Suppression of Methylation-Mediated Transcriptional Gene Silencing by βC1-SAHH Protein Interaction during Geminivirus-Betasatellite Infection


DNA methylation is a fundamental epigenetic modification that regulates gene expression and represses endogenous transposons and invading DNA viruses. As a counter-defense, the geminiviruses encode proteins that inhibit methylation and transcriptional gene silencing (TGS). Some geminiviruses have acquired a betasatellite called DNA β. This study presents evidence that suppression of methylation-mediated TGS by the sole betasatellite-encoded protein, βC1, is crucial to the association of Tomato yellow leaf curl China virus (TYLCCNV) with its betasatellite (TYLCCNB). We show that TYLCCNB complements Beet curly top virus (BCTV) L2- mutants deficient for methylation inhibition and TGS suppression, and that cytosine methylation levels in BCTV and TYLCCNV genomes, as well as the host genome, are substantially reduced by TYLCCNB or βC1 expression. We also demonstrate that while TYLCCNB or βC1 expression can reverse TGS, TYLCCNV by itself is ineffective. Thus its AC2/AL2 protein, known to have suppression activity in other geminiviruses, is likely a natural mutant in this respect. A yeast two-hybrid screen of candidate proteins, followed by bimolecular fluorescence complementation analysis, revealed that βC1 interacts with S-adenosyl homocysteine hydrolase (SAHH), a methyl cycle enzyme required for TGS. We further demonstrate that βC1 protein inhibits SAHH activity in vitro. That βC1 and other geminivirus proteins target the methyl cycle suggests that limiting its product, S-adenosyl methionine, may be a common viral strategy for methylation interference. We propose that inhibition of methylation and TGS by βC1 stabilizes geminivirus/betasatellite complexes.


Vyšlo v časopise: Suppression of Methylation-Mediated Transcriptional Gene Silencing by βC1-SAHH Protein Interaction during Geminivirus-Betasatellite Infection. PLoS Pathog 7(10): e32767. doi:10.1371/journal.ppat.1002329
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002329

Souhrn

DNA methylation is a fundamental epigenetic modification that regulates gene expression and represses endogenous transposons and invading DNA viruses. As a counter-defense, the geminiviruses encode proteins that inhibit methylation and transcriptional gene silencing (TGS). Some geminiviruses have acquired a betasatellite called DNA β. This study presents evidence that suppression of methylation-mediated TGS by the sole betasatellite-encoded protein, βC1, is crucial to the association of Tomato yellow leaf curl China virus (TYLCCNV) with its betasatellite (TYLCCNB). We show that TYLCCNB complements Beet curly top virus (BCTV) L2- mutants deficient for methylation inhibition and TGS suppression, and that cytosine methylation levels in BCTV and TYLCCNV genomes, as well as the host genome, are substantially reduced by TYLCCNB or βC1 expression. We also demonstrate that while TYLCCNB or βC1 expression can reverse TGS, TYLCCNV by itself is ineffective. Thus its AC2/AL2 protein, known to have suppression activity in other geminiviruses, is likely a natural mutant in this respect. A yeast two-hybrid screen of candidate proteins, followed by bimolecular fluorescence complementation analysis, revealed that βC1 interacts with S-adenosyl homocysteine hydrolase (SAHH), a methyl cycle enzyme required for TGS. We further demonstrate that βC1 protein inhibits SAHH activity in vitro. That βC1 and other geminivirus proteins target the methyl cycle suggests that limiting its product, S-adenosyl methionine, may be a common viral strategy for methylation interference. We propose that inhibition of methylation and TGS by βC1 stabilizes geminivirus/betasatellite complexes.


Zdroje

1. GrewalSISElginSCR 2007 Transcription and RNA interference in the formation of heterochromatin. Nature 447 399 406

2. MatzkeMKannoTDaxingerLHuettelBMatzkeAJM 2009 RNA-mediated chromatin-based silencing in plants. Curr Opinion Cell Biol 21 367 376

3. LawJAJacobsenSE 2010 Establishing, maintaining, and modifying DNA methylation patterns in plants and animals. Nature Rev Genet 11 204 220

4. BisaroDM 2006 Silencing suppression by geminivirus proteins. Virology 344 158 168

5. RajaPWolfJNBisaroDM 2010 RNA silencing directed against geminiviruses: post-transcriptional and epigenetic components. Biochim Biophys Acta 1799 337 351

6. FauquetCMBisaroDMBriddonRWBrownJKHarrisonBD 2003 Revision of taxonomic criteria for species demarcation in the family Geminiviridae, and an updated list of begomovirus species. Arch Virol 148 405 421

7. FauquetCMBriddonRWBrownJKMorionesEStanleyJ 2008 Geminivirus strain demarcation and nomenclature. Arch Virol 153 783 821

8. SaundersKBedfordIDBriddonRWMarkhamPGWongSM 2000 A unique virus complex causes Ageratum yellow vein disease. Proc Natl Acad Sci U S A 97 6890 6895

9. BriddonRWMansoorSBedfordIDPinnerMSSaundersK 2001 Identification of DNA components required for induction of cotton leaf curl disease. Virology 285 234 243

10. CuiXTaoXYieYFauquetCMZhouX 2004 A DNAβ associated with Tomato yellow leaf curl China virus is required for symptom induction. J Virol 78 13966 13974

11. BriddonRWStanleyJ 2006 Subviral agents associated with plant single-stranded DNA viruses. Virology 344 198 210

12. SaundersKNormanAGucciardoSStanleyJ 2004 The DNA β satellite component associated with ageratum yellow vein disease encodes an essential pathogenicity determinant (βC1). Virology 324 37 47

13. SaeedMBehjatniaSAAMansoorSZafarYHasnainS 2005 A single complementary-sense transcript of a geminivirus DNA β satellite is a determinant of pathogenicity. Mol Plant Microbe Interact 18 7 14

14. CuiXLiGWangDHuDZhouX 2005 A begomovirus DNAβ-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 79 10764 10775

15. YangJ-YIwasakiMMachidaCMachidaYZhouX 2008 βC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 22 2564 2577

16. Hanley-BowdoinLSettlageSRobertsonD 2004 Reprogramming plant gene expression: a prerequisite to geminivirus replication. Mol Plant Pathol 5 149 156

17. JeskeH 2009 Geminiviruses. Curr Top Immunol Microbiol 331 185 226

18. PilartzMJeskeH 1992 Abutilon mosaic virus double-stranded DNA is packed into minichromosomes. Virology 189 800 802

19. PilartzMJeskeH 2003 Mapping of Abutilon mosaic geminivirus minichromosomes. J Virol 77 10808 10818

20. RajaPSanvilleBCBuchmannRCBisaroDM 2008 Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 82 8997 9007

21. Rodriguez-NegreteEACarrillo-TripJRivera-BustamanteRF 2009 RNA silencing against geminivirus: Complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J Virol 83 1332 1340

22. BuchmannRCAsadSWolfJNMohannathGBisaroDM 2009 Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J Virol 83 5005 5013

23. ZhangZChenHHuangXXiaRZhaoQ 2011 BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23 273 288

24. BroughCLGardinerWEInamdarNZhangXYEhrlichM 1992 DNA methylation inhibits propagation of tomato golden mosaic virus DNA in transfected protoplasts. Plant Mol Biol 18 703 712

25. WangHHaoLShungC-YSunterGBisaroDM 2003 Adenosine kinase is inactivated by geminivirus AL2 and L2 proteins. Plant Cell 15 3020 3032

26. WangHBuckleyKJYangXBuchmannRCBisaroDM 2005 Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J Virol 79 7410 7418

27. YangXBalijiSBuchmannRCWangHLindboJA 2007 Functional modulation of the geminivirus AL2 transcription factor and silencing suppressor by self-interaction. J Virol 81 11972 11981

28. MoffattBAStevensYYAllenMSSniderJDPerieraLA 2002 Adenosine kinase deficiency is associated with developmental abnormalities and reduced transmethylation. Plant Physiol 128 812 821

29. RochaPSCFSheikhMMelchiorreRFagardMBoutetS 2005 An Arabidopsis HOMOLOGY-DEPENDENT GENE SILENCING1 gene codes for an S-adenosyl-L-homocysteine hydrolase required for DNA methylation-dependent gene silencing. Plant Cell 17 404 417

30. Hanley-BowdoinLElmerJSRogersSG 1988 Transient expression of heterologous RNAs using tomato golden mosaic virus. Nucleic Acids Res 16 10511 10528

31. SunterGBisaroDM 1989 Transcription map of the B genome component of tomato golden mosaic virus and comparison with A component transcripts. Virology 173 647 655

32. SunterGGardinerWEBisaroDM 1989 Identification of tomato golden mosaic virus-specific RNAs in infected plants. Virology 170 243 250

33. ShungC-YSunterJSirasanagandlaSSSunterG 2006 Distinct viral sequence elements are necessary for expression of Tomato golden mosaic virus complementary sense transcripts that direct AL2 and AL3 gene expression. Mol Plant Microbe Interact 19 1394 1405

34. ShungC-YSunterG 2009 Regulation of Tomato golden mosaic virus AL2 and AL3 gene expression by a conserved upstream open reading frame. Virology 383 310 318

35. YangXWangYGuoWXieYXieQ 2011 Characterization of small interfering RNAs derived from the geminivirus/betasatellite complex using deep sequencing. PLoS One 6 e16928

36. HormuzdiSGBisaroDM 1995 Genetic analysis of beet curly top virus: Examination of the roles of L2 and L3 genes in viral pathogenesis. Virology 206 1044 1054

37. BoykoAKathiriaPZempFJYaoYPogribnyI 2007 Transgenerational changes in the genome stability and methylation in pathogen-infected plants (virus-induced plant genome instability). Nucleic Acids Res 35 1714 1725

38. LuRMalcuitIMoffettPRuizMTPeartJ 2003 High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 22 5690 5699

39. TranRKZilbermanDde BustosCDittRFHenikoffJG 2005 Chromatin and siRNA pathways cooperate to maintain DNA methylation of small transposable elements in Arabidopsis. Genome Biol 6 R90.91 R90.11

40. ZhangXYazakiJSundaresanACokusSChanSW-L 2006 Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126 1189 1201

41. NakazawaYHiraguriAMoriyamaHFukuharaT 2007 The dsRNA-binding protein DRB4 interacts with the Dicer-like protein DCL4 in vivo and functions in the trans-acting siRNA pathway. Plant Mol Biol 63 777 785

42. LindboJA 2007 TRBO: A high-efficiency Tobacco mosiac virus RNA-based overexpression vector. Plant Physiol 145 1232 1240

43. ErmakGPaszkowskiUWohlmuthMScheidOMPaszkowskiJ 1993 Cytosine methylation inhibits replication of African cassava mosaic virus by two distinct mechanisms. Nucl Acids Res 21 3445 3450

44. ZhouXPXieYTaoXRZhangZKLiZH 2003 Characterization of DNAβ associated with begomoviruses in China and evidence for co-evolution with their cognate DNA A. J Gen Virol 84 237 247

45. TrinksDRajeswaranRShivaprasadPVAkbergenovROakeleyEJ 2005 Supression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J Virol 79 2517 2527

46. SunterGSunterJBisaroDM 2001 Plants expressing tomato golden mosaic virus AL2 or beet curly top virus L2 transgenes show enhanced susceptibility to infection by DNA and RNA viruses. Virology 285 59 70

47. FrommerMMcDonaldLEMillarDSCollisCMWattF 1992 A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci U S A 89 1827 1831

48. McNellisTWMudgettMBLiKAoyamaTHorvathD 1998 Glucocorticoid-inducible expression of bacterial avirulence gene in transgenic Arabidopsis induced hypersensitive cell death. Plant J 14 247 257

49. CloughSJBentAF 1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 735 743

50. HaoLWangHSunterGBisaroDM 2003 Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 15 1034 1048

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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