BACKGROUND: Microbial-associated molecular patterns activate several MAP kinases, which are major regulators of the innate immune response in Arabidopsis thaliana that induce large-scale changes in gene expression. Here, we determine whether microbial-associated molecular pattern-triggered gene expression involves modifications at the chromatin level. RESULTS: Histone acetylation and deacetylation are major regulators of microbial-associated molecular pattern-triggered gene expression and implicate the histone deacetylase HD2B in the reprogramming of defence gene expression and innate immunity. The MAP kinase MPK3 directly interacts with and phosphorylates HD2B, thereby regulating the intra-nuclear compartmentalization and function of the histone deacetylase. CONCLUSIONS: By studying a number of gene loci that undergo microbial-associated molecular pattern-dependent activation or repression, our data reveal a mechanistic model for how protein kinase signaling directly impacts chromatin reprogramming in plant defense.

Center for Plant Molecular Biology University of Tübingen Auf der Morgenstelle 32 72076 Tübingen Germany

Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc Šlechtitelů 27 783 71 Olomouc Czech Republic

Division of Biological and Environmental Sciences and Engineering King Abdullah University of Science and Technology Thuwal 23955 6900 Saudi Arabia

Institute of Plant Sciences Paris Saclay CNRS INRA University Paris Sud University of Evry University Paris Diderot Sorbonne Paris Cite University of Paris Saclay Batiment 630 91405 Orsay France

Laboratory of Molecular Biology Wageningen University Droevendaalsesteeg 1 6708PB Wageningen The Netherlands

Plateforme Biopuces et séquençage IGBMC 1 rue Laurent Fries Parc d'Innovation 67400 Illkirch France

Zobrazit více v PubMed

Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693–705. doi: 10.1016/j.cell.2007.02.005. PubMed DOI

Mercer TR, Mattick JS. Understanding the regulatory and transcriptional complexity of the genome through structure. Genome Res. 2013;23(7):1081–108. doi: 10.1101/gr.156612.113. PubMed DOI PMC

Saze H, Tsugane K, Kanno T, Nishimura T. DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol. 2012;53:766–84. doi: 10.1093/pcp/pcs008. PubMed DOI

Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21(3):381–95. doi: 10.1038/cr.2011.22. PubMed DOI PMC

Bender J. RNA-directed DNA, methylation: getting a grip on mechanism. Curr Biol. 2012;22(10):R400–1. doi: 10.1016/j.cub.2012.04.010. PubMed DOI

Keller C, Kulasegaran-Shylini R, Shimada Y, Hotz HR, Buhler M. Noncoding RNAs prevent spreading of a repressive histone mark. Nat Struct Mol Biol. 2013;20(8):994–1000. doi: 10.1038/nsmb.2619. PubMed DOI

Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature. 2002;415:977–83. doi: 10.1038/415977a. PubMed DOI

Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, et al. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 2008;18(12):1190–8. doi: 10.1038/cr.2008.300. PubMed DOI

Bethke G, Pecher P, Eschen-Lippold L, Tsuda K, Katagiri F, Glazebrook J, et al. Activation of the Arabidopsis thaliana mitogen-activated protein kinase MPK11 by the flagellin-derived elicitor peptide, flg22. Mol Plant Microbe Interact. 2012;25:471–80. doi: 10.1094/MPMI-11-11-0281. PubMed DOI

Djamei A, Pitzschke A, Nakagami H, Rajh I, Hirt H. Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science. 2007;318:453–6. doi: 10.1126/science.1148110. PubMed DOI

Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu S, et al. The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J. 2005;24:2579–89. doi: 10.1038/sj.emboj.7600737. PubMed DOI PMC

Bethke G, Unthan T, Uhrig JF, Poschl Y, Gust AA, Scheel D, et al. Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci U S A. 2009;106:8067–72. doi: 10.1073/pnas.0810206106. PubMed DOI PMC

de la Fuente van Bentem S, Anrather D, Dohnal I, Roitinger E, Csaszar E, Joore J, et al. Site-specific phosphorylation profiling of Arabidopsis proteins by mass spectrometry and peptide chip analysis. J Proteome Res. 2008;7(6):2458–70. doi: 10.1021/pr8000173. PubMed DOI

Zhou C, Labbe H, Sridha S, Wang L, Tian L, Latoszek-Green M, et al. Expression and function of HD2-type histone deacetylases in Arabidopsis development. Plant J. 2004;38:715–24. doi: 10.1111/j.1365-313X.2004.02083.x. PubMed DOI

Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, et al. Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell. 2005;16(1):260–9. doi: 10.1091/mbc.E04-09-0791. PubMed DOI PMC

Frei dit Frey N, Garcia AV, Bigeard J, Zaag R, Bueso E, Garmier M, et al. Functional analysis of Arabidopsis immune-related MAPKs uncovers a role for MPK3 as negative regulator of inducible defences. Genome Biol. 2014;15(6):R87. doi: 10.1186/gb-2014-15-6-r87. PubMed DOI PMC

Ye T, Krebs AR, Choukrallah MA, Keime C, Plewniak F, Davidson I, et al. seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res. 2011;39(6):e35. doi: 10.1093/nar/gkq1287. PubMed DOI PMC

Pitzschke A, Djamei A, Teige M, Hirt H. VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression. Proc Natl Acad Sci U S A. 2009;106(43):18414–9. doi: 10.1073/pnas.0905599106. PubMed DOI PMC

Wang C, Gao F, Wu J, Dai J, Wei C, Li Y. Arabidopsis putative deacetylase AtSRT2 regulates basal defense by suppressing PAD4, EDS5 and SID2 expression. Plant Cell Physiol. 2010;51(8):1291–9. doi: 10.1093/pcp/pcq087. PubMed DOI PMC

Tian L, Fong MP, Wang JJ, Wei NE, Jiang H, Doerge RW, et al. Reversible histone acetylation and deacetylation mediate genome-wide, promoter-dependent and locus-specific changes in gene expression during plant development. Genetics. 2005;169(1):337–45. doi: 10.1534/genetics.104.033142. PubMed DOI PMC

Choi SM, Song HR, Han SK, Han M, Kim CY, Park J, et al. HDA19 is required for the repression of salicylic acid biosynthesis and salicylic acid-mediated defense responses in Arabidopsis. Plant J. 2012;71(1):135–46. doi: 10.1111/j.1365-313X.2012.04977.x. PubMed DOI

Kim KC, Lai Z, Fan B, Chen Z. Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell. 2008;20(9):2357–71. doi: 10.1105/tpc.107.055566. PubMed DOI PMC

Ding B, Bellizzi Mdel R, Ning Y, Meyers BC, Wang GL. HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell. 2012;24(9):3783–94. doi: 10.1105/tpc.112.101972. PubMed DOI PMC

Chen YJ, Wang YN, Chang WC. ERK2-mediated C-terminal serine phosphorylation of p300 is vital to the regulation of epidermal growth factor-induced keratin 16 gene expression. J Biol Chem. 2007;282:27215–28. doi: 10.1074/jbc.M700264200. PubMed DOI

Oya H, Yokoyama A, Yamaoka I, Fujiki R, Yonezawa M, Youn MY, et al. Phosphorylation of Williams syndrome transcription factor by MAPK induces a switching between two distinct chromatin remodeling complexes. J Biol Chem. 2009;284(47):32472–82. doi: 10.1074/jbc.M109.009738. PubMed DOI PMC

Dangl M, Brosch G, Haas H, Loidl P, Lusser A. Comparative analysis of HD2 type histone deacetylases in higher plants. Planta. 2001;213:280–5. doi: 10.1007/s004250000506. PubMed DOI

Wu K, Tian L, Zhou C, Brown D, Miki B. Repression of gene expression by Arabidopsis HD2 histone deacetylases. Plant J. 2003;34:241–7. doi: 10.1046/j.1365-313X.2003.01714.x. PubMed DOI

Bjerling P, Silverstein RA, Thon G, Caudy A, Grewal S, Ekwall K. Functional divergence between histone deacetylases in fission yeast by distinct cellular localization and in vivo specificity. Mol Cell Biol. 2002;22:2170–81. doi: 10.1128/MCB.22.7.2170-2181.2002. PubMed DOI PMC

Segre CV, Chiocca S. Regulating the regulators: the post-translational code of class I HDAC1 and HDAC2. J Biomed Biotechnol. 2011;2011:690848. doi: 10.1155/2011/690848. PubMed DOI PMC

Dequiedt F, Martin M, Von Blume J, Vertommen D, Lecomte E, Mari N, et al. New role for hPar-1 kinases EMK and C-TAK1 in regulating localization and activity of class IIa histone deacetylases. Mol Cell Biol. 2006;26(19):7086–102. doi: 10.1128/MCB.00231-06. PubMed DOI PMC

Sun JM, Chen HY, Moniwa M, Litchfield DW, Seto E, Davie JR. The transcriptional repressor Sp3 is associated with CK2-phosphorylated histone deacetylase 2. J Biol Chem. 2002;277(39):35783–6. doi: 10.1074/jbc.C200378200. PubMed DOI

Sun JM, Chen HY, Davie JR. Differential distribution of unmodified and phosphorylated histone deacetylase 2 in chromatin. J Biol Chem. 2007;282(45):33227–36. doi: 10.1074/jbc.M703549200. PubMed DOI

Wang Y, Curry HM, Zwilling BS, Lafuse WP. Mycobacteria inhibition of IFN-gamma induced HLA-DR gene expression by up-regulating histone deacetylation at the promoter region in human THP-1 monocytic cells. J Immunol. 2005;174(9):5687–94. doi: 10.4049/jimmunol.174.9.5687. PubMed DOI

Basu S, Pathak S, Pathak SK, Bhattacharyya A, Banerjee A, Kundu M, et al. Mycobacterium avium-induced matrix metalloproteinase-9 expression occurs in a cyclooxygenase-2-dependent manner and involves phosphorylation- and acetylation-dependent chromatin modification. Cell Microbiol. 2007;9(12):2804–16. doi: 10.1111/j.1462-5822.2007.00997.x. PubMed DOI

Garcia-Garcia JC, Barat NC, Trembley SJ, Dumler JS. Epigenetic silencing of host cell defense genes enhances intracellular survival of the rickettsial pathogen Anaplasma phagocytophilum. PLoS Pathog. 2009;5(6):e1000488. doi: 10.1371/journal.ppat.1000488. PubMed DOI PMC

Eskandarian HA, Impens F, Nahori MA, Soubigou G, Coppee JY, Cossart P, et al. A role for SIRT2-dependent histone H3K18 deacetylation in bacterial infection. Science. 2013;341(6145):1238858. doi: 10.1126/science.1238858. PubMed DOI

Kim JM, To TK, Nishioka T, Seki M. Chromatin regulation functions in plant abiotic stress responses. Plant Cell Environ. 2010;33:604–11. doi: 10.1111/j.1365-3040.2009.02076.x. PubMed DOI

Bourque S, Dutartre A, Hammoudi V, Blanc S, Dahan J, Jeandroz S, et al. Type-2 histone deacetylases as new regulators of elicitor-induced cell death in plants. New Phytol. 2011;192:127–39. doi: 10.1111/j.1469-8137.2011.03788.x. PubMed DOI

Waterborg JH. Dynamics of histone acetylation in Saccharomyces cerevisiae. Biochemistry. 2001;40:2599–605. doi: 10.1021/bi002480c. PubMed DOI

Scott I. Regulation of cellular homoeostasis by reversible lysine acetylation. Essays Biochem. 2012;52:13–22. doi: 10.1042/bse0520013. PubMed DOI

Sessions A, Burke E, Presting G, Aux G, McElver J, Patton D, et al. A high-throughput Arabidopsis reverse genetics system. Plant Cell. 2002;14:2985–94. doi: 10.1105/tpc.004630. PubMed DOI PMC

Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell. 2007;19:63–73. doi: 10.1105/tpc.106.048298. PubMed DOI PMC

Xiang C, Han P, Lutziger I, Wang K, Oliver DJ. A mini binary vector series for plant transformation. Plant Mol Biol. 1999;40:711–7. doi: 10.1023/A:1006201910593. PubMed DOI

Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735–43. doi: 10.1046/j.1365-313x.1998.00343.x. PubMed DOI

Karimi M, Inze D, Depicker A. GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 2002;7(5):193–5. doi: 10.1016/S1360-1385(02)02251-3. PubMed DOI

Stuitje AR, Verbree EC, van der Linden KH, Mietkiewska EM, Nap JP, Kneppers TJ. Seed-expressed fluorescent proteins as versatile tools for easy (co)transformation and high-throughput functional genomics in Arabidopsis. Plant Biotechnol J. 2003;1:301–9. doi: 10.1046/j.1467-7652.2003.00028.x. PubMed DOI

Bechtold N, Pelletier G. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol. 1998;82:259–66. PubMed

Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M, Qamar SA, et al. The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr Biol. 2007;17(13):1116–22. doi: 10.1016/j.cub.2007.05.046. PubMed DOI

Cardinale F, Jonak C, Ligterink W, Niehaus K, Boller T, Hirt H. Differential activation of four specific MAPK pathways by distinct elicitors. J Biol Chem. 2000;275(47):36734–40. doi: 10.1074/jbc.M007418200. PubMed DOI

Sauer M, Paciorek T, Benkova E, Friml J. Immunocytochemical techniques for whole-mount in situ protein localization in plants. Nat Protoc. 2006;1(1):98–103. doi: 10.1038/nprot.2006.15. PubMed DOI

Azimzadeh J, Nacry P, Christodoulidou A, Drevensek S, Camilleri C, Amiour N, Parcy F, Pastuglia M, Bouchez D. Arabidopsis TONNEAU1 Proteins Are Essential for Preprophase Band Formation and Interact with Centrin. THE PLANT CELL ONLINE. 2008;20(8):2146–2159. PubMed PMC

Colcombet J, Lopez-Obando M, Heurtevin L, Bernard C, Martin K, Berthomé R, Lurin C. Systematic study of subcellular localization of Arabidopsis PPR proteins confirms a massive targeting to organelles. RNA Biology. 2014;10(9):1557–1575. PubMed PMC

Nakagami H, Soukupová H, Schikora A, Zárský V, Hirt H. A Mitogenactivated Protein Kinase Kinase Kinase Mediates Reactive Oxygen Species Homeostasis in . Journal of Biological Chemistry. 2006;281(50):38697–38704. PubMed

Cardinale F, Meskiene I, Ouaked F, Hirt H. Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases. Plant Cell. 2002;14:703–11. doi: 10.1105/tpc.010256. PubMed DOI PMC

Du Z, Zhou X, Ling Y, Zhang Z, Su Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 2010;8:W64–70. doi: 10.1093/nar/gkq310. PubMed DOI PMC

Gendrel AV, Lippman Z, Martienssen R, Colot V. Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods. 2005;2:213–8. doi: 10.1038/nmeth0305-213. PubMed DOI

Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25. doi: 10.1186/gb-2009-10-3-r25. PubMed DOI PMC

Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, et al. Model-based analysis of ChIP-Seq (MACS) Genome Biol. 2008;9:R137. doi: 10.1186/gb-2008-9-9-r137. PubMed DOI PMC

Krebs A, Frontini M, Tora L, GPAT: Retrieval of genomic annotation from large genomic position datasets. BMC Bioinformatics. 2008;9(1):533. PubMed PMC

Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertie L, et al. Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinf. 2008;2008:420747. doi: 10.1155/2008/420747. PubMed DOI PMC

Biochemical and Genetic Interactions of Phospholipase D Alpha 1 and Mitogen-Activated Protein Kinase 3 Affect Arabidopsis Stress Response

Genome-wide transcriptome profiling of transgenic hop (Humulus lupulus L.) constitutively overexpressing HlWRKY1 and HlWDR1 transcription factors