Genome-Wide Analysis of PAPS1-Dependent Polyadenylation Identifies Novel Roles for Functionally Specialized Poly(A) Polymerases in
The poly(A) tail of eukaryotic mRNAs promotes export from the nucleus, translation in the cytoplasm and stability of the mRNA, and changes in poly(A)-tail length can strongly impact on gene expression. The Arabidopsis thaliana genome encodes three nuclear canonical poly(A) polymerases (PAPS1, PAPS2, PAPS4) that fulfill different functions, presumably by preferentially polyadenylating certain subpopulations of pre-mRNAs. Here, we use a fractionation-based technique to assess the transcriptome-wide impact of reduced PAPS1 activity and identify functional classes of transcripts that are particularly sensitive to reduced PAPS1 activity. Analysis of these transcripts identifies two novel biological functions for PAPS1 in ribosome biogenesis and in redox homeostasis that we confirm experimentally. By overlaying our results with information about genome-wide co-expression, we demonstrate that genes co-expressed with PAPS1 are the most strongly affected in terms of poly(A)-tail length and total-abundance changes in the paps1 mutants. This provides strong evidence that the co-expression of these genes with PAPS1 that is seen across thousands of microarrays is at least partly caused by altered activity of the PAPS1 isoform, suggesting that the plant indeed uses modulation of the balance of isoform activities to coordinately regulate the expression of groups of genes.
Vyšlo v časopise:
Genome-Wide Analysis of PAPS1-Dependent Polyadenylation Identifies Novel Roles for Functionally Specialized Poly(A) Polymerases in. PLoS Genet 11(8): e32767. doi:10.1371/journal.pgen.1005474
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005474
Souhrn
The poly(A) tail of eukaryotic mRNAs promotes export from the nucleus, translation in the cytoplasm and stability of the mRNA, and changes in poly(A)-tail length can strongly impact on gene expression. The Arabidopsis thaliana genome encodes three nuclear canonical poly(A) polymerases (PAPS1, PAPS2, PAPS4) that fulfill different functions, presumably by preferentially polyadenylating certain subpopulations of pre-mRNAs. Here, we use a fractionation-based technique to assess the transcriptome-wide impact of reduced PAPS1 activity and identify functional classes of transcripts that are particularly sensitive to reduced PAPS1 activity. Analysis of these transcripts identifies two novel biological functions for PAPS1 in ribosome biogenesis and in redox homeostasis that we confirm experimentally. By overlaying our results with information about genome-wide co-expression, we demonstrate that genes co-expressed with PAPS1 are the most strongly affected in terms of poly(A)-tail length and total-abundance changes in the paps1 mutants. This provides strong evidence that the co-expression of these genes with PAPS1 that is seen across thousands of microarrays is at least partly caused by altered activity of the PAPS1 isoform, suggesting that the plant indeed uses modulation of the balance of isoform activities to coordinately regulate the expression of groups of genes.
Zdroje
1. Eckmann CR, Rammelt C, Wahle E. Control of poly(A) tail length. Wiley Interdiscip Rev RNA. 2011; 2: 348–361. doi: 10.1002/wrna.56 21957022
2. Hunt AG. Messenger RNA 3' end formation in plants. Curr Top Microbiol Immunol. 2008; 326: 151–177. 18630752
3. Millevoi S, Vagner S. Molecular mechanisms of eukaryotic pre-mRNA 3' end processing regulation. Nucleic Acids Res. 2010; 38: 2757–2774. doi: 10.1093/nar/gkp1176 20044349
4. Fuke H, Ohno M. Role of poly (A) tail as an identity element for mRNA nuclear export. Nucleic Acids Res. 2008; 36: 1037–1049. 18096623
5. Dower K, Kuperwasser N, Merrikh H, Rosbash M. A synthetic A tail rescues yeast nuclear accumulation of a ribozyme-terminated transcript. RNA. 2004; 10: 1888–1899. 15547135
6. Dunn EF, Hammell CM, Hodge CA, Cole CN. Yeast poly(A)-binding protein, Pab1, and PAN, a poly(A) nuclease complex recruited by Pab1, connect mRNA biogenesis to export. Genes Dev. 2005; 19: 90–103. 15630021
7. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell. 2009; 136: 731–745. doi: 10.1016/j.cell.2009.01.042 19239892
8. Weill L, Belloc E, Bava FA, Mendez R. Translational control by changes in poly(A) tail length: recycling mRNAs. Nat Struct Mol Biol. 2012; 19: 577–585. doi: 10.1038/nsmb.2311 22664985
9. Preiss T, Muckenthaler M, Hentze MW. Poly(A)-tail-promoted translation in yeast: implications for translational control. RNA. 1998; 4: 1321–1331. 9814754
10. Kojima S, Sher-Chen EL, Green CB. Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev. 2012; 26: 2724–2736. doi: 10.1101/gad.208306.112 23249735
11. Anderson JS, Parker RP. The 3' to 5' degradation of yeast mRNAs is a general mechanism for mRNA turnover that requires the SKI2 DEVH box protein and 3' to 5' exonucleases of the exosome complex. The EMBO journal. 1998; 17: 1497–1506. 9482746
12. Decker CJ, Parker R. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes & development. 1993; 7: 1632–1643.
13. Hsu CL, Stevens A. Yeast cells lacking 5'—>3' exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5' cap structure. Molecular and cellular biology. 1993; 13: 4826–4835. 8336719
14. Parker R. RNA degradation in Saccharomyces cerevisae. Genetics. 2012; 191: 671–702. doi: 10.1534/genetics.111.137265 22785621
15. Eckhart VM, Geber MA. Character variation and geographic range in Clarkia xantiana (Onagraceae): breeding system and phenology distinguish two common subspecies. Madroño. 2000 46: 117–125.
16. Meijer HA, Bushell M, Hill K, Gant TW, Willis AE, Jones P, et al. A novel method for poly(A) fractionation reveals a large population of mRNAs with a short poly(A) tail in mammalian cells. Nucleic Acids Res. 2007; 35: e132. 17933768
17. Subtelny AO, Eichhorn SW, Chen GR, Sive H, Bartel DP. Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature. 2014; 508: 66–71. doi: 10.1038/nature13007 24476825
18. Benoit B, Mitou G, Chartier A, Temme C, Zaessinger S, Wahle E, et al. An essential cytoplasmic function for the nuclear poly(A) binding protein, PABP2, in poly(A) tail length control and early development in Drosophila. Developmental cell. 2005; 9: 511–522. 16198293
19. Cui J, Sartain CV, Pleiss JA, Wolfner MF. Cytoplasmic polyadenylation is a major mRNA regulator during oogenesis and egg activation in Drosophila. Developmental biology. 2013; 383: 121–131. doi: 10.1016/j.ydbio.2013.08.013 23978535
20. Juge F, Zaessinger S, Temme C, Wahle E, Simonelig M. Control of poly(A) polymerase level is essential to cytoplasmic polyadenylation and early development in Drosophila. The EMBO journal. 2002; 21: 6603–6613. 12456666
21. Kashiwabara S, Noguchi J, Zhuang T, Ohmura K, Honda A, Sugiura S, et al. Regulation of spermatogenesis by testis-specific, cytoplasmic poly(A) polymerase TPAP. Science. 2002; 298: 1999–2002. 12471261
22. Kim KW, Wilson TL, Kimble J. GLD-2/RNP-8 cytoplasmic poly(A) polymerase is a broad-spectrum regulator of the oogenesis program. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107: 17445–17450. doi: 10.1073/pnas.1012611107 20855596
23. Suh N, Jedamzik B, Eckmann CR, Wickens M, Kimble J. The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103: 15108–15112. 17012378
24. Gohin M, Fournier E, Dufort I, Sirard M-A. Discovery, identification and sequence analysis of RNAs selected for very short or long poly A tail in immature bovine oocytes. Molecular human reproduction. 2014; 20: 127–138. doi: 10.1093/molehr/gat080 24233545
25. Charlesworth A, Meijer HA, de Moor CH. Specificity factors in cytoplasmic polyadenylation. Wiley Interdiscip Rev RNA. 2013; 4: 437–461. doi: 10.1002/wrna.1171 23776146
26. Mellman DL, Gonzales ML, Song C, Barlow CA, Wang P, Kendziorski C, et al. A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature. 2008; 451: 1013–1017. doi: 10.1038/nature06666 18288197
27. Kuhn U, Gundel M, Knoth A, Kerwitz Y, Rudel S, Wahle E. Poly(A) tail length is controlled by the nuclear poly(A)-binding protein regulating the interaction between poly(A) polymerase and the cleavage and polyadenylation specificity factor. The Journal of biological chemistry. 2009; 284: 22803–22814. doi: 10.1074/jbc.M109.018226 19509282
28. Wahle E. A novel poly(A)-binding protein acts as a specificity factor in the second phase of messenger RNA polyadenylation. Cell. 1991; 66: 759–768. 1878970
29. Hunt AG, Xu R, Addepalli B, Rao S, Forbes KP, Meeks LR, et al. Arabidopsis mRNA polyadenylation machinery: comprehensive analysis of protein-protein interactions and gene expression profiling. BMC Genomics. 2008; 9: 220. doi: 10.1186/1471-2164-9-220 18479511
30. Meeks LR, Addepalli B, Hunt AG. Characterization of genes encoding poly(A) polymerases in plants: evidence for duplication and functional specialization. PLoS One. 2009; 4: e8082. doi: 10.1371/journal.pone.0008082 19956626
31. Trost G, Vi SL, Czesnick H, Lange P, Holton N, Giavalisco P, et al. Arabidopsis poly(A) polymerase PAPS1 limits founder-cell recruitment to organ primordia and suppresses the salicylic acid-independent immune response downstream of EDS1/PAD4. Plant J. 2013.
32. Vi SL, Trost G, Lange P, Czesnick H, Rao N, Lieber D, et al. Target specificity among canonical nuclear poly(A) polymerases in plants modulates organ growth and pathogen response. Proc Natl Acad Sci U S A. 2013; 110: 13994–13999. doi: 10.1073/pnas.1303967110 23918356
33. Shcherbik N, Wang M, Lapik YR, Srivastava L, Pestov DG. Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep. 2010; 11: 106–111. doi: 10.1038/embor.2009.271 20062005
34. Win TZ, Draper S, Read RL, Pearce J, Norbury CJ, Wang SW. Requirement of fission yeast Cid14 in polyadenylation of rRNAs. Mol Cell Biol. 2006; 26: 1710–1721. 16478992
35. Janicke A, Vancuylenberg J, Boag PR, Traven A, Beilharz TH. ePAT: a simple method to tag adenylated RNA to measure poly(A)-tail length and other 3' RACE applications. RNA. 2012; 18: 1289–1295. doi: 10.1261/rna.031898.111 22543866
36. Thomas PE, Wu XH, Liu M, Gaffney B, Ji GL, Li QSQ, et al. Genome-Wide Control of Polyadenylation Site Choice by CPSF30 in Arabidopsis. Plant Cell. 2012; 24: 4376–4388. doi: 10.1105/tpc.112.096107 23136375
37. Sherstnev A, Duc C, Cole C, Zacharaki V, Hornyik C, Ozsolak F, et al. Direct sequencing of Arabidopsis thaliana RNA reveals patterns of cleavage and polyadenylation. Nat Struct Mol Biol. 2012; 19: 845–852. doi: 10.1038/nsmb.2345 22820990
38. Narsai R, Howell KA, Millar AH, O'Toole N, Small I, Whelan J. Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. The Plant cell. 2007; 19: 3418–3436. 18024567
39. Amrani N, Ghosh S, Mangus DA, Jacobson A. Translation factors promote the formation of two states of the closed-loop mRNP. Nature. 2008; 453: 1276–1280. doi: 10.1038/nature06974 18496529
40. Moritz M, Paulovich AG, Tsay YF, Woolford JL Jr. Depletion of yeast ribosomal proteins L16 or rp59 disrupts ribosome assembly. J Cell Biol. 1990; 111: 2261–2274. 2277060
41. Warner JR, Udem SA. Temperature sensitive mutations affecting ribosome synthesis in Saccharomyces cerevisiae. J Mol Biol. 1972; 65: 243–257. 4557193
42. Francis KE, Lam SY, Harrison BD, Bey AL, Berchowitz LE, Copenhaver GP. Pollen tetrad-based visual assay for meiotic recombination in Arabidopsis. Proc Natl Acad Sci U S A. 2007; 104: 3913–3918. 17360452
43. Borges F, Gardner R, Lopes T, Calarco JP, Boavida LC, Slotkin RK, et al. FACS-based purification of Arabidopsis microspores, sperm cells and vegetative nuclei. Plant Methods. 2012; 8: 44. doi: 10.1186/1746-4811-8-44 23075219
44. Reina-Pinto JJ, Voisin D, Teodor R, Yephremov A. Probing differentially expressed genes against a microarray database for in silico suppressor/enhancer and inhibitor/activator screens. Plant J. 2010; 61: 166–175. doi: 10.1111/j.1365-313X.2009.04043.x 19811619
45. Laloi C, Stachowiak M, Pers-Kamczyc E, Warzych E, Murgia I, Apel K. Cross-talk between singlet oxygen- and hydrogen peroxide-dependent signaling of stress responses in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2007; 104: 672–677. 17197417
46. Schwarzlander M, Fricker MD, Muller C, Marty L, Brach T, Novak J, et al. Confocal imaging of glutathione redox potential in living plant cells. Journal of Microscopy. 2008; 231: 299–316. doi: 10.1111/j.1365-2818.2008.02030.x 18778428
47. Vranova E, Atichartpongkul S, Villarroel R, Van Montagu M, Inze D, Van Camp W. Comprehensive analysis of gene expression in Nicotiana tabacum leaves acclimated to oxidative stress. Proc Natl Acad Sci U S A. 2002; 99: 10870–10875. 12122207
48. Zhang J, Addepalli B, Yun K-Y, Hunt AG, Xu R, Rao S, et al. A polyadenylation factor subunit implicated in regulating oxidative signaling in Arabidopsis thaliana. PLoS One. 2008; 3: e2410. doi: 10.1371/journal.pone.0002410 18545667
49. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008; 9: 559. doi: 10.1186/1471-2105-9-559 19114008
50. Beilharz TH, Preiss T. Widespread use of poly(A) tail length control to accentuate expression of the yeast transcriptome. RNA. 2007; 13: 982–997. 17586758
51. Lackner DH, Beilharz TH, Marguerat S, Mata J, Watt S, Schubert F, et al. A network of multiple regulatory layers shapes gene expression in fission yeast. Mol Cell. 2007; 26: 145–155. 17434133
52. Chang H, Lim J, Ha M, Kim VN. TAIL-seq: Genome-wide Determination of Poly(A) Tail Length and 3' End Modifications. Mol Cell. 2014; 53: 1044–1052. doi: 10.1016/j.molcel.2014.02.007 24582499
53. Grigull J, Mnaimneh S, Pootoolal J, Robinson MD, Hughes TR. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Molecular and cellular biology. 2004; 24: 5534–5547. 15169913
54. Suter L, Widmer A. Phenotypic effects of salt and heat stress over three generations in Arabidopsis thaliana. PLoS One. 2013; 8: e80819. doi: 10.1371/journal.pone.0080819 24244719
55. Sarkar D. Package ‘lattice’. 2014.
56. Schmieder R, Lim YW, Edwards R. Identification and removal of ribosomal RNA sequences from metatranscriptomes. Bioinformatics. 2012; 28: 433–435. doi: 10.1093/bioinformatics/btr669 22155869
57. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14: R36. doi: 10.1186/gb-2013-14-4-r36 23618408
58. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25: 2078–2079. doi: 10.1093/bioinformatics/btp352 19505943
59. Anders S, Pyl PT, Huber W. HTSeq–A Python framework to work with high-throughput sequencing data. biorxiv. 2014.
60. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology. 2010; 28: 511–U174. doi: 10.1038/nbt.1621 20436464
61. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004; 5: R80. 15461798
62. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010; 26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308
63. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological). 1995; 57: 289–300.
64. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010; 11: R25. doi: 10.1186/gb-2010-11-3-r25 20196867
65. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, et al. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J. 2004; 37: 914–939. 14996223
66. Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, et al. NCBI GEO: archive for functional genomics data sets—update. Nucleic Acids Res. 2013; 41: D991–995. doi: 10.1093/nar/gks1193 23193258
67. Rustici G, Kolesnikov N, Brandizi M, Burdett T, Dylag M, Emam I, et al. ArrayExpress update—trends in database growth and links to data analysis tools. Nucleic Acids Res. 2013; 41: D987–990. doi: 10.1093/nar/gks1174 23193272
68. Craigon DJ, James N, Okyere J, Higgins J, Jotham J, May S. NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res. 2004; 32: D575–577. 14681484
69. Gautier L, Cope L, Bolstad BM, Irizarry RA. affy—analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004; 20: 307–315. 14960456
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 8
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Exon 7 Contributes to the Stable Localization of Xist RNA on the Inactive X-Chromosome
- YAP1 Exerts Its Transcriptional Control via TEAD-Mediated Activation of Enhancers
- SmD1 Modulates the miRNA Pathway Independently of Its Pre-mRNA Splicing Function
- Molecular Basis of Gene-Gene Interaction: Cyclic Cross-Regulation of Gene Expression and Post-GWAS Gene-Gene Interaction Involved in Atrial Fibrillation