Diurnal gene oscillations modulated by RNA metabolism in tomato

Abstract

SUMMARYDiurnal 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.