Active DNA demethylation regulates MAMP-triggered immune priming in Arabidopsis

Mengling Huang; Ying Zhang; Ying Wang; Jiatao Xie; Jiasen Cheng; Yanping Fu; Daohong Jiang; Xiao Yu; Bo Li

doi:10.1016/j.jgg.2022.02.021

Active DNA demethylation regulates MAMP-triggered immune priming in Arabidopsis

doi: 10.1016/j.jgg.2022.02.021

Mengling Huang^a,b,c,
Ying Zhang^a,b,c,
Ying Wang^a,b,c,
Jiatao Xie^a,b,c,
Jiasen Cheng^a,b,
Yanping Fu^b,
Daohong Jiang^a,b,c,
Xiao Yu^a,b,c,
Bo Li^a,b,c, ,

a. State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, Hubei 430070, China;
b. The Provincial Key Lab of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China;
c. Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China

基金项目:

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 &

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.

详细信息

通讯作者:
Bo Li,E-mail:boli@mail.hzau.edu.cn

计量
- 文章访问数: 44
- HTML全文浏览量: 32
- PDF下载量: 0
- 被引次数: 0
出版历程
- 收稿日期: 2021-10-03
- 修回日期: 2022-02-09
- 录用日期: 2022-02-15
- 网络出版日期: 2023-03-17

Active DNA demethylation regulates MAMP-triggered immune priming in Arabidopsis

Mengling Huang^a,b,c,
Ying Zhang^a,b,c,
Ying Wang^a,b,c,
Jiatao Xie^a,b,c,
Jiasen Cheng^a,b,
Yanping Fu^b,
Daohong Jiang^a,b,c,
Xiao Yu^a,b,c,
Bo Li^{a,b,c
, ,}

a. State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, Hubei 430070, China;
b. The Provincial Key Lab of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China;
c. Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China

Funds:

摘要

摘要: 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.
- Pattern-triggered immunity /
- Immune priming /
- Defense gene expression /
- DNA demethylation /
- Immune signal transduction
Abstract: 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.
- Pattern-triggered immunity /
- Immune priming /
- Defense gene expression /
- DNA demethylation /
- Immune signal transduction

HTML全文

参考文献(60)

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

施引文献

资源附件(0)

访问统计