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Volume 49 Issue 8
Aug.  2022
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Article Contents

Active DNA demethylation regulates MAMP-triggered immune priming in Arabidopsis

doi: 10.1016/j.jgg.2022.02.021
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Technological Self-innovation Foundation (2021ZKPY011, 2017RC001 to B.L.). We thank Dr. Chengguo Duan for sharing the hdp2-2 and rdd-2 mutant seeds and Dr. Qing Li and Dr. Guoliang Li for the help of methylation data analysis. We thank Dr. Wei Chen and Huanran Yin for the hormone measurement. We are grateful to Dr. Kenichi Tsuda, Dr. Ping He, and Dr. Libo Shan for critical reading and constructive suggestions on the manuscript.

This research was supported by the National Natural Science Foundation of China (31770278, 31970125 to B.L.), Fundamental Research Funds for the Central Universities, Huazhong Agricultural University Scientific &

  • Received Date: 2021-10-03
  • Accepted Date: 2022-02-15
  • Rev Recd Date: 2022-02-09
  • Publish Date: 2022-03-12
  • Plants recognize microbe-associated molecular patterns (MAMPs) to activate immune responses and defense priming to defend against pathogen infections. Transcriptional regulation of gene expression is crucial for plant immunity and is mediated by multiple factors, including DNA methylation. However, it remains unknown whether and how DNA demethylation contributes to immune responses in MAMP-triggered immunity. Here, we report that active DNA demethylation is required for MAMP-triggered immunity to bacterial pathogens. The rdd-2 triple mutant carrying mutations in ROS1, DML2, and DML3 that encode DNA glycosylases, which are key DNA demethylation enzymes, exhibits compromised immune responses triggered by the MAMPs flg22 and elf18. Genome-wide methylome analysis reveals that flg22 induces rapid and specific DNA demethylation in an RDD-dependent manner. The expression levels of salicylic acid signaling-related and phytoalexin biosynthesis-related genes are tightly associated with the flg22-induced promoter demethylation. The compromised accumulation of priming compounds and antimicrobial metabolites ultimately leads to a defense priming defect in the rdd-2 mutant. Our results reveal the critical role of active DNA demethylation in the MAMP-triggered immune response and provide unique insight into the molecular mechanism of flg22-modulated DNA demethylation.
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  • Atighi, M.R., Verstraeten, B., De Meyer, T.,Kyndt, T., 2020. Genome-wide DNA hypomethylation shapes nematode pattern-triggered immunity in plants. The New phytologist 227, 545-558
    Barnett, D.W., Garrison, E.K., Quinlan, A.R., Stromberg, M.P.,Marth, G.T., 2011. Bamtools:A c++ api and toolkit for analyzing and managing bam files. Bioinformatics 27, 1691-1692
    Bjornson, M., Pimprikar, P., Nurnberger, T.,Zipfel, C., 2021. The transcriptional landscape of Arabidopsis thaliana pattern-triggered immunity. Nature plants
    Buscaill, P.,Rivas, S., 2014. Transcriptional control of plant defence responses. Curr Opin Plant Biol 20, 35-46
    Chen, C., Chen, H., Zhang, Y., Thomas, H.R., Frank, M.H., He, Y.,Xia, R., 2020. Tbtools:An integrative toolkit developed for interactive analyses of big biological data. Molecular plant 13, 1194-1202
    Cokus, S.J., Feng, S., Zhang, X., Chen, Z., Merriman, B., Haudenschild, C.D., Pradhan, S., Nelson, S.F., Pellegrini, M.,Jacobsen, S.E., 2008. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215-219
    Couto, D.,Zipfel, C., 2016. Regulation of pattern recognition receptor signalling in plants. Nature reviews Immunology 16, 537-552
    Deleris, A., Halter, T.,Navarro, L., 2016. DNA methylation and demethylation in plant immunity. Annual review of phytopathology 54, 579-603
    Dodds, P.N.,Rathjen, J.P., 2010. Plant immunity:Towards an integrated view of plant-pathogen interactions. Nature reviews Genetics 11, 539-548
    Dowen, R.H., Pelizzola, M., Schmitz, R.J., Lister, R., Dowen, J.M., Nery, J.R., Dixon, J.E.,Ecker, J.R., 2012. Widespread dynamic DNA methylation in response to biotic stress. Proceedings of the National Academy of Sciences of the United States of America 109, E2183-2191
    Duan, C.G., Wang, X., Xie, S., Pan, L., Miki, D., Tang, K., Hsu, C.C., Lei, M., Zhong, Y., Hou, Y.J., et al., 2017. A pair of transposon-derived proteins function in a histone acetyltransferase complex for active DNA demethylation. Cell research 27, 226-240
    Feng, H., Conneely, K.N.,Wu, H., 2014. A bayesian hierarchical model to detect differentially methylated loci from single nucleotide resolution sequencing data. Nucleic Acids Res 42
    Halter, T., Wang, J., Amesefe, D., Lastrucci, E., Charvin, M., Singla Rastogi, M.,Navarro, L., 2021. The Arabidopsis active demethylase ros1 cis-regulates defence genes by erasing DNA methylation at promoter-regulatory regions. eLife 10
    Harris, C.J., Scheibe, M., Wongpalee, S.P., Liu, W.L., Cornett, E.M., Vaughan, R.M., Li, X.Q., Chen, W., Xue, Y., Zhong, Z.H., et al., 2018. A DNA methylation reader complex that enhances gene transcription. Science 362, 1182-+
    Hillmer, R.A., Tsuda, K., Rallapalli, G., Asai, S., Truman, W., Papke, M.D., Sakakibara, H., Jones, J.D.G., Myers, C.L.,Katagiri, F., 2017. The highly buffered Arabidopsis immune signaling network conceals the functions of its components. Plos Genet 13
    Huang, H., Liu, R.E., Niu, Q.F., Tang, K., Zhang, B., Zhang, H., Chen, K.S., Zhu, J.K.,Lang, Z.B., 2019. Global increase in DNA methylation during orange fruit development and ripening. Proceedings of the National Academy of Sciences of the United States of America 116, 1430-1436
    Jiang, J., Liu, J., Sanders, D., Qian, S., Ren, W., Song, J., Liu, F.,Zhong, X., 2021. Uvr8 interacts with de novo DNA methyltransferase and suppresses DNA methylation in Arabidopsis. Nature plants 7, 184-197
    Kaplan-Levy, R.N., Brewer, P.B., Quon, T.,Smyth, D.R., 2012. The trihelix family of transcription factors——light, stress and development. Trends in plant science 17, 163-171
    Kim, D., Landmead, B.,Salzberg, S.L., 2015. Hisat:A fast spliced aligner with low memory requirements. Nat Methods 12, 357-U121
    Kim, Y., Tsuda, K., Igarashi, D., Hillmer, R.A., Sakakibara, H., Myers, C.L.,Katagiri, F., 2014. Mechanisms underlying robustness and tunability in a plant immune signaling network. Cell Host Microbe 15, 84-94
    Lang, Z., Wang, Y., Tang, K., Tang, D., Datsenka, T., Cheng, J., Zhang, Y., Handa, A.K.,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. Proceedings of the National Academy of Sciences of the United States of America 114, E4511-E4519
    Le, T.N., Schumann, U., Smith, N.A., Tiwari, S., Au, P.C., Zhu, Q.H., Taylor, J.M., Kazan, K., Llewellyn, D.J., Zhang, R., et al., 2014. DNA demethylases target promoter transposable elements to positively regulate stress responsive genes in Arabidopsis. Genome biology 15, 458
    Lee, S., Fu, F., Xu, S., Lee, S.Y., Yun, D.J.,Mengiste, T., 2016. Global regulation of plant immunity by histone lysine methyl transferases. The Plant cell 28, 1640-1661
    Lewis, L.A., Polanski, K., de Torres-Zabala, M., Jayaraman, S., Bowden, L., Moore, J., Penfold, C.A., Jenkins, D.J., Hill, C., Baxter, L., et al., 2015. Transcriptional dynamics driving mamp-triggered immunity and pathogen effector-mediated immunosuppression in Arabidopsis leaves following infection with pseudomonas syringae pv tomato dc3000. The Plant cell 27, 3038-3064
    Li, B., Jiang, S., Yu, X., Cheng, C., Chen, S., Cheng, Y., Yuan, J.S., Jiang, D., He, P.,Shan, L., 2015. Phosphorylation of trihelix transcriptional repressor asr3 by map kinase4 negatively regulates Arabidopsis immunity. The Plant cell 27, 839-856
    Li, B., Meng, X., Shan, L.,He, P., 2016. Transcriptional regulation of pattern-triggered immunity in plants. Cell Host Microbe 19, 641-650
    Li, F., Cheng, C., Cui, F., de Oliveira, M.V., Yu, X., Meng, X., Intorne, A.C., Babilonia, K., Li, M., Li, B., et al., 2014. Modulation of rna polymerase ii phosphorylation downstream of pathogen perception orchestrates plant immunity. Cell host & microbe 16, 748-758
    Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R.,Proc, G.P.D., 2009. The sequence alignment/map format and samtools. Bioinformatics 25, 2078-2079
    Li, Y.X.,Li, W., 2009. Bsmap:Whole genome bisulfite sequence mapping program. Bmc Bioinformatics 10
    Liao, Y., Smyth, G.K.,Shi, W., 2014. Featurecounts:An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930
    Liu, R.,Lang, Z., 2020. The mechanism and function of active DNA demethylation in plants. Journal of integrative plant biology 62, 148-159
    Lopez Sanchez, A., Stassen, J.H., Furci, L., Smith, L.M.,Ton, J., 2016. The role of DNA (de)methylation in immune responsiveness of Arabidopsis. The Plant journal:for cell and molecular biology 88, 361-374
    Love, M.I., Huber, W.,Anders, S., 2014. Moderated estimation of fold change and dispersion for rna-seq data with deseq2. Genome biology 15
    Luo, C.Y., Hajkova, P.,Ecker, J.R., 2018. Dynamic DNA methylation:In the right place at the right time. Science 361, 1336-1340
    Mauch-Mani, B., Baccelli, I., Luna, E.,Flors, V., 2017. Defense priming:An adaptive part of induced resistance. Annual Review of Plant Biology, Vol 68 68, 485-512
    Mohnike, L., Rekhter, D., Huang, W., Feussner, K., Tian, H., Herrfurth, C., Zhang, Y.,Feussner, I., 2021. The glycosyltransferase ugt76b1 modulates n-hydroxy-pipecolic acid homeostasis and plant immunity. The Plant cell
    Moore, J.W., Loake, G.J.,Spoel, S.H., 2011. Transcription dynamics in plant immunity. The Plant cell 23, 2809-2820
    Navarro, L., Zipfel, C., Rowland, O., Keller, I., Robatzek, S., Boller, T.,Jones, J.D., 2004. The transcriptional innate immune response to flg22. Interplay and overlap with avr gene-dependent defense responses and bacterial pathogenesis. Plant physiology 135, 1113-1128
    Nie, W.F., Lei, M., Zhang, M., Tang, K., Huang, H., Zhang, C., Miki, D., Liu, P., Yang, Y., Wang, X., et al., 2019. Histone acetylation recruits the swr1 complex to regulate active DNA demethylation in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 116, 16641-16650
    Noutoshi, Y., Okazaki, M., Kida, T., Nishina, Y., Morishita, Y., Ogawa, T., Suzuki, H., Shibata, D., Jikumaru, Y., Hanada, A., et al., 2012. Novel plant immune-priming compounds identified via high-throughput chemical screening target salicylic acid glucosyltransferases in Arabidopsis. The Plant cell 24, 3795-3804
    Pandey, S.P.,Somssich, I.E., 2009. The role of wrky transcription factors in plant immunity. Plant physiology 150, 1648-1655
    Pavet, V., Quintero, C., Cecchini, N.M., Rosa, A.L.,Alvarez, M.E., 2006. Arabidopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by pseudomonas syringae. Mol Plant Microbe In 19, 577-587
    Piasecka, A., Jedrzejczak-Rey, N.,Bednarek, P., 2015. Secondary metabolites in plant innate immunity:Conserved function of divergent chemicals. The New phytologist 206, 948-964
    Rajniak, J., Barco, B., Clay, N.K.,Sattely, E.S., 2015. A new cyanogenic metabolite in Arabidopsis required for inducible pathogen defence. Nature 525, 376-379
    Ramirez-Prado, J.S., Abulfaraj, A.A., Rayapuram, N., Benhamed, M.,Hirt, H., 2018. Plant immunity:From signaling to epigenetic control of defense. Trends in plant science 23, 833-844
    Tang, K., Lang, Z., Zhang, H.,Zhu, J.K., 2016. The DNA demethylase ros1 targets genomic regions with distinct chromatin modifications. Nature plants 2, 16169
    Tian, H., Wu, Z., Chen, S., Ao, K., Huang, W., Yaghmaiean, H., Sun, T., Xu, F., Zhang, Y., Wang, S., et al., 2021. Activation of tir signalling boosts pattern-triggered immunity. Nature 598, 500-503
    Tian, T., Liu, Y., Yan, H.Y., You, Q., Yi, X., Du, Z., Xu, W.Y.,Su, Z., 2017. Agrigo v2.0:A go analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res 45, W122-W129
    Tsuda, K., Sato, M., Stoddard, T., Glazebrook, J.,Katagiri, F., 2009. Network properties of robust immunity in plants. Plos Genet 5
    Tsuda, K.,Somssich, I.E., 2015. Transcriptional networks in plant immunity. The New phytologist 206, 932-947
    Vilchez, J.I., Yang, Y., He, D., Zi, H., Peng, L., Lv, S., Kaushal, R., Wang, W., Huang, W., Liu, R., et al., 2020. DNA demethylases are required for myo-inositol-mediated mutualism between plants and beneficial rhizobacteria. Nature plants
    Volz, R., Kim, S.K., Mi, J., Mariappan, K.G., Guo, X., Bigeard, J., Alejandro, S., Pflieger, D., Rayapuram, N., Al-Babili, S., et al., 2018. The trihelix transcription factor gt2-like 1 (gtl1) promotes salicylic acid metabolism, and regulates bacterial-triggered immunity. PLoS Genet 14, e1007708
    Yu, A., Lepere, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., Abraham, A.L., Penterman, J., Fischer, R.L., Voinnet, O., et al., 2013. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proceedings of the National Academy of Sciences of the United States of America 110, 2389-2394
    Yu, X., Feng, B.M., He, P.,Shan, L.B., 2017. From chaos to harmony:Responses and signaling upon microbial pattern recognition. Annual Review of Phytopathology, Vol 55 55, 109-137
    Zeng, W., Huang, H., Lin, X., Zhu, C., Kosami, K.I., Huang, C., Zhang, H., Duan, C.G., Zhu, J.K.,Miki, D., 2021. Roles of demeter in regulating DNA methylation in vegetative tissues and pathogen resistance. Journal of integrative plant biology 63, 691-706
    Zhang, H., Lang, Z.,Zhu, J.K., 2018. Dynamics and function of DNA methylation in plants. Nature reviews Molecular cell biology 19, 489-506
    Zhang, F., Wang, L., Qi, B., Zhao, B., Ko, E.E., Riggan, N.D., Chin, K.,Qiao, H., 2017. Ein2 mediates direct regulation of histone acetylation in the ethylene response. Proceedings of the National Academy of Sciences 114, 10274-10279
    Zhao, K., Kong, D., Jin, B., Smolke, C.D.,Rhee, S.Y., 2021. A novel form of bivalent chromatin associates with rapid induction of camalexin biosynthesis genes in response to a pathogen signal in Arabidopsis. eLife 10
    Zhou, Q.W., Lim, J.Q., Sung, W.K.,Li, G.L., 2019. An integrated package for bisulfite DNA methylation data analysis with indel-sensitive mapping. Bmc Bioinformatics 20
    Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E.J., Jones, J.D.G., Felix, G.,Boller, T., 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764-767
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