Pathogen and plant extracellular conflict: fungal DNases and plant DNA

It is well known that DNA carries genetic information and is normally found inside cells. This view was fundamentally altered with the discovery that DNA can be secreted and that extracellular DNA (exDNA) plays a critical role in mammalian neutrophil immune responses. Neutrophils construct extracellular traps (NETs) of protein and DNA that confine pathogens, preventing spread of infection. As a counter-defense, pathogens of animals produce extracellular enzymes (exDNases) to ‘chew up’ host NET DNA. Does the exDNA/exDNase defense mechanism also operate in plant-microbe interactions? Comparison of wild-type Cochliobolus heterostrophus and an isogenic mutant lacking a candidate secreted DNase demonstrates that the mutant is reduced in virulence to maize, both on leaves, the known site of infection, and also on roots. DNase activity can be demonstrated in fungal culture filtrates and is Mg²⁺-dependent and hyper-induced when plant host leaf material is present. Thus, the missing C. heterostrophus exDNase is a virulence determinant and our findings link the importance of secreted DNases to virulence ability of both animal and plant pathogens. We speculate that the found enzyme degrades plant-secreted DNA, a component of a complex matrix akin to neutrophil extracellular traps of animals. The gene encoding the exDNase is broadly conserved and we hypothesize that the exDNA/exDNase mechanism is operative in most fungal-plant pathogenic interactions, including necrotrophic and hemibiotrophic interactions on both below and above ground plant tissues. This mechanism may be an important new target for controlling plant disease.