Host Plant Resistance
5.3 Genetics of Virulence and Resistance
5.3.1 The pathosystem concept A system may be defined as a pattern of
patterns, and a pattern within a pattern is called a subsystem (Robinson, 1976). A pathosystem is a subsystem of an ecosys- tem and is defined by the phenomenon of parasitism (Robinson, 1980a,b). As with an ecosystem the geographical, biological, conceptual and other boundaries of a pathosystem may be specified as conve- nient (Robinson, 1980b). The plant pathosystem involves plants used as hosts by parasites which includes fungi, bacteria, viruses, insects, mites and nematodes. In a natural pathosystem the evolutionary sur- vival of wild plants is not impaired by their parasites. If the parasitic ability of the parasites were too great then the host might become extinct and consequently so would the parasite, hence there must be an upper limit to the parasitic ability of parasites (Robinson, 1980a). Balance between hosts and their parasites is maintained, their existence testifies to this.
Before addressing the different types of pathosystem, it is first necessary to under- stand some of the terminology associated with epidemiology. In epidemiology, there are two types of infection that correspond to two subdivisions of the epidemic. Allo- infection of a pathogen is an infection obtained from another host individual and is responsible for that part of the epidemic referred to as the exodemic. Auto- infection occurs by reinfection of the
Fig. 5.1.The origin of the term vertical resistance. The amounts of blight suffered by various potato cultivars when exposed to 16 different races of Phytophthora infestans. (a) A cultivar having an R1resistance gene;
(b) a cultivar with an R2resistance gene (see text for further explanation) (after van der Plank, 1963).
same individual host, i.e. it was produced on the same host, and this corresponds to that part of the epidemic referred to as the esodemic. Vertical resistance can only prevent infection and it can only prevent allo-infection that occurs during the exo- demic. Horizontal resistance on the other hand operates during the esodemic, after a matching allo-infection has occurred, to reduce auto-infection.
There are two types of wild patho- system, the discontinuous and the continu- ous. There is also the crop pathosystem under the deterministic control of man.
The discontinuous wild pathosystem is autonomous and combines both the vertical and horizontal pathosystems. The vertical pathosystem reduces the effective parasite population to the spores that happen to allo-infect a matching host individual. In a
pathosystem where a number of pest gen- erations can occur in a single season, the vertical subsystem can have a major influ- ence on the form of the epidemic and its effect on individuals within the pest popu- lation. If a fungal pathogen has four gener- ations per season this results in four separate exodemics, the primary, sec- ondary, tertiary and quaternary exodemics.
The vertical pathosystem will influence how often an individual experiences an exodemic (a spatial effect), how often that exodemic is primary, secondary, tertiary or quaternary and because the amount of damage carries with the sequence of exo- demic, the extent of the damage received.
The primary exodemic is the most damag- ing, but only a few individuals that had matching allo-infections will experience this. The horizontal subsystem will then influence the development of the esodemic which will influence the population size of the subsequent pathogen generation that initiates the secondary exodemic. The number of individuals present in the sec- ondary exodemic will be dependent on the reproductive rate of the fungi which will
itself have been determined by the level of horizontal resistance in each of the infected hosts. All the vertical genotypes will again be equally represented and allo- infection of further individuals will occur in the secondary exodemic but damage will be less than in the primary exodemic.
This process continues through succeed- ing generations after which it is broken by leaf fall in deciduous trees, dieback in herbaceous perennials or seed set in annu- als. The parasite survives the sequential discontinuity as a resting stage.
The continuous wild pathosystem has, as the name implies, no sequential discon- tinuity of host tissue, hence vertical resis- tance is made redundant. Continuous wild pathosystems are controlled exclusively by the horizontal subsystem. There is spatial and sequential continuity of host tissue and as a consequence of this, the esodemic is continuous. Evergreen perennial plant populations provide typical examples, hav- ing genetic uniformity because of their vegetative reproduction and sequential continuity because of their evergreen habit.
Continuity of host tissue is more likely to Maximum
Minimum
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Fig. 5.2. The origin of the term horizontal resistance. The amounts of blight suffered by three potato cultivars having no R genes that were exposed to 16 different races of Phytophthora infestans (see text for further explanation) (after van der Plank, 1963).
occur in the tropics and is more common among perennials than annuals, especially of stems and roots.
Vertical resistance may supplement hori- zontal resistance (which is ubiquitous among plants) in more discontinuous situa- tions (but not necessarily so) so that vertical resistance would be more common in tem- perate zones, among deciduous perennials and among annuals. But horizontal resis- tance remains the basis for control of the pathosystem that is supplemented in some situations by vertical resistance. Vertical subsystems probably occur only in angiosperm hosts and possibly in a few deciduous gymnosperms and evolved as a means of conferring stability in a fluctuating environment (Robinson, 1980b). The hori- zontal subsystem is subject to the changes in positive and negative selection pressures that occur over many generations but remain relatively unbuffered against short- term changes, e.g. marked fluctuations in weather. The parasite may be so favoured by a short-term change in weather that a host is decimated. The vertical subsystem can buffer against such vagaries and hence pro- vide a supplementary level of control.
The deterministic control of crop pathosystems by man has, in the majority of crop pathosystems, promoted an imbal- ance at the subsystems level so that verti- cal resistance has been arbitrarily promoted at the expense of horizontal resistance. The identification of vertical resistance provided breeders with a simple and convenient means of developing pathogen resistant cultivars. The simple major gene inheritance of vertical resis- tance made it easy to manipulate and incorporate into agronomically superior varieties and it was also easily identified under field screening conditions because it conferred complete resistance. The wide- spread adoption of the resistant cultivar creates a selection pressure for virulent pathogen individuals. Any individual pathogen that has a virulent gene at the locus corresponding to the resistance gene of the new crop cultivar has a selective advantage and can multiply rapidly
(Gallun and Khush, 1980). Since crop host plants are usually members of a homoge- neous crop population that have identical genes for resistance, then the descendants of the pathogen individuals having the matching gene will successfully colonize and damage the whole crop. Under these conditions the resistance is said to have broken; although it is still present it is just operationally inactive. This cycle of events has become known as the ‘boom and bust cycle of cultivar production’. Plant breed- ers have not, however, been discouraged because some vertical resistance lasts longer than others and breeders hope they have discovered and utilized one of the long lasting forms.
The length of time that a vertical resis- tance remains active is dependent on the frequency of the matching virulence gene in the pathogen population and the extent to which the cultivar is grown. The rate at which resistance breaking biotypes develop will be partly dependent on the initial frequency of the gene within the pathogen population. In wild pathosys- tems all vertical genomes occur with equal frequency and hence they are of equal strength. But with crop pathosystems where the resistance gene may be derived from a wild host or ancestor, or from a dif- ferent environment, then the strength of the gene is liable to change so that some are strong (a low frequency) or weak (a high initial frequency) (Robinson, 1980a).
A strong vertical resistance is of more ben- efit to the breeder and farmer/grower alike since this will confer resistance for a longer period than weak vertical resis- tance.
Imbalance within the vertical subsys- tem has also occurred in crop pathosys- tems because often only one gene for resistance is incorporated into a cultivar, whereas in their wild counterparts there are secondary vertical genomes in the plant and pathogen population. This enforced simplicity increases the homo- geneity of the vertical subsystems which only serves to render it ineffective. The incorporation of a number of major resis-
tance genes is being used as a means of prolonging vertical resistance.
Further imbalance in the crop pathosys- tem has been introduced through the ero- sion of the horizontal subsystem due to the emphasis placed on selecting for verti- cal resistance. During the breeding for ver- tical resistance, there is a negative selection pressure for horizontal resistance because all the selection takes place dur- ing the exodemic. Plants are not assessed for their performance during the exo- demic. This phenomenon is known as the vertifolia effect, after the potato cultivar in which it came to notice (van der Plank, 1963). This erosion of the horizontal resis- tance contributes to the ‘bust’ of the ‘boom and bust’ cycle because the low level of horizontal resistance present in the matched cultivar increases the effects of its susceptibility. The use of chemicals to protect crops from pests while breeding for yield and quality (the pesticide umbrella) has also contributed to the ero- sion of resistance.
5.3.2 The vertical pathosystem