Shrinkage of Genome Size in a Plant RNA Virus upon Transfer of an Essential Viral Gene into the Host Genome

Tromas, Nicolas; Zwart, Mark P.; Forment, Javier; Elena, Santiago F.

If genome size of RNA viruses is limited by a tradeoff between RNA-dependent RNA polymerases (RdRp) fidelity and decreased replication rates, then examples of enlargement in genome size should be scarce for RNA viruses. There are, however, some examples of the integration of host genetic material into viral RNA genomes, leading to the largest known RNA viruses. For instance, the genome of coronaviruses contains homologous sequences of at least five cellular enzymes that are associated with RNA processing and that may be involved in modulating mutation rate (Snijder et al. 2003 ). Acquisition of a host's ubiquitin gene by certain strains of bovine viral diarrhoea pestivirus resulted in increased pathogenicity (Meyers et al. 1989) . Plant closterovirus genomes encode for a homologue of cellular molecular chaperone HSP70 (Dolja et al. 2006 ) that is required for virion assembly (Satyanarayana et al. 2000) . Finally, a particularly interesting case is the ubiquitous presence of DNA/RNA repair AlkB-like proteins in several groups of plant viruses, including closterovirus, flexivirus, tymovirus, and even one potyvirus (Blackberry virus Y; Susaimuthu et al. 2008) , whose function has been postulated to be both repair of nucleic acid alkylation and suppression of posttranscriptional gene silencing (Aravind and Koonin 2001; Bratlie and Drabløs 2005) . Similarly, the insertion of sequences into a viral genome generally leads to their rapid removal, as has been seen in the case of heterologous genes (Chapman et al. 1992; Guo et al. 1998; Chung et al 2007; Paar et al. 2007; Zwart et al 2014) and repetitions of endogenous noncoding sequences (Nagai et al. 2003; Gritsun and Gould 2006) . Finally, most viruses have a tendency to evolve defective interfering viruses under conditions promoting cellular coinfection (Huang 1973; Roux et al. 1991) , again suggesting a link between genome size and replication. Although demographic conditions may allow for the maintenance of extraneous sequences (Dolja et al. 1993; Zwart et al. 2014) , overall it appears as if genome size is limited and under purifying selection, and that the incorporation or maintenance of foreign sequences comes at a cost to viruses (Sakai et al. 1999; Marks et al. 2005; Holmes 2009; Zwart et al. 2014 ).