1. Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiency
- Author
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Wenfeng Qian, Xiu-Li Hou, Qing Huan, Chun-Ming Liu, Yi Zhang, Ian M. Silverman, Brian D. Gregory, Taolan Zhao, Xiaofeng Cao, Jing Sun, Xiang Yu, and Chunyan Liu
- Subjects
Polyadenylation ,Translational efficiency ,lcsh:QH426-470 ,Arabidopsis ,Guanosine ,Genes, Plant ,Poly(A)-Binding Protein II ,Poly(A) tails ,03 medical and health sciences ,chemistry.chemical_compound ,0302 clinical medicine ,Gene Expression Regulation, Plant ,Poly(A)-binding protein ,RNA, Messenger ,mRNA stability ,Poly(A)-tail G-content ,Gene ,lcsh:QH301-705.5 ,030304 developmental biology ,Regulation of gene expression ,Base Composition ,0303 health sciences ,Messenger RNA ,biology ,Arabidopsis Proteins ,Research ,biology.organism_classification ,Poly(A)-binding proteins ,Cell biology ,lcsh:Genetics ,chemistry ,lcsh:Biology (General) ,Protein Biosynthesis ,biology.protein ,030217 neurology & neurosurgery ,PAB binding efficiency ,Protein Binding - Abstract
Background Polyadenylation plays a key role in producing mature mRNAs in eukaryotes. It is widely believed that the poly(A)-binding proteins (PABs) uniformly bind to poly(A)-tailed mRNAs, regulating their stability and translational efficiency. Results We observe that the homozygous triple mutant of broadly expressed Arabidopsis thaliana PABs, AtPAB2, AtPAB4, and AtPAB8, is embryonic lethal. To understand the molecular basis, we characterize the RNA-binding landscape of these PABs. The AtPAB-binding efficiency varies over one order of magnitude among genes. To identify the sequences accounting for the variation, we perform poly(A)-seq that directly sequences the full-length poly(A) tails. More than 10% of poly(A) tails contain at least one guanosine (G); among them, the G-content varies from 0.8 to 28%. These guanosines frequently divide poly(A) tails into interspersed A-tracts and therefore cause the variation in the AtPAB-binding efficiency among genes. Ribo-seq and genome-wide RNA stability assays show that AtPAB-binding efficiency of a gene is positively correlated with translational efficiency rather than mRNA stability. Consistently, genes with stronger AtPAB binding exhibit a greater reduction in translational efficiency when AtPAB is depleted. Conclusions Our study provides a new mechanism that translational efficiency of a gene can be regulated through the G-content-dependent PAB binding, paving the way for a better understanding of poly(A) tail-associated regulation of gene expression. Electronic supplementary material The online version of this article (10.1186/s13059-019-1799-8) contains supplementary material, which is available to authorized users.
- Published
- 2019