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

• Published in: Plant science (Limerick) 2022-03, Vol.316, p.111178-111178, Article 111178
• Main Authors: Kong, Xiaoyu, Wang, Huacai, Zhang, Mengting, Chen, Xiaoying, Fang, Rongxiang, Yan, Yongsheng
• Format: Article
• Language: English
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Disease resistance; Disease Resistance - genetics; Gene Expression Regulation, Plant; lincRNA; Plant Diseases - genetics; Pre-rRNA processing; Pseudomonas syringae; RNA Precursors - genetics; RNA, Long Noncoding; Salicylic Acid; U3 snoRNA
• ISSN: 0168-9452; 1873-2259
• DOI: 10.1016/j.plantsci.2022.111178

•SUNA1 is a SPA lincRNA and its expression is highly induced by Pst DC3000 infection relying on SA biosynthesis and signaling.•SUNA1 plays a positive role in Arabidopsis defense against Pst DC3000 relying on its snoRNA signature motifs.•SUNA1 modulates SA-controlled pre-rRNA processing and translational efficiency of some defense genes. 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.