Identification of the viral determinant of hypovirulence and host range in Sclerotiniaceae of a genomovirus reconstructed from the plant metagenome

Authors: FENG, CHENCHEN - South Dakota State University; FENG, JIUHUAN - South Dakota State University; WANG, ZIYI - South Dakota State University; PEDERSEN, CONNOR - South Dakota State University; WANG, XIUQING - South Dakota State University; SALEEM, HUMA - South Dakota State University; Domier, Leslie; Marzano, Shin-Yi

Submitted to: Journal of Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/9/2021
Publication Date: 8/10/2021
Citation: Feng, C., Feng, J., Wang, Z., Pedersen, C., Wang, X., Saleem, H., Domier, L.L., Marzano, S.L. 2021. Identification of the viral determinant of hypovirulence and host range in Sclerotiniaceae of a genomovirus reconstructed from the plant metagenome. Journal of Virology. 95(17). Article e00264-21. https://doi.org/10.1128/JVI.00264-21.
DOI: https://doi.org/10.1128/JVI.00264-21

Interpretive Summary: Little is known about the exact host range of widespread genomoviruses. The genome of soybean leaf-associated gemygorvirus-1 (SlaGemV-1) was originally assembled from a metagenomic/metatranscriptomic study without known hosts. Here, we rescued SlaGemV-1 and found that it could infect three important plant pathogenic fungi and Fall armyworm (S. frugiperda, Sf9) insect cells, but not a model nematode, C. elegans, or model plant species. Most importantly, SlaGemV-1 shows promise for inducing hypovirulence of the tested fungal species under family Sclerotiniaceae, including Sclerotinia sclerotiorum, Botrytis cinerea, Monilinia fruticola. The viral determinant of hypovirulence was further identified as replication initiation protein.

Technical Abstract: Uncharacterized viral genomes that encode circular replication-associated proteins of single-stranded DNA viruses have been discovered by metagenomics/metatranscriptomics approaches. Some of these novel viruses are classified under the newly formed Genomoviridae family. Here, we determine the host range of a novel genomovirus, SlaGemV-1, through the transfection of Sclerotinia sclerotiorum with infectious clones. Inoculating with the rescued virions, we further transfected Botrytis cinerea and Monilinia fruticola, two economically important members of family Sclerotiniaceae, and Fusarium oxysporum. SlaGemV-1 causes hypovirulence in S. sclerotiorum, B. cinerea, and M. fruticola. SlaGemV-1 also replicates in Spodoptera frugiperda insect cells, but not in Caenorhabditis elegans nor plants. By expressing viral-encoded genes separately through site-specific integration, the replication protein alone was sufficient to cause debilitation. Our study is the first to demonstrate the reconstruction of a metagenomically discovered genomovirus without known hosts with the potential of inducing hypovirulence, and the infectious clone allows for studying mechanisms of genomovirus-host interactions that are conserved across genera.