Salads Under Siege, E9: Pathogen adaptation

Pathogens continually re-educate themselves to remain successful. We know that on the molecular level, pathogens evolve their gene repertoires in their bid to be competitive with their host species.  Competition is exemplified by the proteins that pathogens secrete during infection, find their molecular target and tickle it in ways that are detrimental to immunity and the ability of plants to fight off the pathogen. Similarly, we also know that host plants deploy their molecular tricks to catch out would be pathogens.

We know already for quite some time that pathogen strains perform differently based on the genetics of either host or microbe. In the case of P. infestans, races of this pathogen had already been identified by virulence and avirulence on distinct potato genotypes, some of which are resistant while others are susceptible. While the host genes responsible were previously identified, the pathogen factors that determined avirulence were yet elusive.

Molecular analyses and genome sequencing finally enabled researchers to identify the factors that specify avirulence on plants carrying the resistance gene R3a. Already in 2005, when functional genomics emerged, computational work allowed the identification of proteins for which secretion are predicted. This advance in combination with facile functional assays in plants provides a quick route to test functions in plants and recognition (Torto et al., 2003; Huitema et al., 2004). A crucial experiment and one demonstrating the idea that effectors can be recognised was by co-expression of both AVR3a and R3a in Nicotiana benthamiana, which led to recognition and hypersensitive cell death responses (Armstrong et al., 2005). As you can see in Figure 1, expression of AVR3a-KI but not AVR3a-EM, leads to cell death, suggesting recognition.

Figure 1. Co-expression of AVR3a-KI with R3a leads to the Hypersensitive Response (HR). Source: Armstrong et al., 2005; Figure 5) 

But wait, what is AVR3a-EM and how is it different from AVR3a-KI? As it turns out, amongst the P. infestans races known at that time, two different versions (alleles) of the AVR3a gene existed. These two alleles encode nearly identical proteins only a few differences. Two of those variations turned out to be important for recognition. The lysine residue at position 80 (K80) and isoleucine at position 103 (I103) conditioned recognition whereas and Glutamic acid (E80) and Methionine (M103) avoided recognition. Importantly, P. infestans races that carried and expressed at least one AVR3aKI allele could not infect potato plants carrying R3a whereas isolates that lacked this allele and only carried AVR3a-EM, could still infect the same potato genotype (still carrying R3a). 

What does this all mean? 

What this work showed is that the pathogen has evolved a version of an effector that is recognised by R3a, to evade recognition. Evolution in action as a response to the emergence and spread of the R3a gene in potato populations!  The evolution of these effector coding genes is continuous and driven by the selection pressures applied by the evolving host species. 

Why is this important?

Breeders are always looking for resistant plant genotypes for their breeding. Years and years of breeding then leads to the creation of a cultivar that is resistant to a set of pathogen races that cause problems on crops. What this and other work is showing, however, is that the introduction of new resistance genes prompts the emergence of new strains that avoid recognition and cause disease again. What this essentially means is that we, as a species, are in a proxy evolutionary arms race with pathogens. At this stage, we are losing it. We simply cannot keep up with these fast-evolving pathogens and need to apply additional measures to keep these microbes at bay. 

REFERENCES

Armstrong, M. R., Whisson, S. C.,  Pritchard, L., Bos, J. I., Venter, E., Avrova, A. O., ... & Hamlin,  N. (2005). An ancestral oomycete locus contains late blight avirulence  gene Avr3a, encoding a protein that is recognized in the host cytoplasm.  Proceedings of the National Academy of Sciences of the United States of America, 102(21), 7766-7771.

Huitema, E., Bos, J. I., Tian, M.,  Win, J., Waugh, M. E., & Kamoun, S. (2004). Linking sequence to  phenotype in Phytophthora–plant interactions. Trends in microbiology, 12(4), 193-200.

Torto, T. A., Li, S., Styer, A., Huitema, E., Testa, A., Gow, N. A., ...  & Kamoun, S. (2003). EST mining and functional expression assays  identify extracellular effector proteins from the plant pathogen  Phytophthora. Genome research, 13(7), 1675-1685.

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