An article in PLoS Pathogens by Morris et al describe a hypothesis about the evolution and origins of plant pathogens applying the parallel theories to the emergence of medically relevant pathogens. The authors highlight the importance of understanding the evolution of organisms in the context of emerging pathogens like Puccinia Ug99 for our ability to design strategies to protect human health and food supplies. Both bacterial and fungal pathogens of plants are discussed but I (perhaps unsurprisingly) focus on the fungi here.
The authors suggest that theories on the emergence of diseases proposed in medical epidemiology apply to plant pathogens as well. Some of these ideas are quite provocative on the evolution of intracellular pathogens and how environmental microbes become pathogenic have been proposed by Arturo Casadevall and colleagues. The idea that some traits are “dual-use” in that they protect or are advantageous to the microbe in its environmental niche, but the traits also play a role in pathogenesis of animals. A good example is the sugar coated capsule of Cryptococcus neoformans which may have evolved in part as protection from predation by amoebae for this basidiomycete yeast fungus. The capsule is one of the most important virulence factors for Cryptococcus as it allows the fungus to escape from macrophages by enlarging until it bursts the white blood cell and may also be a sink for reactive oxygen species (ROS) produced by the macrophages. Ameobae and macrophages use similar approaches to engulf the yeast cells and so this “dual-use” factor may have evolved in defense against amoebae but can also be used as a defense tactic against the animal immune system. In the case of plant pathogens, Morris et al suggest that dual use traits also exist. Genes like efflux pumps play a dual-use role in exporting antimicrobials when encountered from competitors in the soil and protecting the fungus Botrytis cinerea against the plant defense molecule resveratol or the fungicide fenpiclonil. Mycotoxin, or toxins produced by fungi, likely evolved with the primary trait of reducing predation by animals like nematodes have the secondary effect of being toxic to humans and livestock. Traits that evolved to cope with abiotic stress also lead the formation of molecules that allow a fungus to be successful in colonization of a plant host. This includes siderophores which allow a fungus to scavenge iron which is critical for growing in the soil where bioactive iron is not readily available, but also when a host uses iron sequestration as a defense mechanism. Melanin, a compound that can protect against ROS, UV damage, and perhaps even energy acquisition from gamma radiation and in plant pathogens it is an important compound for the formation of appressoria.
By understanding the evolutionary history of either selection or drift that gave rise to these dual-use traits we can learn more about the specificities and roles the pathways play in the primary biology of the organisms in addition to the pathology. Morris et al provide a strong argument that studying the ecology of pathogenic organisms is important to identify more of these dual-use traits, and understanding the evolution of them through studies of related species which may not be animal or plant pathogens, we can reconstruct the steps in history that gave rise to modern pathogens. This knowledge will assist in the identification, classification, and study of emerging diseases and in the battle against the ones that already impact agriculture and health.
I think this article gives a very helpful outline of how and why studying both the primary molecular basis for pathogenesis and the evolutionary and ecological context of the organism are necessary in a pursuit of understanding diseases and their origins. For microbes this can be difficult without a reliable way to find phylogenetically (evolutionarily) closely related species that are good comparison species. By casting a wide sampling net we can at least identify what is out there in terms of microbial diversity. Metagenomic approaches are helping to characterize the microbial composition in detailed and high-throughput ways that culturing or microscopy could not achieve but we still will need to collect cultures and study the relatives of these pathogens to understand when these dual-use traits were acquired, how they may have changed, and what role adaptations have played in the evolution of a successful pathogen.
Morris, C., Bardin, M., Kinkel, L., Moury, B., Nicot, P., & Sands, D. (2009). Expanding the Paradigms of Plant Pathogen Life History and Evolution of Parasitic Fitness beyond Agricultural Boundaries PLoS Pathogens, 5 (12) DOI: 10.1371/journal.ppat.1000693
Casadevall, A. (2008). Evolution of Intracellular Pathogens Annual Review of Microbiology, 62 (1), 19-33 DOI: 10.1146/annurev.micro.61.080706.093305