Transcription Termination and Chimeric RNA Formation Controlled by Arabidopsis thaliana FPA

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Duc, Céline ^a   Sherstnev, Alexander ^a   Cole, Christian ^a   Barton, Geoffrey J ^a   Simpson, Gordon G ^a,b  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; ARABIDOPSIS PROTEIN FPA; ARGONAUTE PROTEIN; RNA; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DCL1 PROTEIN, ARABIDOPSIS; FPA PROTEIN, ARABIDOPSIS; HETEROCHROMATIN; HISTONE DEMETHYLASE; IBM1 PROTEIN, ARABIDOPSIS; MESSENGER RNA; RIBONUCLEASE III; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; ARABIDOPSIS THALIANA; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE LOCUS; GENE MAPPING; GENE SILENCING; GENETIC TRANSCRIPTION; HETEROCHROMATIN; INTRON; NONHUMAN; OPEN READING FRAME; POINT MUTATION; POLYADENYLATION; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN FUNCTION; RNA SPLICING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION TERMINATION; UPREGULATION; ALTERNATIVE RNA SPLICING; ARABIDOPSIS; BIOSYNTHESIS; EXON; GENETICS; METABOLISM; MUTATION;

ALTERNATIVE SPLICING; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL CYCLE PROTEINS; DNA METHYLATION; EXONS; GENE SILENCING; HETEROCHROMATIN; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MUTATION; RIBONUCLEASE III; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSCRIPTION TERMINATION, GENETIC;

EID: 84887292738     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003867     Document Type: Article

References (58)

1. Di Giammartino DC, Nishida K, Manley JL, (2011) Mechanisms and consequences of alternative polyadenylation. Mol Cell 43: 853-866 doi:10.1016/j.molce1.2011.08.017.
2. Proudfoot NJ, (2011) Ending the message: poly(A) signals then and now. Genes Dev 25: 1770-1782 doi:10.1101/gad.17268411.
3. Kuehner JN, Pearson EL, Moore C, (2011) Unravelling the means to an end: RNA polymerase II transcription termination. Nat Rev Mol Cell Biol 12: 283-294 doi:10.1038/nrm3098.
4. Nojima T, Dienstbier M, Murphy S, Proudfoot NJ, Dye MJ, (2013) Definition of RNA Polymerase II CoTC Terminator Elements in the Human Genome. Cell Rep 3: 1080-1092 doi:10.1016/j.celrep.2013.03.012.
5. West S, Proudfoot NJ, (2009) Transcriptional termination enhances protein expression in human cells. Mol Cell 33: 354-364 doi:10.1016/j.molce1.2009.01.008.
6. Mapendano CK, Lykke-Andersen S, Kjems J, Bertrand E, Jensen TH, (2010) Crosstalk between mRNA 3′ end processing and transcription initiation. Mol Cell 40: 410-422 doi:10.1016/j.molce1.2010.10.012.
7. Padmanabhan K, Robles MS, Westerling T, Weitz CJ, (2012) Feedback regulation of transcriptional termination by the mammalian circadian clock PERIOD complex. Science 337: 599-602 doi:10.1126/science.1221592.
8. Akiva P, Toporik A, Edelheit S, Peretz Y, Diber A, et al. (2006) Transcription-mediated gene fusion in the human genome. Genome Res 16: 30-36 doi:10.1101/gr.4137606.
9. Parra G, Reymond A, Dabbouseh N, Dermitzakis ET, Castelo R, et al. (2006) Tandem chimerism as a means to increase protein complexity in the human genome. Genome Res 16: 37-44 doi:10.1101/gr.4145906.
10. Prakash T, Sharma VK, Adati N, Ozawa R, Kumar N, et al. (2010) Expression of conjoined genes: another mechanism for gene regulation in eukaryotes. PLoS One 5: e13284 doi:10.1371/journal.pone.0013284.t002.
11. Dalziel M, Kolesnichenko M, Neves das RP, Iborra F, Goding C, et al. (2011) Alpha-MSH regulates intergenic splicing of MC1R and TUBB3 in human melanocytes. Nucleic Acids Res 39: 2378-2392 doi:10.1093/nar/gkq1125.
12. Maher CA, Kumar-Sinha C, Cao X, Kalyana-Sundaram S, Han B, et al. (2009) Transcriptome sequencing to detect gene fusions in cancer. Nature 458: 97-101 doi:10.1038/nature07638.
13. Kannan K, Wang L, Wang J, Ittmann MM, Li W, et al. (2011) Recurrent chimeric RNAs enriched in human prostate cancer identified by deep sequencing. Proc Natl Acad Sci USA 108: 9172-9177 doi:10.1073/pnas.1100489108.
14. Hornyik C, Terzi LC, Simpson GG, (2010) The spen family protein FPA controls alternative cleavage and polyadenylation of RNA. Dev Cell 18: 203-213 doi:10.1016/j.devce1.2009.12.009.
15. Michaels SD, Amasino RM, (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13: 935-941.
16. Simpson GG, Dijkwel PP, Quesada V, Henderson I, Dean C, (2003) FY is an RNA 3′ end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113: 777-787.
17. Xing D, Zhao H, Xu R, Li QQ, (2008) Arabidopsis PCFS4, a homologue of yeast polyadenylation factor Pcf11p, regulates FCA alternative processing and promotes flowering time. Plant J 54: 899-910 doi:-10.1111/j.1365-313X.2008.03455.x.
18. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C, (2010) Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327: 94-97 doi:10.1126/science.1180278.
19. Veley KM, Michaels SD, (2008) Functional redundancy and new roles for genes of the autonomous floral-promotion pathway. Plant Physiol 147: 682-695 doi:10.1104/pp.108.118927.
20. Bäurle I, Dean C, (2008) Differential interactions of the autonomous pathway RRM proteins and chromatin regulators in the silencing of Arabidopsis targets. PLoS One 3: e2733 doi:10.1371/journal.pone.0002733.
21. Bäurle I, Smith L, Baulcombe DC, Dean C, (2007) Widespread role for the flowering-time regulators FCA and FPA in RNA-mediated chromatin silencing. Science 318: 109-112 doi:10.1126/science.1146565.
22. Sherstnev A, Duc C, Cole C, Zacharaki V, Hornyik C, et al. (2012) Direct sequencing of Arabidopsis thaliana RNA reveals patterns of cleavage and polyadenylation. Nat Struct Mol Biol 19: 845-852 doi:10.1038/nsmb.2345.
23. Ozsolak F, Kapranov P, Foissac S, Kim SW, Fishilevich E, et al. (2010) Comprehensive polyadenylation site maps in yeast and human reveal pervasive alternative polyadenylation. Cell 143: 1018-1029 doi:10.1016/j.ce11.2010.11.020.
24. Zhang X, Xia J, Lii Y, Barrera-Figueroa B, Zhou X, et al. (2012) Genome-wide analysis of plant nat-siRNAs reveals insights into their distribution, biogenesis and function. Genome Biol 13: R20 doi:--10.1186/gb-2012-13-3-r20.
25. Anders S, Huber W, (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106 doi:10.1186/gb-2010-11-10-r106.
26. Coustham V, Li P, Strange A, Lister C, Song J, et al. (2012) Quantitative modulation of polycomb silencing underlies natural variation in vernalization. Science 337: 584-587 doi:10.1126/science.1221881.
27. Stroud H, Greenberg MVC, Feng S, Bernatavichute YV, Jacobsen SE, (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152: 352-364 doi:10.1016/j.ce11.2012.10.054.
28. Garcia D, Garcia S, Pontier D, Marchais A, Renou J-P, et al. (2012) Ago hook and RNA helicase motifs underpin dual roles for SDE3 in antiviral defense and silencing of nonconserved intergenic regions. Mol Cell 48: 109-120 doi:10.1016/j.molce1.2012.07.028.
29. Pontier D, Picart C, Roudier F, Garcia D, Lahmy S, et al. (2012) NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol Cell 48: 121-132 doi:10.1016/j.molce1.2012.07.027.
30. Silveira AB, Trontin C, Cortijo S, Barau J, Del Bem LEV, et al. (2013) Extensive natural epigenetic variation at a de novo originated gene. PLoS Genet 9: e1003437 doi:10.1371/journal.pgen.1003437.s005.
31. Sonmez C, Bäurle I, Magusin A, Dreos R, Laubinger S, et al. (2011) RNA 3′ processing functions of Arabidopsis FCA and FPA limit intergenic transcription. Proc Natl Acad Sci U S A 108: 8508-8513 doi:10.1073/pnas.1105334108.
32. Saze H, Shiraishi A, Miura A, Kakutani T, (2008) Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319: 462-465 doi:10.1126/science.1150987.
33. Rigal M, Kevei Z, Pélissier T, Mathieu O, (2012) DNA methylation in an intron of the IBM1 histone demethylase gene stabilizes chromatin modification patterns. EMBO J 31: 2981-2993 doi:10.1038/emboj.2012.141.
34. Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE, (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10: R62 doi:--10.1186/gb-2009-10-6-r62.
35. Mühlemann O, Eberle AB, Stalder L, Zamudio Orozco R, (2008) Recognition and elimination of nonsense mRNA. Biochim Biophys Acta 1779: 538-549 doi:10.1016/j.bbagrm.2008.06.012.
36. Arciga-Reyes L, Wootton L, Kieffer M, Davies B, (2006) UPF1 is required for nonsense-mediated mRNA decay (NMD) and RNAi in Arabidopsis. Plant J 47: 480-489 doi:-10.1111/j.1365-313X.2006.02802.x.
37. Leivar P, Quail PH, (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16: 19-28 doi:10.1016/j.tplants.2010.08.003.
38. Liu F, Bakht S, Dean C, (2012) Cotranscriptional role for Arabidopsis DICER-LIKE 4 in transcription termination. Science 335: 1621-1623 doi:10.1126/science.1214402.
39. Liu F, Quesada V, Crevillén P, Bäurle I, Swiezewski S, et al. (2007) The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC. Mol Cell 28: 398-407 doi:10.1016/j.molce1.2007.10.018.
40. Jacquier A, (2009) The complex eukaryotic transcriptome: unexpected pervasive transcription and novel small RNAs. Nat Rev Genet 10: 833-844 doi:10.1038/nrg2683.
41. Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C, (2013) R-Loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340: 619-621 doi:10.1126/science.1234848.
42. Tautz D, Domazet-Lošo T, (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12: 692-702 doi:10.1038/nrg3053.
43. Shukla S, Kavak E, Gregory M, Imashimizu M, Shutinoski B, et al. (2011) CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479: 74-79 doi:10.1038/nature10442.
44. Wood AJ, Schulz R, Woodfine K, Koltowska K, Beechey CV, et al. (2008) Regulation of alternative polyadenylation by genomic imprinting. Genes Dev 22: 1141-1146 doi:10.1101/gad.473408.
45. Yaish MWF, Peng M, Rothstein SJ, (2009) AtMBD9 modulates Arabidopsis development through the dual epigenetic pathways of DNA methylation and histone acetylation. Plant J 59: 123-135 doi:10.1111/j.1365 313X.2009.03860.x.
46. Jenal M, Elkon R, Loayza-Puch F, van Haaften G, Kühn U, et al. (2012) The poly(A)-binding protein nuclear 1 suppresses alternative cleavage and polyadenylation sites. Cell 149: 538-553 doi:10.1016/j.ce11.2012.03.022.
47. Martin G, Gruber AR, Keller W, Zavolan M, (2012) Genome-wide analysis of pre-mRNA 3′ end processing reveals a decisive role of human cleavage factor I in the regulation of 3′ UTR length. Cell Rep 1: 753-763 doi:10.1016/j.celrep.2012.05.003.
48. Johnson SA, Kim H, Erickson B, Bentley DL, (2011) The export factor Yra1 modulates mRNA 3′ end processing. Nat Struct Mol Biol 18: 1164-1171 doi:10.1038/nsmb.2126.
49. Sandberg R, Neilson JR, Sarma A, Sharp PA, Burge CB, (2008) Proliferating cells express mRNAs with shortened 3′ untranslated regions and fewer microRNA target sites. Science 320: 1643-1647 doi:10.1126/science.1155390.
50. Mayr C, Bartel DP, (2009) Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138: 673-684 doi:10.1016/j.ce11.2009.06.016.
51. Magrangeas F, Pitiot G, Dubois S, Bragado-Nilsson E, Chérel M, et al. (1998) Cotranscription and intergenic splicing of human galactose-1-phosphate uridylyltransferase and interleukin-11 receptor alpha-chain genes generate a fusion mRNA in normal cells. Implication for the production of multidomain proteins during evolution. J Biol Chem 273: 16005-16010.
52. Cui M, Allen MA, Larsen A, Macmorris M, Han M, et al. (2008) Genes involved in pre-mRNA 3′-end formation and transcription termination revealed by a lin-15 operon Muv suppressor screen. Proc Natl Acad Sci USA 105: 16665-16670 doi:10.1073/pnas.0807104105.
53. Alén C, Kent NA, Jones HS, O'Sullivan J, Aranda A, et al. (2002) A role for chromatin remodeling in transcriptional termination by RNA polymerase II. Mol Cell 10: 1441-1452.
54. Zhang X, Lii Y, Wu Z, Polishko A, Zhang H, et al. (2013) Mechanisms of small RNA generation from cis-NATs in response to environmental and developmental cues. Mol Plant 6: 704-715 doi:10.1093/mp/sst051.
55. Nicol JW, Helt GA, Blanchard SG, Raja A, Loraine AE, (2009) The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25: 2730-2731 doi:10.1093/bioinformatics/btp472.
56. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57: 289-300.
57. Wierzbicki AT, Haag JR, Pikaard CS, (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135: 635-648 doi:10.1016/j.ce11.2008.09.035.
58. Jan CH, Friedman RC, Ruby JG, Bartel DP, (2011) Formation, regulation and evolution of Caenorhabditis elegans 3′UTRs. Nature 469: 97-101 doi:10.1038/nature09616.