Geminivirus Activates to Accelerate Cytoplasmic DCP2-Mediated mRNA Turnover and Weakens RNA Silencing in

English version České info

In higher plants, aberrant RNAs generated during virus replication serve as templates to make small interfering RNAs. These small RNAs are used by host as a defense mechanism to cleave viral RNAs thereby blocking virus replication. The anti-virus defense is attenuated by the host cellular mRNA turnover machinery which clears aberrant RNAs. Viruses may use encoded component(s) to activate host cellular mRNA turnover for their own benefits. In this study, we identified ASYMMETRIC LEAVES2 (AS2) as an activator of mRNA decapping and degradation and an endogenous suppressor of virus silencing. We showed that the geminivirus BV1 protein induces AS2 expression, causes nuclear exit of AS2 to activate mRNA decapping activity and renders infected plants more sensitive to viruses. Similar mechanisms may be used by other viral pathogens to weaken antiviral defenses in host plants and also mammals.

Vyšlo v časopise: Geminivirus Activates to Accelerate Cytoplasmic DCP2-Mediated mRNA Turnover and Weakens RNA Silencing in. PLoS Pathog 11(10): e32767. doi:10.1371/journal.ppat.1005196
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005196

Souhrn

Zdroje

1. Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11: 745–760. doi: 10.1038/nrmicro3120 24129510

2. Vargason JM, Szittya G, Burgyan J, Hall TM (2003) Size selective recognition of siRNA by an RNA silencing suppressor. Cell 115: 799–811. 14697199

3. Zhang X, Yuan YR, Pei Y, Lin SS, Tuschl T, et al. (2006) Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev 20: 3255–3268. 17158744

4. Ying XB, Dong L, Zhu H, Duan CG, Du QS, et al. (2010) RNA-dependent RNA polymerase 1 from Nicotiana tabacum suppresses RNA silencing and enhances viral infection in Nicotiana benthamiana. Plant Cell 22: 1358–1372. doi: 10.1105/tpc.109.072058 20400679

5. Franks TM, Lykke-Andersen J (2008) The control of mRNA decapping and P-body formation. Mol Cell 32: 605–615. doi: 10.1016/j.molcel.2008.11.001 19061636

6. Arribas-Layton M, Wu D, Lykke-Andersen J, Song H (2013) Structural and functional control of the eukaryotic mRNA decapping machinery. Biochim Biophys Acta 1829: 580–589. doi: 10.1016/j.bbagrm.2012.12.006 23287066

7. Xu J, Yang JY, Niu QW, Chua NH (2006) Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development. Plant Cell 18: 3386–3398. 17158604

8. Xu J, Chua NH (2009) Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development. Plant Cell 21: 3270–3279. doi: 10.1105/tpc.109.070078 19855049

9. Gazzani S, Lawrenson T, Woodward C, Headon D, Sablowski R (2004) A link between mRNA turnover and RNA interference in Arabidopsis. Science 306: 1046–1048. 15528448

10. Thran M, Link K, Sonnewald U (2012) The Arabidopsis DCP2 gene is required for proper mRNA turnover and prevents transgene silencing in Arabidopsis. Plant J 72: 368–377. doi: 10.1111/j.1365-313X.2012.05066.x 22639932

11. Tsai WC, Richard EL (2014) Cytoplasmic RNA Granules and Viral Infection. Annual Review of Virology 1: 147–170.

12. Hopkins KC, McLane LM, Maqbool T, Panda D, Gordesky-Gold B, et al. (2013) A genome-wide RNAi screen reveals that mRNA decapping restricts bunyaviral replication by limiting the pools of Dcp2-accessible targets for cap-snatching. Genes Dev 27: 1511–1525. doi: 10.1101/gad.215384.113 23824541

13. Zhou X (2013) Advances in understanding begomovirus satellites. Annu Rev Phytopathol 51: 357–381. doi: 10.1146/annurev-phyto-082712-102234 23915133

14. Gao S, Qu J, Chua NH, Ye J (2010) A new strain of Indian cassava mosaic virus causes a mosaic disease in the biodiesel crop Jatropha curcas. Arch Virol 155: 607–612. doi: 10.1007/s00705-010-0625-0 20224893

15. Fontes EP, Santos AA, Luz DF, Waclawovsky AJ, Chory J (2004) The geminivirus nuclear shuttle protein is a virulence factor that suppresses transmembrane receptor kinase activity. Genes Dev 18: 2545–2556. 15489295

16. Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S (2013) Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol 11: 777–788. doi: 10.1038/nrmicro3117 24100361

17. Yang JY, Iwasaki M, Machida C, Machida Y, Zhou X, et al. (2008) betaC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 22: 2564–2577. doi: 10.1101/gad.1682208 18794352

18. Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, et al. (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101: 533–542. 10850495

19. Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, et al. (2001) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128: 1771–1783. 11311158

20. Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, et al. (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol 43: 467–478. 12040093

21. Li H, Xu L, Wang H, Yuan Z, Cao X, et al. (2005) The Putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and MicroRNA165/166 in Arabidopsis leaf development. Plant Cell 17: 2157–2171. 16006579

22. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743. 10069079

23. Qu J, Ye J, Fang R (2007) Artificial microRNA-mediated virus resistance in plants. J Virol 81: 6690–6699. 17344304

24. Elmayan T, Balzergue S, Beon F, Bourdon V, Daubremet J, et al. (1998) Arabidopsis mutants impaired in cosuppression. Plant Cell 10: 1747–1758. 9761800

25. Li R, Weldegergis BT, Li J, Jung C, Qu J, et al. (2014) Virulence Factors of Geminivirus Interact with MYC2 to Subvert Plant Resistance and Promote Vector Performance. Plant Cell 26: 4991–5008. doi: 10.1105/tpc.114.133181 25490915

26. Ye J, Qu J, Mao HZ, Ma ZG, Rahman NE, et al. (2014) Engineering geminivirus resistance in Jatropha curcus. Biotechnol Biofuels 7: 149. doi: 10.1186/s13068-014-0149-z 25352912

27. Ye J, Qu J, Bui HT, Chua NH (2009) Rapid analysis of Jatropha curcas gene functions by virus-induced gene silencing. Plant Biotechnol J 7: 964–976. doi: 10.1111/j.1467-7652.2009.00457.x 19906247

28. Ye J, Liu P, Zhu C, Qu J, Wang X, et al. (2014) Identification of candidate genes JcARF19 and JcIAA9 associated with seed size traits in Jatropha. Funct Integr Genomics 14: 757–766. doi: 10.1007/s10142-014-0400-5 25228410

29. Muangsan N, Beclin C, Vaucheret H, Robertson D (2004) Geminivirus VIGS of endogenous genes requires SGS2/SDE1 and SGS3 and defines a new branch in the genetic pathway for silencing in plants. Plant J 38: 1004–1014. 15165191

30. Gimenez-Barcons M, Alves-Rodrigues I, Jungfleisch J, Van Wynsberghe PM, Ahlquist P, et al. (2013) The cellular decapping activators LSm1, Pat1, and Dhh1 control the ratio of subgenomic to genomic Flock House virus RNAs. J Virol 87: 6192–6200. doi: 10.1128/JVI.03327-12 23536653

31. Liu SW, Wyatt LS, Orandle MS, Minai M, Moss B (2014) The D10 decapping enzyme of vaccinia virus contributes to decay of cellular and viral mRNAs and to virulence in mice. J Virol 88: 202–211. doi: 10.1128/JVI.02426-13 24155373

32. Covarrubias S, Gaglia MM, Kumar GR, Wong W, Jackson AO, et al. (2011) Coordinated destruction of cellular messages in translation complexes by the gammaherpesvirus host shutoff factor and the mammalian exonuclease Xrn1. PLoS Pathog 7: e1002339. doi: 10.1371/journal.ppat.1002339 22046136

33. Li Y, Dai J, Song M, Fitzgerald-Bocarsly P, Kiledjian M (2012) Dcp2 decapping protein modulates mRNA stability of the critical interferon regulatory factor (IRF) IRF-7. Mol Cell Biol 32: 1164–1172. doi: 10.1128/MCB.06328-11 22252322

34. Moreno AB, Martinez de Alba AE, Bardou F, Crespi MD, Vaucheret H, et al. (2013) Cytoplasmic and nuclear quality control and turnover of single-stranded RNA modulate post-transcriptional gene silencing in plants. Nucleic Acids Res 41: 4699–4708. doi: 10.1093/nar/gkt152 23482394

35. Garcia D, Garcia S, Voinnet O (2014) Nonsense-mediated decay serves as a general viral restriction mechanism in plants. Cell Host Microbe 16: 391–402. doi: 10.1016/j.chom.2014.08.001 25155460

36. Gy I, Gasciolli V, Lauressergues D, Morel JB, Gombert J, et al. (2007) Arabidopsis FIERY1, XRN2, and XRN3 are endogenous RNA silencing suppressors. Plant Cell 19: 3451–3461. 17993620

37. Zorzatto C, Machado JP, Lopes KV, Nascimento KJ, Pereira WA, et al. (2015) NIK1-mediated translation suppression functions as a plant antiviral immunity mechanism. Nature: doi: 10.1038/nature14171 25707794

38. Rajamaki ML, Streng J, Valkonen JP (2014) Silencing Suppressor Protein VPg of a Potyvirus Interacts With the Plant Silencing-Related Protein SGS3. Mol Plant Microbe Interact 27: 1199–1210. doi: 10.1094/MPMI-04-14-0109-R 25099340

39. Okano Y, Senshu H, Hashimoto M, Neriya Y, Netsu O, et al. (2014) In Planta Recognition of a Double-Stranded RNA Synthesis Protein Complex by a Potexviral RNA Silencing Suppressor. Plant Cell 26: 2168–2183. 24879427

40. Guo H, Song X, Xie C, Huo Y, Zhang F, et al. (2013) Rice yellow stunt rhabdovirus protein 6 suppresses systemic RNA silencing by blocking RDR6-mediated secondary siRNA synthesis. Mol Plant Microbe Interact 26: 927–936. doi: 10.1094/MPMI-02-13-0040-R 23634838

41. Du Z, Xiao D, Wu J, Jia D, Yuan Z, et al. (2011) p2 of rice stripe virus (RSV) interacts with OsSGS3 and is a silencing suppressor. Mol Plant Pathol 12: 808–814. doi: 10.1111/j.1364-3703.2011.00716.x 21726383

42. Glick E, Zrachya A, Levy Y, Mett A, Gidoni D, et al. (2008) Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc Natl Acad Sci U S A 105: 157–161. doi: 10.1073/pnas.0709036105 18165314