Did a novel virus contribute to late blight epidemics?

Abstract

Phytophthora infestans is the causal agent of potato and tomato late blight. In this study, we characterized a novel RNA virus, Phytophthora infestans RNA virus 2 (PiRV-2). The PiRV-2 genome is 11,170 nt and lacks a polyA tail. It contains a single large open reading frame (ORF) with short 5- and 3-untranslated regions. The ORF is predicted to encode a polyprotein of 3710 aa (calculated molecular weight 410.94 kDa). This virus lacks significant similarity to any other known viruses, even in the conserved RNA-dependent RNA polymerase region. Comparing isogenic strains with or without the virus demonstrated that the virus stimulated sporangia production in P. infestans and appeared to enhance its virulence. Transcriptome analysis revealed that it achieved sporulation stimulation likely through down-regulation of ammonium and amino acid intake in P. infestans. This virus was faithfully transmitted through asexual reproduction. Survey of PiRV-2 presence in a P. infestans collection found it in most strains in the US-8 lineage, a very successful clonal lineage of P. infestans in North America. We suggest that PiRV-2 may have contributed to its success, raising the intriguing possibility that a potentially hypervirulent virus may contribute to late blight epidemics.\n\nAuthor SummaryPotato late blight, the notorious plant disease behind the Irish Potato Famine, continues to pose a serious threat to potato and tomato production worldwide. While most studies on late blight epidemics focuses on pathogen virulence, host resistance, environmental factors and fungicide resistance, we present evidence in this study that a virus infecting the causal agent, Phytophthora infestans, may have played a role. We characterized a novel RNA virus, Phytophthora infestans RNA virus 2 (PiRV-2) and examined its effects on its host. By comparing identical P. infestans strains except with or without the virus, we found that PiRV-2 stimulated sporulation of P. infestans (a critical factor in late blight epidemics) and increased its virulence. We also profiled gene expression in these strains and identified potential molecular mechanisms through which PiRV-2 asserted its sporulation stimulation effect. In a survey of PiRV-2 presence in a P. infestans collection, we found PiRV-2 in most isolates of the US-8 clonal lineage, a very successfull ineage that dominated potato fields in North America for several decades. We suggest that PiRV-2 may have contributed to its success. Our findings raise the intriguing possibility that a potentially hypervirulent virus may contribute to late blight epidemics.