Structured 3' UTRs destabilize mRNAs in plants

Background: RNA secondary structure (RSS) contains new information code that is unwired to influence the expression of transcription, RNA processing, and protein synthesis among other processes. 3' untranslated regions (3' UTRs) of mRNA also hold the key for many aspects of gene regulation. However, there are often contradictory results regarding the roles of RSS in 3' UTRs in gene expression in different organisms and/or contexts.Results: Here we incidentally discovered that pri-miR159a when embedded in a 3' UTR could promote mRNA accumulation. The enhanced expression is attributed to the earlier polyadenylation of the transcript within the hybrid pri-miR159a-3' UTR and resultantly, a poorly structured 3' UTR. RNA decay assays indicate that poorly structured 3' UTRs could promote mRNA stability, whereas highly structured 3' UTRs destabilize mRNA in vivo. Genome-wide DMS-MaPseq also revealed the prevailing inverse relationship between 3' UTR RSS and transcript accumulation in the whole transcriptome of Arabidopsis, rice, and even human. Mechanistically, transcripts with highly structured 3' UTRs are preferentially degraded by 3'-5' exoribonuclease SOV, leading to decreased expression in Arabidopsis. Finally, we engineered different structured 3' UTRs to an endogenous FT gene and were able to alter the FT-regulated flowering time in Arabidopsis.Conclusion: We concluded that high-structured 3' UTRs typically cause reduced accumulation of the harbored transcripts in Arabidopsis. This pattern can extend to rice and even mammals. Furthermore, our study provides a new strategy by engineering the 3' UTR RSS to modify plant traits in agricultural production and mRNA stability in biotechnology.