Trends in Plant Science
OpinionBalancing selection favors guarding resistance proteins
Section snippets
Guard model
Lack of evidence for direct Avr–R interactions stimulated scientists to propose new models for Avr perception by resistant plants. One interesting model is that R proteins confer recognition of Avr factors only when these Avr factors are complexed with their host virulence targets. This model was initially proposed [10] to explain the role of Prf in AvrPto–Pto signaling and was later referred to as the guard model [11]. In this model, Pto is considered to be the virulence target of AvrPto,
Behavior of R genes in natural plant populations
In nature, the ongoing battle between plants that develop novel resistance specificities and pathogens that try to circumvent recognition by these plants can be seen as an arms race. Such an arms race implies a transient polymorphism of R genes, which means that high disease pressure causes the replacement of old R genes by new ones, resulting in relatively young R genes and monomorphic R gene loci [13]. However, recent studies of functional RPM1 and Pto genes in species of Arabidopsis and
Balancing selection and the cost of virulence
The virulence role of the Avr factor is crucial for balancing selection. Many Avr factors contribute to virulence of the pathogen [25] but their relative contributions are often difficult to assess in laboratory experiments 26, 27, 28. In addition, most pathogens lacking Avr genes were isolated from crops grown as monocultures. These pathogens might have been able to compensate for their reduced virulence during prolonged maintenance on susceptible crops. In nature, this compensation is less
Only some of the Avr–R gene pairs are maintained by balancing selection
Balancing selection can explain many recent observations but does not provide an explanation for the generation of new R genes with novel specificities. Therefore, R gene dynamics in a natural plant population probably reflect a combination of balancing selection and an arms race, the latter perhaps being relatively slow (Fig. 1). As has been suggested previously, R gene analogs (RGAs) are randomly generated, most likely through a birth-and-death process [30]. Most of these new RGAs have no
Selection for guarding R proteins
The proposed model for the behavior of gene-for-gene interactions in natural populations of plants and pathogens (Fig. 1) provides an explanation for the putative prevalence of guarding R proteins. To illustrate the selection process at the molecular level, imagine a particular virulence target in a susceptible host (Fig. 2a) that is modified by an Avr factor of the pathogen (Fig. 2b). This virulence target can represent a complex of multiple cellular components and its Avr-induced modification
Implications for future research
From the model described above and from the available data (Table 1), we predict that guarding is the main mechanism in gene-for-gene-based resistance, although there are already exceptions. For example, AvrPita interacts directly with the R protein Pi-ta [8]. However, it is intriguing that AvrPita is a putative metalloprotease [8], which could hint to its function in virulence for the pathogen. Therefore, it is possible that Pi-ta is the virulence target of AvrPita, and that modification of
Acknowledgements
We apologize to all our colleagues whose work could not be reviewed here because of space limitations. We thank Frank Takken, Marco Kruijt, Bas Brandwagt, Ronelle Roth, Maarten de Kock and Rianne Luderer for critically reading the manuscript, and Jonathan Jones for valuable discussions. We also gratefully acknowledge Jeff Dangl for sharing unpublished data.
References (57)
- et al.
Plant disease-resistance proteins and the gene-for-gene concept
Trends Biochem. Sci.
(1998) Costs of resistance
Curr. Opin. Plant Biol.
(2000)- et al.
Plant–pathogen arms race at the molecular level
Curr. Opin. Plant Biol.
(2000) Recognition specificity for the bacterial avirulence protein AvrPto is determined by Thr-204 in the activation loop of the tomato Pto kinase
Mol. Cell
(1998)A critical analysis of durable resistance
Annu. Rev. Phytopathol.
(1984)Inheritance of pathogenicity in Melampsora lini
Phytopathology
(1942)- et al.
Gene-for-gene coevolution between plants and parasites
Nature
(1992) Gene-for-gene complementarity in plant–pathogen interactions
Annu. Rev. Genet.
(1990)- et al.
Plant resistance genes: their structure, function and evolution
Eur. J. Plant Pathol.
(2000) Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase
Science
(1996)