Metagenomics of plant and fungal viruses reveals an abundance of persistent lifestyles.

Abstract

Most studies of plant viruses have focused on the acute viruses that cause disease in crop and ornamental plants. These viruses are transmitted horizontally, often by insect vectors, and are occasionally transmitted vertically. Although known for at least four decades, the persistent viruses of plants are very poorly studied. These viruses were previously called “cryptic” because they did not appear to illicit any symptoms in infected plants (Boccardo et al., 1987). Persistent plant viruses are not known to be transmitted horizontally, although phylogenetic evidence suggests some level of transmission (Roossinck, 2010). They are vertically transmitted at nearly 100% levels through both ova and pollen (Valverde and Gutierrez, 2007). They have been identified in metagenomic studies by their similarity to known persistent viruses, and because they lack any movement protein, a feature of all known acute viruses that must move through the plant plasmodesmata to establish a systemic infection. Persistent viruses do not move between plant cells, but rather infect every cell and move by cell division. Most plant persistent viruses have double-stranded (ds) RNA genomes, and encode only an RNA dependent RNA polymerase (RdRp) and a coat protein. Of the well-characterized persistent plant viruses, those in the Endornaviridae are the exception. These viruses have a single-stranded (ss) RNA genome, based on their RdRp, and encode a large polyprotein that does not have any apparent coat protein, but encodes a number of additional domains that appear to be derived from diverse sources (Roossinck et al., 2011). They are usually found as dsRNA replicative intermediates. Viruses of fungi have very similar lifestyles to plant persistent viruses, and several virus families are shared between plants and fungi. Phylogenetic evidence indicates that virus transmission has occurred within and between the two kingdoms (Roossinck, 2010; Roossinck et al., 2011). Fungal viruses are even less well-studied than plant viruses, and the diversity of these viruses remains mostly unknown. A majority of known fungal viruses have dsRNA genomes, some have ssRNA genomes, and a few examples of DNA viruses are known (Yu et al., 2010). Recently a negative sense ssRNA virus was characterized from a fungus (Liu et al., 2014). Similar to plant viruses, most fungal viruses have been studied in the context of pathogenic fungi. The discovery of the hypovirulence phenotype of Cryphonectria hypovirus 1 that suppresses the disease phenotype of the chestnut blight fungus led to a search for other examples that could be exploited to mitigate the effects of plant pathogenic fungi [reviewed in Dawe and Nuss (2013)].