Plant/pathogen evolutionary dynamic defies simple arms race model

Grow a disease-resistant plant and it seems that in no time a flourishing garden wilts as the disease finds a way around the plant's defense. The battle between plants and disease-causing pathogens has been compared to an arms race--with each new defense calling forth a new offensive weapon, and neither gaining the upper hand for long. Like the Red Queen in Alice in Wonderland, the plant and the attacking pathogen seem to run very fast to stay in the same place.

To begin to construct a new understanding of the co-evolutionary dynamic of plant/pathogen interaction, a team of University of Chicago researchers review what is known about R-genes, recognition genes, in an article in the June 22, 2001, issue of the journal Science.

Like the immune system in animals, plants depend on special molecules in each cell recognizing foreign invaders to alert the organism to mount its defense. In plants, these defensive molecules, produced by R-genes, are highly varied and are able to recognize a wide array of invading pathogens based on determinants called Avr factors. The highly specific nature of this interaction suggested that R-genes and Avr-genes would undergo an arms race. In this model, novel R-genes, able to recognize new Avr factors, spread to high frequency in the population, followed by pathogen mutations which create Avr factors again able to evade detection.

"When we went looking for the molecular evidence for an arms race, we found that the evolutionary dynamics are actually much more complex," said Joy Bergleson, Ph.D., associate professor of ecology and evolution at the University of Chicago. "In particular, we see that resistant and susceptible alleles (alternative forms of the R-genes) often both persist for very long periods of time."

The presence of ancient and distinct R-gene alleles is inconsistent with a simple arms race model. "We also find examples of loci, clusters of genes, that retain many different alleles, some of which are known to be functionally distinct, another pattern that is inconsistent with the simple notion of an arms race," said Bergelson.

While the presence of functionally distinct alleles that have been retained for long periods of time suggests that a simple arms race model is inadequate, there is some evidence in favor of the model. Studies of the highly variable region of R-genes involved in Avr recognition support the arms race model through evidence of adaptive evolution, suggesting that selection is driving the evolution of the variable region (LLR) of R-genes, particularly in clusters of these genes. This adaptive evolution in the LLR is consistent with an evolutionary arms race with pathogens forcing selection to continually alter their recognition specificity.

"Any new model for the evolutionary dynamics of R-genes has to account for the profound role adaptive evolution plays in R-gene selection and the maintenance of polymorphic alleles over time," said Bergelson. "We need more work to better understand short-term disease dynamics and construct new evolutionary models."

Additional authors of the paper are Martin Kreitman, Ph.D.; Eli A. Stahl, Ph.D. and Dacheng Tian, Ph.D., Department of Ecology and Evolution of the University of Chicago.

This research was supported by grants from the National Institutes of Health, a Packard Fellowship and a Sloan/Department of Energy Fellowship.