Reduced C-to-U RNA editing rates might play a regulatory role in stress response of Arabidopsis

Abstract

C-to-U RNA editing is prevalent in the mitochondrial and chloroplast genes in plants. The C-to-U editing rates are constantly very high. During genome evolution, those edited cytidines are likely to be replaced with thymidines at the DNA level. C-to-U editing events are suggested to be designed for reversing the unfavorable T-to-C DNA mutations. Despite the existing theory showing the importance of editing mechanisms, few studies have investigated the genome-wide adaptive signals of the C-to-U editome or the potential function of C-to-U editing events in the stress response. By analyzing the transcriptome and translatome data of normal and heat-shocked Arabidopsis thaliana and the RNA-seq from cold-stressed plants, combined with genome-wide comparison of mitochondrial/chloroplast genes and nuclear genes from multiple aspects, we present the conservational and translational features of each gene and depict the dynamic mitochondrial/chloroplast C-to-U RNA editome. We found that the tAI (tRNA adaptation index) and basic translation levels are lower for mitochondrial/chloroplast genes than for nuclear genes. Interestingly, although we found adaptive signals for the global C-to-U RNA editome in mitochondrial/chloroplast genes, the C-to-U (T) alteration would usually cause a reduction in the codon tAI value. Moreover, the C-to-U editing rates are significantly reduced under heat or cold stress when compared to the normal condition. This reduction is irrelevant to the temperature-sensitive RNA structures. Several cases have illustrated that under heat stress, the reduced C-to-U editing rates alleviate ribosome stalling and consequently facilitate the local translation. Our study reveals that in Arabidopsis thaliana the mitochondrial/chloroplast C-to-U RNA editing rates are reduced under heat or cold stress. This reduction is associated with the alleviation of decreased tAI/translation rate of edited codons. The regulation of C-to-U editing rates could be the tradeoff between quantity and quality. We profile the dynamic change of C-to-U RNA editome under heat stress and propose a potential role of editing sites in the heat response. Our work should be appealing to the plant physiologists as well as the RNA editing community.

Keywords: Arabidopsis thaliana; C-to-U RNA editing; Reduced editing rates; Stress response; Translation regulation.