The identification of conserved sequence features of co-translationally decayed mRNAs and upstream open reading frames in angiosperm transcriptomes.

Abstract

RNA turnover is essential in maintaining messenger RNA (mRNA) homeostasis during various developmental stages and stress responses. Co-translational mRNA decay (CTRD), a process in which mRNAs are degraded while still associated with translating ribosomes, has recently been discovered to function in yeast and three angiosperm transcriptomes. However, it is still unclear how prevalent CTRD across the plant lineage. Moreover, the sequence features of co-translationally decayed mRNAs have not been well-studied. Here, utilizing a collection of publicly available degradome sequencing datasets for another seven angiosperm transcriptomes, we have confirmed that CTRD is functioning in at least 10 angiosperms and likely throughout the plant lineage. Additionally, we have identified sequence features shared by the co-translationally decayed mRNAs in these species, implying a possible conserved triggering mechanism for this pathway. Given that degradome sequencing datasets can also be used to identify actively translating upstream open reading frames (uORFs), which are quite understudied in plants, we have identified numerous actively translating uORFs in the same 10 angiosperms. These findings reveal that actively translating uORFs are prevalent in plant transcriptomes, some of which are conserved across this lineage. We have also observed conserved sequence features in the regions flanking these uORFs' stop codons that might contribute to ribosome stalling at these sequences. Finally, we discovered that there were very few overlaps between the mRNAs harboring actively translating uORFs and those sorted into the co-translational decay pathway in the majority of the studied angiosperms, suggesting that these two processes might be nearly mutually exclusive in those species. In total, our findings provide the identification of CTRD and actively translating uORFs across a broad collection of plants and provide novel insights into the important sequence features associated with these collections of mRNAs and regulatory elements, respectively.