Abstract
DNA methylation is a dynamic and reversible type of epigenetic mark that contributes to cellular physiology by affecting transcription activity, transposon mobility and genome stability. When plants are infected with pathogens, plant DNA methylation patterns can change, indicating an epigenetic interplay between plant host and pathogen. In most cases methylation can change susceptibility. While DNA hypomethylation appears to be a common phenomenon during the susceptible interaction, the levels and patterns of hypomethylation in transposable elements and genic regions may mediate distinct responses against various plant pathogens. The effect of DNA methylation on the plant immune response and other cellular activities and molecular functions is established by localized differential DNA methylation via cis-regulatory mechanisms as well as through trans-acting mechanisms. Understanding the epigenetic differences that control the phenotypic variations between susceptible and resistant interactions should facilitate the identification of new sources of resistance mediated by epigenetic mechanisms, which can be exploited to endow pathogen resistance to crops.
Similar content being viewed by others
References
Baulcombe DC, Dean C (2014) Epigenetic regulation in plant responses to the environment. Cold Spring Harb Perspect Biol 6:a019471
Brough CL, Gardiner WE, Inamdar NM, Zhang XY, 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 USA 111:12942–12947
Cao X, Aufsatz W, Zilberman D, Mette MF, Huang MS, Matzke M, Jacobsen SE (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 13:2212–2217
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 Sc USA 109:E2183–2191
Du JM, Johnson LM, Jacobsen SE, Patel DJ (2015) DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol 16:519–532
Gaudinier A, Brady SM (2016) Mapping transcriptional networks in plants: data-driven discovery of novel biological mechanisms. Annu Rev Plant Biol 67:575–594
He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62:411–435
Hewezi T (2015) Cellular signaling pathways and posttranslational modifications mediated by nematode effector proteins. Plant Physiol 169:1018–1026
Hewezi T, Baum TJ (2015) Gene silencing in nematode feeding sites. In: Escobar C, Fenoll C (eds) Advances in botanical research. Elsevier BV, Oxford, UK, pp 221–239
Hewezi T, Howe P, Maier TR, Baum TJ (2008) Arabidopsis small RNAs and their targets during cyst nematode parasitism. Mol Plant Microb Interact 21:1622–1634
Hewezi T, Maier TR, Nettleton D, Baum TJ (2012) The Arabidopsis microRNA396-GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection. Plant Physiol 159:321–335
Hewezi T, Piya S, Qi M, Balasubramaniam M, Rice JH, Baum TJ (2016) Arabidopsis miR827 mediates post-transcriptional gene silencing of its ubiquitin E3 ligase target gene in the syncytium of the cyst nematode Heterodera schachtii to enhance susceptibility. Plant J 88:179–192
Hewezi T, Lane T, Piya S, Rambani A, Rice JH, Staton M (2017) Cyst nematode parasitism induces dynamic changes in the root epigenome. Plant Physiol 174:405–420
Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052
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
Kondrashov FA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc Biol Sci 279:5048–5057
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220
Le T-N, Schumann U, Smith NA, Tiwari S, Au P, Zhu Q-H, Taylor J, Kazan K, Llewellyn DJ, Zhang R, Dennis ES, Wang M-B (2014) DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis. Genome Biol 15:458
Li XY, Wang X, Zhang SP, Liu DW, Duan YX, Dong W (2012) Identification of soybean microRNAs involved in soybean cyst nematode infection by deep sequencing. PLoS One 7(6):e39650
Liu J, Chen N, Grant JN, Cheng ZM, Stewart CN Jr, Hewezi T (2015) Soybean kinome: functional classification and gene expression patterns. J Exp Bot 66:1919–1934
López Sánchez A, Stassen JHM, Furci L, Smith LM, Ton J (2016) The role of DNA (de)methylation in immune responsiveness of Arabidopsis. Plant J 88:361–374
Lv DQ, Liu SW, Zhao JH, Zhou BJ, Wang SP, Guo HS, Fang YY (2016) Replication of a pathogenic non-coding RNA increases DNA methylation in plants associated with a bromodomain-containing viroid-binding protein. Sci Rep 6:35751
Martinez G, Castellano M, Tortosa M, Pallas V, Gomez G (2014) A pathogenic non-coding RNA induces changes in dynamic DNA methylation of ribosomal RNA genes in host plants. Nucl Acids Res 42:1553–1562
Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408
Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJM (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21:367–376
Pavet V, Quintero C, Cecchini NM, Rosa AL, Alvarez ME (2006) Arabidopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by pseudomonas syringae. Mol Plant Microb Interact 19:577–587
Penterman J, Uzawa R, Fischer RL (2007) Genetic interactions between DNA demethylation and methylation in Arabidopsis. Plant Physiol 145:1549–1557
Piya S, Kihm C, Rice JH, Baum TJ, Hewezi T (2017) Cooperative regulatory functions of miR858 and MYB83 during cyst nematode parasitism. Plant Physiol 174:1897–1912
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
Rambani A, Rice JH, Liu J, Lane T, Ranjan P, Mazarei M, Pantalone V, Stewart CN, Staton M, Hewezi T (2015) The methylome of soybean roots during the compatible interaction with the soybean cyst nematode. Plant Physiol 168:1364–1377
Regulski M, Lu Z, Kendall J, Donoghue MTA, Reinders J, Llaca V, Deschamps S, Smith A, Levy D, McCombie WR, Tingey S, Rafalski A, Hicks J, Ware D, Martienssen RA (2013) The maize methylome influences mRNA splice sites and reveals widespread paramutation-like switches guided by small RNA. Genome Res 23:1651–1662
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. N Phytol 199:464–475
Satge C, Moreau S, Sallet E, Lefort G, Auriac MC, Rembliere C, Cottret L, Gallardo K, Noirot C, Jardinaud MF, Gamas P (2016) Reprogramming of DNA methylation is critical for nodule development in Medicago truncatula. Nat Plants 2. doi: 10.1038/NPLANTS.2016.1166
Secco D, Wang C, Shou H, Schultz MD, Chiarenza S, Nussaume L, Ecker JR, Whelan J, Lister R (2015) Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 4:e09343
Takuno S, Gaut BS (2011) Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol Biol Evol 29:219–227
Wang H, Hao L, Shung CY, 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 MB, Masuta C, Smith NA, Shimura H (2012) RNA silencing and plant viral diseases. Mol Plant Microb Interact 25:1275–1285
Wassenegger M, Heimes S, Riedel L, Sanger HL (1994) RNA-directed de novo methylation of genomic sequences in plants. Cell 76:567–576
Wibowo A, Becker C, Marconi G, Durr J, Price J, Hagmann J, Papareddy R, Putra H, Kageyama J, Becker J et al (2016) Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. eLife 5:e13546
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 USA 112:E7293–E7302
Yu A, Lepere G, Jay F, Wang J, Bapaume L, Wang Y, Abraham AL, Penterman J, Fischer RL, Voinnet O, Navarro L (2013) Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc Natl Acad Sc USA 110:2389–2394
Zhang Z, Chen H, Huang X, Xia R, Zhao Q, Lai J, Teng K, Li Y, Liang L, Du Q, Zhou X, Guo H, Xie Q (2011) BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23:273–288
Zhao JH, Fang YY, Duan CG, Fang RX, Ding SW, Guo HS (2016) Genome-wide identification of endogenous RNA-directed DNA methylation loci associated with abundant 21-nucleotide siRNAs in Arabidopsis. Sci Rep 6:36247
Zhu J-K (2009) Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43:143–166
Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2006) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69
Acknowledgements
Work in the Hewezi laboratory on epigenetics was funded by the Tennessee Soybean Promotion Board, the University of Tennessee Institute of Agriculture, and the National Science Foundation Program (Award#: IOS-1145053).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Vibha Srivastava.
Rights and permissions
About this article
Cite this article
Hewezi, T., Pantalone, V., Bennett, M. et al. Phytopathogen-induced changes to plant methylomes. Plant Cell Rep 37, 17–23 (2018). https://doi.org/10.1007/s00299-017-2188-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-017-2188-y