Distinct Activation of Defense-Related Gene Networks in Rosetted Versus Symptomless Shoots in Rose Rosette Virus-Infected Roses

Rose rosette virus (RRV) causes witches’ broom disease in roses. This study examined whether differences in disease in these spatially distinct domains are associated with local changes in defense-related hormones and transcriptional reprogramming. The levels of defense-related phytohormones salicylic acid (SA), jasmonic acid (JA), 9-lipoxygenase (9-LOX), 13-lipoxygenase (13-LOX), and derived oxylipins were different in these distinct tissues. We curated differentially expressed genes involved in the biosynthesis, storage, and signaling of SA, JA, and oxylipins to reveal how specific defense pathways correlate with these distinct disease states. Gene ontology (GO) analysis and the Disease Resistance Analysis and Gene Orthology 3 (DRAGO3) pipeline revealed stress-associated genes and classical resistance (R) gene families that were differently expressed in these distinct tissue domains. Promoter analysis of defense-associated transcription factors and histone modifiers revealed hormone responsive elements, suggesting complex hormone crosstalk is involved in defense-related gene expression. We confirmed by RT-qPCR, a notable subset of defense genes in the chromosome 5 hotspot, specifically in the linkage group 5 (LG5) quantitative trait loci, linked to reduced RRV susceptibility, was altered in both field-infected and greenhouse-inoculated plants. The association of high versus low disease states with distinct defense hormone signatures and gene expression patterns suggests that local immune states, rather than whole-plant defenses, determine whether a cane becomes rosetted or remains asymptomatic.