Genome Biology
Abstract
Background
Polyadenylation plays a key role in producing mature mRNAs in eukaryotes. It has been 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 0.8–28%. These guanosines frequently cut 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 assay 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.
| 论文编号: | DOI:10.1186/s13059-019-1799-8 |
| 论文题目: | Impact of Poly(A)-tail G-content on Arabidopsis PAB Binding and Their Role in Enhancing Translational Efficiency |
| 英文论文题目: | Impact of Poly(A)-tail G-content on Arabidopsis PAB Binding and Their Role in Enhancing Translational Efficiency |
| 第一作者: | Taolan Zhao, Qing Huan, Jing Sun, Chunyan Liu, Xiuli Hou, Xiang Yu, Ian M. Silverman, Yi Zhang, Brian D. Gregory, Chun-Ming Liu, Wenfeng Qian, and Xiaofeng Cao |
| 英文第一作者: | Taolan Zhao, Qing Huan, Jing Sun, Chunyan Liu, Xiuli Hou, Xiang Yu, Ian M. Silverman, Yi Zhang, Brian D. Gregory, Chun-Ming Liu, Wenfeng Qian, and Xiaofeng Cao |
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| 发表年度: | 2019-09-09 |
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| 摘要: | Background Polyadenylation plays a key role in producing mature mRNAs in eukaryotes. It has been 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 0.8–28%. These guanosines frequently cut 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 assay 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. |
| 英文摘要: | Background Polyadenylation plays a key role in producing mature mRNAs in eukaryotes. It has been 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 0.8–28%. These guanosines frequently cut 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 assay 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. |
| 刊物名称: | Genome Biology |
| 英文刊物名称: | Genome Biology |
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| 其它备注: | Taolan Zhao, Qing Huan, Jing Sun, Chunyan Liu, Xiuli Hou, Xiang Yu, Ian M. Silverman, Yi Zhang, Brian D. Gregory, Chun-Ming Liu, Wenfeng Qian, and Xiaofeng Cao. Impact of Poly(A)-tail G-content on Arabidopsis PAB Binding and Their Role in Enhancing Translational Efficiency. Genome Biology. DOI:10.1186/s13059-019-1799-8 |
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