Bioinformatic and experimental analyses revealed pathogen-derived pathoPEP candidates predicted to control plant miRNA expression and infection

Abstract

The partners of an ecological association tend to copy the biological system of their hosts. We hypothesized that microorganisms, particularly pathogens, have acquired the ability to express short peptides (pathoPEPs) homologous to host miPEPs, thus modulating the expression of the corresponding host microRNA (miRNA) and the function of miRNA-targeted genes. The pathosystem involving interactions between Brassica napus and its pathogen Plasmodiophora brassicae was studied. The data set contains RNA-seq and ribosomal profiling from two plant genotypes inoculated with one pathogen isolate. Using in silico analysis, we identified three putative pathoPEPs produced by P. brassicae and their targeted plant miRNA genes. A link between the level of infection of B. napus by P. brassicae and the expression of pathoPEPs and their targeted miRNA genes was found, with the expression of the latter two being inversely related. Finally, we identified differential expression and translation of genes predicted to be targets of pathoPEP-regulated miRNAs. These genes, involved in auxin pathway, immune defense, root architecture, or carbohydrate metabolism, are thought to enable P. brassicae, through its pathoPEPs, to hijack plant's metabolic pathways (e.g., hormonal pathways, sugar synthesis, root morphology), thereby facilitating its invasion. Using in silico approaches, the involvement of miPEPs from this host–pathogen system as a host post-transcriptional regulatory pathway is described herein for the first time.