Absence of SICKLE triggers programed cell death by disturbing alternative splicing and decay of mRNAs

• Published in: Plant physiology (Bethesda) 2023-07, Vol.192 (3), p.2523-2536
• Main Authors: Wu, Chengyun, Zhen, Weibo, Wang, Xingsong, Li, Yan, Wang, Wei, Hu, Zhubing
• Format: Article
• Language: English
• Subjects: Alternative Splicing; Apoptosis; Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Gene Expression Regulation, Plant; RNA Stability; RNA, Messenger - genetics; Salicylic Acid - metabolism
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1093/plphys/kiad192

Abstract Programed cell death (PCD) plays fundamental roles in plant development and responses to environmental stresses. Here, we report a protein, SICKLE (SIC), which represses PCD. In Arabidopsis (Arabidopsis thaliana), the loss-of-function mutant of SIC, sic-4, hyperaccumulated lariat intronic RNAs (lariRNAs) and exhibited PCD. The gene encoding an RNA debranching enzyme 1 (DBR1), a rate-limiting enzyme for lariRNAs decay, was overexpressed to reduce the level of lariRNAs in the sic-4 mutant, which led to suppression of PCD. Meanwhile, another lariRNAs hyper-accumulating mutant, dbr1-2, also exhibited PCD, further indicating that sic-4 PCD is caused by hyper-accumulation of lariRNAs. Transcriptional profiling analyses revealed that the sic-4 mutation disturbed alternative splicing and decay of mRNAs associated with salicylic acid (SA) homeostasis, a well-known molecule functioning in PCD regulation. Moreover, SA is dramatically increased in sic-4 and the disruption of SA biosynthesis and signaling suppressed PCD in the mutant, demonstrating that SA functions downstream of sic-4. Taken together, our results demonstrate that SIC is involved in regulating SA-triggered PCD. SICKLE is involved in the regulation of salicylic acid-triggered programmed cell death in Arabidopsis by affecting alternative splicing and decay of mRNAs.