Arabidopsis Pentatricopeptide Repeat Protein GEND2 Participates in Mitochondrial RNA Editing

• Published in: Plant and cell physiology 2024-12, Vol.65 (11), p.1849-1861
• Main Authors: Nie, Yaqing, Li, Yan, Yuan, Penglai, Wu, Chengyun, Wang, Xiaoqing, Wang, Chunfei, Xu, Xiumei, Shen, Zhenguo, Hu, Zhubing
• Format: Article
• Language: English
• Subjects: Arabidopsis - genetics; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Gene Expression Regulation, Plant; Mitochondria - genetics; Mitochondria - metabolism; Mitochondrial Proteins - genetics; Mitochondrial Proteins - metabolism; Mutation - genetics; Plant Roots - genetics; Plant Roots - growth & development; RNA Editing - genetics; RNA, Mitochondrial - genetics; RNA, Mitochondrial - metabolism
• ISSN: 0032-0781; 1471-9053; 1471-9053
• DOI: 10.1093/pcp/pcae108

In Arabidopsis, RNA editing alters more than 500 cytidines (C) to uridines (U) in mitochondrial transcripts, a process involving the family of pentatricopeptide repeat (PPR) proteins. Here, we report a previously uncharacterized mitochondrial PLS-type PPR protein, GEND2, which functions in the mitochondrial RNA editing. The T-DNA insertion in the 5'-untranslated region of GEND2, referred to as gend2-1, results in defective root development compared to wild-type (WT) plants. A comprehensive examination of mitochondrial RNA-editing sites revealed a significant reduction in the gend2-1 mutant compared to WT plants, affecting six specific mitochondrial RNA editing sites, notably within the mitochondrial genes CcmFn-1, RPSL2 and ORFX. These genes encode critical components of cytochrome protein maturation pathway, mitochondrial ribosomal subunit and twin arginine translocation subunits, respectively. Further analysis of the transcriptional profile of the gend2-1 mutant and WT revealed a striking induction of expression in a cluster of genes associated with mitochondrial dysfunction and regulated by ANAC017, a key regulator coordinating organelle functions and stress responses. Intriguingly, the gend2-1 mutation activated an ANAC017-dependent signaling aimed at countering cell wall damage induced by cellulose synthase inhibitors, as well as an ANAC017-independent pathway that retarded root growth under normal condition. Collectively, our findings identify a novel mitochondrial PLS-type PPR protein GEND2, which participates in the editing of six specific mitochondrial RNA editing sites. Furthermore, the gend2-1 mutation triggers two distinct pathways in plants: an ANAC017-dependent pathway and ANAC017-independent pathway.