Nuclear envelope dynamics in connection to chromatin remodeling.

The nucleus is a central organelle of eukaryotic cells undergoing dynamic structural changes during cellular fundamental processes such as proliferation and differentiation. These changes rely on the integration of developmental and stress signals at the nuclear envelope (NE), orchestrating responses at the nucleo-cytoplasmic interface for efficient genomic functions such as DNA transcription, replication and repair. While in animals, correlation has already been established between NE dynamics and chromatin remodeling using last-generation tools and cutting-edge technologies, this topic is just emerging in plants, especially in response to mechanical cues. This review summarizes recent data obtained in this field with more emphasis on the mechanical stress response. It also highlights similarities/differences between animal and plant cells at multiples scales, from the structural organization of the nucleo-cytoplasmic continuum to the functional impacts of NE dynamics.

Lysine 27 of histone H3.3 is a fine modulator of developmental gene expression and stands as an epigenetic checkpoint for lignin biosynthesis in Arabidopsis.

Chromatin is a dynamic platform within which gene expression is controlled by epigenetic modifications, notably targeting amino acid residues of histone H3. Among them is lysine 27 of H3 (H3K27), the trimethylation of which by the Polycomb Repressive Complex 2 (PRC2) is instrumental in regulating spatiotemporal patterns of key developmental genes. H3K27 is also subjected to acetylation and is found at sites of active transcription. Most information on the function of histone residues and their associated modifications in plants was obtained from studies of loss-of-function mutants for the complexes that modify them. To decrypt the genuine function of H3K27, we expressed a non-modifiable variant of H3 at residue K27 (H3.3K27A ) in Arabidopsis, and developed a multi-scale approach combining in-depth phenotypical and cytological analyses, with transcriptomics and metabolomics. We uncovered that the H3.3K27A variant causes severe developmental defects, part of them are reminiscent of PRC2 mutants, part of them are new. They include early flowering, increased callus formation and short stems with thicker xylem cell layer. This latest phenotype correlates with mis-regulation of phenylpropanoid biosynthesis. Overall, our results reveal novel roles of H3K27 in plant cell fates and metabolic pathways, and highlight an epigenetic control point for elongation and lignin composition of the stem.

TOR represses stress responses through global regulation of H3K27 trimethylation in plants.

Target of rapamycin (TOR) functions as a central sensory hub linking a wide range of external stimuli to gene expression. The mechanisms underlying stimulus-specific transcriptional reprogramming by TOR remain elusive. Here, we describe an in silico analysis in Arabidopsis demonstrating that TOR-repressed genes are associated with either bistable or silent chromatin states. Both states regulated by the TOR signaling pathway are associated with a high level of histone H3K27 trimethylation (H3K27me3) deposited by CURLY LEAF in a specific context with LIKE HETEROCHROMATIN PROTEIN1. The combination of the two epigenetic histone modifications H3K4me3 and H3K27me3 implicates a bistable feature that alternates between an 'on' and an 'off' state, allowing rapid transcriptional changes upon external stimuli. The chromatin remodeler SWI2/SNF2 ATPase BRAHMA activates TOR-repressed genes only at bistable chromatin domains to rapidly induce biotic stress responses. Here, we demonstrate both in silico and in vivo that TOR represses transcriptional stress responses through global maintenance of H3K27me3.

Epigenetic silencing of clustered tRNA genes in Arabidopsis.

Beyond their key role in translation, cytosolic transfer RNAs (tRNAs) are involved in a wide range of other biological processes. Nuclear tRNA genes (tDNAs) are transcribed by the RNA polymerase III (RNAP III) and cis-elements, trans-factors as well as genomic features are known to influence their expression. In Arabidopsis, besides a predominant population of dispersed tDNAs spread along the 5 chromosomes, some clustered tDNAs have been identified. Here, we demonstrate that these tDNA clusters are transcriptionally silent and that pathways involved in the maintenance of DNA methylation play a predominant role in their repression. Moreover, we show that clustered tDNAs exhibit repressive chromatin features whilst their dispersed counterparts contain permissive euchromatic marks. This work demonstrates that both genomic and epigenomic contexts are key players in the regulation of tDNAs transcription. The conservation of most of these regulatory processes suggests that this pioneering work in Arabidopsis can provide new insights into the regulation of RNA Pol III transcription in other organisms, including vertebrates.

Chromatin Manipulation and Editing: Challenges, New Technologies and Their Use in Plants.

An ongoing challenge in functional epigenomics is to develop tools for precise manipulation of epigenetic marks. These tools would allow moving from correlation-based to causal-based findings, a necessary step to reach conclusions on mechanistic principles. In this review, we describe and discuss the advantages and limits of tools and technologies developed to impact epigenetic marks, and which could be employed to study their direct effect on nuclear and chromatin structure, on transcription, and their further genuine role in plant cell fate and development. On one hand, epigenome-wide approaches include drug inhibitors for chromatin modifiers or readers, nanobodies against histone marks or lines expressing modified histones or mutant chromatin effectors. On the other hand, locus-specific approaches consist in targeting precise regions on the chromatin, with engineered proteins able to modify epigenetic marks. Early systems use effectors in fusion with protein domains that recognize a specific DNA sequence (Zinc Finger or TALEs), while the more recent dCas9 approach operates through RNA-DNA interaction, thereby providing more flexibility and modularity for tool designs. Current developments of "second generation", chimeric dCas9 systems, aiming at better targeting efficiency and modifier capacity have recently been tested in plants and provided promising results. Finally, recent proof-of-concept studies forecast even finer tools, such as inducible/switchable systems, that will allow temporal analyses of the molecular events that follow a change in a specific chromatin mark.

Interactive and noninteractive roles of histone H2B monoubiquitination and H3K36 methylation in the regulation of active gene transcription and control of plant growth and development.

Covalent modifications of histones are essential to control a wide range of processes during development and adaptation to environmental changes. With the establishment of reference epigenomes, patterns of histone modifications were correlated with transcriptionally active or silenced genes. These patterns imply the need for the precise and dynamic coordination of different histone-modifying enzymes to control transcription at a given gene. Classically, the influence of these enzymes on gene expression is examined separately and their interplays rarely established. In Arabidopsis, HISTONE MONOUBIQUITINATION2 (HUB2) mediates H2B monoubiquitination (H2Bub1), whereas SET DOMAIN GROUP8 (SDG8) catalyzes H3 lysine 36 trimethylation (H3K36me3). In this work, we crossed hub2 with sdg8 mutants to elucidate their functional relationships. Despite similar phenotypic defects, sdg8 and hub2 mutations broadly affect genome transcription and plant growth and development synergistically. Also, whereas H3K4 methylation appears largely dependent on H2Bub1, H3K36me3 and H2Bub1 modifications mutually reinforce each other at some flowering time genes. In addition, SDG8 and HUB2 jointly antagonize the increase of the H3K27me3 repressive mark. Collectively, our data provide an important insight into the interplay between histone marks and highlight their interactive complexity in regulating chromatin landscape which might be necessary to fine-tune transcription and ensure plant developmental plasticity.

Arabidopsis MZT1 homologs GIP1 and GIP2 are essential for centromere architecture.

Centromeres play a pivotal role in maintaining genome integrity by facilitating the recruitment of kinetochore and sister-chromatid cohesion proteins, both required for correct chromosome segregation. Centromeres are epigenetically specified by the presence of the histone H3 variant (CENH3). In this study, we investigate the role of the highly conserved γ-tubulin complex protein 3-interacting proteins (GIPs) in Arabidopsis centromere regulation. We show that GIPs form a complex with CENH3 in cycling cells. GIP depletion in the gip1gip2 knockdown mutant leads to a decreased CENH3 level at centromeres, despite a higher level of Mis18BP1/KNL2 present at both centromeric and ectopic sites. We thus postulate that GIPs are required to ensure CENH3 deposition and/or maintenance at centromeres. In addition, the recruitment at the centromere of other proteins such as the CENP-C kinetochore component and the cohesin subunit SMC3 is impaired in gip1gip2. These defects in centromere architecture result in aneuploidy due to severely altered centromeric cohesion. Altogether, we ascribe a central function to GIPs for the proper recruitment and/or stabilization of centromeric proteins essential in the specification of the centromere identity, as well as for centromeric cohesion in somatic cells.

Interplay of the histone methyltransferases SDG8 and SDG26 in the regulation of transcription and plant flowering and development.

Histone methylations play fundamental roles in epigenetic regulation of transcription in many eukaryotes. In the model plant Arabidopsis thaliana as in human, a same histone lysine residue (e.g. H3K4 or H3K36) can be a potential target substrate for various different histone lysine methyltransferases (HKMTs). Using powerful genetic tool in Arabidopsis, we here investigate the interplay between two close HKMT homologues, SET DOMAIN GROUP 8 (SDG8) and SDG26, in regulating transcription and plant growth and development. We show that the sdg8 mutation is epistatic to the sdg26 one, leading to a sdg8 sdg26 double mutant exhibiting defects similar to sdg8 (reduced level of H3K36me3, increased level of H3K36me1, reduced plant body size, early flowering associated with reduced expression of FLC and MAFs and increased expression of FT and SOC1), but opposite to sdg26 (increased rosette size, late flowering associated with increased FLC and MAF5 expression and reduced FT and SOC1 expression). In parallel to the finding of the epistasis of SDG8, our study also unravels novel functions of SDG26 in H3K36me1 deposition and in the interplay with SDG8 in regulating the genome-wide gene expression. The implication of various HKMTs in establishing different forms of histone methylation and gene-context-specific chromatin modifications likely provides an advantageous mechanism for the regulation of transcription to cope with complex and plastic growth and developmental programs in plants and possibly also in other organisms.

ZRF1 Chromatin Regulators Have Polycomb Silencing and Independent Roles in Development.

Histone H2A monoubiquitination (H2Aub1), catalyzed by Polycomb-Repressive Complex1 (PRC1), is a key epigenetic mark in Polycomb silencing. However, little is known about how H2Aub1 is read to exert downstream physiological functions. The animal ZUOTIN-RELATED FACTOR1 (ZRF1) has been reported to bind H2Aub1 to promote or repress the expression of varied target genes. Here, we show that the Arabidopsis (Arabidopsis thaliana) ZRF1 homologs, AtZRF1a and AtZRF1b, are key regulators of multiple processes during plant growth and development. Loss of function of both AtZRF1a and AtZRF1b in atzrf1a atzrf1b mutants causes seed germination delay, small plant size, abnormal meristem activity, abnormal flower development, as well as gametophyte transmission and embryogenesis defects. Some of these defects overlap with those described previously in the PRC1-defective mutants atbmi1a atbmi1b and atring1a atring1b, but others are specific to atzrf1a atzrf1b In line with this, 4,519 genes (representing more than 14% of all genes) within the Arabidopsis genome are found differentially expressed in atzrf1a atzrf1b seedlings, and among them, 114 genes are commonly up-regulated in atring1a atring1b and atbmi1a atbmi1b Finally, we show that in both atzrf1a atzrf1b and atbmi1a atbmi1b seedlings, the seed developmental genes ABSCISIC ACID INSENSITIVE3, CRUCIFERIN3, and CHOTTO1 are derepressed, in association with the reduced levels of H2Aub1 and histone H3 lysine-27 trimethylation (H3K27me3). Collectively, our results indicate that AtZRF1a/b play both PRC1-related and PRC1-unrelated functions in regulating plant growth and development and that AtZRF1a/b promote H2Aub1 and H3K27me3 deposition in gene suppression. Our work provides novel insight into the mechanisms of function of this family of evolutionarily conserved chromatin regulators.

The trxG family histone methyltransferase SET DOMAIN GROUP 26 promotes flowering via a distinctive genetic pathway.

Histone methylation is a major component in numerous processes such as determination of flowering time, which is fine-tuned by multiple genetic pathways that integrate both endogenous and environmental signals. Previous studies identified SET DOMAIN GROUP 26 (SDG26) as a histone methyltransferase involved in the activation of flowering, as loss of function of SDG26 caused a late-flowering phenotype in Arabidopsis thaliana. However, the SDG26 function and the underlying molecular mechanism remain largely unknown. In this study, we undertook a genetic analysis by combining the sdg26 mutant with mutants of other histone methylation enzymes, including the methyltransferase mutants Arabidopsis trithorax1 (atx1), sdg25 and curly leaf (clf), as well as the demethylase double mutant lsd1-like1 lsd1-like2 (ldl1 ldl2). We found that the early-flowering mutants sdg25, atx1 and clf interact antagonistically with the late-flowering mutant sdg26, whereas the late-flowering mutant ldl1 ldl2 interacts synergistically with sdg26. Based on microarray analysis, we observed weak overlaps in the genes that were differentially expressed between sdg26 and the other mutants. Our analyses of the chromatin of flowering genes revealed that the SDG26 protein binds at the key flowering integrator SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1/AGAMOUS-LIKE 20 (SOC1/AGL20), and is required for histone H3 lysine 4 trimethylation (H3K4me3) and histone H3 lysine 36 trimethylation (H3K36me3) at this locus. Together, our results indicate that SDG26 promotes flowering time through a distinctive genetic pathway, and that loss of function of SDG26 causes a decrease in H3K4me3 and H3K36me3 at its target gene SOC1, leading to repression of this gene and the late-flowering phenotype.

The Arabidopsis CUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting.

Protein ubiquitylation regulates a broad variety of biological processes in all eukaryotes. Recent work identified a novel class of cullin-containing ubiquitin ligases (E3s) composed of CUL4, DDB1, and one WD40 protein, believed to act as a substrate receptor. Strikingly, CUL4-based E3 ligases (CRL4s) have important functions at the chromatin level, including responses to DNA damage in metazoans and plants and, in fission yeast, in heterochromatin silencing. Among putative CRL4 receptors we identified MULTICOPY SUPPRESSOR OF IRA1 (MSI1), which belongs to an evolutionary conserved protein family. MSI1-like proteins contribute to different protein complexes, including the epigenetic regulatory Polycomb repressive complex 2 (PRC2). Here, we provide evidence that Arabidopsis MSI1 physically interacts with DDB1A and is part of a multimeric protein complex including CUL4. CUL4 and DDB1 loss-of-function lead to embryo lethality. Interestingly, as in fis class mutants, cul4 mutants exhibit autonomous endosperm initiation and loss of parental imprinting of MEDEA, a target gene of the Arabidopsis PRC2 complex. In addition, after pollination both MEDEA transcript and protein accumulate in a cul4 mutant background. Overall, our work provides the first evidence of a physical and functional link between a CRL4 E3 ligase and a PRC2 complex, thus indicating a novel role of ubiquitylation in the repression of gene expression.

Combinatorial functions of diverse histone methylations in Arabidopsis thaliana flowering time regulation.

Previous studies in Arabidopsis thaliana have identified several histone methylation enzymes, including Arabidopsis trithorax1 (ATX1)/set domain group 27 (SDG27), ATX2/SDG30, LSD1-LIKE1 (LDL1), LDL2, SDG8, SDG25, and curly leaf (CLF)/SDG1, as regulators of the key flowering repressor flowering locus C (FLC) and the florigen flowering locus T (FT). However, the combinatorial functions of these enzymes remain largely uninvestigated. Here, we investigated functional interplays of different histone methylation enzymes by studying higher order combinations of their corresponding gene mutants. We showed that H3K4me2/me3 and H3K36me3 depositions occur largely independently and that SDG8-mediated H3K36me3 overrides ATX1/ATX2-mediated H3K4me2/me3 or LDL1/LDL2-mediated H3K4 demethylation in regulating FLC expression and flowering time. By contrast, a reciprocal inhibition was observed between deposition of the active mark H3K4me2/me3 and/or H3K36me3 and deposition of the repressive mark H3K27me3 at both FLC and FT chromatin; and the double mutants sdg8 clf and sdg25 clf displayed enhanced early-flowering phenotypes of the respective single mutants. Collectively, our results provide important insights into the interactions of different types of histone methylation and enzymes in the regulation of FLC and FT expression in flowering time control.

MSI4/FVE interacts with CUL4-DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis.

Flowering at the right time is crucial to ensure successful plant reproduction and seed yield and is dependent on both environmental and endogenous parameters. Among the different pathways that impinge on flowering, the autonomous pathway promotes floral transition independently of day length through the repression of the central flowering repressor flowering locus C (FLC). FLC blocks floral transition by repressing flowering time integrators such as flowering locus T (FT). MSI4/FVE is a key regulator of the autonomous pathway that reduces FLC expression. Here we report that the MSI4 protein is a DDB1 and CUL4-associated factor that represses FLC expression through its association with a CLF-Polycomb Repressive Complex 2 (PRC2) in Arabidopsis. Thus, the lack of MSI4 or decreased CUL4 activity reduces H3K27 trimethylation on FLC, but also on its downstream target FT, resulting in increased expression of both genes. Moreover, CUL4 interacts with FLC chromatin in an MSI4-dependant manner, and the interaction between MSI4 and CUL4-DDB1 is necessary for the epigenetic repression of FLC. Overall our work provides evidence for a unique functional interaction between the cullin-RING ubiquitin ligase (CUL4-DDB1(MSI4)) and a CLF-PRC2 complex in the regulation of flowering timing in Arabidopsis.

High nitrogen insensitive 9 (HNI9)-mediated systemic repression of root NO3- uptake is associated with changes in histone methylation.

In plants, root nitrate uptake systems are under systemic feedback repression by the N satiety of the whole organism, thus adjusting the N acquisition capacity to the N demand for growth; however, the underlying molecular mechanisms are largely unknown. We previously isolated the Arabidopsis high nitrogen-insensitive 9-1 (hni9-1) mutant, impaired in the systemic feedback repression of the root nitrate transporter NRT2.1 by high N supply. Here, we show that HNI9 encodes Arabidopsis INTERACT WITH SPT6 (AtIWS1), an evolutionary conserved component of the RNA polymerase II complex. HNI9/AtIWS1 acts in roots to repress NRT2.1 transcription in response to high N supply. At a genomic level, HNI9/AtIWS1 is shown to play a broader role in N signaling by regulating several hundred N-responsive genes in roots. Repression of NRT2.1 transcription by high N supply is associated with an HNI9/AtIWS1-dependent increase in histone H3 lysine 27 trimethylation at the NRT2.1 locus. Our findings highlight the hypothesis that posttranslational chromatin modifications control nutrient acquisition in plants.

Interphase chromatin organisation in Arabidopsis nuclei: constraints versus randomness.

The spatial chromatin organisation and molecular interactions within and between chromatin domains and chromosome territories (CTs) are essential for fundamental processes such as replication, transcription and DNA repair via homologous recombination. To analyse the distribution and interaction of whole CTs, centromeres, (sub)telomeres and ~100-kb interstitial chromatin segments in endopolyploid nuclei, specific FISH probes from Arabidopsis thaliana were applied to 2-64C differentiated leaf nuclei. Whereas CTs occupy a distinct and defined volume of the nucleus and do not obviously intermingle with each other in 2-64C nuclei, ~100-kb sister chromatin segments within these CTs become more non-cohesive with increasing endopolyploidy. Centromeres, preferentially located at the nuclear periphery, may show ring- or half-moon like shapes in 2C and 4C nuclei. Sister centromeres tend to associate up to the 8C level. From 16C nuclei on, they become progressively separated. The higher the polyploidy level gets, the more separate chromatids are present. Due to sister chromatid separation in highly endopolyploid nuclei, the centromeric histone variant CENH3, the 180-bp centromeric repeats and pericentromeric heterochromatin form distinct subdomains at adjacent but not intermingling positions. The (sub)telomeres are frequently associated with each other and with the nucleolus and less often with centromeres. The extent of chromatid separation and of chromatin decondensation at subtelomeric chromatin segments varies between chromosome arms. A mainly random distribution and similar shapes of CTs even at higher ploidy levels indicate that in general no substantial CT reorganisation occurs during endopolyploidisation. Non-cohesive sister chromatid regions at chromosome arms and at the (peri)centromere are accompanied by a less dense chromatin conformation in highly endopolyploid nuclei. We discuss the possible function of this conformation in comparison to transcriptionally active regions at insect polytene chromosomes.

Arabidopsis SET DOMAIN GROUP2 is required for H3K4 trimethylation and is crucial for both sporophyte and gametophyte development.

Histone H3 lysine 4 trimethylation (H3K4me3) is abundant in euchromatin and is in general associated with transcriptional activation in eukaryotes. Although some Arabidopsis thaliana SET DOMAIN GROUP (SDG) genes have been previously shown to be involved in H3K4 methylation, they are unlikely to be responsible for global genome-wide deposition of H3K4me3. Most strikingly, sparse knowledge is currently available about the role of histone methylation in gametophyte development. In this study, we show that the previously uncharacterized SDG2 is required for global H3K4me3 deposition and its loss of function causes wide-ranging defects in both sporophyte and gametophyte development. Transcriptome analyses of young flower buds have identified 452 genes downregulated by more than twofold in the sdg2-1 mutant; among them, 11 genes, including SPOROCYTELESS/NOZZLE (SPL/NZZ) and MALE STERILITY1 (MS1), have been previously shown to be essential for male and/or female gametophyte development. We show that both SPL/NZZ and MS1 contain bivalent chromatin domains enriched simultaneously with the transcriptionally active mark H3K4me3 and the transcriptionally repressive mark H3K27me3 and that SDG2 is specifically required for the H3K4me3 deposition. Our data suggest that SDG2-mediated H3K4me3 deposition poises SPL/NZZ and MS1 for transcriptional activation, forming a key regulatory mechanism in the gene networks responsible for gametophyte development.

Chromatin modification and remodelling: a regulatory landscape for the control of Arabidopsis defence responses upon pathogen attack.

Due to their sessile lifestyle, plants have to cope with an ever-changing environment and to defend themselves against a multitude of biotic aggressors that compromise their development and reproduction. Responses to various biotic stresses largely depend on the plant's capacity to modulate rapidly and specifically its transcriptome. In a stress type-dependent manner, external signals are translocated into the nucleus to activate transcription factors, resulting in the increased expression of particular sets of defence-related genes. Among mechanisms of transcriptional regulation, chromatin remodelling accomplished through the activity of histone-modifying enzymes and ATP-dependent chromatin-remodelling complexes is emerging as a key process in the orchestration of plant biotic stress responses. In this review, we summarize and discuss roles that chromatin-remodelling mechanisms may play in regulating Arabidopsis defence responses.

The art of painting chromosome loops.

How to get a metre of DNA into a tiny space while preserving its functional characteristics? This question seems easy to pose, but the answer is far from being trivial. Facing this riddle, salvation came from technical improvements in microscopy and in situ hybridisation techniques applied to cytogenetics. Here, we would like to look into the past at one of these pure cytogenetics articles that makes a breakthrough in addressing this question in plant science. Our choice fell on the work published two decades ago by Fransz et al. (2002). Besides the elegant manner in which DNA probes were organised to bring into light the out-looping arrangement of interphase chromosomes in Arabidopsis thaliana nuclei, this article perfectly illustrates that painting is not reserved to the fine art. As for whether emotional expression prioritised by artists can sometimes hide behind scientific empirical evidence, there is only a small step to make to the general case.

Histone modifications in transcriptional activation during plant development.

In eukaryotic cell nuclei, chromatin states dictated by different combinations of post-translational modifications of histones, such as acetylation, methylation and monoubiquitination of lysine residues, are part of the multitude of epigenomes involved in the fine-tuning of all genetic functions and in particular transcription. During the past decade, an increasing number of 'writers', 'readers' and 'erasers' of histone modifications have been identified. Characterization of these factors in Arabidopsis has unraveled their pivotal roles in the regulation of essential processes, such as floral transition, cell differentiation, gametogenesis, and plant response/adaptation to environmental stresses. In this review we focus on histone modification marks associated with transcriptional activation to highlight current knowledge on Arabidopsis 'writers', 'readers' and 'erasers' of histone modifications and to discuss recent findings on molecular mechanisms of integration of histone modifications with the RNA polymerase II transcriptional machinery during transcription of the flowering repressor gene FLC.

Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi.

As sessile organisms, plants have to endure a wide variety of biotic and abiotic stresses, and accordingly they have evolved intricate and rapidly inducible defense strategies associated with the activation of a battery of genes. Among other mechanisms, changes in chromatin structure are thought to provide a flexible, global, and stable means for the regulation of gene transcription. In support of this idea, we demonstrate here that the Arabidopsis (Arabidopsis thaliana) histone methyltransferase SET DOMAIN GROUP8 (SDG8) plays a crucial role in plant defense against fungal pathogens by regulating a subset of genes within the jasmonic acid (JA) and/or ethylene signaling pathway. We show that the loss-of-function mutant sdg8-1 displays reduced resistance to the necrotrophic fungal pathogens Alternaria brassicicola and Botrytis cinerea. While levels of JA, a primary phytohormone involved in plant defense, and camalexin, a major phytoalexin against fungal pathogens, remain unchanged or even above normal in sdg8-1, induction of several defense genes within the JA/ethylene signaling pathway is severely compromised in response to fungal infection or JA treatment in mutant plants. Both downstream genes and, remarkably, also upstream mitogen-activated protein kinase kinase genes MKK3 and MKK5 are misregulated in sdg8-1. Accordingly, chromatin immunoprecipitation analysis shows that sdg8-1 impairs dynamic changes of histone H3 lysine 36 methylation at defense marker genes as well as at MKK3 and MKK5, which normally occurs upon infection with fungal pathogens or methyl JA treatment in wild-type plants. Our data indicate that SDG8-mediated histone H3 lysine 36 methylation may serve as a memory of permissive transcription for a subset of defense genes, allowing rapid establishment of transcriptional induction.