’ population. The authors concluded
that these differences may have contributed to the recently
expanded geographic range for P. striiformis. Similarly,
Katsuya & Green (1967) explained the replacement of
wheat stem rust (P. graminis) pathotype 15B by a new
pathotype (56) in Canada by a differential effect of
temperature. In a competition experiment performed
under controlled conditions, they showed that the relative
fitness of these pathotypes was reversed between 15 and
20°C, with the ‘new’ pathotype being more frequent at
higher temperatures. It should be mentioned, however,
that Katsuya & Green (1967) used a single isolate for each
pathotype and thus ignored the potential within-pathotype
diversity.
These studies suggest that temperature may sometimes
lead to large population shifts within a pathogen species.
However, more subtle effects can also operate in a local
adaptation context. There is indeed evidence that the
effect of temperature on pathogen aggressiveness may affect
parasite performance through genotype-by-environment
interactions (Price et al., 2004; Laine, 2008). With a fitness
estimate based on latent period and spore production,
Laine (2008) demonstrated that both the strength and the
direction of local adaptation of the powdery mildew
fungus, Podosphaera plantaginis in a metapopulation of
Plantago lanceolata could change with temperature.
In particular, in one of the host subpopulations, the
Plant Pathology (2009) 58, 409–424
 Aggressiveness of plant pathogens
sympatric pathogen population was better adapted than
the allopatric populations at 17°C, whereas it was clearly
maladapted at 23°C.
Changes in population structure related to
aggressiveness
Major shifts in pathogen populations have sometimes
been linked to invasion by a more aggressive population.
One of the most well-documented situations is that of the
relatively recent replacement of clonal lineage US-1 of
P. infestans in the USA by new genotypes. Almost all
isolates of this pathogen collected from the Columbia
Basin, Idaho, in 1992 were of the US-1 genotype, whereas
97% were identified as US-8 by 1995 (Miller et al., 1997).
Miller et al. (1998) compared the aggressiveness level of
22 isolates from different clonal lineages, including six
US-1 isolates and three US-8, on four potato cultivars
with different levels of quantitative resistance. They found
that US-8 isolates had a higher lesion expansion rate, a
higher sporulation capacity and a shorter latent period
than US-1 isolates. Moreover, US-8 isolates rotted tuber
slices faster than other isolates, confirming previous
studies (Lambert & Currier, 1997). From these data, the
authors concluded that relative differences in aggressive-
ness may partially explain the shift in the P. infestans
population in the Columbia Basin from the US-1 to the
US-8 lineage. Even though they relied on a small number
of isolates (one to six per lineage), and despite significant
intra-lineage variability, the quantitative differences between
lineages presented by Miller et al. (1998) were consistent
for several aggressiveness components and were confirmed
by other similar studies (e.g. Kato et al., 1997; Lambert &
Currier, 1997) and studies investigating defence responses
by potato genotypes to virulent US-1 and US-8 genotype
isolates (e.g. Wang et al., 2008). A comparable situation
occurred in Europe, where exotic P. infestans genotypes
displaced the old population (mating type A1) in only a
few years in the 1980s. Higher infection efficiency and
spore production per lesion produced by new than by old
genotypes was postulated by Day & Shattock (1997) to
explain the displacement. Interestingly, ‘old’ isolates were
clearly less aggressive on two cultivars with quantitative
resistance, but differences were less distinguishable on a
less resistant cultivar. In addition to higher aggressiveness,
resistance to the fungicide metalaxyl may have influenced
these population shifts (Day & Shattock, 1997; Miller et al.,
1998).
Differential adaptation to host cultivars, related to
quantitative traits, may sometimes influence the structure
of pathogen populations. Goyeau et al. (2006) surveyed
P. triticina populations in France between 1999 and 2002.
On wheat cv. Soissons the pathogen was present at a
relatively high frequency (9–15%) in the host population
and a single pathotype represented 30–60% of the pathogen
population, even though more than 10 other compatible
pathotypes were detected on the same cultivar, but at
much lower frequencies. Since this pathotype distribution
was found only on cv. Soissons and on a closely related
Plant Pathology (2009) 58, 409 – 424
417
cultivar, and lasted for several years, the authors hypoth-
esized that a greater level of aggressiveness could explain
the dominance of a single pathotype. This hypothesis was
later confirmed in greenhouse experiments: the dominant
pathotype had a shorter latent period, greater spore
production and larger lesion size on cv. Soissons than did
other pathotypes (Pariaud et al., 2007).
One of the clearest demonstrations of the central
importance of aggressiveness to pathogen evolution
has been made with the wild pathosystem Melampsora
lini–Linum marginale by Thrall & Burdon (2003). In
southern Australia, M. lini develops recurrent rust
epidemics in an L. marginale metapopulation. In this
system, the pathogen disperses more broadly than the host
and a pattern of local adaptation to the host population
has been demonstrated. The authors showed a negative
relationship between aggressiveness (measured as spore
production per lesion) and average qualitative virulence
(defined here as the average ability of a pathogen population
to overcome the diversity of resistance genes present in
the host population). This trade-off was identified as the
central cause preventing the most virulent pathotypes from
invading all host sub-populations and finally dominating the
system. It is likely that such trade-offs between qualitative
virulence and aggressiveness play an important role in
generating local adaptation in gene-for-gene systems by
impeding the emergence and evolution of pathotypes that
are both highly aggressive and capable of multiplying on
all host genotypes.
Quantitative adaptation to host cultivars
Most of what we know about pathogen evolution in
agricultural systems is based on qualitative gene-for-gene
virulence. However, it is now clear that selection for quan-
titative traits influences pathogen evolution in agricultural
pathosystems, and it has been repeatedly demonstrated
that selection for quantitative traits can result in differential
adaptation to host cultivars. This was shown by artificial
selection experiments (Leonard, 1969), but a differential
adaptation to the host of origin in field epidemics was also
demonstrated (Ahmed et al., 1996).
Differential adaptation to host cultivars in artificial
selection experiments
One of the first studies of pathogen quantitative adaptation
based on artificial selection was published by Leonard
(1969). He maintained a genetically heterogeneous popu-
lation of P. graminis f.sp. avenae on two different host
genotypes for seven asexual generations and showed that
the mean infection efficiency of the population had
increased by approximately 10–15% at the end of the
experiment on the host on which it had been grown, but
not on the other one. Leonard’s results were later confirmed
by two different studies. Chin & Wolfe (1984) sampled
powdery mildew (B. graminis f.sp. hordei) on two different
barley cultivars grown either in pure stands or in mixture.
When collected in pure stands, isolates had a higher
multiplication rate (up to 22–24%) on the cultivar from
418 B. Pariaud et al.
which they were isolated than on the other one, but this
did not occur when the cultivars were grown in mixture.
This result was confirmed and extended in a field study
with wheat powdery mildew (B. graminis f.sp. tritici)
by Villaréal & Lannou (2000). They demonstrated that
selection for quantitative traits operated in the pathogen
population on the scale of a single epidemic and resulted
in a higher aggressiveness level at the end of the crop
season on the host genotype on which the pathogen
population multiplied. They compared the average
infection efficiency of a spontaneous B. graminis population
before and after seven successive pathogen generations on
pure stands of two different cultivars, a mixture of both,
or alternate stands of each cultivar. In this system, the
average infection efficiency of the pathogen increased on
the pure stands, but did not significantly change in the
host mixture or when the cultivars were changed at
each pathogen generation (alternate stands). Moreover, in
some plots, mixtures and alternate sowings tended to select
for pathogen populations with identical aggressiveness
levels on both cultivars.
Differential adaptation to the host cultivar was tested in
selection experiments with different pathosystems. Caten
(1974) multiplied six isolates of P. infestans for successive
generations on tubers from three potato cultivars and
then tested their growth capacity on tubers of the same
cultivars. After six generations, and except for a resistant
cultivar, pathogen aggressiveness increased by 10% in
homologous combinations (where source and test cultivars
were the same) compared to heterologous combinations.
In other studies, however, experimental selection did not
demonstrate quantitative adaptation to the host (Alexander
et al., 1985; Kolmer, 1990).
Adaptation to the cultivar of origin
Several authors have investigated whether populations
isolated from a given cultivar in the field are more aggressive
on this cultivar than on others.
In both field and greenhouse experiments, Bonman et al.
(1989) observed that Korean isolates of M. grisea induced
more disease on japonica rice cultivars than Philippine
isolates. Japonica cultivars are predominant in Korea,
whereas indica cultivars are more frequent in the
Philippines. Since the isolates tested in this experiment
produced compatible reactions on all the cultivars tested, the
authors concluded that specificity in adaptation to genetic
background was the primary cause of these differential
interactions, underlining, however, that japonica and
indica rice cultivars represent different germplasms.
Andrivon et al. (2007) obtained similar results in
P. infestans, comparing French and Moroccan populations
on the potato cvs Bintje (prevalent in France, but not
grown in Morocco) and Désirée (popular in Morocco, but
cultivated to a very small extent in France). French and
Moroccan populations globally had greater lesion sizes
and sporulation capacities on detached leaflets of cvs
Bintje and Désirée, respectively.
Similarly, Ahmed et al. (1995) found that M. graminicola
isolates from California induced more disease on Californian
than on Oregonian cultivars, while the reverse result was
obtained for Oregonian isolates. In another study, Ahmed
et al. (1996) sampled M. graminicola isolates from winter
wheat cultivars in field plots near crop maturity and
measured their aggressiveness, defined by disease severity,
on seedlings of the same wheat cultivars in the green-
house. In two separate experiments, the linear contrast
between homologous (where source and test cultivars are
the same) and heterologous combinations was highly
significant. On two susceptible cultivars, aggressiveness
was 17.2% greater in homologous than heterologous
combinations. The authors concluded that M. graminicola
isolates were better adapted to the host cultivar from
which they originated than to other cultivars. However, in
another study with the same pathosystem, Cowger &
Mundt (2002) found only weak evidence that the fungal
population was subject to selection for greater aggressive-
ness on its host of origin.
Some studies gave mixed results or found no evidence
at all for quantitative adaptation to the cultivar of origin.
Jeffrey et al. (1962) compared nine isolates of P. infestans
grown on potato tubers of three cultivars, including their
cultivar of origin. They found evidence of adaptation to
the cultivar of origin for lesion growth rate, but not for
latent period. Knott & Mundt (1991) sampled populations
of P. triticina in field plots and tested their aggressiveness
in a growth chamber on seedlings of the same cultivars,
but found no evidence of increased infection efficiency or
shortened latent period on the cultivar of origin. Similarly,
Zhan et al. (2002) found no clear evidence of increased
lesion size for M. graminicola isolates on the wheat cultivar
from which they were isolated.
This lack of clarity could partly result from the limited
number of isolates tested (three in Bonman et al., 1989;
five in Zhan et al., 2002), which may not represent the
original population properly. In addition, since a differential
effect between seedlings and adult plants was shown
(Milus & Line, 1980), it is possible that seedling tests
(Knott & Mundt, 1991; Zhan et al., 2002) may not reveal
quantitative differences in aggressiveness components
selected on adult plants.
Adaptation to quantitative resistance
Among the studies on pathogen adaptation to host
cultivars, a few specifically refer to identified quantitative
resistances.
Lehman & Shaner (1997) studied adaptation of P. triticina
on a partially resistant cultivar in an artificial-selection
experiment. They made an isolate population from 200–
300 uredinia collected from volunteer seedlings in the field.
The population was grown for five asexual generations
under greenhouse conditions on adult plants of a wheat
cultivar with quantitative resistance (determined by four
different genes with unequal effects), then tested on five
different cultivars, including three other partially resistant
cultivars and a susceptible check. At each generation, a
truncation selection procedure was applied: the spores
produced by early erupting uredinia (lesions) were collected
Plant Pathology (2009) 58, 409–424
 Aggressiveness of plant pathogens
separately from those of later erupting uredinia. This
resulted in strong selection for a shortened latent period.
Before selection, the latent period was 4.3 days longer on
the resistant cultivar than on a susceptible control. This
difference was reduced to 2.3 days after selection, which
means that the selected population overcame 47% of
the resistance. The authors estimated that the selected
population had overcome at least one of the resistance
genes with partial effects. It is interesting to note that the
data (Fig. 2 in their paper) suggested that the latent period
was reduced on all resistant cultivars but did not change
on the susceptible control (this effect was not statistically
significant on the additional cultivars). This selection for
a shorter latent period also changed spore production
per lesion, which increased on the resistant cultivar but
decreased on the susceptible check. These results were
globally confirmed in a later experiment (Lehman &
Shaner, 2007).
Kolmer & Leonard (1986) obtained an increased lesion
size in C. heterostrophus by artificial selection on maize
cultivars with partial resistance. They studied successive
pathogen generations on five different cultivars and, at
each pathogen generation, they mated the seven (out of 25)
most aggressive isolates, i.e. those showing the greatest
lesion sizes. This resulted in a significant increase in lesion
length, both across all the cultivars tested (5–10%) and
specifically on the cultivar of selection (14%).
Clifford & Clothier (1974) sampled P. hordei isolates
on three different cultivars and multiplied these field
populations in the laboratory for between four and seven
generations, on seedlings of the host of origin. One of the
cultivars (Vada) was known to exhibit quantitative
resistance that reduced infection efficiency. This study
clearly showed a differential adaptation to the cultivar
of origin, with significant interactions between ‘isolate
population’ and cultivar. Moreover, populations multiplied
on Vada showed increased infection efficiency on this
cultivar, as well as on the other cultivars. In this experiment,
the increase in infectivity was associated with a decrease
in spore production per lesion. However, given the density
dependence of spore production for such pathogens, it is
possible that the decrease in spore production simply
resulted from a density effect.
In order to evaluate the long-term durability of quan-
titative resistance, it is of primary importance to understand
how the deployment of such resistance affects aggressiveness
in pathogen populations. Very few reports have compared
the selective effect of susceptible and quantitatively resistant
cultivars on pathogen populations. A theoretical model
(Gandon & Michalakis, 2000) predicts that increasing
levels of quantitative host resistance will select for increasing
levels of damage caused by the parasite to its host
(‘virulence’ as defined in ecology). An experimental study
by Cowger & Mundt (2002) was in accordance with this
prediction: changes in average aggressiveness (estimated
by disease severity) of M. graminicola were compared
during field epidemics on six cultivars differing in their
resistance levels. It appeared that the highest levels of
aggressiveness at the end of the epidemics were found on
Plant Pathology (2009) 58, 409 – 424
419
the more resistant cultivars, and the data presented tended
to support the conclusion that resistant hosts select for
more aggressive pathogens than susceptible hosts. In a
recent study on the same pathosystem (Krenz et al., 2008),
evidence for adaptation to Madsen, a quantitatively resistant
wheat cultivar, remained equivocal because of an incon-
sistency among results obtained in the different trials.
However, it was previously shown that the quantitative
resistance of this cultivar was gradually eroded (Mundt
et al., 2002a), which, together with other studies (Ahmed
et al., 1996; Zhan et al., 2002), suggests an adaptation of
pathogen populations to Madsen’s quantitative resistance.
Results obtained with M. graminicola on the selective
effect exerted by quantitative resistance on a fungal
pathogen are consistent with other reports on different
systems. For example, potato cyst nematodes (Globodera
pallida) reared for 12 generations on four partially resistant
potato genotypes exhibited an increased reproductive
rate, whereas those raised on susceptible potato cultivars
did not (Phillips & Blok, 2008). Moreover, selection
was specific to the source of resistance used: populations
selected on a particular source of resistance reproduced
better on hosts with that source of resistance. Pink et al.
(1992) suggested that the multiplication of lettuce mosaic
virus in lettuce (Lactuca sativa) cultivars with quantitative
resistance may have contributed to the emergence of more
aggressive viral strains.
It is interesting to note that a similar adaptation effect
was found in M. graminicola toward a multisite fungicide
(Cowger & Mundt, 2002): isolates from sprayed plots
were more aggressive than isolates from unsprayed ones.
The authors suggested that the multisite fungicide and
quantitative host resistance exercised similar selective
pressures on the fungal populations.
Aggressiveness in an evolutionary perspective
Current uses of the term ‘aggressiveness’ in plant pathology
are operational for a discipline that primarily aims at
reducing the impact of diseases on crop yield and quality.
However, to understand how adaptation of pathogens to
their hosts and environments is translated in terms of
aggressiveness, it is essential to be able to link the concept
of aggressiveness to other concepts used in evolutionary
epidemiology, i.e. fitness and virulence (Galvani, 2003).
Fitness is generally defined as the per capita rate of
increase of an individual or a gene copy (Futuyma, 1997).
It is frequently measured as the average number of
secondary infections produced from a single infected host
in the absence of density-dependent constraints [also
known as R0 (May & Anderson, 1983); see Salvaudon
et al. (2007) for a plant pathogen application]. Although
focussing on among-host transmission seems natural for
many animal pathogens, it may be more relevant in some
plant pathogens to measure fitness as the average number
of secondary lesions produced from a single initial lesion
in the absence of density-dependent constraints, including
alloinfection (among-host transmission) and autoinfection
(within-host multiplication).
420 B. Pariaud et al.
In evolutionary epidemiology, as well as in animal
and human epidemiology, and unlike in plant pathology,
virulence is defined as the quantity of damage induced by
a pathogen on its host, and is measured in units of host
fitness and/or mortality (Poulin & Combes, 1999; Read
et al., 1999). Virulence is generally assumed to be a direct
consequence of within-host pathogen multiplication,
although this direct causative relationship can be questioned
(Day, 2002).
Aggressiveness, because it describes the ability of a
pathogen to cause severe epidemics at the host population
scale, combines both notions of pathogen fitness and
virulence. Both fitter and more virulent pathogens are
generally considered as more aggressive since they will
cause faster epidemics or more damage to the host popu-
lation, respectively. However, aggressiveness cannot be
considered strictly equivalent to pathogen fitness. Fitness-
related traits such as spore viability or inter-seasonal
survival are not usually considered aggressiveness traits.
Similarly, aggressiveness in plant pathology is not a
synonym for virulence in evolutionary epidemiology since
many aggressiveness components (e.g. sporulation rate)
do not quantify a decrease in host fitness or survival. In
addition, other parameters that would be relevant to
measuring pathogen virulence, such as decrease in host
photosynthetic ability (usually larger than the effect
accounted for by lesion size, see Bastiaans, 1991) and
induced necrosis (pathogen-induced senescence, distinct
from necrotic infected tissue, e.g. Magboul et al., 1992)
are not usually measured.
As seen above, aggressiveness can be broken down into
several components and each of these components is
likely to evolve (e.g. Leonard, 1969; Kolmer & Leonard,
1986; Lehman & Shaner, 1997, 2007). Recognizing that
aggressiveness results from the expression of elementary
quantitative components should make it possible to
benefit from the predictions of evolutionary epidemiology
models. For instance, most of these theoretical approaches
assume that within-host multiplication harms hosts (i.e.
causes virulence), so that fitness results from a trade-off
between pathogen transmission and virulence (Day, 2003;
Galvani, 2003). As a consequence, aggressiveness com-
ponents that are more closely related to transmission are
not expected to evolve under the same evolutionary
forces as aggressiveness components linked to virulence.
Establishing the correspondence between aggressiveness
components, transmission and virulence is not always
easy, however. Lesion size can be related to virulence
(Bastiaans, 1991). The latent period may have a twofold
status, since a shorter latent period accelerates transmission
but a longer latency could allow a greater development of
the pathogen’s organs within host tissues and increase its
ability to exploit the host. Infection efficiency, spore pro-
duction rate and infectious period are transmission traits,
but also participate in within-host multiplication through
autoinfection.
Some difficulties met in this analysis obviously come from
evolutionary epidemiology models making a distinction
between within- and among host scales, which is not
always relevant in plant pathology. Although many
animal diseases are caused by parasites with systemic
effects that globally reduce the host viability, many plant
parasites have localized effects and do not affect their host
in a systemic manner. This is particularly true for foliar
parasites, for which it has been demonstrated that the
effect on the host is largely limited to a local reduction in
photosynthetic capacity (Bastiaans, 1991; Robert et al.,
2004). However, the pathogen can increase dramatically
on an infected host leaf through autoinfection (see Lannou
et al., 2008), which is analogous to within-host multipli-
cation in animal diseases. The consequence is that the
correspondence between aggressiveness components,
transmission and virulence depends on the scale con-
sidered. At the scale of the lesion for instance, lesion
growth may be considered as causing virulence (i.e. killing
local host tissues), and other traits (infection efficiency, spore
production, etc.) would correspond to transmission.
Theoretical work on pathogen evolution progresses
much faster than experimental work, and the lack of
experimental evidence to evaluate theoretical predictions
and model hypotheses has been emphasized (Ebert &
Bull, 2003). The growing body of experimental data on
pathogen adaptation for quantitative traits, based on the
study of crop pathogens, could offer opportunities to fill
this gap, provided that the traits measured are clearly
linked to parameters that underlie evolution.
The extent of phenotypic variability and of heritability
of these traits is likely to radically condition the durability
of resistant cultivars. Collecting more information on
the genetic architecture of aggressiveness components
could bring valuable information for the development of
quantitative resistance. Nonetheless, considering the huge
evolutionary potential of plant pathogens, the design
of quantitative resistance should take advantage of the
potential trade-offs between aggressiveness components,
in order to enhance the sustainability of crop resistance.
Such trade-offs would reflect the constraint for the
pathogen to simultaneously invest in different traits,
such as sporulation or within-host growth. It is there-
fore most important that plant pathologists record, to the
greatest extent possible, all aggressiveness components in
pathogen adaptation studies, and check for any negative
correlations between them. Further study on the survival
of pathogens during intercropping, although difficult in
most pathosystems, would bring additional valuable
information for both understanding pathogen evolution
and improving disease management.
A major question related to host resistance durability
is to evaluate to what extent plant pathogens can be con-
sidered specialists on a given host cultivar or generalists.
It remains difficult at this time to produce an answer from the
experimental data presented above. Clifford & Clothier
(1974) observed a non-specific increase of aggressiveness
in P. hordei induced by repeated multiplication on a cultivar
with quantitative resistance, but other results obtained in
artificial-selection experiments (Leonard, 1969; Chin &
Wolfe, 1984; Villaréal & Lannou, 2000), as well as field
data (Ahmed et al., 1996), suggested that selection for
Plant Pathology (2009) 58, 409–424
 Aggressiveness of plant pathogens
aggressiveness led to specific adaptation to a given host.
Here again, more data are needed on the level of specificity
of each individual aggressiveness component.
A growing body of evidence shows that pathogen
populations may quantitatively adapt to their compatible
hosts under laboratory, experimental field and natural
conditions, resulting in modifications of their aggressive-
ness. The speed and nature of such adaptations will deter-
mine the durability of quantitative resistance in cultivated
landscapes.
References
Ahmed HU, Mundt CC, Coakley SM, 1995. Host–pathogen
relationship of geographically diverse isolates of
Septoria tritici and wheat cultivars. Plant Pathology 44,
838–47.
Ahmed HU, Mundt CC, Hoffer ME, Coakley SM, 1996.
Selective influence of wheat cultivars on pathogenicity of
Mycosphaerella graminicola (anamorph Septoria tritici).
Phytopathology 86, 454– 8.
Alexander HM, Groth JV, Roelfs AP, 1985. Virulence changes
in Uromyces appendiculatus after five asexual generations on
a partially resistant cultivar of Phaseolus vulgaris.
Phytopathology 75, 449–53.
Andrivon D, Pilet F, Montarry J et al., 2007. Adaptation of
Phytophthora infestans to partial resistance in potato:
evidence from French and Moroccan populations.
Phytopathology 97, 338– 43.
Ballini E, Morel J-B, Droc G et al., 2008. A genome-wide
meta-analysis of rice blast resistance genes and quantitative
trait loci provides new insights into partial and complete
resistance. Molecular Plant-Microbe Interactions 21,
859–68.
Barrett JA, 1985. The gene-for-gene hypothesis: parable or
paradigm. In: Rollinson D, Anderson RM, eds. Ecology and
Genetics of Host-Parasite Systems. London, UK: Academic
Press, 215–25.
Bastiaans L, 1991. Ratio between virtual and visual lesion size
as a measure to describe reduction in leaf photosynthesis of
rice due to leaf blast. Phytopathology 81, 611–5.
Blanch PA, Asher MJC, Burnett JH, 1981. Inheritance of
pathogenicity and cultural characters in Gaeumannomyces
graminis var. tritici. Transactions of the British Mycological
Society 77, 391–9.
Bonman JM, Bandong JM, Lee YH, Lee EJ, 1989. Race-specific
partial resistance to blast in temperate japonica rice cultivars.
Plant Disease 73, 496–9.
Bronson CR, Ellingboe AH, 1986. The influence of four
unnecessary genes for virulence on the fitness of Erysiphe
graminis f.sp. tritici. Phytopathology 76, 154– 8.
Carlisle DJ, Cooke LR, Watson S, Brown AE, 2002. Foliar
aggressiveness of Northern Ireland isolates of Phytophthora
infestans on detached leaflets of three potato cultivars.
Plant Pathology 51, 424– 34.
Carson ML, 1998. Aggressiveness and perennation of isolates of
Cochliobolus heterostrophus from North Carolina. Plant
Disease 82, 1043 –7.
Caten CE, 1974. Intra-racial variation in Phytophthora
infestans and adaptation to field resistance for potato blight.
Annals of Applied Biology 77, 259–70.
Plant Pathology (2009) 58, 409 – 424
421
Caten CE, Person C, Groth JV, Dhahi SJ, 1984. The genetics of
pathogenic aggressiveness in three dikaryons of Ustilago
hordei. Canadian Journal of Botany 62, 1209–19.
Chin KM, Wolfe MS, 1984. Selection of Erysiphe graminis in
pure and mixed stands of barley. Plant Pathology 33,
535–46.
Clifford BC, Clothier RB, 1974. Physiologic specialization of
Puccinia hordei on barley hosts with non-hypersensitive
resistance. Transactions of the British Mycological Society 63,
421–30.
Cohen Y, Rotem J, 1970. The relationship of sporulation to
photosynthesis in some obligatory and facultative parasites.
Phytopathology 60, 1600 –4.
Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK, 2005. An
introduction to markers, quantitative trait loci (QTL)
mapping and marker-assisted selection for crop improvement:
the basic concepts. Euphytica 142, 169 –96.
Cowger C, Mundt CC, 2002. Aggressiveness of Mycosphaerella
graminicola isolates from susceptible and partially resistant
wheat cultivars. Phytopathology 92, 624 –30.
Cowger C, Hoffer ME, Mundt CC, 2000. Specific adaptation by
Mycosphaerella graminicola to a resistant wheat cultivar.
Plant Pathology 49, 445 –51.
Cumagun CJR, Miedaner T, 2003. Aggressiveness of 42 isolates
of Gibberella zeae (Fusarium graminearum) in wheat under
field and greenhouse conditions. Zeitschrift für
Pflanzenkrankheiten und Pflanzenschutz 110, 554 –9.
Cumagun CJR, Miedaner T, 2004. Segregation for
aggressiveness and deoxynivalenol production of a
population of Gibberella zeae causing head blight of wheat.
European Journal of Plant Pathology 110, 789 –99.
Cumagun CJR, Bowden RL, Jurgenson JE, Leslie JF, Miedaner
T, 2004. Genetic mapping of pathogenicity and
aggressiveness of Gibberella zeae (Fusarium graminearum)
toward wheat. Phytopathology 94, 520 –6.
Day JP, Shattock RC, 1997. Aggressiveness and other factors
relating to displacement of populations of Phytophthora
infestans in England and Wales. European Journal of Plant
Pathology 103, 379–91.
Day T, 2002. Virulence evolution via host exploitation and
toxin production in spore-producing pathogens. Ecology
Letters 5, 471–6.
Day T, 2003. Virulence evolution and the timing of disease
life-history events. Trends in Ecology & Evolution 18, 113–8.
Develey-Rivière MP, Galiana E, 2007. Resistance to pathogens
and host developmental stage: a multifaceted relationship
within the plant kingdom. New Phytologist 175, 405–16.
Dowkiw A, Husson C, Frey P, Pinon J, Bastien C, 2003. Partial
resistance to Melampsora larici-populina leaf rust in hybrid
poplars: genetic variability in inoculated excised leaf disk
bioassay and relationship with complete resistance.
Phytopathology 93, 421–7.
Ebbole DJ, 2007. Magnaporthe as a model for understanding
host–pathogen interactions. Annual Review of
Phytopathology 45, 437–56.
Ebert D, Bull JJ, 2003. Challenging the trade-off model for the
evolution of virulence: is virulence management feasible?
Trends in Microbiology 11, 15–20.
Emge RG, Kingsolver CH, Johnson DR, 1975. Growth of
the sporulating zone of Puccinia striiformis and its
relationship to stripe rust epiphytology. Phytopathology
65, 679–81.
422 B. Pariaud et al.
Eversmeyer MG, Kramer CL, Browder LE, 1980. Effect of
temperature and host:parasite combination on the latent
period of Puccinia recondita in seedling wheat plants.
Phytopathology 70, 938– 41.
FBPP, 1973. A Guide to the Use of Terms in Plant Pathology.
Kew, UK: Commonwealth Mycological Institute:
Phytopathological Papers No 17.
Flier WG, Turkensteen LJ, 1999. Foliar aggressiveness of
Phytophthora infestans in three potato growing regions in the
Netherlands. European Journal of Plant Pathology 105,
381–8.
Flor HH, 1955. Host-parasite interaction in flax rust. its genetics
and other implications. Phytopathology 45, 680–5.
Flor HH, 1971. Current status of the gene-for-gene concept.
Annual Review of Phytopathology 9, 275–96.
Futuyma DJ, 1997. Evolutionary Biology, 3rd edn. Sunderland,
MA, USA: Sinauer Associates.
Galvani AP, 2003. Epidemiology meets evolutionary ecology.
Trends in Ecology and Evolution 18, 132–9.
Gandon S, Michalakis Y, 2000. Evolution of parasite virulence
against qualitative or quantitative host resistance.
Proceedings of the Royal Society of London, Series B 267,
985–90.
Gilbert J, Abramson D, McCallum B, Clear R, 2001.
Comparison of Canadian Fusarium graminearum isolates for
aggressiveness, vegetative compatibility, and production of
ergosterol and mycotoxins. Mycopathologia 153, 209–15.
Gilles T, Fitt BDL, McCartney HA, Papastamati K, Steed JM,
2001. The roles of ascospores and conidia of Pyrenopeziza
brassicae in light leaf spot epidemics on winter oilseed rape
(Brassica napus) in the UK. Annals of Applied Biology 138,
141–52.
Gout L, Kuhn ML, Vincenot L et al., 2007. Genome structure
impacts molecular evolution at the AvrLm1 avirulence locus
of the plant pathogen Leptosphaeria maculans.
Environmental Microbiology 9, 2978–92.
Goyeau H, Park R, Schaeffer B, Lannou C, 2006. Distribution
of pathotypes with regard to host cultivars in French wheat
leaf rust populations. Phytopathology 96, 264–73.
Grant MW, Archer SA, 1983. Calculation of selection
coefficients against unnecessary genes for virulence from field
data. Phytopathology 73, 547–51.
Halama P, Skajennikoff M, Dehorter B, 1999. Tetra analysis of
mating type, mutations, esterase and aggressiveness in
Phaeosphaeria nodorum. Mycological Research 103, 43–9.
Hamid AH, Ayers JE, Schein RD, Hill RR, 1982a. Components
of fitness attributes in Cochliobolus carbonum race 3.
Phytopathology 72, 1166–9.
Hamid AH, Ayers JE, Hill RR, 1982b. Host × isolate interaction
in corn inbreds inoculated with Cochliobolus carbonum race
3. Phytopathology 72, 1169–73.
Hawthorne BT, Ball RD, Reesgeorge J, 1994. Genetic-analysis
of variation of pathogenicity in Nectria haematococca
(Fusarium solani) on Cucurbita sp. Mycological Research 98,
1183–91.
Hill JP, Nelson RR, 1982. The heritability of three parasitic
fitness attributes of Helminthosporium maydis race
T. Phytopathology 72, 525–8.
Holliday P, 1998. A Dictionary of Plant Pathology. Cambridge,
UK: Cambridge University Press.
Hovmøller MS, Munk L, Østergård H, 1993. Observed and
predicted changes in virulence gene frequencies at 11 loci in
a local barley powdery mildew population. Phytopathology
83, 253–60.
Imhoff MW, Leonard KJ, Main CE, 1982. Pattern of bean rust
lesion size increase and spore production. Phytopathology 72,
441–6.
Jeffrey SIB, Jinks JL, Grindle M, 1962. Interracial variation in
Phytophthora infestans and field resistance to potato blight.
Genetica 32, 323–38.
Jensen B, Munk L, 1997. Nitrogen-induced changes in colony
density and spore production of Erysiphe graminis f.sp.
hordei on seedlings of six spring barley cultivars.
Plant Pathology 46, 191–202.
Jinks JL, Grindle M, 1963. Changes induced by training in
Phytophthora infestans. Heredity 18, 245–64.
Johnson DA, 1980. Effect of low temperature on the latent
period of slow and fast rusting winter wheat genotypes.
Plant Disease 64, 1006 –8.
Kardin MK, Groth JV, 1989. Density-dependent fitness
interactions in the bean rust fungus. Phytopathology 79,
409–12.
Karolewski Z, Evans N, Fitt BDL, Todd AD, Baierl A, 2002.
Sporulation of Pyrenopeziza brassicae (light leaf spot) on
oilseed rape (Brassica napus) leaves inoculated with
ascospores or conidia at different temperatures and wetness
durations. Plant Pathology 51, 654–65.
Kato M, Mizubuti ES, Goodwin SB, Fry WE, 1997. Sensitivity
to protectant fungicides and pathogenic fitness of clonal
lineages of Phytophthora infestans in the United States.
Phytopathology 87, 973–8.
Katsuya K, Green GJ, 1967. Reproductive potentials of races
15B and 56 of wheat stem rust. Canadian Journal of Botany
45, 1077–91.
Knott EA, Mundt CC, 1991. Latent period and infection
efficiency of Puccinia recondita f.sp. tritici populations
isolated from different wheat cultivars. Phytopathology 81,
435–9.
Kolmer JA, 1990. Selection of virulence phenotypes in a
heterogeneous, asexual population of Puccinia recondita
f.sp. tritici. Phytopathology 80, 1377–81.
Kolmer JA, 1993. Selection in a heterogeneous population of
Puccinia recondita f.sp. tritici. Phytopathology 83, 909 –14.
Kolmer JA, Leonard KJ, 1986. Genetic selection and adaptation
of Cochliobolus heterostrophus to corn hosts with partial
resistance. Phytopathology 76, 774 –7.
Krenz JE, Sackett KE, Mundt CC, 2008. Specificity of
incomplete resistance to Mycosphaerella graminicola in
wheat. Phytopathology 98, 555–61.
Krupinsky JM, 1989. Variability in Septoria musiva in
aggressiveness. Phytopathology 79, 413 –6.
Kuhn RC, Ohm HW, Shaner GE, 1978. Slow leaf-rusting
resistance in wheat against twenty-two isolates of Puccinia
recondita. Phytopathology 68, 651–6.
Labbé P, Berticat C, Berthomieu A et al., 2007. Forty years
of erratic insecticide resistance evolution in the mosquito
Culex pipiens. PLoS Genetics 3, e205. doi:10.1371/
journal.pgen.0030205.
Laine AL, 2008. Temperature-mediated patterns of local
adaptation in a natural plant–pathogen metapopulation.
Ecology Letters 11, 327–37.
Lambert DH, Currier AI, 1997. Differences in tuber rot
development for North American clones of Phytophthora
infestans. American Potato Journal 74, 39–43.
Plant Pathology (2009) 58, 409–424
 Aggressiveness of plant pathogens
Lannou C, Mundt CC, 1997. Evolution of a pathogen
population in host mixtures: rate of emergence of complex
races. Theoretical and Applied Genetics 94, 991–9.
Lannou C, Soubeyrand S, Frezal L, Chadœuf J, 2008.
Autoinfection in wheat leaf rust epidemics. New Phytologist
177, 1001–11.
Leach JE, Vera Cruz CM, Bai J, Leung H, 2001. Pathogen fitness
penalty as a predictor of durability of disease resistance genes.
Annual Review of Phytopathology 39, 187–224.
Lehman JS, Shaner G, 1996. Genetic variation in latent period
among isolates of Puccinia recondita f.sp. tritici on partially
resistant wheat cultivars. Phytopathology 86, 633– 41.
Lehman JS, Shaner G, 1997. Selection of populations of
Puccinia recondita f.sp. tritici for shortened latent period on
a partially resistant wheat cultivar. Phytopathology 87,
170–6.
Lehman JS, Shaner G, 2007. Heritability of latent period
estimated from wild-type and selected populations of Puccinia
triticina. Phytopathology 97, 1022–9.
Leonard KJ, 1969. Selection in heterogeneous populations of
Puccinia graminis f.sp. avenae. Phytopathology 59, 1851–7.
Leonard KJ, 1977. Virulence, temperature optima, and
competitive abilities of isolines of races T and O of Bipolaris
maydis. Phytopathology 67, 1273–9.
Leonard KJ, Thakur RP, Leath S, 1988. Incidence of Bipolaris
and Exserohilum species in corn leaves in North Carolina.
Plant Disease 72, 1034–8.
Levin BR, Perrot V, Walker N, 2000. Compensatory mutations,
antibiotic resistance and the population genetics of adaptive
evolution in bacteria. Genetics 154, 985–97.
Lind M, Dalman K, Stenlid J, Karlsson B, Olson A, 2007.
Identification of quantitative trait loci affecting virulence in
the Basidiomycete Heterobasidion annosum s.l. Current
Genetics 52, 35–44.
Lovell DJ, Hunter T, Powers SJ, Parker SR, Van den Bosch F,
2004. Effect of temperature on latent period of septoria leaf
blotch on winter wheat under outdoor conditions.
Plant Pathology 53, 170–81.
Magboul AM, Geng S, Gilchrist DG, Jackson LF, 1992.
Environmental influence on the infection of wheat by
Mycosphaerella graminicola. Phytopathology 82, 1407–13.
May RM, Anderson RM, 1983. Epidemiology and genetics in
the coevolution of parasites and hosts. Proceedings of the
Royal Society of London, Series B 219, 281–313.
Mehta YR, Zadoks JC, 1970. Uredospore production and
sporulation period of Puccinia recondita f.sp. triticina on
primary leaves of wheat. Netherlands Journal of Plant
Pathology 76, 267–76.
Menzies JG, MacNeill BH, 1987. Effect of unnecessary genes for
virulence on six components of parasitic fitness in Erysiphe
graminis f.sp. tritici. Canadian Journal of Plant Pathology 9,
214–7.
Miller JS, Hamm PB, Johnson DA, 1997. Characterization of
the Phytophthora infestans population in the Columbia Basin
of Oregon and Washington from 1992 to 1995.
Phytopathology 87, 656–60.
Miller JS, Johnson DA, Hamm PB, 1998. Aggressiveness of
isolates of Phytophthora infestans from the Columbia Basin
of Washington and Oregon. Phytopathology 88, 190–7.
Milus EA, Line RF, 1980. Characterization of resistance to leaf
rust in Pacific Northwest wheat lines. Phytopathology 70,
167–72.
Plant Pathology (2009) 58, 409 – 424
423
Milus EA, Seyran E, McNew R, 2006. Aggressiveness of
Puccinia striiformis f.sp. tritici isolates in the south-central
States. Plant Disease 90, 847–52.
Montarry J, Corbière R, Andrivon D, 2007. Is there a trade-off
between aggressiveness and overwinter survival in
Phytophthora infestans? Functional Ecology 21, 603–10.
Mundt CC, Cowger C, Garrett KA, 2002a. Relevance of
integrated disease management to resistance durability.
Euphytica 124, 245–52.
Mundt CC, Nieva LP, Vera Cruz CM, 2002b. Variation for
aggressiveness within and between lineages of Xanthomonas
oryzae pv. oryzae. Plant Pathology 51, 163–8.
Ohm HW, Shaner GE, 1975. Segregation for slow leaf-rusting
in wheat. Agronomy Abstracts 67, 59.
Østergård H, 1987. Estimating relative fitness in asexually
reproducing plant pathogen populations. Theoretical and
Applied Genetics 74, 87–94.
Pariaud B, Robert C, Goyeau H, Lannou C, 2007. Quantitative
adaptation of wheat leaf rust populations (Puccinia triticina)
to a host cultivar and correlations between components of
aggressiveness. Phytopathology 97, S89.
Parlevliet JE, 1977. Evidence of differential interaction in the
polygenic Hordeum vulgare – Puccinia hordei relation during
epidemic development. Phytopathology 67, 776–8.
Parlevliet JE, 1993. What is durable resistance, a general outline.
In: Jacobs T, Parlevliet JE, eds. Durability of Disease
Resistance. Dordrecht, the Netherlands: Kluwer Academic
Publishers, 23–39.
Paxman GJ, 1963. Variation in Phytophthora infestans.
European Potato Journal 6, 14–23.
Phillips MS, Blok VC, 2008. Selection for reproductive ability in
Globodera pallida populations in relation to quantitative
resistance from Solanum vernei and S. tuberosum ssp.
andigena CPC2802. Plant Pathology 57, 573–80.
Pink DAC, Lot H, Johnson R, 1992. Novel pathotypes of lettuce
mosaic virus – breakdown of a durable resistance? Euphytica
63, 169–74.
Poulin R, Combes C, 1999. The concept of virulence:
interpretations and implications. Parasitology Today 15,
474–5.
Price JS, Bever JD, Clay K, 2004. Genotype, environment,
and genotype by environment interactions determine
quantitative resistance to leaf rust (Coleosporium asterum)
in Euthamia graminifolia (Asteraceae). New Phytologist 162,
729–43.
Pringle A, Taylor JW, 2002. The fitness of filamentous fungi.
Trends in Microbiology 10, 474–81.
Read AF, Aaby P, Antia R et al., 1999. Group report: what can
evolutionary biology contribute to understanding virulence?
In: Stearns SC, ed. Evolution in Health and Disease. Oxford,
UK: Oxford University Press, 205–15.
Robert C, Bancal MO, Lannou C, 2004. Wheat leaf rust
uredospore production on adult plants: influence of leaf
nitrogen content and septoria tritici blotch. Phytopathology
94, 712–21.
Rouse DI, Nelson RR, MacKenzie DR, Armitage CR, 1980.
Components of rate-reducing resistance in seedlings of four
wheat cultivars and parasitic fitness in six isolates of Erysiphe
graminis f.sp. tritici. Phytopathology 70, 1097–100.
Sache I, 1997. Effect of density and age of lesions on sporulation
capacity and infection efficiency in wheat leaf rust (Puccinia
recondita f.sp. tritici). Plant Pathology 46, 581–9.
424 B. Pariaud et al.
Sackett KE, Mundt CC, 2005. The effects of dispersal gradient
and pathogen life cycle components on epidemic velocity in
computer simulations. Phytopathology 95, 992–1000.
Salvaudon L, Héraudet V, Shykoff JA, 2007. Genotype-specific
interactions and the trade-off between host and parasite
fitness. BMC Evolutionary Biology 7, 189.
Scharen AL, Eyal Z, 1983. Analysis of symptoms on spring and
winter wheat cultivars inoculated with different isolates of
Septoria nodorum. Phytopathology 73, 143–7.
Schlötterer C, 2003. Hitchhiking mapping – functional
genomics from the population genetics perspective.
Trends in Genetics 19, 32–8.
Schoustra SE, Slakhorst M, Debets AJM, Hoekstra RF, 2006.
Reducing the cost of resistance; experimental evolution in the
filamentous fungus Aspergillus nidulans. Journal of
Evolutionary Biology 19, 1115–27.
Shaner GE, 1980. Probits for analyzing latent period data in
studies of slow rusting resistance. Phytopathology 70, 1179–
82.
Shaw MW, 1990. Effects of temperature, leaf wetness and
cultivar on the latent period of Mycosphaerella graminicola
on winter wheat. Plant Pathology 39, 255–68.
Shurtleff MC, Averre CW, 1997. Glossary of Plant-Pathological
Terms. St Paul, MN, USA: APS Press.
Singh RP, Huerta-Espino J, William HM, 2005. Genetics and
breeding for durable resistance to leaf and stripe rusts in
wheat. Turkish Journal of Agriculture and Forestry 29,
121–7.
Storz JF, 2005. Using genome scans of DNA polymorphism to
infer adaptive population divergence. Molecular Ecology 14,
671–88.
Subrahmanyam P, MacDonald D, Subba Rao PV, 1983.
Influence of host genotype on uredospore production and
germinability in Puccinia arachidis. Phytopathology 73,
726–9.
Thrall PH, Burdon JJ, 2003. Evolution of virulence in a plant
host-pathogen metapopulation. Science 299, 1735–7.
Thurston HD, 1961. The relative survival ability of races of
Phytophthora infestans in mixtures. Phytopathology 51,
748–55.
Tiedemann AV, 1996. Single and combined effects of nitrogen
fertilization and ozone on fungal leaf diseases on wheat.
Journal of Plant Diseases and Protection 103, 409–19.
Tomerlin JR, Eversmeyer MG, Kramer CL, Browder LE, 1983.
Temperature and host effects on latent and infectious periods
and on urediniospore production of Puccinia recondita f.sp.
tritici. Phytopathology 73, 414–9.
Turechek WW, Stevenson KL, 1998. Effects of host resistance,
temperature, leaf wetness, and leaf age on infection and lesion
development of pecan scab. Phytopathology 88, 1294–301.
Van der Plank JE, 1963. Plant Diseases: Epidemics and Control.
New York, USA: Academic Press.
Van der Plank JE, 1968. Disease Resistance in Plants. New
York, USA: Academic Press.
Van Ginkel M, Scharen AL, 1988. Host-pathogen relationships
of wheat and Septoria tritici. Phytopathology 78, 762–6.
Vera Cruz CM, Bai J, Oña I et al., 2000. Predicting durability of
a disease resistance gene based on an assessment of the fitness
loss and epidemiological consequences of avirulence gene
mutation. Proceedings of the National Academy of Sciences,
USA 97, 13500–5.
Villaréal LMM, Lannou C, 2000. Selection for increased spore
efficacy by host genetic background in a wheat powdery
mildew population. Phytopathology 90, 1300–6.
Wang X, El Hadrami A, Adam LR, Daayf F, 2008. Differential
activation and suppression of potato defence responses by
Phytophthora infestans isolates representing US-1 and US-8
genotypes. Plant Pathology 57, 1026–37.
Weltz HG, Nagarajan S, Kranz J, 1990. Short-term virulence
dynamics of Erysiphe graminis f.sp. hordei in a single
epidemic on two susceptible barley cultivars. Zeitschrift für
Pflanzenkrankheiten und Pflanzenschutz 97, 250 –62.
Xu JR, Peng YL, Dickman MB, Sharon A, 2006. The dawn of
fungal pathogen genomics. Annual Review of
Phytopathology 44, 337–66.
Young ND, 1996. QTL mapping and quantitative disease
resistance in plants. Annual Review of Phytopathology 34,
479–501.
Zhan J, Mundt CC, Hoffer ME, McDonald BA, 2002. Local
adaptation and effect of host genotype on the rate of pathogen
evolution: an experimental test in a plant pathosystem.
Journal of Evolutionary Biology 15, 634 –47.
Plant Pathology (2009) 58, 409–424