A SA-regulated lincRNA promotes Arabidopsis disease resistance by modulating pre-rRNA processing

Regulation of gene expression at translational level has been shown critical for plant defense against pathogen infection. Pre-rRNA processing is essential for ribosome biosynthesis and thus affects protein translation. It remains unknown if plants modulate pre-rRNA processing as a translation regulatory mechanism for disease resistance. In this study, we show a 5' snoRNA capped and 3' polyadenylated (SPA) lincRNA named SUNA1 promotes disease resistance involved in modulating pre-rRNA processing in Arabidopsis. SUNA1 expression is highly induced by Pst DC3000 infection, which is impaired in SA biosynthesis-defective mutant sid2 and signaling mutant npr1. Consistently, SA triggers SUNA1 expression dependent on NPR1. Functional analysis indicates that SUNA1 plays a positive role in Arabidopsis defense against Pst DC3000 relying on its snoRNA signature motifs. Potential mechanism study suggests that the nucleus-localized SUNA1 interacts with the nucleolar methyltransferase fibrillarin to modulate SA-controlled pre-rRNA processing, then enhancing the translational efficiency (TE) of some defense genes in Arabidopsis response to Pst DC3000 infection. NPR1 appears to have similar effects as SUNA1 on pre-rRNA processing and TE of defense genes. Together, these studies reveal one kind of undescribed antibacterial translation regulatory mechanism, in which SA-NPR1-SUNA1 signaling cascade controls pre-rRNA processing and TE of certain defense genes in Arabidopsis.