Abstract
Frequencies of CpG and UpA dinucleotides in most plant RNA virus genomes show degrees of suppression comparable to those of vertebrate RNA viruses. While pathways that target CpG and UpAs in HIV-1 and echovirus 7 genomes and restrict their replication have been partly characterised, whether an analogous process drives dinucleotide underrepresentation in plant viruses remains undetermined. We examined replication phenotypes of compositionally modified mutants of potato virus Y (PVY) in which CpG or UpA frequencies were maximised in non-structural genes (including helicase and polymerase encoding domains) while retaining protein coding. PYV mutants with increased CpG dinucleotide frequencies showed a dose-dependent reduction in systemic spread and pathogenicity and up to 1000-fold attenuated replication kinetics in distal sites on agroinfiltration of tobacco plants (Nicotiana benthamiana). Even more extraordinarily, comparably modified UpA-high mutants displayed no pathology and over a million-fold reduction in replication. Tobacco plants with knockdown of RDP6 displayed similar attenuation of CpG- and UpA-high mutants suggesting that restriction occurred independently of the plant siRNA antiviral responses. Despite the evolutionary gulf between plant and vertebrate genomes and encoded antiviral strategies, these findings point towards the existence of novel virus restriction pathways in plants functionally analogous to innate defence components in vertebrate cells.
Highlights
There is increasing evidence that many phenotypic properties of a virus and aspects of its interaction with hosts are determined by structural and compositional attributes of its genome
We have recently obtained evidence that, in addition to CpG dinucleotides, UpA dinucleotides may be targeted by zinc finger antiviral protein (ZAP) and by RNAseL, a site-specific RNA nuclease may contribute to the attenuation of high CpG mutants of E721
To quantify the degree of suppression of CpG and UpA dinucleotides in plant viruses and how this compares with host plant genomic composition, we first analysed CpG, CHG, CHH and TpA frequencies in genomic DNA and in the subset of coding sequences expressed as mRNAs in several example plants
Summary
There is increasing evidence that many phenotypic properties of a virus and aspects of its interaction with hosts are determined by structural and compositional attributes of its genome. Viruses may display compositional abnormalities, most notably, suppression of the frequencies of CpG and UpA dinucleotides that have, in mammalian RNA viruses and retroviruses, been shown to influence replication[3,4,5,6]. In part, these biases in RNA viruses may be influenced by the genomic composition of the hosts they infect, potentially mirroring the suppression of CpG and TpA dinucleotides in vertebrate and plant DNA genomes[7,8,9]. An Agrobacterium tumefaciens mediated delivery method for the infectious clone of PVYNTN was used to investigate the effect of elevated dinucleotide frequencies on virus replication and systemic spread in Nicotiana benthamiana
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