The evolution of novel fungal genes from non-retroviral RNA viruses

Endogenous derivatives of non-retroviral RNA viruses are thought to be absent or rare in eukaryotic genomes because integration of RNA viruses in host genomes is impossible without reverse transcription. However, such derivatives have been proposed for animals, plants and fungi, often based on surrogate bioinformatic evidence. At present, there is little known of the evolution and function of integrated non-retroviral RNA virus genes. Here, we provide direct evidence of integration by sequencing across host-virus gene boundaries and carry out phylogenetic analyses of fungal hosts and totivirids (dsRNA viruses of fungi and protozoans). Further, we examine functionality by tests of neutral evolution, comparison of residues that are necessary for viral capsid functioning and assays for transcripts, dsRNA and viral particles.

Sequencing evidence from gene boundaries was consistent with integration. We detected previously unknown integrated Totivirus-like sequences in three fungi (Candida parapsilosis, Penicillium marneffei and Uromyces appendiculatus). The phylogenetic evidence strongly indicated that the direction of transfer was from Totivirus to fungus. However, there was evidence of transfer of Totivirus-like sequences among fungi. Tests of selection indicated that integrated genes are maintained by purifying selection. Transcripts were apparent for some gene copies, but, in most cases, the endogenous sequences lacked the residues necessary for normal viral functioning.

Our findings reveal that horizontal gene transfer can result in novel gene formation in eukaryotes despite miniaturized genomic targets and a need for co-option of reverse transcriptase.