NBS-LRR deriving sRNAs uniquely in nuclear-replicating virus-infected tomato plants target components of the photosynthetic machinery

Plant viruses modify gene expression in infected tissues by altering the micro (mi)RNA-mediated regulation of genes. Among conserved miRNA targets there are transcripts coding for transcription factors, RNA silencing core and disease resistance proteins. Paralogs in these gene families are widely present in plant genomes and are known to respond differently to miRNA-mediated regulation during plant virus infections. Using genome-wide approaches applied to Solanum lycopersicum infected by a nuclear-replicating virus we highlighted miRNA-mediated cleavage events that could not be revealed in virus-free systems: among them, we confirmed the targeting of one of the two Argonaute1 paralogs, seven transcriptional factors from five different families cleaved by miR156, miR160, miR166, miR169 and miR172 and one RX-Coiled-coil (RX-CC), nucleotide binding (NBS), leucine rich (LRR) mRNA cleaved by miR6024. Interestingly, in most cases short indels close to the target sites discriminated cleavage of duplicates, indicating a functional significance of short indels in fine-tuning gene expression in plant-virus interaction. miR6024-mediated cleavage, uniquely in virus-infected tissues, triggers the production of several unique 21nt secondary siRNAs. These secondary siRNAs, rather than being involved in the cascade regulation of other NBS-LRR paralogs, explained cleavages of several mRNAs annotated as defence related proteins and components of the photosynthetic machinery. Outputs of these data explain part of the phenotype plasticity in plants, including the appearance of yellowing symptoms in the viral pathosystem.