Abstract
Plants have developed diverse molecular mechanisms to resist viruses. RNA silencing plays a dominant role in antiviral defense. Recent studies have correlated plant antiviral silencing to epigenetic modification in genomic DNA and protein by remodeling the expression levels of coding genes. The plant host methylation level is reprogrammed in response to viral challenge. Genomes of some viruses have been implicated in the epigenetic modification via small RNA-mediated transcriptional gene silencing and post-transcriptional gene silencing. These mechanisms can be primed prior to a virus attack through methylation changes for antiviral defense. This review highlights the findings concerning the methylation changes in plant–virus interactions and demonstrates a possible direction to improve the understanding of plant host methylation regulation in response to viral infection.
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References
Alvarez ME, Nota F, Cambiagno DA (2010) Epigenetic control of plant immunity. Mol Plant Pathol 11:563–576
Aran D, Sabato S, Hellman A (2013) DNA methylation of distal regulatory sites characterizes dysregulation of cancer genes. Genome Biol 14:R21
Baulcombe DC, Dean C (2014) Epigenetic regulation in plant responses to the environment. Cold Spring Harbor Perspect Biol 6:a019471
Becker C, Hagmann J, Müller J, Koenig D, Stegle O, Borgwardt K, Weigel D (2011) Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480:245
Bian X-Y, Rasheed MS, Seemanpillai MJ, Rezaian MA (2006) Analysis of silencing escape of Tomato leaf curl virus: an evaluation of the role of DNA methylation. Mol Plant Microbe Interact 19:614–624
Blevins T, Rajeswaran R, Aregger M, Borah BK, Schepetilnikov M, Baerlocher L, Farinelli L, Meins F Jr, Hohn T, Pooggin MM (2011) Massive production of small RNAs from a non-coding region of Cauliflower mosaic virus in plant defense and viral counter-defense. Nucleic Acids Res 39:5003–5014. https://doi.org/10.1093/nar/gkr119
Boyko A, Kovalchuk I (2011) Genetic and epigenetic effects of plant–pathogen interactions: an evolutionary perspective. Mol Plant 4:1014–1023
Boyko A, Kathiria P, Zemp FJ, Yao Y, Pogribny I, Kovalchuk I (2007) Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (virus-induced plant genome instability). Nucleic Acids Res 35:1714–1725
Brocard M, Ruggieri A, Locker N (2017) m6A RNA methylation, a new hallmark in virus–host interactions. J Gen Virol 98:2207–2214
Brough CL, Gardiner WE, Inamdar NM, Zhang X-Y, Ehrlich M, Bisaro DM (1992) DNA methylation inhibits propagation of tomato golden mosaic virus DNA in transfected protoplasts. Plant Mol Biol 18:703–712
Buchmann RC, Asad S, Wolf JN, Mohannath G, Bisaro DM (2009) Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J Virol 83:5005–5013
Butterbach P, Verlaan MG, Dullemans A, Lohuis D, Visser RG, 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. Proc Natl Acad Sci 111:12942–12947
Castellano M, Martinez G, Pallas V, Gomez G (2015) Alterations in host DNA methylation in response to constitutive expression of Hop stunt viroid RNA in Nicotiana benthamiana plants. Plant Pathol 64:1247–1257
Castellano M, Martinez G, Marques MC, Moreno-Romero J, Köhler C, Pallas V, Gomez G (2016) Changes in the DNA methylation pattern of the host male gametophyte of viroid-infected cucumber plants. J Exp Bot 67:5857–5868
Chen H, Zhang Z, Teng K, Lai J, Zhang Y, Huang Y, Li Y, Liang L, Wang Y, Chu C, Guo H, Xie Q (2010) Up-regulation of LSB1/GDU3 affects geminivirus infection by activating the salicylic acid pathway. Plant J 62:12–23. https://doi.org/10.1111/j.1365-313X.2009.04120.x
Coursey T, Regedanz E, Bisaro DM (2018) Arabidopsis RNA polymerase V mediates enhanced compaction and silencing of geminivirus and transposon chromatin during host recovery from infection. J Virol 92:e01320
Cuerda-Gil D, Slotkin RK (2016) Non-canonical RNA-directed DNA methylation. Nat Plants 2:16163
Deleris A, Halter T, Navarro L (2016) DNA methylation and demethylation in plant immunity. Annu Rev Phytopathol 54:579
Diez CM, Roessler K, Gaut BS (2014) Epigenetics and plant genome evolution. Curr Opin Plant Biol 18:1–8
Ding B, Wang GL (2015) Chromatin versus pathogens: the function of epigenetics in plant immunity. Front Plant Sci 6:675
Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539
Dong Q, Li X, Wang C-Z, Xu S, Yuan G, Shao W, Liu B, Zheng Y, Wang H, Lei X (2018) Roles of the CSE1L-mediated nuclear import pathway in epigenetic silencing. Proc Natl Acad Sci 115:E4013–E4022
Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, Dixon JE, Ecker JR (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci 109:E2183–E2191
Du J, Johnson LM, Jacobsen SE, Patel DJ (2015) DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol 16:519
Duan C-G, Fang Y-Y, Zhou B-J, Zhao J-H, Hou W-N, Zhu H, Ding S-W, Guo H-S (2012) Suppression of Arabidopsis ARGONAUTE1-mediated slicing, transgene-induced RNA silencing, and DNA methylation by distinct domains of the Cucumber mosaic virus 2b protein. Plant Cell 24:259–274
Ebhardt HA, Thi EP, Wang M-B, Unrau PJ (2005) Extensive 3′ modification of plant small RNAs is modulated by helper component-proteinase expression. Proc Natl Acad Sci 102:13398–13403
Eichten SR, Schmitz RJ, Springer NM (2014) Epigenetics: beyond chromatin modifications and complex genetic regulation. Plant Physiol 165:933
Espinas NA, Hidetoshi S, Yusuke S (2016) Epigenetic control of defense signaling and priming in plants. Front Plant Sci 7:1201
Furner IJ, Matzke M (2011) Methylation and demethylation of the Arabidopsis genome. Curr Opin Plant Biol 14:137–141
Guo HS, Ding SW (2002) A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J 21:398–407
Guo H, Zhu P, Wu X, Li X, Wen L, Tang F (2013) Single-cell methylome landscapes of mouse embryonic stem cells and early embryos analyzed using reduced representation bisulfite sequencing. Genome Res 23:2126–2135
Hackett JA, Surani MA (2013) DNA methylation dynamics during the mammalian life cycle. Philos Trans R Soc B 368:20110328
Hamera S, Song X, Su L, Chen X, Fang R (2012) Cucumber mosaic virus suppressor 2b binds to AGO4-related small RNAs and impairs AGO4 activities. Plant J 69:104–115
Ivanov KI, Eskelin K, Bašić M, De S, Lõhmus A, Varjosalo M, Mäkinen K (2016) Molecular insights into the function of the viral RNA silencing suppressor HCP ro. Plant J 85:30–45
Jackel JN, Buchmann RC, Singhal U, Bisaro DM (2015) Analysis of geminivirus AL2 and L2 proteins reveals a novel AL2 silencing suppressor activity. J Virol 89:3176–3187
Jackel JN, Storer JM, Coursey T, Bisaro DM (2016) Arabidopsis RNA polymerases IV and V are required to establish H3K9 methylation, but not cytosine methylation, on geminivirus chromatin. J Virol 90:7529–7540
Jackson JP, Lindroth AM, Cao X, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–560
Jones AL, Thomas CL, Maule AJ (1998) De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. EMBO J 17:6385–6393
Jones L, Hamilton AJ, Voinnet O, Thomas CL, Maule AJ, Baulcombe DC (1999) RNA–DNA interactions and DNA methylation in post-transcriptional gene silencing. Plant Cell 11:2291–2301
Kawakatsu T, S-C Huang, Jupe F, Sasaki E, Schmitz RJ, Urich MA, Castanon R, Nery JR, Barragan C, He Y (2016) Epigenomic diversity in a global collection of Arabidopsis thaliana accessions. Cell 166:492–505
Kim MJ, Huh SU, Ham B-K, Paek K-H (2008) A novel methyltransferase methylates Cucumber mosaic virus 1a protein and promotes systemic spread. J Virol 82:4823–4833
Kushwaha NK, Bhardwaj M, Chakraborty S (2017) The replication initiator protein of a geminivirus interacts with host monoubiquitination machinery and stimulates transcription of the viral genome. PLoS Pathog 13:e1006587
Lang Z, Wang Y, Tang K, Tang D, Datsenka T, Cheng J, Zhang Y, Handa AK, Zhu J-K (2017) Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. Proc Natl Acad Sci 114:E4511–E4519
Li F, Xu X, Huang C, Gu Z, Cao L, Hu T, Ding M, Li Z, Zhou X (2015a) The AC5 protein encoded by Mungbean yellow mosaic India virus is a pathogenicity determinant that suppresses RNA silencing-based antiviral defenses. New Phytol 208:555–569
Li X, Li L, Yan J (2015b) Dissecting meiotic recombination based on tetrad analysis by single-microspore sequencing in maize. Nat Commun 6:6648
Liu Z-W, Shao C-R, Zhang C-J, Zhou J-X, Zhang S-W, Li L, Chen S, Huang H-W, Cai T, He X-J (2014) The SET domain proteins SUVH2 and SUVH9 are required for Pol V occupancy at RNA-directed DNA methylation loci. PLoS Genet 10:e1003948
Llave C (2010) Virus-derived small interfering RNAs at the core of plant–virus interactions. Trends Plant Sci 15:701–707
Lozsa R, Csorba T, Lakatos L, Burgyan J (2008) Inhibition of 3′ modification of small RNAs in virus-infected plants require spatial and temporal co-expression of small RNAs and viral silencing-suppressor proteins. Nucleic Acids Res 36:4099–4107
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 Res 42:1553–1562
Martínez-Pérez M, Aparicio F, López-Gresa MP, Bellés JM, Sánchez-Navarro JA, Pallás V (2017) Arabidopsis m6A demethylase activity modulates viral infection of a plant virus and the m6A abundance in its genomic RNAs. Proc Natl Acad Sci 114:10755–10760
Mason G, Noris E, Lanteri S, Acquadro A, Accotto GP, Portis E (2008) Potentiality of methylation-sensitive amplification polymorphism (MSAP) in identifying genes involved in tomato response to tomato yellow leaf curl sardinia virus. Plant Mol Biol Rep 26:156
Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394
Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL (2007) DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci 104:6752–6757
Pikaard C, Haag J, Pontes O, Blevins T, Cocklin R (2012) A transcription fork model for pol IV and pol v—dependent RNA-directed DNA methylation. In: Cold Spring Harbor symposia on quantitative biology, 2012. Cold Spring Harbor Laboratory Press, pp 205–212
Pooggin MM (2013) How can plant DNA viruses evade siRNA-directed DNA methylation and silencing? Int J Mol Sci 14:15233–15259
Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11:745
Quadrana L, Colot V (2016) Plant transgenerational epigenetics. Annu Rev Genet 50:467–491
Raja P, Sanville BC, Buchmann RC, Bisaro DM (2008) Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 82:8997–9007
Raja P, Jackel JN, Li S, Heard IM, Bisaro DM (2014) Arabidopsis double-stranded RNA binding protein DRB3 participates in methylation-mediated defense against geminiviruses. J Virol 88:2611–2622
Ramesh SV, Sahu PP, Prasad M, Praveen S, Pappu HR (2017) Geminiviruses and plant hosts: a closer examination of the molecular arms race. Viruses 9:256
Rodríguez-Negrete EA, Carrillo-Tripp J, Rivera-Bustamante RF (2009) RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J Virol 83:1332–1340
Rodríguez-Negrete E, Lozano-Durán R, Piedra-Aguilera A, Cruzado L, Bejarano ER, Castillo AG (2013) Geminivirus Rep protein interferes with the plant DNA methylation machinery and suppresses transcriptional gene silencing. New Phytol 199:464–475
Sahu PP, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M (2013) Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 32:1151
Sahu PP, Sharma N, Puranik S, Prasad M (2014) Post-transcriptional and epigenetic arms of RNA silencing: a defense machinery of naturally tolerant tomato plant against Tomato leaf curl New Delhi virus. Plant Mol Biol Rep 32:1015–1029
Sato Y, Miyashita S, Ando S, Takahashi H (2017) Increased cytosine methylation at promoter of the NB-LRR class R gene RCY1 correlated with compromised resistance to cucumber mosaic virus in EMS-generated src mutants of Arabidopsis thaliana. Physiol Mol Plant Pathol 100:151–162
Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, Santos F, Popp C, Thienpont B, Dean W, Reik W (2012) The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48:849–862
Sharma N, Sahu PP, Puranik S, Prasad M (2013) Recent advances in plant–virus interaction with emphasis on small interfering RNAs (siRNAs). Mol Biotechnol 55:63–77
Stael S, Kmiecik P, Willems P, Kelen KVD, Coll SN (2015) Plant innate immunity—sunny side up? Trends Plant Sci 20:3–11
Stroud H, Greenberg MV, Feng S, Bernatavichute YV, Jacobsen SE (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152:352–364
Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ, Jacobsen SE (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21:64
Tu YC, Tsai WS, Wei JY, Chang KY, Tien CC, Hsiao HY, Fu SF (2017) The C2 protein of Tomato leaf curl Taiwan virus is a pathogenicity determinant that interferes with expression of host genes encoding chromomethylases. Physiol Plant 161:515
Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86
Wada Y, Miyamoto K, Kusano T, Sano H (2004) Association between up-regulation of stress-responsive genes and hypomethylation of genomic DNA in tobacco plants. Mol Genet Genom 271:658–666
Wang X, Moazed D (2017) DNA sequence-dependent epigenetic inheritance of gene silencing and histone H3K9 methylation. Science 356:88–91. https://doi.org/10.1126/science.aaj2114
Wang H, Hao L, Shung C-Y, Sunter G, Bisaro DM (2003) Adenosine kinase is inactivated by geminivirus AL2 and L2 proteins. Plant Cell 15:3020–3032
Wang H, Buckley KJ, Yang X, Buchmann RC, Bisaro DM (2005) Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J Virol 79:7410–7418
Wang M-B, Masuta C, Smith NA, Shimura H (2012) RNA silencing and plant viral diseases. Mol Plant Microbe Interact 25:1275–1285
Wang B, Li F, Huang C, Yang X, Qian Y, Xie Y, Zhou X (2014) V2 of tomato yellow leaf curl virus can suppress methylation-mediated transcriptional gene silencing in plants. J Gen Virol 95:225–230
Wang B, Yang X, Wang Y, Xie Y, Zhou X (2018a) Tomato yellow leaf curl virus V2 interacts with host histone deacetylase 6 to suppress methylation-mediated transcriptional gene silencing in plants. J Virol. https://doi.org/10.1128/jvi.00036-18
Wang C, Wang C, Xu W, Zou J, Qiu Y, Kong J, Yang Y, Zhang B, Zhu S (2018b) Epigenetic changes in the regulation of Nicotiana tabacum response to cucumber mosaic virus infection and symptom recovery through single-base resolution methylomes. Viruses 10:402. https://doi.org/10.3390/v10080402
Yadav RK, Chattopadhyay D (2011) Enhanced viral intergenic region–specific short interfering RNA accumulation and DNA methylation correlates with resistance against a geminivirus. Mol Plant Microbe Interact 24:1189–1197
Yang LP, Fang YY, An CP, Dong L, Zhang ZH, Chen H, Xie Q, Guo HS (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. Plant J 73:910–917
Yang DL, Zhang G, Tang K, Li J, Yang L, Huang H, Zhang H, Zhu JK (2016a) Dicer-independent RNA-directed DNA methylation in Arabidopsis. Cell Res 26:1264. https://doi.org/10.1038/cr.2016.122
Yang L, Xu Y, Liu Y, Meng D, Jin T, Zhou X (2016b) HC-Pro viral suppressor from tobacco vein banding mosaic virus interferes with DNA methylation and activates the salicylic acid pathway. Virology 497:244–250
Ye R, Chen Z, Lian B, Rowley MJ, Xia N, Chai J, Li Y, He XJ, Wierzbicki AT, Qi Y (2016) A Dicer-independent route for biogenesis of siRNAs that direct DNA methylation in Arabidopsis. Mol Cell 61:222
Yong-Villalobos L, González-Morales SI, Wrobel K, Gutiérrez-Alanis D, Cervantes-Peréz SA, Hayano-Kanashiro C, Oropeza-Aburto A, Cruz-Ramírez A, Martínez O, Herrera-Estrella L (2015) Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc Natl Acad Sci 112:E7293–E7302
Yu A, Lepère G, Jay F, Wang J, Bapaume L, Wang Y, Abraham AL, Penterman J, Fischer RL, Voinnet O (2013) Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc Natl Acad Sci 110:2389–2394
Zemach A, Kim MY, Hsieh P-H, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153:193–205
Zhang H, Zhu J-K (2011) RNA-directed DNA methylation. Curr Opin Plant Biol 14:142–147
Zhang Z, Chen H, Huang X, Xia R, Zhao Q, Lai J, Teng K, Li Y, Liang L, Du Q (2011) BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23:273–288
Zhang H, Lang Z, Zhu J-K (2018) Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol 19:489–506
Zheng B, Wang Z, Li S, Yu B, Liu J-Y, Chen X (2009) Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev 23:2850–2860
Zhong S, Fei Z, Chen Y-R, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31:154
Zhong X, Du J, Hale CJ, Gallego-Bartolome J, Feng S, Vashisht AA, Chory J, Wohlschlegel JA, Patel DJ, Jacobsen SE (2014) Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157:1050–1060
Zhu QH, Shan WX, Ayliffe M, Wang MB (2015) Epigenetic mechanisms: an emerging player in plant–microbe interactions. Mol Plant Microbe Interact 29:187
Zhu P, Guo H, Ren Y, Hou Y, Dong J, Li R, Lian Y, Fan X, Hu B, Gao Y (2018) Single-cell DNA methylome sequencing of human preimplantation embryos. Nat Genet 50:12
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This study was funded by Basic Scientific Research Foundation of the Chinese Academy of Inspection and Quarantine (2018JK006).
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Wang, C., Wang, C., Zou, J. et al. Epigenetics in the plant–virus interaction. Plant Cell Rep 38, 1031–1038 (2019). https://doi.org/10.1007/s00299-019-02414-0
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DOI: https://doi.org/10.1007/s00299-019-02414-0