Chromatin modification and remodelling: a regulatory landscape for the control of Arabidopsis defence responses upon pathogen attack
2012; Wiley; Volume: 14; Issue: 6 Linguagem: Inglês
10.1111/j.1462-5822.2012.01785.x
ISSN1462-5822
AutoresAlexandre Berr, Rozenn Ménard, Thierry Heitz, Wen‐Hui Shen,
Tópico(s)Plant Stress Responses and Tolerance
ResumoCellular MicrobiologyVolume 14, Issue 6 p. 829-839 MicroreviewFree Access Chromatin modification and remodelling: a regulatory landscape for the control of Arabidopsis defence responses upon pathogen attack Alexandre Berr, Corresponding Author Alexandre Berr Institut de Biologie Moléculaire des Plantes (IBMP), Unité Propre de Recherche 2357 du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France. E-mail Alexandre.Berr@ibmp-cnrs.unistra.fr; Tel. (+33) 3 88 41 72 94; Fax (+33) 3 88 61 44 42. Search for more papers by this authorRozenn Ménard, Rozenn Ménard Institut de Biologie Moléculaire des Plantes (IBMP), Unité Propre de Recherche 2357 du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France.Search for more papers by this authorThierry Heitz, Thierry Heitz Institut de Biologie Moléculaire des Plantes (IBMP), Unité Propre de Recherche 2357 du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France.Search for more papers by this authorWen-Hui Shen, Wen-Hui Shen Institut de Biologie Moléculaire des Plantes (IBMP), Unité Propre de Recherche 2357 du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France.Search for more papers by this author Alexandre Berr, Corresponding Author Alexandre Berr Institut de Biologie Moléculaire des Plantes (IBMP), Unité Propre de Recherche 2357 du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France. E-mail Alexandre.Berr@ibmp-cnrs.unistra.fr; Tel. (+33) 3 88 41 72 94; Fax (+33) 3 88 61 44 42. Search for more papers by this authorRozenn Ménard, Rozenn Ménard Institut de Biologie Moléculaire des Plantes (IBMP), Unité Propre de Recherche 2357 du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France.Search for more papers by this authorThierry Heitz, Thierry Heitz Institut de Biologie Moléculaire des Plantes (IBMP), Unité Propre de Recherche 2357 du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France.Search for more papers by this authorWen-Hui Shen, Wen-Hui Shen Institut de Biologie Moléculaire des Plantes (IBMP), Unité Propre de Recherche 2357 du Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg, 12 rue du Général Zimmer, 67084 Strasbourg Cedex, France.Search for more papers by this author First published: 09 March 2012 https://doi.org/10.1111/j.1462-5822.2012.01785.xCitations: 50AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Summary 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. Introduction Plants are exposed to severe or fluctuating environmental conditions and have to fend off a wide range of biotic attacks by herbivores or microbial pathogens. Like animals, higher plants possess constitutive defence barriers (i.e. pre-existing physical and/or biochemical impediments), but lack an adaptive immune system generating antibodies and circulatory cells dedicated to detect and neutralize pathogens. Plants substantially rely on an innate immune system to counteract microbial infections. Tolerance and/or resistance can be acquired from rapidly inducible defence mechanisms, in which phytohormone signalling networks play pivotal roles (Pieterse et al., 2009; Robert-Seilaniantz et al., 2011). In contrast to animals that possess specialized endocrine glands to produce hormones, most plant cells appear able to synthesize phytohormones. Thus, all living plant cells have the potential to detect invading pathogens, to respond to the infection by initiating a proper defence programme through the build-up of a specific hormone blend, and eventually to establish a broad systemic alert state spreading from a local infection. An essential and common component of plant stress responses resides in the plant capacity to reprogramme its gene expression. Particularly, the stimulation of a given stress signalling pathway after pathogen detection is integrated into the plant cell nucleus through a set of regulatory transcription factor cascades, which prioritizes defence over growth-related cellular functions (Moore et al., 2011). Among mechanisms involved in this vital transcriptional reprogramming, the importance of chromatin modifications and remodelling in the transcriptional regulation of defence-related genes is rapidly emerging. We will highlight here recent examples illustrating how epigenetic modifications condition major steps leading to immunity, ranging from initial pathogen perception to hormonal homeostasis changes for antimicrobial effector expression, to the establishment of a systemic protection in distal tissues. Plant innate immunity Plant detection of microbial pathogens Basal resistance, a common form of innate immunity, is triggered in the host by a small number of pattern-recognition receptors (PRRs). PRRs specifically recognize broadly conserved microbe-/pathogen-associated molecular patterns (MAMPs/PAMPs), including specific proteins, lipopolysaccharides or cell wall components, leading to MAMP/PAMP-triggered plant immunity (MTI/PTI). As a counter-attack, pathogens have improved their colonization strategy by evolving their capacity to deliver effector proteins into host cells in order to suppress or overcome MTI/PTI, resulting in effector-triggered susceptibility (ETS). An additional level of resistance associated with vigorous defence induction is attained when cultivar- or ecotype-specific resistance (R) gene products acquire the ability to recognize such race-specific effectors derived from avirulence (avr) genes, thereby activating effector-triggered immunity (ETI; Jones and Dangl, 2006). ETI usually triggers a localized cell death at the infection site, in a process known as the hypersensitive response (HR), which along with antimicrobial responses will restrict most pathogen growth. Finally, after an initial attack, local PTI as well as ETI trigger systemic acquired resistance (SAR), providing an enhanced response in distal plant tissues in case of subsequent challenge by a wide range of pathogens (Durrant and Dong, 2004; Mishina and Zeier, 2007). Signal convergence towards the nucleus Pathogenic signal perception generally takes place at the cell surface or in the cytoplasm and this information has to be transduced into the nucleus to allow appropriate transcriptional responses. Early events after pathogen sensing include ion fluxes, production of reactive oxygen species and phosphorylation cascades (Garcia-Brugger et al., 2006). These rapid cellular alerts shape massive hormonal changes acting as secondary signals that will be perceived in the nucleus. Particularly, the accumulation of the defence-specialized hormones salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) and their respective signalling pathways form a complex network of signal amplification and transduction leading ultimately to the transcriptional activation of defence genes (Verhage et al., 2010; Fig. 1). Figure 1Open in figure viewerPowerPoint Simplified model for the principal signalling pathways involved in the response to biotic stresses in Arabidopsis. Genes involved in the ET-, JA- and SA-dependent signalling pathways are indicated in italic. Using Arabidopsis, the genetic dissection of defence circuits has identified important factors involved in the transduction of defence signals across cell compartments (Garcia and Parker, 2009). Upon pathogen attack, the signalling protein ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) associates with PHYTOALEXIN DEFICIENT 4 (PAD4) or even with R gene products such as RESISTANCE TO PSEUDOMONAS SYRINGAE 4 (RPS4) or the bacterial effector protein AvrRps4 to form distinct functional complexes. These complexes shuttle between cytoplasm and nucleus where EDS1 will further interact with transcription factors for the transcriptional reprogramming of SA- and defence-related genes (Garcia et al., 2010; Bhattacharjee et al., 2011; Heidrich et al., 2011). Similarly, under pathogen stress, the nucleocytoplasmic R protein SNC1 (SUPPRESSOR OF npr1-1, CONSTITUTIVE1) represses the expression of DEFENSE NO DEATH 1 (DND1), DND2 and other negative regulators of plant innate immunity through its association, in the nucleus, with the transcriptional co-repressor TOPLESS-RELATED1 (TPR1; Zhu et al., 2010). NONEXPRESSER OF PR GENES 1 (NPR1) is a key regulator of SA-mediated defence responses. In the absence of SA, NPR1 forms homo-oligomers in the cytoplasm, which are largely excluded from the nucleus. Upon stimulation, SA accumulation promotes their reduction to monomeric NPR1 that can then relocate to the nucleus and activate the expression of Pathogenesis-Related (PR) genes (e.g. PR1) by interacting with TGA transcription factors (Dong, 2004). Additionally, mutants in components of the nucleocytoplasmic trafficking machinery, like MODIFIER OF SNC1, 3 (MOS3), MOS6 and MOS7, are affected in immune responses. Consistently, the mos7-1 allele presents a defect in the nuclear accumulation of EDS1, NPR1 and SNC1 (Cheng et al., 2009). These examples illustrate the importance of macromolecule movements, and particularly nuclear relocalization of regulatory proteins in preparing subsequent transcriptional changes to establish plant immunity. JA hormone perception also relies on nuclear event (Pauwels and Goossens, 2011). In the absence of jasmonoyl-isoleucine (JA-Ile; the active form of JA), distinct JASMONATE ZIM-DOMAIN (JAZ) proteins associate in the nucleus with NOVEL INTERACTOR of JAZ (NINJA) to recruit the co-repressor TOPLESS and inhibit multiple JA-responsive transcription factors, including MYC2. Under stress, JA-Ile accumulation is perceived by the F-box protein CORONATINE INSENSITIVE1 (COI1) and promotes the assembly of the COI1-JAZ co-receptor as part of the SCFCOI1 ubiquitin E3 ligase complex, leading to poly-ubiquitination and subsequent degradation of JAZ repressors by the 26S proteasome. JAZ degradation relieves repression of target transcription factors, permitting the expression of downstream JA-responsive genes (Pauwels and Goossens, 2011), including genes encoding PR proteins [e.g. PLANT DEFENSIN1.2a (PDF1.2a), THIONIN2.1 (THI2.1) and VEGETATIVE STORAGE PROTEIN2 (VSP2)]. Collectively, the aforementioned nuclear processes appear fundamental in the rapid connection between signal perception and transcriptional regulation of defence-related genes, thus leading to the question of a direct or indirect functional link between these nuclear processes and the chromatin-remodelling machinery in plant innate immunity. Chromatin remodelling in plant innate immunity Chromatin structure and dynamics In eukaryotes, the accessibility of the transcriptional machinery to DNA is highly dependent on nucleosome positioning and chromatin architecture. Basically, genes located in condensed heterochromatin regions are frequently silenced, while genes located in loosened euchromatin regions are generally transcribed. Persistent/transient changes within the chromatin structure are accomplished by different mechanisms including post-translational histone modifications (PTMs), histone variants replacement and ATP-dependent chromatin remodelling. Protruding from the globular nucleosome core, the histone tails may undergo diverse reversible PTMs (i.e. acetylation, methylation, phosphorylation, ubiquitination, sumoylation, carbonylation and glycosylation; Kouzarides, 2007) that can directly modulate the chromatin structure, or serve as platform to recruit specific 'readers/effectors' which will determine their functional outcomes (Yun et al., 2011). Typically, histone acetylation by histone acetyltransferases (HATs) is generally associated with transcriptional activation, while histone deacetylation by histone deacetylases (HDAs) is linked to transcriptional repression. Depending on their targets, histone methylation and/or ubiquitination can either activate or repress transcription. Genome-wide analyses in Arabidopsis revealed that tri-methylations of H3K4 and H3K36 (H3K4me3 and H3K36me3) and mono-ubiquitination of H2B (H2Bub) are enriched at actively expressed genes, whereas H3K27me3 is associated with repressed genes and H3K9me2 and H4K20me1 are enriched at constitutive heterochromatin and silenced transposons (Zhang et al., 2007; 2009; Roudier et al., 2011). Arabidopsis harbours 37 putative SET-domain proteins with some of them experimentally demonstrated to exhibit histone methyltransferase (HMT) activity (Thorstensen et al., 2011). It also possesses four LSD1-like proteins and 21 JmiC-domain proteins that are effective or predicted histone demethylases (Chen et al., 2011). H2Bub has also been well characterized in Arabidopsis, and its deposition requires the E2 ubiquitin-conjugating enzymes AtUBC1 and AtUBC2 and the E3 enzymes HISTONE MONOUBIQUITINATION1 (HUB1) and HUB2 (Fleury et al., 2007; Liu et al., 2007; Xu et al., 2009). In addition, more than 40 genes encode putative ATP-dependent chromatin-remodelling factors, which can be subdivided into at least five families, based on their ATPase subunits: (i) the SWI/SNF group, (ii) the ISWI group, (iii) the NURD/Mi-2/CHD group, (iv) the INO80 group and (v) the SWR1 group. Within complexes, ATP-dependent chromatin-remodelling enzymes use the energy of ATP hydrolysis to remodel chromatin structure by destabilizing histone–DNA contacts, moving histone octamers or even catalysing the incorporation of specific histone variants (Clapier and Cairns, 2009). The involvement of histone modifications and ATP-dependent chromatin-remodelling enzymes in establishing rapid, reversible and/or heritable differential patterns of gene expression in the regulation of essential developmental processes, such as flowering time control, cell fate maintenance or seed development has been well studied (reviewed in Clapier and Cairns, 2009; Shen and Xu, 2009; Berr and Shen, 2010; Berr et al., 2011). In contrast, these mechanisms have gained only recently increased interest as potential transcriptional regulators in plant innate immunity (Table 1; see below). Table 1. Histone-modifying enzymes and chromatin-remodelling factors involved in the response to biotic pathogens. Functional Gene Mutant phenotype and functional consequences References Name Expression Category Subcategory Inducer Repressor Histone-modifying enzymes Histone deacetylases HDA6 MeJA and ACC Downregulation of the basal expression of ET/JA-responsive genes (i.e. PDF1.2, VSP2, JIN1 and ERF1) Zhou et al. (2005); Wu et al. (2008) HDA19/HD1 A. brassicicola, MeJA and ACC Increased sensitivity to A. brassicicola; downregulation of the basal expression of ET/JA-responsive genes (i.e. PDF1.2, VSP2, JIN1 and ERF1) Zhou et al. (2005) Pst DC3000 and SA Increased sensitivity to Pst DC3000; enhanced basal expression of SA-responsive genes (i.e. PR1, PR4 and PR5) Tian et al. (2005); Kim et al. (2008) SRT2 Pst DC3000 Mutant more resistant to Pst DC3000; repressed basal and induced expression of SA-biosynthesis genes (i.e. PAD4, EDS5 and SID2) Wang et al. (2010) Histone methyltransferases SDG8/ASHH2/CCR1/EFS/ LAZ2 Botrytis cinerea Increased sensitivity to necrotrophic fungi; downregulation of the basal and induced expression of ET/JA-responsive genes (i.e. PDF1.2 and VSP2) Berr et al. (2010) Pst DC3000 Increased sensitivity to Pst DC3000; decreased basal expression of particular NB-LRR genes (i.e. LAZ5 or RPM1); decreased inducibility of SA-responding genes (i.e. WRKY70 and PR1) Palma et al. (2010); De-La-Peña et al. (2011) ATX1 No change upon SA, JA or Pst DC3000 infection Downregulation of the basal and induced expression of SA-responsive genes (i.e. PR1 and WRKY70); upregulation of the basal and induced expression of ET/JA responsive genes (i.e. THI2.1) Alvarez-Venegas et al. (2007) SDG37/ASHR1 Pst DC3000 Increased sensitivity to Pst DC3000; decreased inducibility of SA-responding genes (i.e. WRKY70 and PR1) De-La-Peña et al. (2011) H2B ubiquitin–ligase HUB1 B. cinerea and A. brassicicola Increased sensitivity to necrotrophic fungi; reduced cell wall thickness; No altered expression of PDF1.2 in responses to B. cinerea infection Dhawan et al. (2009) ATP-dependent chromatin-remodelling complex SWR1-like complex PIE/CHR13, ARP6/SUF3/ESD1 and SEF No change upon SA, JA or Pst DC3000 infection Enhanced resistance to Pst DC3000; increased basal expression of several genes upstream and downstream of the SA signalling pathway March-Diaz et al. (2008) Snf2-like protein SYD/CHR3 Wounding Increased sensitivity to B. cinerea; downregulation of the basal and induced expression of ET/JA-responsive genes (i.e. PDF1.2a, VSP2 and MYC2) Walley et al. (2008) Histone modifications in the SA signalling pathway mediated plant defence and SAR Salicylic acid plays an important signalling role in establishing plant resistance against biotrophic pathogens such as Pseudomonas syringae bacteria as well as in SAR activation (Jones and Dangl, 2006). The SA pathway is substantially controlled by histone modifications, although current information is still fragmentary. For example, the HDAC SIRTUIN2 (SRT2) suppresses the expression of the SA biosynthetic genes PAD4, EDS5 and SID2 and, consistently, SRT2 expression is downregulated upon Pseudomonas syringae pv. tomato (Pst DC3000) infection, thereby permitting SA production and expression of defence-related genes (Wang et al., 2010). In addition, loss of HDA19 activity results in enhanced basal expression of many downstream SA-responsive genes (e.g. PR1, PR4 and PR5; Tian et al., 2005). HDA19 was reported to physically interact with both WRKY38 and WRKY62, two transcriptional activators that activate unknown negative regulators to repress defence genes (Kim et al., 2008). Interestingly, HDA19 also interacts with the above-mentioned transcriptional co-repressor TPR1 (Zhu et al., 2010). Therefore, upon pathogen attack, probably within different multiprotein complexes, HDA19 may participate through its histone deacetylase activity in the repression of several negative defence regulators, leading to the activation of plant immune responses. Increased methylation at H3K4 and acetylation at H3K9 and H3K14 at PR1 chromatin was first reported in sni1 (suppressor of npr1-1, inducible 1) mutants compared with wild-type plants under normal growth conditions (Mosher et al., 2006). Treatment with the SA analogue benzo(1,2,3)thiadiazole-7-carbothioic acid S-methyl ester (BTH) does not further increase histone methylation and acetylation in mutants, whereas an increase was monitored in wild-type plants 48 h after treatment. SNI1 encodes a leucine-rich nuclear protein lacking homology with known chromatin-modifying enzymes and DNA-binding domains. The sni1 mutation in the npr1-1 background shows almost rescued PR1 expression as well as pathogen resistance (Li et al., 1999). These results indicate that SNI1 may be required to modify chromatin, probably by inhibiting or counter-acting HATs or HMTs. Interestingly, H3K4me3 is present on PR1 promoter chromatin before any stimulation and its level increases upon BTH treatment (Mosher et al., 2006). Therefore, H3K4me3 seems to be readily in place as a 'permissive' mark, providing the appropriate chromatin state for efficient induction of PR1 expression when needed. Upon stimulation, the increased H3K4me3 level participates in the activation of PR1 expression. Conversely, another group reported that no significant change in the levels of H3K4me2 and me3 could be detected on PR1 chromatin in wild-type plants 24 h after SA treatment (Alvarez-Venegas et al., 2007). This discrepancy may result from different timings in sample preparation (48 h versus 24 h after treatment), implying that H3K4me3 level is not immediately increased on PR1 upon treatment but is increased later in association with enhanced PR1 expression, establishing a long and/or short term stress memory necessary for plant effective defence against pathogen infection. The HMT ATX1 was described as critical for basal resistance against Pst DC3000 (Alvarez-Venegas et al., 2006). ATX1 positively regulates the SA-inducible expression of WRKY70, which encodes a key transcription factor regulating cross-talk between the SA and JA signalling pathways (Fig. 1), and also participates indirectly in the regulation of the JA-inducible THI1.2 gene expression (Alvarez-Venegas et al., 2006; 2007). ATX1 may however affect PR1 expression through a WRKY70-independent mechanism, as wrky70 mutant did not show altered SA-induced PR1 transcription (Ren et al., 2008). Another HMT, SDG8, which is the major Arabidopsis H3K36 di- and tri-methyltransferase (Xu et al., 2008), was also reported as required for Pst DC3000-triggered plant defence (Palma et al., 2010). Indeed, SDG8 seems to sustain the basal expression level of particular R genes (i.e. RPM1 or LAZ5, but not RPS2 or RPS4; Palma et al., 2010). LAZ5 is not expressed in sdg8 mutants. Moreover, LAZ5 is induced by BTH treatment or Pst DC3000 inoculation in wild-type plants but not in sdg8 mutants. Using chromatin immunoprecipitation (ChIP) assays, authors observed a significant decrease in H3K36me3 on LAZ5 chromatin in resting sdg8 mutants. Furthermore, upon stimulation, they did not detect any significant increase in the level of H3K36me3 on LAZ5 chromatin in wild-type plants. Therefore, SDG8 may establish a 'permissive' chromatin structure by methylating H3K36 on particular R genes chromatin, resulting in their basal expression. Interestingly, the 'permissive' state established by SDG8 seems also indispensable to potentiate proper R genes transcriptional induction upon stimulation. More recently, De-La-Peña and colleagues reported that sdg8 and sdg7 mutants are more sensitive than wild-type to P. syringae infection (De-La-Peña et al., 2011). Other R genes were proposed to be under epigenetic control. For example, the transcription of RPP7 is enhanced by the nuclear protein EDM2, which contains two Plant Homeodomain (PHD)-finger-like domains (Tsuchiya and Eulgem, 2011). PHD fingers were recently added to the large family of epigenetic 'readers' able to specifically recognize histone PTMs and unmodified histone tails (Musselman and Kutateladze, 2011). EDM2 was proposed to cooperate within a large protein complex with EMSY-like (AtEML) members, harbouring an Agenet domain (i.e. related to the Tudor domain family of epigenetic 'readers'; Bottomley, 2004). Beyond regulation of defences at primary infection sites, SAR is associated with gene priming in systemic tissues, in which some defence-related genes are expressed more rapidly and strongly upon a subsequent challenge (Conrath, 2011). SAR implies the generation, spread and perception of signal(s) that establish a kind of stress 'memory' for enhanced defence gene transcription. Jaskiewicz and colleagues recently found that priming of the WRKY6, WRKY29 and WRKY52 genes was associated with an increase in H3 acetylation and H3K4me3 at gene promoters (Jaskiewicz et al., 2011). Even if histone-modifying enzymes involved in this priming mechanism are not yet known, this finding suggests a causal link between histone modifications and stress memory within an individual. Recently, DNA methylation was reported to be implicated in the transmission of a stress memory, endowing the progeny of Pst DC3000-inoculated Arabidopsis plants with enhanced resistance, thus providing evidence for a transgenerational SAR (Luna et al., 2012; Slaughter et al., 2012). Furthermore, NPR1 seems important for transmitting this memory by establishing a differential pattern of histone PTMs (i.e. acetylation and H3K27 methylation) between SA- and JA-dependent defence genes. These important findings suggest that systemic signals (i.e. epigenetic modifications) are not limited to SAR establishment in the stimulated individual, but they also impact the germline to prime its progeny. More studies are necessary to firmly establish histone PTMs dynamic during pathogenic infections and to identify involved enzyme players. However, histone acetylation and methylation nowadays appear to be very important in establishing a 'permissive' chromatinian context rendering defence genes transcriptionally inducible. Moreover, in a similar way as DNA methylation, histone-modifying enzymes may also participate in retaining stress memory through successive generations. Histone modifications in the JA/ET signalling pathway-mediated plant defence Jasmonic acid and ET are prominent to mediate efficient defences after herbivorous insect attacks or infection by necrotrophic microbes (Rojo et al., 1999; Thomma et al., 2001; Glazebrook, 2005). Among necrotrophs, fungal pathogens are known to produce HDA inhibitors. The fungus Alternaria brassicicola produces a toxin called depudecin, known to inhibit HDA activity in vitro and in vivo (Matsumoto et al., 1992; Oikawa et al., 1995; Kwon et al., 1998; 2003); however, depudecin mutants maintain virulence in Arabidopsis (Wight et al., 2009). Thus, the hypothesis that pathogens may directly manipulate their host's transcription through modulation of the histone acetylation level still needs to be verified. Regarding defence-related genes, no significant change in the level of H3K9 and H3K14 acetylation on PDF1.2a promoter was detected 24 h after MeJA treatment (Koornneef et al., 2008). Therefore, a direct involvement of histone acetylation in the transcriptional induction of JA/ET-dependent genes upon fungal infection is still lacking. However, several lines of evidence suggest that HDAs may promote defence responses against fungal pathogens. In Arabidopsis, the highly similar RPD3/HDA1-type deacetylase genes HDA6 and HDA19 were reported to be induced by JA or by the ET precursor ACC, whereas this was not the case for other RPD3-like HDA genes, such as HDA5, HDA8, HDA9 and HDA14, nor the HD2-type HD2A (Zhou et al., 2005). Overexpression of HDA19 leads to increased expression of ERF1, a gene that integrates JA/ET signalling pathways (Fig. 1), and to increased plant resistance to A. brassicicola. Interestingly, several JA/ET-induced PR genes were found to be upregulated in the HDA19-overexpressing transgenic line and downregulated in the silenced one (Zhou et al., 2005). However, regarding the multiple developmental abnormalities of hda19 mutants (Wu et al., 2000; 2003; Tian and Chen, 2001; Tian et al., 2005; Zhou et al., 2005), it could not be excluded that the effect observed on the JA/ET-inducible gene expression may be indirect. Similar to HDA19 deficiency, the HDA6-deficient lines displayed downregulated expression of JA-responsive genes (i.e. PDF1.2a, VSP2, JIN1 and ERF1; Wu et al., 2008). HDA6 was shown to interact in planta with the F-box protein COI1 (Devoto et al., 2002) as well as with the transcriptional repressor JAZ1 that form a co-receptor in presence of JA-Ile (Zhu et al., 2011). Therefore one may hypothesize that JA-Ile regulates the association between the SCFCOI1 complex, JAZ and HDA6. Thus, under high JA-Ile, JAZ and HDA6 proteins may be preferentially recruited to the SCFCOI1 for degradation. Under low JA-Ile, JAZ proteins would associate with HDA6 and together repress JA-responsive genes. In a different mechanism, HUB1 catalysing H2B mono-ubiquitination was reported as required together with the Mediator subunit MED21 for the resistance to necrotrophic pathogens (Dhawan et al., 2009). Despite the clear decreased and increased susceptibility to pathogens of 35S : HUB1 and hub1–6 plants, respectively, the expression of the defence marker PDF1.2a was not altered in these two backgrounds, suggesting that HUB1 may act on plant defence independently of the classical JA/ET signalling pathway. In addition, because hub1–6 mutants present a reduced cell wall thickness, authors proposed that HUB1 might regulate resistance by altering plant cell wall-related defence mechanisms (Dhawan et al., 2009). It remains to be investigated whether and how H2Bub is involved in plant defence. Regarding histone methylation, we found that SDG8, in addition to be involved in the transcription
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