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Epigenetic Changes in Host Ribosomal DNA Promoter Induced by an Asymptomatic Plant Virus Infection

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Epigenetic Changes in Host Ribosomal DNA Promoter Induced by an Asymptomatic Plant Virus Infection

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dc.contributor.author Pérez-Cañamás, Miryam es_ES
dc.contributor.author Hevia, Elizabeth es_ES
dc.contributor.author HERNANDEZ FORT, CARMEN es_ES
dc.date.accessioned 2021-05-11T03:31:53Z
dc.date.available 2021-05-11T03:31:53Z
dc.date.issued 2020-04 es_ES
dc.identifier.uri http://hdl.handle.net/10251/166140
dc.description.abstract [EN] DNA cytosine methylation is one of the main epigenetic mechanisms in higher eukaryotes and is considered to play a key role in transcriptional gene silencing. In plants, cytosine methylation can occur in all sequence contexts (CG, CHG, and CHH), and its levels are controlled by multiple pathways, including de novo methylation, maintenance methylation, and demethylation. Modulation of DNA methylation represents a potentially robust mechanism to adjust gene expression following exposure to different stresses. However, the potential involvement of epigenetics in plant-virus interactions has been scarcely explored, especially with regard to RNA viruses. Here, we studied the impact of a symptomless viral infection on the epigenetic status of the host genome. We focused our attention on the interaction between Nicotiana benthamiana and Pelargonium line pattern virus (PLPV, family Tombusviridae), and analyzed cytosine methylation in the repetitive genomic element corresponding to ribosomal DNA (rDNA). Through a combination of bisulfite sequencing and RT-qPCR, we obtained data showing that PLPV infection gives rise to a reduction in methylation at CG sites of the rDNA promoter. Such a reduction correlated with an increase and decrease, respectively, in the expression levels of some key demethylases and of MET1, the DNA methyltransferase responsible for the maintenance of CG methylation. Hypomethylation of rDNA promoter was associated with a five-fold augmentation of rRNA precursor levels. The PLPV protein p37, reported as a suppressor of post-transcriptional gene silencing, did not lead to the same effects when expressed alone and, thus, it is unlikely to act as suppressor of transcriptional gene silencing. Collectively, the results suggest that PLPV infection as a whole is able to modulate host transcriptional activity through changes in the cytosine methylation pattern arising from misregulation of methyltransferases/demethylases balance. es_ES
dc.description.sponsorship This work was funded by Ministerio de Economia y Competitividad (MINECO, Spain)-European Regional Development Fund (FEDER) (grants BFU2012-36095 and BFU2015-70261 to C.H) and by the Generalitat Valenciana (GVA, Valencia, Spain) (grant PROMETEO/2019/012 to C.H.). E.H. was the recipient of a contract from MINECO-FEDER and M.P.-C. was the recipient of contracts from MINECO-FEDER and GVA. es_ES
dc.language Inglés es_ES
dc.publisher MDPI AG es_ES
dc.relation.ispartof Biology es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject RNA virus es_ES
dc.subject DNA methylation es_ES
dc.subject Transcriptional gene silencing es_ES
dc.subject Plant virus es_ES
dc.subject METHYLTRASFERASE 1 es_ES
dc.subject Demethylases es_ES
dc.subject Viral suppressor of RNA silencing es_ES
dc.subject Tombusviridae es_ES
dc.title Epigenetic Changes in Host Ribosomal DNA Promoter Induced by an Asymptomatic Plant Virus Infection es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.3390/biology9050091 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BFU2012-36095/ES/ANALISIS DE UNA RELACION COMENSALISTA VIRUS-PLANTA: ESTUDIO DE DETERMINANTES DE ACUMULACION VIRAL Y DE POSIBLES ALTERACIONES EPIGENETICAS EN EL GENOMA DEL HUESPED/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BFU2015-70261-P/ES/ESTUDIO DE LA MODULACION DE LOS PROCESOS DE TRADUCCION Y DE SUPRESION DEL SILENCIAMIENTO EN UN VIRUS DE RNA DE PLANTAS/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GVA//PROMETEO%2F2019%2F012/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto de Reconocimiento Molecular y Desarrollo Tecnológico - Institut de Reconeixement Molecular i Desenvolupament Tecnològic es_ES
dc.contributor.affiliation Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes es_ES
dc.description.bibliographicCitation Pérez-Cañamás, M.; Hevia, E.; Hernandez Fort, C. (2020). Epigenetic Changes in Host Ribosomal DNA Promoter Induced by an Asymptomatic Plant Virus Infection. Biology. 9(5):1-13. https://doi.org/10.3390/biology9050091 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.3390/biology9050091 es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 13 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 9 es_ES
dc.description.issue 5 es_ES
dc.identifier.eissn 2079-7737 es_ES
dc.identifier.pmid 32353984 es_ES
dc.identifier.pmcid PMC7285159 es_ES
dc.relation.pasarela S\432755 es_ES
dc.contributor.funder Ministerio de Economía, Industria y Competitividad es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.contributor.funder European Regional Development Fund es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.description.references Wang, A. (2015). Dissecting the Molecular Network of Virus-Plant Interactions: The Complex Roles of Host Factors. Annual Review of Phytopathology, 53(1), 45-66. doi:10.1146/annurev-phyto-080614-120001 es_ES
dc.description.references Garcia‐Ruiz, H. (2019). Host factors against plant viruses. Molecular Plant Pathology, 20(11), 1588-1601. doi:10.1111/mpp.12851 es_ES
dc.description.references Garcia-Ruiz, H. (2018). Susceptibility Genes to Plant Viruses. Viruses, 10(9), 484. doi:10.3390/v10090484 es_ES
dc.description.references Han, G. (2019). Origin and evolution of the plant immune system. New Phytologist, 222(1), 70-83. doi:10.1111/nph.15596 es_ES
dc.description.references García, J. A., & Pallás, V. (2015). Viral factors involved in plant pathogenesis. Current Opinion in Virology, 11, 21-30. doi:10.1016/j.coviro.2015.01.001 es_ES
dc.description.references Whitham, S. A., Yang, C., & Goodin, M. M. (2006). Global Impact: Elucidating Plant Responses to Viral Infection. Molecular Plant-Microbe Interactions®, 19(11), 1207-1215. doi:10.1094/mpmi-19-1207 es_ES
dc.description.references Eichten, S. R., Schmitz, R. J., & Springer, N. M. (2014). Epigenetics: Beyond Chromatin Modifications and Complex Genetic Regulation. Plant Physiology, 165(3), 933-947. doi:10.1104/pp.113.234211 es_ES
dc.description.references Feng, S., Jacobsen, S. E., & Reik, W. (2010). Epigenetic Reprogramming in Plant and Animal Development. Science, 330(6004), 622-627. doi:10.1126/science.1190614 es_ES
dc.description.references Matzke, M. A., Kanno, T., & Matzke, A. J. M. (2015). RNA-Directed DNA Methylation: The Evolution of a Complex Epigenetic Pathway in Flowering Plants. Annual Review of Plant Biology, 66(1), 243-267. doi:10.1146/annurev-arplant-043014-114633 es_ES
dc.description.references Zhang, H., Lang, Z., & Zhu, J.-K. (2018). Dynamics and function of DNA methylation in plants. Nature Reviews Molecular Cell Biology, 19(8), 489-506. doi:10.1038/s41580-018-0016-z es_ES
dc.description.references Movahedi, A., Sun, W., Zhang, J., Wu, X., Mousavi, M., Mohammadi, K., … Zhuge, Q. (2015). RNA-directed DNA methylation in plants. Plant Cell Reports, 34(11), 1857-1862. doi:10.1007/s00299-015-1839-0 es_ES
dc.description.references Matzke, M. A., & Mosher, R. A. (2014). RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nature Reviews Genetics, 15(6), 394-408. doi:10.1038/nrg3683 es_ES
dc.description.references Gong, Z., Morales-Ruiz, T., Ariza, R. R., Roldán-Arjona, T., David, L., & Zhu, J.-K. (2002). ROS1, a Repressor of Transcriptional Gene Silencing in Arabidopsis, Encodes a DNA Glycosylase/Lyase. Cell, 111(6), 803-814. doi:10.1016/s0092-8674(02)01133-9 es_ES
dc.description.references Penterman, J., Zilberman, D., Huh, J. H., Ballinger, T., Henikoff, S., & Fischer, R. L. (2007). DNA demethylation in the Arabidopsis genome. Proceedings of the National Academy of Sciences, 104(16), 6752-6757. doi:10.1073/pnas.0701861104 es_ES
dc.description.references Zhu, J.-K. (2009). Active DNA Demethylation Mediated by DNA Glycosylases. Annual Review of Genetics, 43(1), 143-166. doi:10.1146/annurev-genet-102108-134205 es_ES
dc.description.references Baulcombe, D. C., & Dean, C. (2014). Epigenetic Regulation in Plant Responses to the Environment. Cold Spring Harbor Perspectives in Biology, 6(9), a019471-a019471. doi:10.1101/cshperspect.a019471 es_ES
dc.description.references Ding, B., & Wang, G.-L. (2015). Chromatin versus pathogens: the function of epigenetics in plant immunity. Frontiers in Plant Science, 6. doi:10.3389/fpls.2015.00675 es_ES
dc.description.references Butterbach, P., Verlaan, M. G., Dullemans, A., Lohuis, D., Visser, R. G. F., Bai, Y., & Kormelink, R. (2014). Tomato yellow leaf curl virus resistance by Ty-1 involves increased cytosine methylation of viral genomes and is compromised by cucumber mosaic virus infection. Proceedings of the National Academy of Sciences, 111(35), 12942-12947. doi:10.1073/pnas.1400894111 es_ES
dc.description.references Raja, P., Sanville, B. C., Buchmann, R. C., & Bisaro, D. M. (2008). Viral Genome Methylation as an Epigenetic Defense against Geminiviruses. Journal of Virology, 82(18), 8997-9007. doi:10.1128/jvi.00719-08 es_ES
dc.description.references Yang, L.-P., Fang, Y.-Y., An, C.-P., Dong, L., Zhang, Z.-H., Chen, H., … Guo, H.-S. (2013). C2-mediated decrease in DNA methylation, accumulation of siRNAs, and increase in expression for genes involved in defense pathways in plants infected with beet severe curly top virus. The Plant Journal, 73(6), 910-917. doi:10.1111/tpj.12081 es_ES
dc.description.references Kanazawa, A., Inaba, J., Shimura, H., Otagaki, S., Tsukahara, S., Matsuzawa, A., … Masuta, C. (2010). Virus-mediated efficient induction of epigenetic modifications of endogenous genes with phenotypic changes in plants. The Plant Journal, 65(1), 156-168. doi:10.1111/j.1365-313x.2010.04401.x es_ES
dc.description.references Kon, T., & Yoshikawa, N. (2014). Induction and maintenance of DNA methylation in plant promoter sequences by apple latent spherical virus-induced transcriptional gene silencing. Frontiers in Microbiology, 5. doi:10.3389/fmicb.2014.00595 es_ES
dc.description.references Otagaki, S., Kawai, M., Masuta, C., & Kanazawa, A. (2011). Size and positional effects of promoter RNA segments on virus-induced RNA-directed DNA methylation and transcriptional gene silencing. Epigenetics, 6(6), 681-691. doi:10.4161/epi.6.6.16214 es_ES
dc.description.references Diezma‐Navas, L., Pérez‐González, A., Artaza, H., Alonso, L., Caro, E., Llave, C., & Ruiz‐Ferrer, V. (2019). Crosstalk between epigenetic silencing and infection by tobacco rattle virus in Arabidopsis. Molecular Plant Pathology, 20(10), 1439-1452. doi:10.1111/mpp.12850 es_ES
dc.description.references Wang, C., Wang, C., Xu, W., Zou, J., Qiu, Y., Kong, J., … Zhu, S. (2018). Epigenetic Changes in the Regulation of Nicotiana tabacum Response to Cucumber Mosaic Virus Infection and Symptom Recovery through Single-Base Resolution Methylomes. Viruses, 10(8), 402. doi:10.3390/v10080402 es_ES
dc.description.references Wang, C., Wang, C., Zou, J., Yang, Y., Li, Z., & Zhu, S. (2019). Epigenetics in the plant–virus interaction. Plant Cell Reports, 38(9), 1031-1038. doi:10.1007/s00299-019-02414-0 es_ES
dc.description.references Scheets, K., Jordan, R., White, K. A., & Hernández, C. (2015). Pelarspovirus, a proposed new genus in the family Tombusviridae. Archives of Virology, 160(9), 2385-2393. doi:10.1007/s00705-015-2500-5 es_ES
dc.description.references Castaño, A., & Hernández, C. (2005). Complete nucleotide sequence and genome organization of Pelargonium line pattern virus and its relationship with the family Tombusviridae. Archives of Virology, 150(5), 949-965. doi:10.1007/s00705-004-0464-y es_ES
dc.description.references Castaño, A., Ruiz, L., & Hernández, C. (2009). Insights into the translational regulation of biologically active open reading frames of Pelargonium line pattern virus. Virology, 386(2), 417-426. doi:10.1016/j.virol.2009.01.017 es_ES
dc.description.references Pérez-Cañamás, M., & Hernández, C. (2015). Key Importance of Small RNA Binding for the Activity of a Glycine-Tryptophan (GW) Motif-containing Viral Suppressor of RNA Silencing. Journal of Biological Chemistry, 290(5), 3106-3120. doi:10.1074/jbc.m114.593707 es_ES
dc.description.references Alonso, M., & Borja, M. (2005). High incidence of Pelargonium line pattern virus infecting asymptomatic Pelargonium spp. in Spain. European Journal of Plant Pathology, 112(2), 95-100. doi:10.1007/s10658-005-0803-1 es_ES
dc.description.references Ivars, P., Alonso, M., Borja, M., & Hernández, C. (2004). Development of a Non-radioactive Dot-blot Hybridisation Assay for the Detection of Pelargonium Flower Break Virus and Pelargonium line Pattern Virus. European Journal of Plant Pathology, 110(3), 275-283. doi:10.1023/b:ejpp.0000019798.87567.22 es_ES
dc.description.references Pérez-Cañamás, M., Blanco-Pérez, M., Forment, J., & Hernández, C. (2017). Nicotiana benthamiana plants asymptomatically infected by Pelargonium line pattern virus show unusually high accumulation of viral small RNAs that is neither associated with DCL induction nor RDR6 activity. Virology, 501, 136-146. doi:10.1016/j.virol.2016.11.018 es_ES
dc.description.references Tucker, S., Vitins, A., & Pikaard, C. S. (2010). Nucleolar dominance and ribosomal RNA gene silencing. Current Opinion in Cell Biology, 22(3), 351-356. doi:10.1016/j.ceb.2010.03.009 es_ES
dc.description.references Blanco-Pérez, M., & Hernández, C. (2016). Evidence supporting a premature termination mechanism for subgenomic RNA transcription in Pelargonium line pattern virus: identification of a critical long-range RNA–RNA interaction and functional variants through mutagenesis. Journal of General Virology, 97(6), 1469-1480. doi:10.1099/jgv.0.000459 es_ES
dc.description.references Pérez-Cañamás, M., & Hernández, C. (2018). New Insights into the Nucleolar Localization of a Plant RNA Virus-Encoded Protein That Acts in Both RNA Packaging and RNA Silencing Suppression: Involvement of Importins Alpha and Relevance for Viral Infection. Molecular Plant-Microbe Interactions®, 31(11), 1134-1144. doi:10.1094/mpmi-02-18-0050-r es_ES
dc.description.references Li, L.-C., & Dahiya, R. (2002). MethPrimer: designing primers for methylation PCRs. Bioinformatics, 18(11), 1427-1431. doi:10.1093/bioinformatics/18.11.1427 es_ES
dc.description.references Hetzl, J., Foerster, A. M., Raidl, G., & Scheid, O. M. (2007). CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulphite sequencing. The Plant Journal, 51(3), 526-536. doi:10.1111/j.1365-313x.2007.03152.x es_ES
dc.description.references Liu, D., Shi, L., Han, C., Yu, J., Li, D., & Zhang, Y. (2012). Validation of Reference Genes for Gene Expression Studies in Virus-Infected Nicotiana benthamiana Using Quantitative Real-Time PCR. PLoS ONE, 7(9), e46451. doi:10.1371/journal.pone.0046451 es_ES
dc.description.references McStay, B., & Grummt, I. (2008). The Epigenetics of rRNA Genes: From Molecular to Chromosome Biology. Annual Review of Cell and Developmental Biology, 24(1), 131-157. doi:10.1146/annurev.cellbio.24.110707.175259 es_ES
dc.description.references Pikaard, C. S. (2000). The epigenetics of nucleolar dominance. Trends in Genetics, 16(11), 495-500. doi:10.1016/s0168-9525(00)02113-2 es_ES
dc.description.references Buchmann, R. C., Asad, S., Wolf, J. N., Mohannath, G., & Bisaro, D. M. (2009). Geminivirus AL2 and L2 Proteins Suppress Transcriptional Gene Silencing and Cause Genome-Wide Reductions in Cytosine Methylation. Journal of Virology, 83(10), 5005-5013. doi:10.1128/jvi.01771-08 es_ES
dc.description.references Rodríguez‐Negrete, E., Lozano‐Durán, R., Piedra‐Aguilera, A., Cruzado, L., Bejarano, E. R., & Castillo, A. G. (2013). Geminivirus R ep protein interferes with the plant DNA methylation machinery and suppresses transcriptional gene silencing. New Phytologist, 199(2), 464-475. doi:10.1111/nph.12286 es_ES
dc.description.references Yang, L., Xu, Y., Liu, Y., Meng, D., Jin, T., & Zhou, X. (2016). HC-Pro viral suppressor from tobacco vein banding mosaic virus interferes with DNA methylation and activates the salicylic acid pathway. Virology, 497, 244-250. doi:10.1016/j.virol.2016.07.024 es_ES
dc.description.references Alonso, C., Ramos‐Cruz, D., & Becker, C. (2018). The role of plant epigenetics in biotic interactions. New Phytologist, 221(2), 731-737. doi:10.1111/nph.15408 es_ES
dc.description.references Sáez-Vásquez, J., & Delseny, M. (2019). Ribosome Biogenesis in Plants: From Functional 45S Ribosomal DNA Organization to Ribosome Assembly Factors. The Plant Cell, 31(9), 1945-1967. doi:10.1105/tpc.18.00874 es_ES
dc.description.references Jan, E., Mohr, I., & Walsh, D. (2016). A Cap-to-Tail Guide to mRNA Translation Strategies in Virus-Infected Cells. Annual Review of Virology, 3(1), 283-307. doi:10.1146/annurev-virology-100114-055014 es_ES
dc.description.references Cao, M., Du, P., Wang, X., Yu, Y.-Q., Qiu, Y.-H., Li, W., … Ding, S.-W. (2014). Virus infection triggers widespread silencing of host genes by a distinct class of endogenous siRNAs inArabidopsis. Proceedings of the National Academy of Sciences, 111(40), 14613-14618. doi:10.1073/pnas.1407131111 es_ES
dc.description.references Martinez, G., Castellano, M., Tortosa, M., Pallas, V., & Gomez, G. (2013). A pathogenic non-coding RNA induces changes in dynamic DNA methylation of ribosomal RNA genes in host plants. Nucleic Acids Research, 42(3), 1553-1562. doi:10.1093/nar/gkt968 es_ES
dc.description.references Csorba, T., Kontra, L., & Burgyán, J. (2015). viral silencing suppressors: Tools forged to fine-tune host-pathogen coexistence. Virology, 479-480, 85-103. doi:10.1016/j.virol.2015.02.028 es_ES
dc.description.references Deleris, A., Halter, T., & Navarro, L. (2016). DNA Methylation and Demethylation in Plant Immunity. Annual Review of Phytopathology, 54(1), 579-603. doi:10.1146/annurev-phyto-080615-100308 es_ES
dc.description.references Le, T.-N., Schumann, U., Smith, N. A., Tiwari, S., Au, P. C. K., Zhu, Q.-H., … Wang, M.-B. (2014). DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis. Genome Biology, 15(9). doi:10.1186/s13059-014-0458-3 es_ES
dc.description.references Yu, A., Lepere, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., … Navarro, L. (2013). Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proceedings of the National Academy of Sciences, 110(6), 2389-2394. doi:10.1073/pnas.1211757110 es_ES
dc.description.references Palukaitis, P., & García-Arenal, F. (2003). Cucumoviruses. Advances in Virus Research, 241-323. doi:10.1016/s0065-3527(03)62005-1 es_ES
dc.description.references Ratcliff, F., Martin-Hernandez, A. M., & Baulcombe, D. C. (2008). Technical Advance: Tobacco rattle virus as a vector for analysis of gene function by silencing. The Plant Journal, 25(2), 237-245. doi:10.1046/j.0960-7412.2000.00942.x es_ES


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