Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector

Abstract

Mycoviruses are usually transmitted horizontally via hyphal anastomosis and vertically via sexual/asexual spores. Previously, we reported that a gemycircularvirus, Sclerotinia sclerotiorum hypovirulenceassociated DNA virus 1 (SsHADV-1), could infect its fungal host extracellularly. Here, we discovered that SsHADV-1 could infect a mycophagous insect, Lycoriella ingenua, and use it as a transmission vector. Virus acquired by larvae feeding on colonies of a virus-infected strain of S. sclerotiorum was replicated and retained in larvae, pupae, adults, and eggs. Virus could be transmitted to insect offspring when larvae were injected with virus particles and allowed to feed on a nonhost fungus. Virus replication in insect cells was further confirmed by inoculating Spodoptera frugiperda cells with virus particles and analyzing with RT-PCR, Northern blot, immunofluorescence, and flow cytometry assays. Larvae could transmit virus once they acquired virus by feeding on virus-infected fungal colony. Offspring larvae hatched from viruliferous eggs were virus carriers and could also successfully transmit virus. Virus transmission between insect and fungus also occurred on rapeseed plants. Virus-infected isolates produced less repellent volatile substances to attract adults of L. ingenua. Furthermore, L. ingenua was easily observed on Sclerotinia lesions in rapeseed fields, and viruliferous adults were captured from fields either sprayed with a virus-infected fungal strain or nonsprayed. Our findings may facilitate the exploration of mycoviruses for control of fungal diseases and enhance our understanding of the ecology of SsHADV-1 and other newly emerging SsHADV-1-like viruses, which were recently found to be widespread in various niches including human HIV-infected blood, human and animal feces, insects, plants, and even sewage. mycovirus | biological control | mycophagous insect | mutualism | gemycircularvirus

Novel, diverse RNA viruses from Mediterranean isolates of the phytopathogenic fungus, Rosellinia necatrix: insights into evolutionary biology of fungal viruses

“…However, SsHADV1 has been shown to enter host fungal cells in media and the leaves of plants (host to the viral host fungus) via an unknown extracellular route (Yu et al, 2013). Interestingly, SsHADV1 is replicated in and transmitted from fungi to fungi by a mycophagous insect, Lycoriella ingenua (Liu et al, 2016). Other vector organisms such as mites and/or nematodes are implicated in the horizontal transmission of some fungal viruses (mycoviruses), but these reports have not been substantiated Yaegashi et al, 2013;Petrzik et al, 2016).…”

Virus-mediated suppression of host non-self recognition facilitates horizontal transmission of heterologous viruses

“…Furthermore, hypovirulence-associated mycoviruses also have potential to be used to control fungal disease [34]. With the exception of SsHADV1 [35, 36], mycoviruses lack extracellular phases in their life cycles and are not known to have transmission vectors; they are transmitted vertically via propagation and horizontally via hyphal anastomosis. To date, only very few mycoviruses that infect ascomycetous fungi were reported to be transmitted via sexual spores, most mycoviruses are transmitted via asexual spores [37, 38].…”

A tripartite ssDNA mycovirus from a plant pathogenic fungus is infectious as cloned DNA and purified virions

“…These viruses have small (~2 to 2.4 kb), circular ssDNA genomes, and they encode rolling-circle replication initiation proteins (Rep) that are mostly similar to those of geminiviruses, as well as unique capsid proteins (9,10). Of all the identified genomoviruses, only Sclerotinia sclerotiorum hypovirulence-associated DNA virus 1 (SsHADV-1) (species, Sclerotinia gemycircularvirus 1; genus, Gemycircularvirus) has been associated with known hosts, S. sclerotiorum (11) and a mycophagous fly, Lycoriella ingenua (12).…”