RESISTANCE IN POPULATIONS
A. ESCAPE AND A VOIDANCE
1993) offer new opportullitles to study populations and their interconnections on a large scale. The relative importance of studies at a smaller, local, scale may decrease, but understanding of processes at a small scale will still be required to underpin understanding of processes at a higher level.
The phenomenon of population will remain central in the following sections where host - pathogen interactions are considered at the population level, but there is an additional problem in considering host - pathogen interactions: the scale of the host population often does not fit the scale of the pathogen population. This drawback must be tackled in studies of host - pathogen interactions.
168 J. Frantzen
Disease escape is also possible even though the pathogen is present in a host population. A good example is provided by the attack of Ammophila arena ria (marram grass) by pathogenic soil organisms (Van der Putten and Troelstra, 1990). This clonal plant grows on the beach and dunes in The Netherlands. The plants grew well at sites where fresh, windblown sand was deposited continuously from the sea side because soil pathogens were not able to develop in the fresh sand. In contrast, plants growing at neighbouring sites without continuous sand deposition degenerated as soil pathogens developed well at these sites. Thus escape of plants from disease depended on factors governing sand deposition.
Disease escape is not uncommon in wild and weed pathosystems. Plants may use their seeds to escape from disease (Augspurger, 1983; Parker, 1987). Seeds are dispersed and offspring may establish at some distance from the mother plant. If the mother plant is infected by a pathogen, the pathogen may not be able to bridge the distance between mother plant and offspring and so the offspring may escape from disease. Plants may also use their ability for clonal growth to escape from disease (Wennstrom and Ericson, 1992; Frantzen, 1994b). New ramets may be produced at some distance from the mother ramet. If the mother ramet is infected by a pathogen, the pathogen may be not able to bridge the distance between mother ramet and daughter ramets and, so, the new ramets may escape from disease.
Disease escape also exists in crop pathosystems. Epidemics in crops may start from a relatively small amount of inoculum surviving within the field from a previous cropping period, or coming from outside; these are called focal epidemics (Zadoks and Schein, 1979). Plants in the vicinity of the inoculum are most likely to be infected whereas plants further away may escape from disease. The epidemic will progress and the rate of progress will be governed by, among other factors, environmental conditions and dispersal capacity of the pathogen. Thus the epidemic rate and the position of a plant relative to the inoculum source determine the probability and time of infection of that plant.
Disease escape has particular importance in multiline cultivars and variety mixtures.
The rationale behind the use of multilines and variety mixtures is to create a heterogeneous crop with respect to disease resistance characters, while at the same time maintaining homogeneity with respect to characters determining quality and quantity of the yield (Wolfe, 1985). Consider the case where inoculum of one race of a pathogen enters the population and infects a susceptible plant (Fig. 3). Spores will be produced on this plant, and then encounter two subsequent problems. Firstly the distance to the next susceptible plant is relatively large compared to that in a homogeneous susceptible crop.
Secondly, the spores may be caught by the surrounding, resistant plants: this is called the "barrier effect" (Wolfe, 1985). The net result is that susceptible plants may escape from disease. Such disease escape is independent of the race arriving or present in the crop, unless that race is pathogenic to all plant genotypes. We will discuss the likelihood of such a super race later.
Disease escape is the rule rather than the exception in wild, weed and crop pathosystems. The concept of multi lines and variety mixtures is based on it.
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Infection by race V3Figure 3. Concept of multi lines I variety mixture illustrated by a plant mixture of which each plant has one resistance gene (RI. R2. R3. R4) and the crop is attacked by one virulent pathogen race (V3).
Until now, we have considered escape as a chance event. Whether infection occurs or not depends on environmental conditions and the fortuitous position of a plant. A form of escape may also depend on the genotype of the plant, in which case it is known as avoidance. Examples of avoidance were given by Agrios (1980), although he did not use the term. Later, Dinoor and Eshed (1984) noted that "under the selection pressure imposed by pathogens, early- or late-maturing plants may have an advantage in that they avoid the impact of disease". The terms escape and avoidance were distinguished explicitly by Burdon (1987a). In his opinion escape is the result of a fortuitous set of circumstances whereas disease avoidance has a genetic base. Because of this genetic base, he classified avoidance as a (passive) resistance mechanism.
A voidance may be based on physical protection of susceptible tissue against a pathogen, or on differences between genotypes in rate of development. Classical examples of the former are varieties of barley and wheat in which the flowers remain closed, reducing the probability of contact between the stigmas and the pathogen Ustilago nuda, a smut disease. Open flowering varieties are more prone to disease. There is some doubt whether this type of avoidance can justifiably be considered as separate from mechanisms of resistance in the strict sense (see section III. C). The physical protection could be considered as falling within constitutive resistance. In contrast, the second type of avoidance, based on differences between genotypes in growth rate is more distinct from resistance sensu stricto. We will tum first to weed pathosystems to illustrate this distinction.
The perennial Silene alba is frequently infected by the anther-smut Ustilago violacea (more recently called Microbotryum violaceum) and teliospores are florally transmitted by insects. Biere and Antonovics (1996) observed that plant families differed significantly in time of onset of flowering and plants flowering late had a lower probability of becoming infected, i.e. avoided disease. The disease avoidance
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mechanism therefore had two components, (1) differences between plant stages in susceptibility to the pathogen (only susceptible in the flowering stage), and (2) differences between plant families (genotypes) in growth rate. A similar phenomenon was observed for the annual plant Senecio vulgaris and the rust fungus Puccinia lagenophorae (1. Frantzen and H. MUller-Scharer, unpublished). Plants at a young stage were less susceptible than plants at an older stage, probably because spores adhered less to the leaves of young plants. The plant families used in the experiments differed in rate of development and, therefore, the number of plants present in a susceptible state at the time of inoculation differed between families. Two plant families avoided disease compared to the third family. Again, this system showed the two components of the avoidance mechanism: the differences between plant stages in susceptibility, and the differences in rate of development.
The rate of development also may govern avoidance in crop pathosystems (Agrios, 1980).
For example, timing of blossoming and fruit set may vary between apple varieties and some of the varieties may blossom at a time when a pathogen is not infectious. The use of the mechanism of avoidance in agriculture may, however, be constrained by factors not related to crop protection, e.g. feasibility of harvest, and yield quality.
Avoidance is a disease defence mechanism that can be distinguished from resistance. It may be quite common. Its use in agriculture may be constrained by factors not related to crop protection.