Review

Blackwell Publishing Ltd

Research review
A conceptual model for the
development of Phytophthora disease
in Quercus robur

Author for correspondence:

U. Jnsson
Tel. +46 46 2229561
Email: ulrika.jonsson@ekol.lu.se

U. Jnsson
Plant Ecology and Systematics, Department of Ecology, Ecology Building, Lund University, SE223 62
Lund, Sweden

Received: 19 December 2005

Accepted: 24 February 2006

Summary
Key words: Phytophthora, oak decline,
root damage, carbon allocation,
nutrients, soil moisture, Quercus robur
(pedunculate oak).

Here, a conceptual model is presented for the development of Phytophthora disease

in pedunculate oak. The model is presented using the causal loop diagram tool and
gives an overview of how various abiotic and biotic factors, such as soil moisture,
nutrient availability and mycorrhizal colonization, may affect the reproduction and
the infective capacity of soil-borne Phytophthora species, the susceptibility of the
host and subsequent disease development. It is suggested that the link between
the root damage caused by Phytophthora species and overall tree vitality is in the
assimilation and allocation of carbon within the plants. The potential impact of
environmental factors on these processes is discussed. The model is presented with
reference to scenarios related to variation in soil moisture and nutrient availability.
The need for species-specific validation of the model and the implications of the
model are discussed.
New Phytologist (2006) 171: 5568
The Authors (2006). Journal compilation New Phytologist (2006)
doi: 10.1111/j.1469-8137.2006.01743.x

Introduction
During the past decade, several studies have demonstrated
the involvement of soil-borne species of the well-known plant
pathogenic genus Phytophthora in European oak decline.
Brasier et al. (1993) suggested that Phytophthora cinnamomi
contributed to oak decline of Quercus ilex and Quercus suber
in Iberia. Blaschke (1994) observed progressive deterioration
of fine roots and mycorrhizal systems in mature declining
Quercus robur and suggested that the damage was caused by
Phytophthora species. Since then, 12 other Phytophthora species
have been recovered from oak stands growing in a wide variety
of soil conditions across Europe ( Jung & Blaschke, 1996;

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Jung et al., 1996, 2000, 2002; Robin et al., 1998; Gallego

et al., 1999; Hansen & Delatour, 1999; Vettraino et al., 2002;
Balci & Halmschlager, 2003). The most frequently recovered
species is the oak-specific Phytophthora quercina ( Jung et al.,
1999, 2000; Vettraino et al., 2002; Balci & Halmschlager,
2003; Jnsson et al., 2003a). A number of studies have demonstrated that P. quercina, as well as many other Phytophthora
species recovered from oak stands, can cause significant root
rot in oak seedlings grown in glasshouses ( Jung et al., 1996,
1999, 2003b; Robin & Desprez-Loustau, 1998; Robin et al.,
1998; Luque et al., 2000; Sanchez et al., 2002; Jnsson et al.,
2003b; Jnsson, 2004a) as well as in mature trees in the field
( Jung et al., 2000; Jnsson, 2004b). Furthermore, significant

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correlations have been found between the presence of

Phytophthora species in the rhizosphere soil and crown
transparency of mature oaks in several European countries
( Jung et al., 2000; Vettraino et al., 2002; Balci & Halmschlager,
2003; Jnsson et al., 2005).
Although Phytophthora species have been shown to be
involved in the decline of oaks, the link between the root
damage caused by the pathogens and the overall tree vitality
is poorly understood. In addition, the development of the
disease is unclear. The response of the trees to these pathogens
varies widely, ranging from remaining healthy, despite close
association with the pathogen, to succumbing to death shortly
after infection by the pathogen. This indicates that other
factors, biotic and/or abiotic, must be involved in the decline.
From studies on other plant species, mainly agricultural crops,
it is well-known that Phytophthora diseases are highly sensitive
to the prevailing environmental conditions (Erwin & Ribeiro,
1996). By using the information available from other host
Phytophthora combinations, as well as knowledge of forest tree
physiology and the responses of forest trees to stress, a more
comprehensive picture of the Phytophthora disease on oak could
be obtained.
The aim of this paper is thus to present a conceptual model
for the development of Phytophthora disease in pedunculate
oak. The model represents my understanding of the problem
and is an attempt to make my understanding transparent to
other scientists, thereby creating a basis for discussions on the
development of Phytophthora disease in oaks and other forest
tree species. The conceptual model gives an overview of how
various abiotic and biotic factors may affect the reproduction
and infective capacity of Phytophthora, the susceptibility of the
host and the subsequent disease expression. It is suggested that
the link between the root damage caused by the pathogens
and the overall tree vitality is in the carbon (C) assimilation
and allocation patterns within trees. A conceptual model for
the C assimilation and allocation in oaks is thus included in
the conceptual model for the development of Phytophthora
disease in Q . robur. The method chosen to present the
conceptual model is described and the literature on which the
model is based is reviewed in the Theoretical background
section. The model for the development of Phytophthora
disease in Q. robur is presented and its limitations and possible
implications are discussed.

Method
To illustrate the interactions between the host, the pathogen
and the numerous environmental factors involved, the Causal
Loop Diagram (CLD) tool was used. This tool is widely
used in systems analysis and systems dynamics studies,
where complex multidimensional problems require a holistic
approach and studies cannot be carried out solely on isolated
parts of the system (Haraldsson, 2004). Similarly, the present
work assumes a close interdependence between the host and

New Phytologist (2006) 171: 5568

the pathogen, and a strong response of their relationship to

environmental factors. As indicated by their name, CLDs are
diagrams that map the causal relationships between the
parameters constituting a system, thus creating an integrated
network of relationships that is presented in a readable and
transparent way. The CLD developed in this study attempts
to summarize the direct and indirect effects, as well as the
feedback involved in the host-pathogen-environment
system.
The CLDs presenting the conceptual model can be seen in
Figs 1 and 2. The arrows in the CLD represent the causalities
as they carry the effect of the variable at the tail of the arrow
(origin) to the variable at the head of the arrow (target). As
CLDs are conceptual, the only possible changes in the variables
are either an increase or a decrease. All changes take place
over time, but are driven by changes in another variable. A
state of no change is also possible, and thus a variable may
be constant over time. An arrow with a positive causality sign
implies that a change in the origin variable drives a similar
change in the target variable (i.e. an increase in the origin leads
to an increase in the target, and a decrease leads to a decrease).
Arrows with negative causality signs imply a change in the
opposite direction (i.e. an increase in the origin leads to a
decrease in the target, and a decrease leads to an increase). This
means that the arrows themselves do not indicate whether
a variable increases or decreases with time. Bearing in mind
this simple rule regarding arrows, CLDs are able to reproduce
dynamic behaviour that involves changes between increases
and decreases in different variables as the entire system
changes with time. In a balancing system, feedback loops
move the system in the direction towards fluctuation around
an equilibrium point. A feedback loop may also be reinforcing
(i.e. move the system away from the equilibrium point).

Theoretical background
Linking root damage caused by Phytophthora to overall
tree vitality
Plants appear to exhibit a number of rapid responses to
infection by Phytophthora species. Cahill & Weste (1983)
reported an increase in the rate of respiration of eucalypts as
a response to infection by Phytophthora cinnamomi. Increased
respiration rate is a general phenomenon occurring in plants
subjected to stress (Smeedegard-Petersen, 1984; Agrios, 1997;
Orcutt & Nielsen, 2000), and occurs in susceptible plants as
well as resistant plants (Cahill & Weste, 1983). However, in
resistant plants, the increase and the reversion to normal levels
is usually much more rapid than in susceptible plants (Goodman
et al., 1986). Furthermore, the increase in respiration in
resistant plants is probably caused by the initiation of defence
mechanisms that enable the plant to limit the area affected by
the pathogen, while for susceptible plants, a great proportion
of the increase in respiration is likely to be caused by the

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Fig. 1 A conceptual model of how different abiotic and biotic factors influence the aggressiveness of Phytophthora quercina, the susceptibility
of Quercus robur and the subsequent disease development. The variable Phytophthora activity includes all processes that affect the capacity
of the pathogen to infect roots (such as sporangial production, zoospore production, dispersion, adhesion, cyst germination, mycelial growth
and oospore germination); CH, carbohydrates. Note that arrows only indicate the direction of the causality. An arrow with a positive causality
sign implies that a change in the affecting factor drives a change in the affected factor in the same direction. Arrows with negative causality
signs imply a change in the opposite direction. Heavy arrows indicate major feedback loops in the system. For further information and a
description of the causal loop diagram (CLD), see the section A conceptual model for the Phytophthora disease in oak.

invasion and destruction of host tissue (Smeedegard-Petersen,

1984; Cahill et al., 1993; Orcutt & Nielsen, 2000).
In addition to an increase in respiration upon infection
with Phytophthora, seedlings of Castanea sativa, Eucalyptus
sieberi, Fagus sylvatica, Q. ilex and Q. suber have been found
to exhibit a significant reduction in stomatal conductance and
transpiration, as well as reduced leaf water potential and
soil- to leaf-hydraulic conductance (Dawson & Weste, 1984;
Robin et al., 1998, 2001; Maurel et al., 2001a,b, 2004;
Fleischmann et al., 2004). These effects are usually explained
as being the result of disease-induced water stress caused by
impaired water uptake. However, in several studies, the decrease
in stomatal conductance preceded the changes in the water
relations in the plants (Dawson & Weste, 1982; Robin et al.,
1998, 2001; Maurel et al., 2001a,b). Maurel et al. (2001b)
demonstrated a linear decrease in stomatal conductance

with the percentage of necrotic roots, while the soil- to

leaf-hydraulic conductance and leaf water potential were not
affected until the percentage of root rot reached 5060%.
This indicates that stomatal closure may be induced by some
factor other than water stress, such as nutrient limitation or
the presence of elicitin (a toxin produced by certain Phytophthora
species; see, for example, Heiser et al., 1999). However, elicitins
were found not to influence the activity of stomata in chestnut
saplings (Maurel et al., 2004), leaving nutrient limitation as
the more plausible factor.
Infection by Phytophthora species may also influence the
allocation of C. Cahill & McComb (1992) and Cahill et al.
(1993) found an increase in the activity of phenylalanine
ammonia lyase (PAL) upon infection of resistant eucalypts
with P. cinnamomi. This is an essential enzyme in the shikimic
acid pathway, which, together with the pentose phosphate

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Fig. 2 A more detailed causal loop diagram describing how nutrient and water availability may influence the carbon (C) assimilation and
allocation in plants. CH, carbohydrates; photosynthesis nutrients are potassium (K), magnesium (Mg) and manganese (Mn); growth nutrients
are nitrogen (N), phosphorus (P) and sulphur (S). Note that arrows only indicate the direction of the causality. An arrow with a positive causality
sign implies that a change in the affecting factor drives a change in the affected factor in the same direction. Arrows with negative causality
signs imply a change in the opposite direction. For further information and a description of the causal loop diagram (CLD), see the section
A conceptual model for the Phytophthora disease in oak.

pathway, is used to produce phenolic compounds in plants

(Taiz & Zeiger, 2002). Phenolic compounds have been shown
to limit the infection of Phytophthora and other pathogens
(Afek & Sztejnberg, 1988; Cahill & McComb, 1992; Cahill
et al., 1993), as well as impairing the performance of phyllophagous insects (Joseph et al., 1993; Schafellner et al., 1994;
Httenschwiler & Schafellner, 1999). However, it has been
suggested that the allocation of C to production of phenols
diverts resources from the growth of plants (see the section
The C assimilation and allocation of forest trees), and a large
investment in defence against Phytophthora attack may thus
result in retardation of growth.
Since infection by Phytophthora seems to have a substantial
impact on the respiration, assimilation and allocation of C
within the plant, I hypothesize that Phytophthora affect the
plants primarily through their influence on the C budget of
plants. This influence is mediated through reductions in
water or nutrient uptake as a consequence of root damage,
but depends on the prevailing environmental conditions,
thus leading to variable expressions of the disease. In order to

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understand how environmental conditions may influence the

effect that Phytophthora infection has on C assimilation and
allocation in trees, it is necessary to look more thoroughly into
the C physiology of forest trees.
The C assimilation and allocation of forest trees
Several different theories for the allocation of C between
growth and defence have been put forward during recent
decades, ranging from coevolution and sequential evolution
to the role of the plants resources in modifying defensive
responses (reviewed in Hartley & Jones, 1997; Farrar & Jones,
2000). For long-lived plants growing on relatively infertile
soils, such as acidified soils in temperate or boreal regions,
nutrient availability is strongly limiting for growth. Bryant
et al. (1983) thus suggested that the type and amount of
chemical defence will vary with the environmental availability
of nutrients and on the basis of the C/nutrient balance in the
plant tissue (the carbon/nutrient balance hypothesis). Briefly,
the carbon/nutrient balance hypothesis assumes that growth

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is generally more severely affected than photosynthesis under

conditions of nutrient stress, resulting in the accumulation of
carbohydrates. When carbohydrates are produced in excess of
growth requirements, this excess is allocated to the production
of C-based secondary metabolites such as phenols. Nitrogenbased secondary metabolites, on the other hand, decline. The
plant phenotypic response to C stress is essentially the converse.
Accordingly, severe drought, with reductions in stomatal
conductance and consequently C assimilation (Horner, 1990),
results in the preferential allocation of C to primary metabolites
and a decrease in the formation of C-based secondary compounds (Bryant et al., 1983). Herms & Mattson (1992) later
extended the hypothesis of Bryant et al. (1983) by adopting a
more comprehensive approach, addressing the issue of growth
and differentiation from the cell to the species level (growth/
differentiation balance hypothesis).
A large body of evidence is consistent with the C/nutrient
balance hypotheses and the growth/differentiation balance
hypothesis (Bryant et al., 1987; Muzika, 1993; Hikosaka et al.,
2005; Northrup et al., 1995a,b), suggesting that the C/
nutrient balance in plant tissue may be suitable as a predictor
of metabolic and biosynthetic changes in carbohydrate production and allocation in a number of different plant species.
I suggest that these hypotheses are also applicable to oaks
growing in temperate forests where growth is primarily
limited by soil resources. The defence system of oaks largely
constitutes phenolic metabolites, such as tannins (Feeny, 1970).
Phenols originate from phenylalanine, which is a product of
the shikimic acid pathway (Taiz & Zeiger, 2002). Certain
amino acids share this pathway and phenylalanine can thus be
used for either protein or phenolic synthesis (Taiz & Zeiger,
2002). The competition between phenols and other compounds for C is thus obvious ( Jones & Hartley, 1999), and
a trade-off between growth and defence, depending on the
resource availability, seems reasonable. However, growth and
defence may not be fundamentally alternative options for a
tree in all cases. Some tree species use defence compounds such
as terpenes. Terpenes originate from the mevalonic acid pathway
(Taiz & Zeiger, 2002), in which a direct nitrogen-based competitor for the C is lacking. In these species, the levels of defence
compounds have been shown to be insensitive to changes in
nutrient availability (Muzika, 1993; Honkanen et al., 1999).
A generally held opinion for the mechanism behind the
allocation of C between roots and shoots is that there is a functional balance between the size and activity of the shoot and
the size and activity of the root system, with above-ground
parts being favoured when factors perceived by the leaves
(CO2 and light) are limiting, while growth of below-ground
parts are favoured when factors perceived by the roots (water
and nutrients) are limiting (Lambers et al., 1998; Marschner,
2003). A proportionally large investment in roots under
moderately dry conditions is common in Quercus species
(Osonubi & Davies, 1981; van Hees, 1997; Vivin & Guehl,
1997). This is probably caused by the stronger influence of

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drought on leaf expansion than photosynthesis, resulting in

an increase in the availability of carbohydrates, and thus
enhanced export to the roots (Ericsson et al., 1996; Lambers
et al., 1998). Shading, on the other hand, usually results in a
reduction of the root : shoot ratio of oak seedlings (van Hees,
1997; van Hees & Clerkx, 2003). However, Ericsson et al.
(1996) suggested that the effect of nutrient availability on the
C assimilation and allocation in trees is slightly more complex.
According to their studies on birch, a shortage of nitrogen
(N), phosphorus (P) or sulphur (S) usually results in an
increased allocation of C to the roots, thereby favouring root
growth over shoot growth, while a shortage of potassium (K),
magnesium (Mg) or manganese (Mn) results in a decrease in
the allocation of assimilates to the roots (Ericsson, 1995;
Ericsson et al., 1996). The increased allocation of C to roots
as a consequence of shortages of N, P and S is, according to
Ericsson et al. (1996) not an example of a rational plant
reaction. Rather, it appears to reflect a situation in which the
availability of assimilates is not limiting for structural growth.
Roots are the organ whose growth is least suppressed when the
formation of new tissues rather than C fixation is the process
most strongly inhibited by mineral shortage. This is likely to
be caused by the close proximity between sites of mineral
uptake and mineral utilization in the roots, and thus efficient
capture of the limiting nutrient in the root meristems.
Consequently, root growth is favoured over shoot growth.
The decrease in assimilates as a consequence of a shortage of K,
Mg or Mn is, according to Ericsson et al. (1996), a function
of their influence on the photosynthetic apparatus in plants.
Potassium is important for stomata regulation, Mg for capturing light energy and Mn for photosynthetic O2 evolution. In
addition, K and Mg are components of enzymes essential to
C fixation (Lambers et al., 1998; Marschner, 2003). Thus,
limitation by K, Mg and Mn causes a reduction in C fixation
and thus in assimilate availability. The suppression of root
growth compared with shoot growth when plants are low in
nonstructural carbohydrates is most probably a consequence
of the roots being the organ most distant from the supply of
the growth-limiting substrate (carbohydrates). It is important
to note that Ericsson et al. (1996) describe the allocation in
terms of fractions of carbohydrates and nutrients. Substantial
cycling between roots and shoot of C and nutrients has been
demonstrated, and a large fraction of the N taken up by roots
is still exported to the shoot under N-limiting growth conditions. However, a larger fraction of the N will be used in the
root under N-limited conditions than in more favourable N
situations.
The literature reviewed above indicates that both roots and
shoots exert some control over the net acquisition and allocation of C. Farrar & Jones (2003) suggested a shared control
hypothesis in which each flux that contributes to the net
acquisition of C exerts some degree of control over the
process. However, the processes governing the distribution of
C between different plant parts are not well understood.

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The influence of abiotic and biotic factors on

Phytophthora activity and disease development
Water availability Phytophthora diseases are multicyclic,
which means that inoculum may multiply rapidly when the
environmental conditions, the most important of which is the
presence of free water, are favourable (Erwin & Ribeiro, 1996).
Phytophthora diseases may thus develop epidemically when
the soil remains excessively wet for prolonged periods and
temperatures remain fairly low (Erwin & Ribeiro, 1996).
However, regarding the development of disease in oak, drought
or variations in water availability, especially fluctuations between
drought and flooding, also seem to be detrimental to the fineroot system (Brasier et al., 1993; Robin et al., 2001; Sanchez
et al., 2002). Jung et al. (2003a) demonstrated the ability of
P. quercina to survive during periods of drought, and found
higher amounts of root damage to seedlings under conditions
where drought and flooding were alternated, than when moist
soil conditions prevailed between flooding cycles. The high
amount of damage following alternating flood and drought
conditions may result from the simultaneous increase in the
production of sporangia upon rewetting and the production
of new, unsuberized fine roots, which are highly susceptible
to infection. Extended periods of drought may also increase
root exudation, thereby facilitating the initial establishment
of soil-borne pathogens in the roots (Duniway, 1977), and may,
in the event of an increase in soil moisture, favour Phytophthora
over other soil microorganisms, since Phytophthora respond
very rapidly to changes in soil moisture. Restricted water
availability may also critically reduce the tolerance of the
host to the pathogen through its negative influence on the
defence mechanisms of the plants (see the section The C
assimilation and allocation of forest trees). Predisposition
of plants to infection by Phytophthora as a consequence of
drought has been demonstrated by, among others, Duniway
(1977), Blaker & MacDonald (1981) and Hper &
Alabouvette (1996).
Chemical properties of soil In general, Phytophthora diseases
are considered to be more severe at higher pH values
(Schmitthenner & Canaday, 1983). This is supported by the
increase in the activity of Phytophthora with increasing pH
(Klisiewicz, 1970; Muchovej et al., 1980; Byrt et al., 1982).
For the Phytophthora species found in oak stands, Jung et al.
(2000) showed that sporangia cannot be formed at pH(H2O)
values below 4.0. In addition, the production of sporangia was
found to increase with increasing pH, at least up to pH 5.
Concentrations of aluminium (Al) and calcium (Ca) in the
soil are often inversely and intimately related to soil pH, and
may also affect the aggressiveness of Phytophthora. High
concentrations of Al have been shown to inhibit mycelial
growth, as well as sporangial formation and germination (Maas,
1976; Muchovej et al., 1980; Benson, 1993; Andrivon, 1995).
Because of the negative effects of pH and Al on the activity of

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Phytophthora, it has been suggested that these diseases do not

occur on acidic, Al-rich soils. However, Jnsson et al. (2003b)
and Jnsson (2004a,b) showed that P. quercina could cause
substantial root damage to seedlings as well as mature trees under
acidic conditions (pH < 4.3, Al concentrations > 100 g g1).
This may possibly be caused by an increased susceptibility of
trees in acidified soils (see the section The C assimilation and
allocation of forest trees) or an adverse effect of Al on roots.
A number of studies have demonstrated that elevated concentrations of Al in the rooting medium may lead to disruption
of cell function and impaired root growth of trees (DeWald
et al., 1990; Kochian, 1995; Matsumo, 2000). Conversely,
Quercus species seem to be relatively tolerant to the concentrations of Al found in natural soils (Keltjens & van Loenen,
1989; Thornton et al., 1989).
Phytophthora diseases are usually regarded as more severe at
high Ca levels (Schmitthenner & Canaday, 1983; Erwin &
Ribeiro, 1996). However, there are also examples of high concentrations of Ca having no effect on or suppressing disease
(Klotz et al., 1958; Muchovej et al., 1980; von Broembsen &
Deacon, 1997) and a number of studies have demonstrated
negative effects of high concentrations of Ca on the activity of
Phytophthora in vitro (von Broembsen & Deacon, 1997; Hill
et al., 1998; Messenger et al., 2000). Although the results with
regard to Ca are contradictory, it is obvious that minimum
levels of this element are necessary for zoospore production and
cyst germination (Halsall & Forrester, 1977; von Broembsen
& Deacon, 1996, 1997; Xu & Morris, 1998), for Phytophthora
infection of roots through its effect on zoospore taxis and
adhesion to solid surfaces (Gubler et al., 1989; Deacon &
Donaldson, 1993), as well as for the stimulation of oospore
germination (Ribeiro, 1983). With regard to the relatively low
concentrations of Ca found in the soil solution in temperate
oak forest soils (Berger & Glatzel, 1994; Freer-Smith & Read,
1995; Bakker et al., 1999), and the relatively high concentrations that are usually necessary to suppress disease, it seems
likely that increasing concentrations of Ca in this type of forest
soil would accelerate rather than suppress the development of
disease in oaks.
The results are also inconsistent for K, Mg and P, both with
regard to in vitro activity and disease development in vivo
(Kincaid et al., 1970; Newhook & Podger, 1972; Maas, 1976;
Halsall & Forrester, 1977; Grau et al., 1989; Phukan, 1993;
Hill et al., 1998; Appiah et al., 2005). It is possible that the
impact of these elements on disease development is more
closely related to host susceptibility than to pathogen aggressiveness (see the section The C assimilation and allocation
of forest trees), and are thus strongly dependent on their relations to N. This is supported by the decrease in disease severity
when complete fertilizer is applied (Schmitthenner &
Canaday, 1983; Pacumbaba et al., 1997).
The effect of N on disease development seems to depend
on both the hostpathogen combination and the type of
soil N (Klotz et al., 1958; Newhook & Podger, 1972; Lee &

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Zentmeyer, 1982; Halsall et al., 1983; Utkhede & Smith, 1995;

Das et al., 2003). In general, increasing concentrations of
NO3 stimulate the activity of Phytophthora (von Broembsen
& Deacon, 1997; Jung et al., 2003a), while the effect of NH4+
and organic N seem to be smaller (Elliott, 1989; Jung et al.,
2003a). For P. quercina and Q. robur, Jung et al. (2003a) found
that the production of sporangia in vitro increased with
increasing concentrations of nitrate in the soil leachate, and
that the difference in the fine-root length and the number of
fine-root tips between uninfected and infected seedlings also
increased with increasing nitrate concentration in the soil.
Studies of little leaf disease caused by P. cinnamomi in shortleaf pine (Pinus echinata), growing in degraded soils in the
south-eastern USA, have shown that fertilization with N may
prevent symptom development in healthy trees and improve
the condition of little leaf trees in early stages of disease
(Tainter & Baker, 1996). However, in situations where N is in
excess of plant demand, Phytophthora are likely to have an
advantage because of the nitrate-induced stimulation of sporangia, the lower availability of C-based defence compounds
in roots (see the section The C assimilation and allocation of
forest trees), and possibly also a greater susceptibility of tissues
as a consequence of nutrient imbalances (Marschner, 2003).
Biotic factors A number of studies have shown that various
biotic populations in the soil influence the severity of disease
caused by Phytophthora species, most likely by exerting
competitive pressure on the Phytophthora species, thereby
excluding them from the root surface (Marx, 1972; Weste &
Vithanage, 1977; Keast & Tonkin, 1983; Malajczuk, 1983).
In particular, mycorrhizal colonization of roots has been
suggested to be an efficient barrier to Phytophthora infection
(Zak, 1964; Marx, 1972; Barham et al., 1974; Branzanti et al.,
1999). Using agar plates and liquid cultures, Marx (1969)
demonstrated an inhibitory effect of several ectomycorrhizal
species on the growth of mycelia, as well as on the motility and
germination of zoospores of P. cinnamomi. Furthermore, the
presence of fully developed mycorrhiza with a fungal mantle
and a Hartig net on individual roots of shortleaf pine seedlings
was seen to provide resistance to zoospore and mycelial
infection, and to have a protective influence on adjacent
nonmycorrhizal roots (Marx & Davey, 1969a,b; Marx, 1970).
The protective effect of the mycorrhizal symbiosis was evident
throughout at the whole root system of the seedlings (Marx,
1973). By contrast, nonmycorrhizal roots and roots with
incomplete fungal mantles were infected by the pathogen
(Marx & Davey, 1969a,b; Marx, 1970; Barham et al., 1974).
Similar results were found by Branzanti et al. (1999) when
investigating the importance of ectomycorrhizal fungi in the
reduction of chestnut ink disease.
These results suggest that mycorrhizal colonization and the
presence of other microorganisms in the rhizosphere soil may
render oak trees less susceptible to infection by Phytophthora
species, although root infection is probably not completely

Review

inhibited ( Jnsson, 2004a). However, low vitality of oak trees

(Causin et al., 1996; Kovacs et al., 2000) and a high input of
N into ecosystems (Brunner, 2001; Nilsson, 2004) have been
found to influence the ectomycorrhizal colonization of roots
and mycelial growth of ectomycorrhiza negatively, and may
thus counteract these positive effects.

A conceptual model for the Phytophthora disease

in oak
Based on the literature presented in the Theoretical background section, a conceptual model for the development of
disease in oak as a consequence of Phytophthora infection was
developed (Fig. 1). The aim of the model is to give an overview
of how different environmental conditions, including abiotic
as well as biotic factors, act simultaneously on the host
pathogen system, sometimes accelerating disease development,
and sometimes retarding it. The model is applicable to the
interaction between soil-borne Phytophthora species and
Q. robur growing in acid forest soils (pH < 5) in a temperate
climate. Only the effects of the pathogen on the fine-root
system are considered, since damage to the stem of oak as a
consequence of Phytophthora infections is limited. The processes
that influence the capacity of Phytophthora to infect roots,
such as sporangial and zoospore production, dispersion, taxis,
adhesion and cyst germination, are collected in one variable
called Phytophthora activity. The variable microbial activity
does not include Phytophthora or other pathogens, since
these are considered separately. For simplicity, some of the
information regarding the C assimilation and allocation has
not been included in Fig. 1. For a more detailed illustration of
the C submodel, see Fig. 2. The purpose of the C submodel
is to elucidate the balance between root and shoot growth
and allocation to secondary metabolites in the trees. The
model thus only describes these three pools of carbohydrates
in the tree and the flow of carbohydrates between them.
Carbohydrates required for maintenance and construction of
new tissue are included in the parameter metabolized CH for
growth. It is assumed that nutrient uptake is strongly correlated
to fine-root length (Atkinson, 2000), and that an increase in
the allocation of carbohydrates to roots results in an increase
in the live root length rather than an increase in the uptake
efficiency per unit length of root. In addition, the model does
not consider various groups of C-based compounds or individual
compounds, and it does not explain the physiological processes.
Despite differing results with regard to the influence of Ca on
the reproduction and dispersion of Phytophthora, and on
disease development, it was assumed that an increase in the
concentration of Ca enhances the activity of Phytophthora
at the concentrations found in acidic oak forest soils (see the
section The influence of abiotic and biotic factors on
Phytophthora activity and disease development). It was also
assumed that K, Mg and P, which have been demonstrated to
have variable effects on Phytophthora diseases, influence the

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development of disease primarily through their effects on C

assimilation and allocation patterns in the trees. Temperature
is likely to have a certain effect on Phytophthora activity and
may also influence the C allocation in trees. However, the
effects of temperature are often overridden by concomitant
changes in water and nutrient availability and growth patterns
of plants (Pregitzer et al., 2000; Pregitzer, 2003), and thus
temperature was not included in the model. Note that
increased soil moisture does not necessarily imply increased
uptake of water. However, the link has been included since
low availability of water will lead to a reduced water uptake.
To illustrate how the CLD in Fig. 1 can be used to predict
tree response to Phytophthora infection under different conditions, two different climatic scenarios are considered. The
subscenarios have been chosen to illustrate a situation that has
been common in European forests until now tree growth is
limited by N and two situations that may become more
common in the future as a consequence of soil acidification
and an extensive deposition of N an excess of N in the
ecosystem and limitation of tree growth by a base cation.
Scenario 1: Heavy rain or prolonged periods of rain
Assuming that soil moisture increases, as a result of heavy rain
or prolonged periods of rain, the production and dispersion of
Phytophthora zoospores will increase, thereby increasing the
probability of root infection and, consequently, root damage.
Root damage may lead to an increased leakage of carbohydrates from the roots, thereby facilitating zoospore taxis of
Phytophthora (Carlile, 1983). When the zoospores can find
the roots easily, this is likely to result in a higher degree of
infection and thus an increase in the amount of damage.
Microbial competition may also be reduced under anaerobic
conditions in the soil, thus enhancing the effect of flooding on
root infection by Phytophthora. Lack of O2 may also cause
hypoxic damage and thus facilitate Phytophthora infection.
However, Q. robur is relatively tolerant to both hypoxia and
the oxidative stress imposed on roots when the waterlogged
conditions cease (Colin-Belgrand et al., 1991; Wagner &
Dreyer, 1997), and anaerobic conditions are thus not likely to
cause direct damage to roots. Infection by Phytophthora may
initiate defence reactions in the plants, and more C will then
be allocated to the production of secondary metabolites. The
fraction of carbohydrates available for metabolization for
growth will then decrease. Continuous infection by
Phytophthora may empty the stores of carbohydrates in the
tree, and subsequently cause retardation of growth. If growth
is reduced, this may, together with the damage caused by
pathogen infection, result in a reduction in the length of live
roots, and thus in impaired uptake of water and nutrients.
Tree growth is limited by N If damage or growth reduction
as a consequence of Phytophthora infection results in shortage
of N, an element which is important for metabolizing

New Phytologist (2006) 171: 5568

carbohydrates for growth (see the section The C assimilation

and allocation of forest trees), the available mineral is likely to
be metabolized in the root first because of the close proximity
of the sites of uptake and mineral assimilation. Consequently,
only a small proportion of the N will be transported to the
shoot. Less carbohydrates will thus be metabolized in the
shoot, resulting in a reduction in shoot growth. A larger
fraction of carbohydrates will then instead be available for
transport to the roots, and may thus be used for metabolization in the root, and subsequently root growth, provided that
there is sufficient N in the root to metabolize it. Roots lost
owing to pathogen infection may then be replaced and
ectomycorrhizal colonization may be promoted, thus limiting
root infection by Phytophthora. Furthermore, the relatively
high availability of nonstructural carbohydrates is likely to
lead to an increased flow through pathways that result in the
synthesis of C-rich secondary metabolites, some of which may
be used to protect the trees towards various stress factors.
Nitrogen-limited trees may therefore have a good protection
and may also be able to maintain a high root production,
replacing roots that are lost as a result of, for example,
Phytophthora infection. However, severe N-deficiency may
eventually lead to a reduction in the leaf area, and subsequently in the rate of photosynthesis, thus resulting in a
lower availability of nonstructural carbohydrates.
High N deposition has resulted in excess N in the ecosystem
If there is a high availability of N, a large fraction of the
available carbohydrates is likely to be invested in growth,
particularly shoot growth (see the section The C assimilation
and allocation of forest trees), while the amount allocated to
root growth and the production of secondary metabolites will
be low. Tree tissue may thus become more susceptible to root
infection and damage, and the ability of the tree to replace lost
roots will be low. Moreover, an accumulation of NO3 in the
soil may influence the development of the disease through the
positive effect of NO3 on zoospore production.
Tree growth is limited by K or Mg If the reduction in
nutrient uptake instead results in a shortage of K or Mg,
elements that are important for photosynthesis, the rate of
photosynthesis will be reduced and, subsequently, so will C
fixation. Since the carbohydrates are formed in the photosynthetically active part of the seedlings, the available carbohydrates will probably be metabolized for growth in the
above-ground part first, leading to a low translocation of C to
the roots and, consequently, low root growth compared with
shoot growth. In addition, little carbohydrate will be available
for the production of C-based secondary metabolites. If root
growth, and thus live root length, is decreased, the uptake of
base cations is likely to be further impaired, and the ability of
the tree to replace roots lost as a result of pathogen infection
and to protect its tissue will be low. Low C allocation to roots
may also lead to reduced ectomycorrhization and growth of

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Research review

external mycelia (Brunner, 2001), thereby further increasing

the potential for Phytophthora to infect roots. However, soils
in which K or Mg limit tree growth are often acid, implying
a low pH, low concentrations of Ca and high concentrations
of Al. All of these factors may influence the Phytophthora
activity negatively and may thus decrease the probability of
root infection. However, if infection takes place, the tree is
bound to have a low resistance towards the pathogen.
Scenario 2: Tree growth is limited by water
If we instead assume there is a drought, this will have the
reverse effect on sporangial production and the dispersion of
zoospores. Drought may thus decrease the degree of root
infection. However, severe drought may also decrease the rate
of photosynthesis and subsequently impede the replenishment of the pools of carbohydrates in the plant. Carbon will
then be preferentially allocated to primary metabolites in the
shoot and the fraction of C allocated to roots and the production of secondary metabolites will decrease. A long period of
drought may thus completely empty the stores of carbohydrates
in the plant. Plant tissue will then become more susceptible to
damage and in the event of an increase in soil moisture, the
ability of Phytophthora to infect the tree and cause damage to
the roots may increase. In addition, drought influences the
soil microbial community negatively, thereby increasing the
potential for Phytophthora to infect roots in the event of a
subsequent increase in soil moisture, since these pathogens
respond extremely quickly to an increase in moisture. Secondary
pathogens often follow the infection of roots by Phytophthora,
and may exacerbate root damage, thus increasing the carbohydrate leakage from the roots, and, possibly thereby influencing
the activity in the rhizosphere of Phytophthora as well as other
microbes.
To summarize Fig. 1, soil-borne Phytophthora species have
the ability to reduce the live root length of oak substantially.
However, as long as the tree can sustain new root production
to replace the lost roots, nutrient and water uptake will not be
affected. The continuous production of new fine roots, to
replace those lost because of pathogen infection, is likely to
gradually deplete the carbohydrate stores. The susceptibility
of the tree to pathogen infection as well as to other types of
stress may thus increase. If environmental conditions are
favourable for the pathogen, the live root length of the host is
likely to eventually decrease, leading to a lower capacity for
water and nutrient uptake. Depending on the nutrient
limiting the tree, growth or photosynthetic rate may be more
strongly affected. If the rate of photosynthesis is reduced,
smaller amounts of carbohydrates will be available for compensatory growth and for the production of secondary
metabolites involved in resistance. Tree vitality will subsequently decrease, as disease development is accelerated through
negative feedback loops, as presented in Fig. 1. The range of
field responses to Phytophthora, from slow decline to sudden

Review

death of trees, is likely to reflect differences in the interaction

between the pathogen and the host, as a consequence of their
response to different abiotic and biotic factors.

Discussion
This paper presents a conceptual model for the development
of Phytophthora disease in oak. By using a CLD to describe the
interaction between the host, the pathogen and the environment, and by emphasizing changes in the susceptibility of the
host as well as the aggressiveness of the pathogen, it was my
intention to visualize the connections and the feedback in the
hostPhytophthora system in a more comprehensive way than
has previously been done. When reviewing the literature and
creating the conceptual model, it became apparent that many
environmental factors that are regarded as influencing the
development of disease, as a result of their effect on aggressiveness of Phytophthora might also affect the susceptibility of the
tree. These effects are sometimes additive, increasing both
the aggressiveness of the pathogen and the susceptibility of the
host. At other times, the effects counteract each other, and the
balance between pathogen growth and host resistance may
thus remain unchanged. The CLD enables detection of such
causalities and may, in addition, facilitate the interpretation of
fictive disease development when creating scenarios.
The C assimilation and allocation in trees is a disputable
topic. The studies we found for Quercus species regarding the
influence of N on the production of defence compounds
(Thomas & Schafellner, 1999) and the influence of drought
on C assimilation and root : shoot ratios (Osonubi & Davies,
1981; van Hees, 1997; Vivin & Guehl, 1997) support the theories suggested by Bryant et al. (1983), Herms and Mattson
(1992) and Ericsson et al. (1996). In addition, a previous
pathogenicity test in the glasshouse suggests that soil nutrient
availability and the nutrient status in oak seedlings influence
the production and the allocation of biomass to roots differently, depending on whether N or a base cation is limiting
( Jnsson, 2004b). However, none of these experiments were
designed to test the theories and more research is needed to
confirm whether they are valid for oak. It also seems likely that
these theories are applicable primarily to the constitutive
defences of plants. In the case of induced defences, it seems
probable that plant signalling may overshadow the C/nutrient
balance and redirect the flow of carbohydrates to the wounded
area. This suggests that the C/nutrient balance hypothesis is
of importance primarily for the continuous maintenance of
defences, such as during repeated infection or when the plant
is subjected to multiple forms of stress. Sheen et al. (1999)
suggested that carbohydrate concentrations may provide a
path to control responses to light, nutrient concentrations and
stresses, while plant hormones may govern intrinsic developmental responses.
The information used to determine the influence of environmental variables on the development of disease was gathered

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from various hostpathogen combinations, ranging from

Phytophthora diseases on agricultural crops to Phytophthora
species on Q. robur. The effects of Phytophthora species have
often been described as being host specific, and generalizations
regarding the effects of various environmental factors, as in
this paper, are therefore questionable. In addition, much of
the data for trees have been gathered from experiments on
seedlings. The response of seedlings and mature trees to
pathogens and environmental conditions will probably differ.
This must be taken into account when interpreting the model.
However, the aim of this model was to create a basis for
further discussion. To validate the model, substantial research
on the susceptibility of oak, the aggressiveness of the pathogen
and the final disease outcome will be required. Furthermore,
the interaction between Phytophthora and other factors that
have been suggested to contribute to the complex course of
European oak decline, such as defoliators, frost and secondary
pathogens (Thomas et al., 2002), must be investigated.
If the allocation patterns in oak change as a consequence of
a change in the nutrient that is limiting the growth of the tree,
this may have serious implications for oak decline in Europe
in the future. Nitrogen has hitherto been the limiting nutrient
for tree growth in the major part of the temperate as well as
the boreal zone. However, the extensive deposition of N
during the past decades, together with substantial acidificationinduced leaching of nutrients from the soil, has led to a situation in which N is no longer bound to be limiting. Instead,
base cations, such as Mg and K, have been shown to limit the
growth of trees in certain regions (Httl, 1990; Thelin, 2000).
According to the C/nutrient balance hypothesis, this implies
a reduced capacity for trees to assimilate C and a reduction in
the allocation of C to roots and the production of defence
compounds (Bryant et al., 1983; Herms & Mattson, 1992;
Ericsson et al., 1996). Several studies have implied a reduction
in the ability of forest trees to protect themselves against
parasites and frost damage as a consequence of N fertilization
(Flckiger & Braun, 1999; Httenschwiler & Schafellner, 1999;
Jnsson et al., 2004). Acidification-induced reductions in
soil-available K and Mg, and a high N availability, may thus
accelerate the damage caused by Phytophthora in oak in
Europe. No evidence of excess N or nutrient imbalances in
European oak stands has yet been reported (Berger & Glatzel,
1994; Thomas et al., 2002), but considering the high acidity
of soils and the small pools of base cations, the continued
input of acidifying compounds is likely to eventually lead to
nutrient deficiencies and decreased ecosystem stability.

Conclusions
The conceptual model presented in this paper is an attempt
to bring together the current knowledge on Phytophthorainduced diseases in oaks. By visualizing the available information and shifting the focus from single causal relationships to
a dynamic network of relationships incorporating simult-

New Phytologist (2006) 171: 5568

aneous multiple effects on the hostpathogen interaction,

gaps in our knowledge can be identified, new questions raised
and hypotheses proposed. In addition, the development of the
disease caused by Phytophthora species in pedunculate oak
may be investigated under different conditions by using fictive
scenarios. However, since the model is based on literature
from a wide range of hostpathogen combinations, and since
the effects of environmental factors on pathogen aggressiveness and host susceptibility vary substantially, species-specific
studies are necessary to validate the model. In vitro studies of
the influence of nutrient availability on the growth and
reproduction of P. quercina are currently being undertaken
and will be followed by investigations on C assimilation and
allocation patterns in oaks growing under differing conditions
and infected with Phytophthora.

Acknowledgements
This project was funded by The Swedish Research Council for
the Environment, Agricultural Sciences and Spatial Planning.
U. Rosengren is acknowledged for assistance in the initiation
of this work and for commenting on previous versions of
the manuscript. S. Belyazid is gratefully acknowledged for
interesting and fruitful discussions, useful comments on the
manuscript and for technical assistance. H. Sheppard corrected
the language.

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