Zhang Yingying, Xu Pengfei, Xue Wanxin, Zhu Weimin, Yu Xiang
Shanghai Key Laboratory of Protected Horticulture Technology, The Protected Horticulture Institute, Shanghai Academy of Agricultural Sciences, Shanghai, 201403, China.
Joint International Research Laboratory of Metabolic and Developmental Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, 200240, China.
Plant J. 2023 Nov;116(3):728-743. doi: 10.1111/tpj.16400. Epub 2023 Jul 26.
Diurnal rhythms are known to regulate the expression of a large number of genes, coordinating plant growth and development with diel changes in light and temperature. However, the impact of RNA metabolism on rhythmic gene oscillations in plant is not yet fully understood. To address this question, we performed transcriptome and degradome profiling on tomato leaves at 6 time points during one 24 h cycle, using RNA-seq and genome-wide mapping of uncapped and cleavage transcripts (GMUCT). Time-series profiling of RNA-seq revealed 9342 diurnal-oscillated genes, which were enriched in various metabolic processes. To quantify the general level of RNA degradation for each gene, we utilized the Proportion Uncapped (PU) metric, which represents the GMUCT/RNA-seq ratio. Oscillated PU analysis revealed that 3885 genes were regulated by rhythmic RNA degradation. The RNA decay of these diurnal genes was highly coordinated with mRNA downregulation during oscillation, highlighting the critical role of internal transcription-degradation balance in rhythmic gene oscillation. Furthermore, we identified 2190 genes undergoing co-translational RNA decay (CTRD) with 5' phosphate read ends enriched at the boundary of ribosomes stalling at translational termination sites. Interestingly, diurnal-changed mRNAs with large amplitudes tended to be co-translationally decay, suggesting that CTRD contributed to the rapid turnover of diurnal mRNAs. Finally, we also identified several genes, whose miRNA cleavage efficiency oscillated in a diurnal manner. Taken together, these findings uncovered the vital functions of RNA metabolism, including rhythmic RNA degradation, CTRD, and miRNA cleavage, in modulating the diurnal mRNA oscillations during diel change at post-transcriptional level in tomato.
已知昼夜节律可调节大量基因的表达，使植物的生长发育与光照和温度的昼夜变化相协调。然而，RNA代谢对植物节律性基因振荡的影响尚未完全了解。为了解决这个问题，我们在一个24小时周期的6个时间点对番茄叶片进行了转录组和降解组分析，采用RNA测序和无帽及切割转录本的全基因组图谱分析（GMUCT）。RNA测序的时间序列分析揭示了9342个昼夜振荡基因，这些基因在各种代谢过程中富集。为了量化每个基因的RNA降解总体水平，我们使用了无帽比例（PU）指标，它代表GMUCT/RNA测序比率。振荡PU分析表明，3885个基因受节律性RNA降解调控。这些昼夜基因的RNA衰变与振荡过程中的mRNA下调高度协调，突出了内部转录-降解平衡在节律性基因振荡中的关键作用。此外，我们鉴定了2190个经历共翻译RNA衰变（CTRD）的基因，其5'磷酸化读端在核糖体在翻译终止位点停滞的边界处富集。有趣的是，具有大幅度昼夜变化mRNA倾向于共翻译衰变，这表明CTRD有助于昼夜mRNA的快速周转。最后，我们还鉴定了几个基因，其miRNA切割效率呈昼夜振荡。综上所述，这些发现揭示了RNA代谢在转录后水平调节番茄昼夜变化期间昼夜mRNA振荡中的重要功能，包括节律性RNA降解、CTRD和miRNA切割。
