Natural cross-kingdom transmission of a novel ssDNA mycovirus confers broad-spectrum resistance to plant diseases

Abstract

Cross-kingdom virus transmission between plants and fungi remains rare in nature. Here, a novel circular ssDNA virus, Diaporthe pseudophoenicicola DNA virus 1 (DpDV1), was identified from the phytopathogenic fungus Diaporthe pseudophoenicicola. DpDV1 attenuates the pathogenicity of both its original and experimental host fungi, demonstrating its potential as a biocontrol agent against fungal phytopathogens. Remarkably, DpDV1 displays bidirectional plant-fungal transmission capability without inducing observable phenotypic changes in plant hosts, overcoming the limitations imposed by vegetative incompatibility in conventional hypovirulence-based biocontrol approaches. Immunocytochemical localization assays revealed DpDV1 is localized in the chloroplasts of plant cells, demonstrating its cross-kingdom transmission. Furthermore, we demonstrated DpDV1 can cross-protect plants against plant viruses, establishing foundations for cross-protection-based management of plant virus diseases. Hence, we report a novel ssDNA mycovirus and provide evidence of mycovirus cross-kingdom transmission between plant and fungi, providing innovative strategies for mycovirus biocontrol of plant fungal and viral diseases.