Abstract

Species of Armillaria are distributed globally and include some of the most important pathogens of forest and ornamental trees. Some of them form large long-living clones that are considered as one of the largest organisms on earth and are capable of long-range spore-mediated transfer as well as vegetative spread by drought-resistant hyphal cords called rhizomorphs. However, the virus community infecting these species has remained unknown. In this study we used dsRNA screening and high-throughput sequencing to search for possible virus infections in a collection of Armillaria isolates representing three different species: Armillaria mellea from South Africa, A. borealis from Finland and Russia (Siberia) and A. cepistipes from Finland. Our analysis revealed the presence of both negative-sense RNA viruses and positive-sense RNA viruses, while no dsRNA viruses were detected. The viruses included putative new members of virus families Mymonaviridae, Botourmiaviridae and Virgaviridae and members of a recently discovered virus group tentatively named “ambiviruses” with ambisense bicistronic genomic organization. We demonstrated that Armillaria isolates can be cured of viruses by thermal treatment, which enables the examination of virus effects on host growth and phenotype using isogenic virus-infected and virus-free strains.

Highlights

  • Species of Armillaria are distributed globally and include some of the most important pathogens of forest and ornamental trees

  • We describe the first genome sequences of mycoviruses hosted by the notorious, globally distributed plant pathogens of genus Armillaria

  • Many Armillaria species and other important root-rot fungi, such as Heterobasidion spp. (Bondarzewiaceae; Basidiomycota) and Rosellinia necatrix (Xylariaceae; Ascomycota), form large and long-living clonal individuals, which can be considered as optimal targets for viral biocontrol agents

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Summary

Introduction

Species of Armillaria are distributed globally and include some of the most important pathogens of forest and ornamental trees. The A. mellea lineage has a transcontinental distribution in Europe, North America, Asia and Middle East, and it occurs as an alien species after being introduced by human activities beyond its natural distribution range This fungus was introduced into South Africa by the Dutch settlers more than 300 years ­ago[8] and has escaped from the planted environment to the sensitive and ecologically important natural woody habitat of the surrounding Table M­ ountain[9]. Fungal viruses (mycoviruses) infect hosts representing diverse fungal taxa and various lifestyles including ascomycetous and basidiomycetous micro- and macrofungi, as well as early-diverging fungal lineages such as Chytridiomycota, Blastocladiomycota, Neocallimastigomycota, Zoopagomycota and ­Mucoromycota[14,15,16,17] They are commonly found in edible mushrooms like the cultivated button mushroom (Agaricus bisporus) and Scientific Reports | (2021) 11:7336

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