#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Misregulation of Underlies the Developmental Abnormalities Caused by Three Distinct Viral Silencing Suppressors in Arabidopsis


In Arabidopsis, micro (mi)RNAs and trans-acting (ta-si)RNAs synthesized directly or indirectly through the DICER-LIKE-1 (DCL1) ribonuclease have roles in patterning and hormonal responses, while DCL2,3,4-dependent small-interfering (si)RNAs are mainly involved in silencing of transposable elements and antiviral defense. Viral suppressors of RNA silencing (VSRs) produced by phytoviruses to counter plant defense may perturb plant developmental programs because of the collision of their inhibitory effects with the regulatory action of endogenous miRNAs and ta-siRNAs. This could explain the similar developmental aberrations displayed by Arabidopsis miRNA/ta-siRNA pathway mutants, including dcl1, and by some VSR-expressing plants. Nonetheless, the molecular bases for these morphological aberrations have remained mysterious, and their contribution to viral disease symptoms/virulence unexplored. The extent of VSR inhibitory actions to other types of endogenous small RNAs remains also unclear. Here, we present an in-depth analysis of transgenic Arabidopsis expressing constitutively HcPro, P19 and P15, three unrelated VSRs. We show that VSR expression has comparable, yet modest effects on known miRNA and ta-siRNA target RNA levels, similar to those observed using an hypomorphic dcl1 mutation. However, by combining results of transcriptome studies with deep-sequencing data from immuno-precipitated small RNAs, additional, novel endogenous targets of miRNA and ta-siRNA were identified, unraveling an unsuspected complexity in the origin and scope-of-action of these molecules. Other stringent analyses pinpointed misregulation of the miR167 target AUXIN RESPONSE FACTOR 8 (ARF8) as a major cause for the developmental aberrations exhibited by VSR transgenic plants, but also for the phenotypes induced during normal viral infection caused by the HcPro-encoding Turnip mosaic virus (TuMV). Neither RNA silencing, its suppression by VSRs, nor the virulence/accumulation of TuMV was altered by mutations in ARF8. These findings have important implications for our understanding of viral disease symptoms and small RNA-directed regulation of plant growth/development.


Vyšlo v časopise: Misregulation of Underlies the Developmental Abnormalities Caused by Three Distinct Viral Silencing Suppressors in Arabidopsis. PLoS Pathog 7(5): e32767. doi:10.1371/journal.ppat.1002035
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002035

Souhrn

In Arabidopsis, micro (mi)RNAs and trans-acting (ta-si)RNAs synthesized directly or indirectly through the DICER-LIKE-1 (DCL1) ribonuclease have roles in patterning and hormonal responses, while DCL2,3,4-dependent small-interfering (si)RNAs are mainly involved in silencing of transposable elements and antiviral defense. Viral suppressors of RNA silencing (VSRs) produced by phytoviruses to counter plant defense may perturb plant developmental programs because of the collision of their inhibitory effects with the regulatory action of endogenous miRNAs and ta-siRNAs. This could explain the similar developmental aberrations displayed by Arabidopsis miRNA/ta-siRNA pathway mutants, including dcl1, and by some VSR-expressing plants. Nonetheless, the molecular bases for these morphological aberrations have remained mysterious, and their contribution to viral disease symptoms/virulence unexplored. The extent of VSR inhibitory actions to other types of endogenous small RNAs remains also unclear. Here, we present an in-depth analysis of transgenic Arabidopsis expressing constitutively HcPro, P19 and P15, three unrelated VSRs. We show that VSR expression has comparable, yet modest effects on known miRNA and ta-siRNA target RNA levels, similar to those observed using an hypomorphic dcl1 mutation. However, by combining results of transcriptome studies with deep-sequencing data from immuno-precipitated small RNAs, additional, novel endogenous targets of miRNA and ta-siRNA were identified, unraveling an unsuspected complexity in the origin and scope-of-action of these molecules. Other stringent analyses pinpointed misregulation of the miR167 target AUXIN RESPONSE FACTOR 8 (ARF8) as a major cause for the developmental aberrations exhibited by VSR transgenic plants, but also for the phenotypes induced during normal viral infection caused by the HcPro-encoding Turnip mosaic virus (TuMV). Neither RNA silencing, its suppression by VSRs, nor the virulence/accumulation of TuMV was altered by mutations in ARF8. These findings have important implications for our understanding of viral disease symptoms and small RNA-directed regulation of plant growth/development.


Zdroje

1. ChapmanEJCarringtonJC 2007 Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8 884 896

2. ParkMYWuGGonzalez-SulserAVaucheretHPoethigRS 2005 Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci U S A 102 3691 3696

3. YuBYangZLiJMinakhinaSYangM 2005 Methylation as a crucial step in plant microRNA biogenesis. Science 307 932 935

4. VoinnetO 2009 Origin, biogenesis, and activity of plant microRNAs. Cell 136 669 687

5. MalloryACBartelDPBartelB 2005 MicroRNA-Directed Regulation of Arabidopsis AUXIN RESPONSE FACTOR17 Is Essential for Proper Development and Modulates Expression of Early Auxin Response Genes. Plant Cell 17 1360 1375

6. MatzkeMABirchlerJA 2005 RNAi-mediated pathways in the nucleus. Nat Rev Genet 6 24 35

7. VaucheretH 2005 MicroRNA-dependent trans-acting siRNA production. Sci STKE pe43

8. AllenEXieZGustafsonAMCarringtonJC 2005 microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121 207 221

9. AdenotXElmayanTLauresserguesDBoutetSBoucheN 2006 DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16 927 932

10. GarciaDCollierSAByrneMEMartienssenRA 2006 Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16 933 938

11. DunoyerPBrosnanCASchottGWangYJayF 2010 An endogenous, systemic RNAi pathway in plants. Embo J 29 1699 1712

12. DingSWVoinnetO 2007 Antiviral immunity directed by small RNAs. Cell 130 413 426

13. MorelJ-BGordonCMourrainPBeclinCBoutetS 2002 Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14 629 639

14. QuFYeXMorrisJT 2008 Arabidopsis DRB4, AGO1, AGO7, and RDR6 participate in a DCL4-initiated antiviral RNA silencing pathway negatively regulated by DCL1. Proc Natl Acad Sci U S A 105 14732 14737

15. WuQWangXDingSW 2010 Viral suppressors of RNA-based viral immunity: host targets. Cell Host Microbe 8 12 5

16. VargasonJMSzittyaGBurgyanJTanaka HallTM 2003 Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115 799 811

17. MalloryACReinhartBJBartelDVanceVBBowmanLH 2002 A viral suppressor of RNA silencing differentially regulates the accumulation of short interfering RNAs and micro-RNAs in tobacco. Proc Natl Acad Sci U S A 99 15228 15233

18. DunoyerPLecellierCHParizottoEAHimberCVoinnetO 2004 Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell 16 1235 1250

19. ChapmanEJProkhnevskyAIGopinathKDoljaVVCarringtonJC 2004 Viral RNA silencing suppressors inhibit the microRNA pathway at an intermediate step. Genes Dev 18 1179 1186

20. Ruiz-FerrerVVoinnetO 2009 Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60 485 510

21. HaasGAzevedoJMoissiardGGeldreichAHimberC 2008 Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. Embo J 27 2102 2112

22. VoinnetO 2005 Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6 206 220

23. KimWBenhamedMServetCLatrasseDZhangW 2009 Histone acetyltransferase GCN5 interferes with the miRNA pathway in Arabidopsis. Cell Res 19 899 909

24. VoinnetO 2001 RNA silencing as a plant immune system against viruses. Trends Genet 17 449 459

25. TurckFRoudierFFarronaSMartin-MagnietteMLGuillaumeE 2007 Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3 e86

26. GustafsonAMAllenEGivanSSmithDCarringtonJC 2005 ASRP: the Arabidopsis Small RNA Project Database. Nucleic Acids Res 33 D637 640

27. XieZAllenEWilkenACarringtonJC 2005 DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci U S A 102 12984 12989

28. TodescoMRubio-SomozaIPaz-AresJWeigelD 2010 A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet 6 e1001031

29. Katiyar-AgarwalSGaoSVivian-SmithAJinH 2007 A novel class of bacteria-induced small RNAs in Arabidopsis. Genes Dev 21 3123 3134

30. MiSCaiTHuYChenYHodgesE 2008 Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133 116 127

31. LindowMJacobsenANygaardSMangYKroghA 2007 Intragenomic matching reveals a huge potential for miRNA-mediated regulation in plants. PLoS Comput Biol 3 e238

32. LiljegrenSJDittaGSEshedYSavidgeBBowmanJL 2000 SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404 766 770

33. Moreno-RisuenoMAVan NormanJMMorenoAZhangJAhnertSE 2010 Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329 1306 1311

34. LuCJeongDHKulkarniKPillayMNobutaK 2008 Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci U S A 105 4951 4956

35. WuMFTianQReedJW 2006 Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133 4211 4218

36. ZhaoY 2010 Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61 49 64

37. GoetzMVivian-SmithAJohnsonSDKoltunowAM 2006 AUXIN RESPONSE FACTOR8 is a negative regulator of fruit initiation in Arabidopsis. Plant Cell 18 1873 1886

38. ParizottoEADunoyerPRahmNHimberCVoinnetO 2004 In vivo investigation of the transcription, processing, endonucleolytic activity, and functional relevance of the spatial distribution of a plant miRNA. Genes Dev 18 2237 2242

39. ValocziAVarallyayEKauppinenSBurgyanJHaveldaZ 2006 Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J 47 140 151

40. BrodersenPSakvarelidze-AchardLBruun-RasmussenMDunoyerPYamamotoYY 2008 Widespread translational inhibition by plant miRNAs and siRNAs. Science 320 1185 1190

41. LanetEDelannoyESormaniRFlorisMBrodersenP 2009 Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21 1762 1768

42. EulalioAHuntzingerEIzaurraldeE 2008 Getting to the root of miRNA-mediated gene silencing. Cell 132 9 14

43. FabianMRSonenbergNFilipowiczW 2010 Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79 351 379

44. FabianMRMathonnetGSundermeierTMathysHZipprichJT 2009 Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol Cell 35 868 880

45. LlaveCXieZKasschauKDCarringtonJC 2002 Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297 2053 2056

46. MontgomeryTAHowellMDCuperusJTLiDHansenJE 2008 Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133 128 141

47. TakedaAIwasakiSWatanabeTUtsumiMWatanabeY 2008 The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 49 493 500

48. OkamuraKLiuNLaiEC 2009 Distinct mechanisms for microRNA strand selection by Drosophila Argonautes. Mol Cell 36 431 444

49. GhildiyalMXuJSeitzHWengZZamorePD 2010 Sorting of Drosophila small silencing RNAs partitions microRNA* strands into the RNA interference pathway. Rna 16 43 56

50. VaucheretH 2008 Plant ARGONAUTES. Trends Plant Sci 13 350 358

51. WuMFTianQReedJW 2006 Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133 4211 4218

52. EndresMWGregoryBDGaoZForemanAWMlotshwaS 2010 Two plant viral suppressors of silencing require the ethylene-inducible host transcription factor RAV2 to block RNA silencing. PLoS Pathog 6 e1000729

53. GriggSPCanalesCHayATsiantisM 2005 SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437 1022 1026

54. SeitzH 2009 Redefining microRNA targets. Curr Biol 19 870 873

55. Ambros V MicroRNAs: genetically sensitized worms reveal new secrets. Curr Biol 20 598 600

56. NavarroLDunoyerPJayFArnoldBDharmasiriN 2006 A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312 436 439

57. PadmanabhanMSShiferawHCulverJN 2006 The Tobacco mosaic virus replicase protein disrupts the localization and function of interacting Aux/IAA proteins. Mol Plant Microbe Interact 19 864 873

58. SiddiquiSASarmientoCTruveELehtoHLehtoK 2008 Phenotypes and functional effects caused by various viral RNA silencing suppressors in transgenic Nicotiana benthamiana and N. tabacum. Mol Plant Microbe Interact 21 178 187

59. DunoyerPHimberCRuiz-FerrerVAliouaAVoinnetO 2007 Intra- and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat Genet 39 848 856

60. KuriharaYTakashiYWatanabeY 2006 The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. Rna 12 206 212

61. HurkmanWJTanakaCK 1986 Solubilization of Plant Membrane Proteins for Analysis by Two-Dimensional Gel Electrophoresis. Plant Physiol 81 802 806

62. AzevedoJGarciaDPontierDOhnesorgeSYuA 2010 Argonaute quenching and global changes in Dicer homeostasis caused by a pathogen-encoded GW repeat protein. Genes Dev 24 904 915

63. CroweMLSerizetCThareauVAubourgSRouzeP 2003 CATMA: a complete Arabidopsis GST database. Nucleic Acids Res 31 156 158

64. HilsonPSmallIKuiperMT 2003 European consortia building integrated resources for Arabidopsis functional genomics. Curr Opin Plant Biol 6 426 429

65. LurinCAndresCAubourgSBellaouiMBittonF 2004 Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16 2089 2103

66. GagnotSTambyJPMartin-MagnietteMLBittonFTaconnatL 2008 CATdb: a public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucleic Acids Res 36 D986 990

67. GeYDudoitSSpeedTP 2003 Resampling-based multiple testing for microarray data analysis. Test 12 1 77

68. GendrelAVLippmanZMartienssenRColotV 2005 Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2 213 218

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 5
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#