Studying Plant-Pathogen Interactions in the Genomics Era: Beyond Molecular Koch's Postulates to Systems Biology

Molecular factors enabling microbial pathogens to cause plant diseases have been sought with increasing efficacy over three research eras that successively introduced the tools of disease physiology, single-gene molecular genetics, and genomics. From this work emerged a unified model of the interactions of biotrophic and hemibiotrophic pathogens, which posits that successful pathogens typically defeat two levels of plant defense by translocating cytoplasmic effectors that suppress the first defense (surface arrayed against microbial signatures) while evading the second defense (internally arrayed against effectors). As is predicted from this model and confirmed by sequence pattern–driven discovery of large repertoires of cytoplasmic effectors in the genomes of many pathogens, the coevolution of (hemi)biotrophic pathogens and their hosts has generated pathosystems featuring extreme complexity and apparent robustness. These findings highlight the need for a fourth research era of systems biology in which virulence factors are studied as pathosystem components, and pathosystems are studied for their emergent properties.