Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiency
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...
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doaj-409e97ce59b7408c86f3fca23a68684e2020-11-25T02:43:32ZengBMCGenome Biology1474-760X2019-09-0120111210.1186/s13059-019-1799-8Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiencyTaolan Zhao0Qing Huan1Jing Sun2Chunyan Liu3Xiuli Hou4Xiang Yu5Ian M. Silverman6Yi Zhang7Brian D. Gregory8Chun-Ming Liu9Wenfeng Qian10Xiaofeng Cao11State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesState Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesState Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesState Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesUniversity of Chinese Academy of SciencesDepartment of Biology, University of PennsylvaniaDepartment of Biology, University of PennsylvaniaLaboratory for Genome Regulation and Human Health and Center for Genome Analysis, ABLife IncDepartment of Biology, University of PennsylvaniaUniversity of Chinese Academy of SciencesState Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesState Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of SciencesAbstract 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.http://link.springer.com/article/10.1186/s13059-019-1799-8Poly(A) tailsPoly(A)-binding proteinsPAB binding efficiencyPoly(A)-tail G-contentmRNA stabilityTranslational efficiency |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
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 Xiaofeng Cao |
spellingShingle |
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 Xiaofeng Cao Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiency Genome Biology Poly(A) tails Poly(A)-binding proteins PAB binding efficiency Poly(A)-tail G-content mRNA stability Translational efficiency |
author_facet |
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 Xiaofeng Cao |
author_sort |
Taolan Zhao |
title |
Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiency |
title_short |
Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiency |
title_full |
Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiency |
title_fullStr |
Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiency |
title_full_unstemmed |
Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiency |
title_sort |
impact of poly(a)-tail g-content on arabidopsis pab binding and their role in enhancing translational efficiency |
publisher |
BMC |
series |
Genome Biology |
issn |
1474-760X |
publishDate |
2019-09-01 |
description |
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. |
topic |
Poly(A) tails Poly(A)-binding proteins PAB binding efficiency Poly(A)-tail G-content mRNA stability Translational efficiency |
url |
http://link.springer.com/article/10.1186/s13059-019-1799-8 |
work_keys_str_mv |
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