Home LiteratureArticle Details
PMID: 31481099 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Impact of poly(A)-tail G-content on Arabidopsis PAB binding and their role in enhancing translational efficiency.

Genome biology ·Vol. 20 ·No. 1 ·2019-00-03 ·Pages 189

Zhao T, Huan Q, Sun J, Liu C, Hou X, Yu X, Silverman IM, Zhang Y, Gregory BD, Liu CM, Qian W, Cao X

Abstract

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. 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. 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.

Keywords
Arabidopsis PAB binding efficiency Poly(A) tails Poly(A)-binding proteins Poly(A)-tail G-content Translational efficiency mRNA stability
MeSH Terms
Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism,physiology Base Composition Gene Expression Regulation, Plant Genes, Plant Guanosine/analysis Poly(A)-Binding Protein II/genetics,metabolism,physiology Poly(A)-Binding Proteins/genetics,metabolism,physiology Protein Binding Protein Biosynthesis RNA, Messenger/chemistry,metabolism
Chemicals
Arabidopsis Proteins Poly(A)-Binding Protein II Poly(A)-Binding Proteins RNA, Messenger Guanosine
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Zhao Taolan
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China. | Key Laboratory of Genetic Network Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China. | University of Chinese Academy of Sciences, Beijing, 100049, China.
Huan Qing
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China. | Key Laboratory of Genetic Network Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China.
Sun Jing
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China.
Liu Chunyan
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China.
Hou Xiuli
University of Chinese Academy of Sciences, Beijing, 100049, China. | Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
Yu Xiang
Department of Biology, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Silverman Ian M
Department of Biology, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Zhang Yi
Laboratory for Genome Regulation and Human Health and Center for Genome Analysis, ABLife Inc, Wuhan, 430075, Hubei, China.
Gregory Brian D
Department of Biology, University of Pennsylvania, Philadelphia, PA, 19104, USA.
Liu Chun-Ming
University of Chinese Academy of Sciences, Beijing, 100049, China. | Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
Qian Wenfeng ORCID
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China. wfqian@genetics.ac.cn. | Key Laboratory of Genetic Network Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China. wfqian@genetics.ac.cn. | University of Chinese Academy of Sciences, Beijing, 100049, China. wfqian@genetics.ac.cn.
Cao Xiaofeng
State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China. xfcao@genetics.ac.cn. | University of Chinese Academy of Sciences, Beijing, 100049, China. xfcao@genetics.ac.cn. | CAS Center for Excellence in Molecular Plant Sciences, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China. xfcao@genetics.ac.cn.
References (59)
59 references, click to expand
  1. Interaction of eIF4G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation.
    Curr Biol. 2000 Sep 21;10(18):1147-50 PMID: 10996799
  2. The structure, function and evolution of proteins that bind DNA and RNA.
    Nat Rev Mol Cell Biol. 2014 Nov;15(11):749-60 PMID: 25269475
  3. A spatial and temporal map of C. elegans gene expression.
    Genome Res. 2011 Feb;21(2):325-41 PMID: 21177967
  4. A common function for mRNA 5' and 3' ends in translation initiation in yeast.
    Genes Dev. 1995 Dec 1;9(23):2997-3007 PMID: 7498795
  5. Uridylation prevents 3' trimming of oligoadenylated mRNAs.
    Nucleic Acids Res. 2013 Aug;41(14):7115-27 PMID: 23748567
  6. HTSeq--a Python framework to work with high-throughput sequencing data.
    Bioinformatics. 2015 Jan 15;31(2):166-9 PMID: 25260700
  7. Arabidopsis thaliana class II poly(A)-binding proteins are required for efficient multiplication of turnip mosaic virus.
    J Gen Virol. 2008 Sep;89(Pt 9):2339-2348 PMID: 18753244
  8. mTAIL-seq reveals dynamic poly(A) tail regulation in oocyte-to-embryo development.
    Genes Dev. 2016 Jul 15;30(14):1671-82 PMID: 27445395
  9. A protein of molecular weight 78,000 bound to the polyadenylate region of eukaryotic messenger RNAs.
    Proc Natl Acad Sci U S A. 1973 Mar;70(3):924-8 PMID: 4515002
  10. mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos.
    Elife. 2016 Jul 30;5: PMID: 27474798
  11. Global translational reprogramming is a fundamental layer of immune regulation in plants.
    Nature. 2017 May 25;545(7655):487-490 PMID: 28514447
  12. Translational dynamics revealed by genome-wide profiling of ribosome footprints in Arabidopsis.
    Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):E203-12 PMID: 24367078
  13. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  14. Multiple portions of poly(A)-binding protein stimulate translation in vivo.
    EMBO J. 2000 Sep 1;19(17):4723-33 PMID: 10970864
  15. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation.
    Nat Biotechnol. 2010 May;28(5):511-5 PMID: 20436464
  16. The ProteomeXchange consortium in 2017: supporting the cultural change in proteomics public data deposition.
    Nucleic Acids Res. 2017 Jan 4;45(D1):D1100-D1106 PMID: 27924013
  17. Efficient RNA polyuridylation by noncanonical poly(A) polymerases.
    Mol Cell Biol. 2007 May;27(10):3612-24 PMID: 17353264
  18. Mixed tailing by TENT4A and TENT4B shields mRNA from rapid deadenylation.
    Science. 2018 Aug 17;361(6403):701-704 PMID: 30026317
  19. Poly(A) binding proteins: are they all created equal?
    Wiley Interdiscip Rev RNA. 2013 Mar-Apr;4(2):167-79 PMID: 23424172
  20. Unexpected complexity of poly(A)-binding protein gene families in flowering plants: three conserved lineages that are at least 200 million years old and possible auto- and cross-regulation.
    Genetics. 2003 Jan;163(1):311-9 PMID: 12586718
  21. Poly(A)-tail profiling reveals an embryonic switch in translational control.
    Nature. 2014 Apr 3;508(7494):66-71 PMID: 24476825
  22. Pyicos: a versatile toolkit for the analysis of high-throughput sequencing data.
    Bioinformatics. 2011 Dec 15;27(24):3333-40 PMID: 21994224
  23. Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch- and specific clock-controlled genes.
    Proc Natl Acad Sci U S A. 2002 Aug 20;99(17):11513-8 PMID: 12167669
  24. Affinity purification of ARE-binding proteins identifies polyA-binding protein 1 as a potential substrate in MK2-induced mRNA stabilization.
    Biochem Biophys Res Commun. 2003 Feb 14;301(3):665-70 PMID: 12565831
  25. Genome-Wide Analysis of PAPS1-Dependent Polyadenylation Identifies Novel Roles for Functionally Specialized Poly(A) Polymerases in Arabidopsis thaliana.
    PLoS Genet. 2015 Aug 25;11(8):e1005474 PMID: 26305463
  26. Nanopore detachment kinetics of poly(A) binding proteins from RNA molecules reveals the critical role of C-terminus interactions.
    Biophys J. 2012 Mar 21;102(6):1427-34 PMID: 22455926
  27. Control of poly(A) tail length.
    Wiley Interdiscip Rev RNA. 2011 May-Jun;2(3):348-61 PMID: 21957022
  28. The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro.
    Mol Cell Biol. 1989 Feb;9(2):659-70 PMID: 2565532
  29. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling.
    Science. 2009 Apr 10;324(5924):218-23 PMID: 19213877
  30. An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro.
    Mol Cell Biol. 1999 Jul;19(7):4552-60 PMID: 10373504
  31. Human PABP binds AU-rich RNA via RNA-binding domains 3 and 4.
    Eur J Biochem. 2004 Jan;271(2):450-7 PMID: 14717712
  32. The organization and regulation of mRNA-protein complexes.
    Wiley Interdiscip Rev RNA. 2017 Jan;8(1): PMID: 27324829
  33. The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes.
    EMBO J. 1998 Sep 15;17(18):5427-37 PMID: 9736620
  34. Recognition of polyadenylate RNA by the poly(A)-binding protein.
    Cell. 1999 Sep 17;98(6):835-45 PMID: 10499800
  35. Co-ordinated Regulations of mRNA Synthesis and Decay during Cold Acclimation in Arabidopsis Cells.
    Plant Cell Physiol. 2017 Jun 1;58(6):1090-1102 PMID: 28444357
  36. Tales of poly(A): a review.
    Gene. 1990 Jul 16;91(2):151-8 PMID: 1976572
  37. TAIL-seq: genome-wide determination of poly(A) tail length and 3' end modifications.
    Mol Cell. 2014 Mar 20;53(6):1044-52 PMID: 24582499
  38. Regulation of Poly(A) Tail and Translation during the Somatic Cell Cycle.
    Mol Cell. 2016 May 5;62(3):462-471 PMID: 27153541
  39. A particle associated with the polyadenylate segment in mammalian messenger RNA.
    Proc Natl Acad Sci U S A. 1972 Nov;69(11):3247-50 PMID: 4508317
  40. Structure and function of poly(A) binding proteins.
    Biochim Biophys Acta. 2004 May 25;1678(2-3):67-84 PMID: 15157733
  41. The role of mammalian poly(A)-binding proteins in co-ordinating mRNA turnover.
    Biochem Soc Trans. 2012 Aug;40(4):856-64 PMID: 22817748
  42. Fast gapped-read alignment with Bowtie 2.
    Nat Methods. 2012 Mar 04;9(4):357-9 PMID: 22388286
  43. The PRIDE database and related tools and resources in 2019: improving support for quantification data.
    Nucleic Acids Res. 2019 Jan 8;47(D1):D442-D450 PMID: 30395289
  44. Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms.
    Genes Dev. 2005 Jan 1;19(1):104-13 PMID: 15630022
  45. Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation.
    Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9046-51 PMID: 9256432
  46. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.
    Genome Biol. 2013 Apr 25;14(4):R36 PMID: 23618408
  47. Protein tightly bound to globin mRNA.
    Biochem Biophys Res Commun. 1972 Apr 14;47(1):88-95 PMID: 5027144
  48. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics.
    Nat Protoc. 2009;4(5):698-705 PMID: 19373234
  49. Poly(A)-binding proteins are required for diverse biological processes in metazoans.
    Biochem Soc Trans. 2014 Aug;42(4):1229-37 PMID: 25110030
  50. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools.
    Nucleic Acids Res. 2012 Jan;40(Database issue):D1202-10 PMID: 22140109
  51. EIN2-directed translational regulation of ethylene signaling in Arabidopsis.
    Cell. 2015 Oct 22;163(3):670-83 PMID: 26496607
  52. A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability.
    Mol Cell Biol. 1987 Sep;7(9):3268-76 PMID: 3313012
  53. The mechanism of eukaryotic translation initiation and principles of its regulation.
    Nat Rev Mol Cell Biol. 2010 Feb;11(2):113-27 PMID: 20094052
  54. Integrative genome-wide analysis reveals HLP1, a novel RNA-binding protein, regulates plant flowering by targeting alternative polyadenylation.
    Cell Res. 2015 Jul;25(7):864-76 PMID: 26099751
  55. Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans.
    Nature. 2002 Aug 29;418(6901):975-9 PMID: 12214599
  56. The roles of cytoplasmic poly(A)-binding proteins in regulating gene expression: a developmental perspective.
    Brief Funct Genomic Proteomic. 2004 Aug;3(2):125-41 PMID: 15355595
  57. Class II members of the poly(A) binding protein family exhibit distinct functions during Arabidopsis growth and development.
    Translation (Austin). 2017 Feb 17;5(1):e1295129 PMID: 28702277
  58. Ensembl BioMarts: a hub for data retrieval across taxonomic space.
    Database (Oxford). 2011 Jul 23;2011:bar030 PMID: 21785142
  59. Expression Atlas: gene and protein expression across multiple studies and organisms.
    Nucleic Acids Res. 2018 Jan 4;46(D1):D246-D251 PMID: 29165655
Article Info
Journal
Genome biology
Abbr.
Genome Biol
ISSN
1474-760X
DOI
10.1186/s13059-019-1799-8
Email
wfqian@genetics.ac.cn
xfcao@genetics.ac.cn
Published
2019-00-03
Epub
2019-00-03
Pages
189
Language
English
Region
England
NLM ID
100960660
PMCID
PMC6724284
Subset
IM
External Links
PubMed source DOI: 10.1186/s13059-019-1799-8 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2