Testing the efficiency of natural hypovirulence for biological control of chestnut blight under field conditions

Global increases in connectivity have greatly accelerated the frequency of biological invasions across most of Earth's ecosystems, including forests. Once invasive organisms become established in a naïve environment, they are difficult to eradicate or contain; thus, management strategies often focus on mitigating their impacts. As the use of chemical pesticides in forests is increasingly prohibited, biological control of pests and diseases has gained importance as an environmentally friendly alternative. Virus-mediated hypovirulence in the chestnut blight fungus Cryphonectria parasitica is one of the few successful examples of biological control of an invasive forest pathogen. However, experiments testing the stability of this system in situ are still missing. In this study, we conducted a field experiment in chestnut stands with naturally established hypovirulence in Switzerland, Croatia, and North Macedonia to evaluate the effectiveness of CHV1-mediated biocontrol of chestnut blight under different vegetative compatibility (vc) type population structures. Our results demonstrate that CHV1 is highly effective as a biological control agent against C. parasitica. Artificially initiated bark cankers of various vc types were rapidly infected by resident CHV1 strains, which significantly reduced canker growth and sporulation, thereby increasing the survival chances of the infected chestnut sprouts. Under field conditions, vegetative incompatibility barriers proved to be far less restrictive for virus transmission than predicted in vitro. Furthermore, our study demonstrates that the immigration of new fungal genotypes into existing cankers is an inherent component of the epidemiology of C. parasitica, which significantly contributes to the spread of CHV1. These results are particularly favourable for ensuring the success of hypovirulence-mediated biocontrol of chestnut blight in Europe. However, our conclusions cannot be automatically translated to genetically distant vc types from outside Europe, whose accidental introduction should be further avoided.