Pseudouridylation of chloroplast ribosomal RNA contributes to low temperature acclimation in rice

Abstract

Summary Ribosomal RNAs (rRNAs) undergo many modifications during transcription and maturation; homeostasis of rRNA modifications is essential for chloroplast biogenesis in plants. The chloroplast acts as a hub to sense environmental signals, such as cold temperature. However, how RNA modifications contribute to low temperature responses remains unknown. Here we reveal that pseudouridine (Ψ) modification of rice chloroplast rRNAs mediated by the pseudouridine synthase (OsPUS1) contributes to cold tolerance at seedling stage. Loss‐function of OsPUS1 leads to abnormal chloroplast development and albino seedling phenotype at low temperature. We find that OsPUS1 is accumulated upon cold and binds to chloroplast precursor rRNAs (pre‐rRNAs) to catalyse the pseudouridylation on rRNA. These modifications on chloroplast rRNAs could be required for their processing, as the reduction of mature chloroplast rRNAs and accumulation of pre‐rRNAs are observed in ospus1‐1 at low temperature. Therefore, the ribosome activity and translation in chloroplasts is disturbed in ospus1‐1. Furthermore, transcriptome and translatome analysis reveals that OsPUS1 balances growth and stress‐responsive state, preventing excess reactive oxygen species accumulation. Taken together, our findings unveil a crucial function of Ψ in chloroplast ribosome biogenesis and cold tolerance in rice, with potential applications in crop improvement.

Physiological analysis reveals the mechanism of accelerated growth recovery for rice seedlings by nitrogen application after low temperature stress

“…ROS can integrate environmental stress signals, activate gene expression in response to stress, and thus brings about a balance between plant defense and growth ( Wang et al., 2022c ). Stress induces excessive production of ROS (including , H 2 O 2 and OH - ) in plants ( Liu et al., 2018 ), resulting in oxidation and increased soluble protein concentrations, which is beneficial in enhancing plant tolerance to stress, but can also have an impact on normal plant physiological processes ( Yang et al., 2014 ; Fanourakis et al., 2020 ).…”

A mitochondrial pentatricopeptide repeat protein enhances cold tolerance by modulating mitochondrial superoxide in rice

“…Previously, we reported that OsPUS1 was required for the maturation of chloroplast rRNAs at low temperature 12 . Therefore, we wondered whether the defects of chloroplast rRNA processing were rescued in ospus1-1 sop10-1 .…”

“…Our previous study identified a mutant of chloroplast-localized pseudouridine synthase, ospus1-1 , which displayed albino seedlings under low temperature 12 . Dysfunction of OsPUS1 leads to aberrant chloroplast ribosome biogenesis and thus defective chloroplast development at low temperatures, which disturbs the balance between growth and stress responses and enhances ROS accumulation.…”

Multiple omics revealed the growth-promoting mechanism of Bacillus velezensis strains on ramie

“…Pseudouridines are commonly present in evolutionarily conserved and functionally crucial sections of rRNA, tRNA, and additional noncoding RNA molecules. Pseuduridine modification helps stabilize RNA structure and ribosome biogenesis and activity and regulates rRNA processing, pre-mRNA splicing, and protein synthesis, thereby controlling growth, development, and response to stress in different organisms ( Lu et al., 2017 ; Adachi et al., 2019 ; Sun et al., 2019 ; Wang et al., 2022 ). Ferulic acid and other phenolic acids have an inhibitory effect on plant growth, which can inhibit plant nutrient absorption, photosynthesis, respiration, the function and activity of various enzymes, endogenous hormone synthesis, and protein synthesis ( Hussain and Reigosa, 2021 ; John and Sarada, 2012 ).…”