Context-Dependent Dual Role of SKI8 Homologs in mRNA Synthesis and Turnover
Eukaryotic mRNA transcription and turnover is controlled by an enzymatic machinery that includes RNA polymerase II and the 3′ to 5′ exosome. The activity of these protein complexes is modulated by additional factors, such as the nuclear RNA polymerase II-associated factor 1 (Paf1c) and the cytoplasmic Superkiller (SKI) complex, respectively. Their components are conserved across uni- as well as multi-cellular organisms, including yeast, Arabidopsis, and humans. Among them, SKI8 displays multiple facets on top of its cytoplasmic role in the SKI complex. For instance, nuclear yeast ScSKI8 has an additional function in meiotic recombination, whereas nuclear human hSKI8 (unlike ScSKI8) associates with Paf1c. The Arabidopsis SKI8 homolog VERNALIZATION INDEPENDENT 3 (VIP3) has been found in Paf1c as well; however, whether it also has a role in the SKI complex remains obscure so far. We found that transgenic VIP3-GFP, which complements a novel vip3 mutant allele, localizes to both nucleus and cytoplasm. Consistently, biochemical analyses suggest that VIP3–GFP associates with the SKI complex. A role of VIP3 in the turnover of nuclear encoded mRNAs is supported by random-primed RNA sequencing of wild-type and vip3 seedlings, which indicates mRNA stabilization in vip3. Another SKI subunit homolog mutant, ski2, displays a dwarf phenotype similar to vip3. However, unlike vip3, it displays neither early flowering nor flower development phenotypes, suggesting that the latter reflect VIP3's role in Paf1c. Surprisingly then, transgenic ScSKI8 rescued all aspects of the vip3 phenotype, suggesting that the dual role of SKI8 depends on species-specific cellular context.
Vyšlo v časopise:
Context-Dependent Dual Role of SKI8 Homologs in mRNA Synthesis and Turnover. PLoS Genet 8(4): e32767. doi:10.1371/journal.pgen.1002652
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002652
Souhrn
Eukaryotic mRNA transcription and turnover is controlled by an enzymatic machinery that includes RNA polymerase II and the 3′ to 5′ exosome. The activity of these protein complexes is modulated by additional factors, such as the nuclear RNA polymerase II-associated factor 1 (Paf1c) and the cytoplasmic Superkiller (SKI) complex, respectively. Their components are conserved across uni- as well as multi-cellular organisms, including yeast, Arabidopsis, and humans. Among them, SKI8 displays multiple facets on top of its cytoplasmic role in the SKI complex. For instance, nuclear yeast ScSKI8 has an additional function in meiotic recombination, whereas nuclear human hSKI8 (unlike ScSKI8) associates with Paf1c. The Arabidopsis SKI8 homolog VERNALIZATION INDEPENDENT 3 (VIP3) has been found in Paf1c as well; however, whether it also has a role in the SKI complex remains obscure so far. We found that transgenic VIP3-GFP, which complements a novel vip3 mutant allele, localizes to both nucleus and cytoplasm. Consistently, biochemical analyses suggest that VIP3–GFP associates with the SKI complex. A role of VIP3 in the turnover of nuclear encoded mRNAs is supported by random-primed RNA sequencing of wild-type and vip3 seedlings, which indicates mRNA stabilization in vip3. Another SKI subunit homolog mutant, ski2, displays a dwarf phenotype similar to vip3. However, unlike vip3, it displays neither early flowering nor flower development phenotypes, suggesting that the latter reflect VIP3's role in Paf1c. Surprisingly then, transgenic ScSKI8 rescued all aspects of the vip3 phenotype, suggesting that the dual role of SKI8 depends on species-specific cellular context.
Zdroje
1. SchaefferDClarkAKlauerAATsanovaBvan HoofA 2011 Functions of the cytoplasmic exosome. Adv Exp Med Biol 702 79 90
2. SelthLASigurdssonSSvejstrupJQ 2010 Transcript Elongation by RNA Polymerase II. Annu Rev Biochem 79 271 293
3. GoodrichJATjianR 2010 Unexpected roles for core promoter recognition factors in cell-type-specific transcription and gene regulation. Nat Rev Genet 11 549 558
4. KimYJBjorklundSLiYSayreMHKornbergRD 1994 A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell 77 599 608
5. SoutourinaJWydauSAmbroiseYBoschieroCWernerM 2011 Direct interaction of RNA polymerase II and mediator required for transcription in vivo. Science 331 1451 1454
6. AnsariSAHeQMorseRH 2009 Mediator complex association with constitutively transcribed genes in yeast. Proc Natl Acad Sci U S A 106 16734 16739
7. BackstromSElfvingNNilssonRWingsleGBjorklundS 2007 Purification of a plant mediator from Arabidopsis thaliana identifies PFT1 as the Med25 subunit. Mol Cell 26 717 729
8. GillmorCSParkMYSmithMRPepitoneRKerstetterRA 2010 The MED12-MED13 module of Mediator regulates the timing of embryo patterning in Arabidopsis. Development 137 113 122
9. AutranDJonakCBelcramKBeemsterGTKronenbergerJ 2002 Cell numbers and leaf development in Arabidopsis: a functional analysis of the STRUWWELPETER gene. EMBO J 21 6036 6049
10. HeYDoyleMRAmasinoRM 2004 PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev 18 2774 2784
11. OhSZhangHLudwigPvan NockerS 2004 A mechanism related to the yeast transcriptional regulator Paf1c is required for expression of the Arabidopsis FLC/MAF MADS box gene family. Plant Cell 16 2940 2953
12. ZhangHRansomCLudwigPvan NockerS 2003 Genetic analysis of early flowering mutants in Arabidopsis defines a class of pleiotropic developmental regulator required for expression of the flowering-time switch flowering locus C. Genetics 164 347 358
13. JaehningJA 2010 The Paf1 complex: platform or player in RNA polymerase II transcription? Biochim Biophys Acta 1799 379 388
14. OhSParkSvan NockerS 2008 Genic and global functions for Paf1C in chromatin modification and gene expression in Arabidopsis. PLoS Genet 4 e1000077 doi:10.1371/journal.pgen.1000077
15. ParkSOhSEk-RamosJvan NockerS 2010 PLANT HOMOLOGOUS TO PARAFIBROMIN is a component of the PAF1 complex and assists in regulating expression of genes within H3K27ME3-enriched chromatin. Plant Physiol 153 821 831
16. ZhangHvan NockerS 2002 The VERNALIZATION INDEPENDENCE 4 gene encodes a novel regulator of FLOWERING LOCUS C. Plant J 31 663 673
17. GoodrichJPuangsomleePMartinMLongDMeyerowitzEM 1997 A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386 44 51
18. HouseleyJLaCavaJTollerveyD 2006 RNA-quality control by the exosome. Nat Rev Mol Cell Biol 7 529 539
19. OrbanTIIzaurraldeE 2005 Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 11 459 469
20. WangLLewisMSJohnsonAW 2005 Domain interactions within the Ski2/3/8 complex and between the Ski complex and Ski7p. RNA 11 1291 1302
21. ZhuBMandalSSPhamADZhengYErdjument-BromageH 2005 The human PAF complex coordinates transcription with events downstream of RNA synthesis. Genes Dev 19 1668 1673
22. BrownJTBaiXJohnsonAW 2000 The yeast antiviral proteins Ski2p, Ski3p, and Ski8p exist as a complex in vivo. RNA 6 449 457
23. AroraCKeeKMalekiSKeeneyS 2004 Antiviral protein Ski8 is a direct partner of Spo11 in meiotic DNA break formation, independent of its cytoplasmic role in RNA metabolism. Mol Cell 13 549 559
24. JolivetSVezonDFrogerNMercierR 2006 Non conservation of the meiotic function of the Ski8/Rec103 homolog in Arabidopsis. Genes Cells 11 615 622
25. BordonneRBanroquesJAbelsonJGuthrieC 1990 Domains of yeast U4 spliceosomal RNA required for PRP4 protein binding, snRNP-snRNP interactions, and pre-mRNA splicing in vivo. Genes Dev 4 1185 1196
26. SmithRLJohnsonAD 2000 Turning genes off by Ssn6-Tup1: a conserved system of transcriptional repression in eukaryotes. Trends Biochem Sci 25 325 330
27. AllemeerschJDurinckSVanderhaeghenRAlardPMaesR 2005 Benchmarking the CATMA microarray. A novel tool for Arabidopsis transcriptome analysis. Plant Physiol 137 588 601
28. SantuariLPradervandSAmiguet-VercherAMThomasJDorceyE 2010 Substantial deletion overlap among divergent Arabidopsis genomes revealed by intersection of short reads and tiling arrays. Genome Biol 11 R4
29. AlonsoJMStepanovaANLeisseTJKimCJChenH 2003 Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301 653 657
30. LevinJZYassourMAdiconisXNusbaumCThompsonDA 2010 Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 7 709 715
31. ChekanovaJAGregoryBDReverdattoSVChenHKumarR 2007 Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131 1340 1353
32. XuRRQiSDLuLTChenCTWuCAZhengCC 2011 A DExD/H box RNA helicase is important for K+ deprivation responses and tolerance in Arabidopsis thaliana. FEBS J 278 2296 2306
33. MouchelCFBriggsGCHardtkeCS 2004 Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 18 700 714
34. OssowskiSSchneebergerKLucas-LledoJIWarthmannNClarkRM 2010 The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327 92 94
35. AndersonJSParkerRP 1998 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. EMBO J 17 1497 1506
36. SiboutRPlantegenetSHardtkeCS 2008 Flowering as a condition for xylem expansion in Arabidopsis hypocotyl and root. Curr Biol 18 458 463
37. ScacchiEOsmontKSBeuchatJSalinasPNavarrete-GomezM 2009 Dynamic, auxin-responsive plasma membrane-to-nucleus movement of Arabidopsis BRX. Development 136 2059 2067
38. CurtisMDGrossniklausU 2003 A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133 462 469
39. LiHDurbinR 2009 Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 1754 1760
40. HardtkeCSGohdaKOsterlundMTOyamaTOkadaK 2000 HY5 stability and activity in arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J 19 4997 5006
41. ShevchenkoAWilmMVormOMannM 1996 Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68 850 858
42. WilmMShevchenkoAHouthaeveTBreitSSchweigererL 1996 Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379 466 469
43. KellerANesvizhskiiAIKolkerEAebersoldR 2002 Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74 5383 5392
44. NesvizhskiiAIKellerAKolkerEAebersoldR 2003 A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75 4646 4658
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 4
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