Identification of a negative-strand RNA virus with natural plant and fungal hosts.

The presence of viruses that spread to both plant and fungal populations in nature has posed intriguingly scientific question. We found a negative-strand RNA virus related to members of the family Phenuiviridae, named Valsa mali negative-strand RNA virus 1 (VmNSRV1), which induced strong hypovirulence and was prevalent in a population of the phytopathogenic fungus of apple Valsa canker (Valsa mali) infecting apple orchards in the Shaanxi Province of China. Intriguingly, VmNSRV1 encodes a protein with a viral cell-to-cell movement function in plant tissue. Mechanical leaf inoculation showed that VmNSRV1 could systemically infect plants. Moreover, VmNSRV1 was detected in 24 out of 139 apple trees tested in orchards in Shaanxi Province. Fungal inoculation experiments showed that VmNSRV1 could be bidirectionally transmitted between apple plants and V. mali, and VmNSRV1 infection in plants reduced the development of fungal lesions on leaves. Additionally, the nucleocapsid protein encoded by VmNSRV1 is associated with and rearranged lipid droplets in both fungal and plant cells. VmNSRV1 represents a virus that has adapted and spread to both plant and fungal hosts and shuttles between these two organisms in nature (phyto-mycovirus) and is potential to be utilized for the biocontrol method against plant fungal diseases. This finding presents further insights into the virus evolution and adaptation encompassing both plant and fungal hosts.

Infection of Two Heterologous Mycoviruses Reduces the Virulence of Valsa mali, a Fungal Agent of Apple Valsa Canker Disease.

Mycovirus infection has been widely shown to attenuate the virulence of phytopathogenic fungi. Valsa mali is an agriculturally important fungus that causes Valsa canker disease in apple trees. In this study, two unrelated mycoviruses [Cryphonectria hypovirus 1 (CHV1, genus Hypovirus, and single-stranded RNA) and Mycoreovirus 1 (MyRV1, genus Mycoreovirus, double-stranded RNA)] that originated from Cryphonectria parasitica (chestnut blight fungus) were singly or doubly introduced into V. mali via protoplast fusion. CHV1 and MyRV1 stably infected V. mali and caused a reduction in fungal vegetative growth and virulence. Co-infection of both viruses further reduced the virulence of V. mali but compromised the stability of CHV1 infection and horizontal transmission through hyphal anastomosis. Infections of MyRV1 and, to a lesser extent, CHV1 up-regulated the transcript expression of RNA silencing-related genes in V. mali. The accumulation of CHV1 (but not MyRV1) was elevated by the knockdown of dcl2, a key gene of the RNA silencing pathway. Similarly, the accumulation of CHV1 and the efficiency of the horizontal transmission of CHV1 during co-infection was restored by the knockdown of dcl2. Thus, CHV1 and MyRV1 are potential biological control agents for apple Valsa canker disease, but co-infection of both viruses has a negative effect on CHV1 infection in V. mali due to the activation of antiviral RNA silencing by MyRV1 infection.