Here is finally the post I promised that I had wanted to write for quite a while, and can finally write because it was one of the questions on my PhD qualifying exams.
In the 1940s, Harold H. Flor, made a large number of crosses of flax rust races (this is not a trivial exercise, you try mating these minute fungi with each other). He then identified how pathogenicity (the ability to cause disease) on flax was inherited (1). He would use all the flax rust progeny he obtained to infect (inoculate) a large number of available flax lines, and he would score the reaction of the plant to the pathogen (immune, resistance, semi-resistant, susceptible).
If that wasn't enough, Flor also made a large number of crosses of the host, each of which was resistant to none, one, or several races of the flax rust pathogen Melampsori lini. So, he would cross two races of flax, cross the resulting progeny with itself, and analyze the second generation. The reason for this is that the genes involved are often dominant and that you do not see the effect of individual alleles in the first generation (if that doesn't make sense, leave me a note in the comments, I'd be happy to elaborate). In the second generation, the recessive genes segregate and you can see all sorts of fun stuff going on. Flor inoculated all the second generation flax progeny to study the inheritance of resistance. He published those results in a separate paper (2).
Flor found that both resistance in plants as well as avirulence (= lack of virulence/pathogenicity; does not cause disease) in the pathogens were inherited. He also noted that even if the plant had a resistance gene (R), it was only resistant if the pathogen infecting the plant had a particular gene, which is now called an avirulence (Avr) gene. That's kind of weird, isn't it? If the plant has a resistance gene, why should it not be resistant to the pathogen all the time?? Flor also found that in almost all the cases he looked at, resistance was dominant over susceptible, and avirulent was dominant over virulent. Note: Flor used the word "factor" instead of "genes."
Based on Flor's results he formulated what is now called the gene-for-gene hypothesis (3):
For every gene in the plant that confers resistance, there is a corresponding gene in the pathogen that confers avirulence.
Since the genetics of both the host and the pathogen need to be taken into account, we pathologists put this in a quadratic check like this:
On the top row are the possible genotypes of the host. Flax is a diploid organism, i.e. it has two copies of every chromosome. As a result, there are two alleles of every gene (one from each chromosome), so the host can be RR (homozygous resistant), rr (homozygous lacking resistance), or Rr (heterozygous, one allele confers resistance, the other does not). Because resistance is dominant, the Rr plant will be resistant and react no different than the RR plants. The same argument goes for the genotype of the pathogen which is given in the first column of the quadratic check, with AA (homozygous avirulent), aa (homozygous virulent), and Aa (heterozygous, one allele confers avirulence, the other does not; the pathogen will act completely avirulent, because A is dominant over a) possibilities. The only way the plant is resistant is if it carries an R gene, and is infected with a pathogen that carries an Avr gene. In all other combinations, the plant will get disease.
From an evolutionary point of view this makes little sense. Microbes propagate very rapidly compared to the host. Why would a pathogen hang on to a gene that will prevent it from making a set of host plants sick? Why why why?? Microbes evolve so fast, you would think that pathogens with mutations of the Avr gene would have a distinct advantage over those that have a functional Avr gene.
The answer to this question is that Avr genes serve some other purpose in the pathogen, or are actually genes that contribute to pathogenicity, except of course, when it is recognized by the host. The exact same gene can therefore be a pathogenicity in one host-pathogen interaction, and an avirulence gene in another. An example of this is Avr4, an avirulence protein from the plant-pathogenic fungus Cladosporium fulvum. The pathogen is avirulent (cannot cause disease) if it has the Avr4 gene, and if the host it is trying to infect (in this case tomato) has the Cf-4 resistance gene. A recent paper (4) showed that if the Avr4 gene is deleted, the pathogen becomes less virulent, and that introduction of this gene in plants, made the plant more susceptible to a number of other pathogens. Avr4 therefore only contributes to resistance if the host has the corresponding resistance gene, Cf-4, otherwise Avr4 is a virulence factor.
The evolution of R and Avr genes is the result of an arms race going on between host and pathogen, where the host tries to prevent the infection, while the pathogen tries to bypass the host defenses to make the host sick (5,6). This can result in evolution at a pace higher than you would expect without this constant battle.
More on avirulence genes in my next mega-post. Which shouldn't take too long to appear, I have a rough skeleton already. In yet another post I will give some examples from Flor's original papers, and explain how he deduced the genetics of the host and the pathogen. The number of crosses he did is mind-boggling.
(1) Flor, H.H. (1946) Genetics of pathogenicity in Melampsora lini. Journal of Agricultural Research 73: 335-357.
(2) Flor, H.H. (1947) Inheritance of reaction to rust in flax. Journal of Agricultural Research 74:241-262.
(3) Flor, H.H. (1955) Host-parasite interaction in flax rust - its genetics and other implications. Phytopathology 45:680-685.
(4) van Esse, H. P., Bolton, M.D., Stergiopoulos, I., de Wit, P.J.G.M, and Thomma, B.P.H.J. (2007) The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Molecular Plant-Microbe Interactions 20:1092-1101.
(5) Maor, R, and Shirasu, K. (2005) The arms race continues: battle strategies between plants and fungal pathogens. Current Opinion in Microbiology 8:399-404.
(6) van der Does, H.C. and Rep, M. (2007) Virulence genes and the evolution of host specificity in plant-pathogenic fungi. Molecular Plant-Microbe Interactions 20:1175-1182.
Can someone explain this to me?
1 hour ago