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Epigenetic regulation of plant immunity: from chromatin codes to plant disease resistance

Epigenetic regulation of plant immunity: from chromatin codes to plant disease resistance aBIOTECH https://doi.org/10.1007/s42994-023-00101-z aBIOTECH REVIEW Epigenetic regulation of plant immunity: from chromatin codes to plant disease resistance 1,2 1,2& Si-Si Xie , Cheng-Guo Duan Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China University of the Chinese Academy of Sciences, Beijing 100049, China Received: 17 January 2023 / Accepted: 1 March 2023 Abstract Facing a deteriorating natural environment and an increasing serious food crisis, bioengineering-based breeding is increasing in importance. To defend against pathogen infection, plants have evolved mul- tiple defense mechanisms, including pathogen-associated molecular pattern (PAMP)-triggered immu- nity (PTI) and effector-triggered immunity (ETI). A complex regulatory network acts downstream of these PTI and ETI pathways, including hormone signal transduction and transcriptional reprogram- ming. In recent years, increasing lines of evidence show that epigenetic factors act, as key regulators involved in the transcriptional reprogramming, to modulate plant immune responses. Here, we sum- marize current progress on the regulatory mechanism of DNA methylation and histone modifications in plant defense responses. In addition, we also discuss the application of epigenetic mechanism-based resistance strategies in plant disease breeding. Keywords Histone modification, DNA methylation, Transcriptional reprogramming, Plant immunity, Disease resistance INTRODUCTION numbers, including mono-, di-, and tri-methylation (me1/2/3). Histone lysine methylation is a critical and Histone modifications and DNA methylation complex epigenetic marker that dynamically controls the transition between different transcriptional states. In eukaryotes, the genomic information is packaged as Another well-studied histone modification is histone nucleosomes, the basic units of chromatin. Each nucle- acetylation. It is generally assumed that histone acety- osome is composed of a core histone octamer (two lation interferes with the interaction within the nucle- copies of four core histone proteins H2A, H2B, H3, and osome, thereby leading to a more loose chromatin state H4) and 147 bp DNA. The N-terminal tails of these for transcriptional activation (Shahbazian and Grunstein histones are easily accessed and modified with various 2007). These epigenetic marks are dynamically regu- covalent modifications, such as methylation, acetylation, lated by different factors, including the enzymes that ubiquitination, phosphorylation, etc. (Kouzarides 2007), can catalyze/remove (‘‘writers/erasers’’) the modifica- a process called histone post-translational modification tion to/from the histone, and the proteins (‘‘readers’’) (PTM). Among them, histone methylation is a well- that recognize and link the modification with other characterized PTM. Histone methylation usually occurs molecules. Epigenetic modifications are generally able at lysine and arginine residues with different methyl to implement transcriptional and/or posttranscriptional regulation of such marked genes. More importantly, growing evidence shows that histone modification & Correspondence: cgduan@cemps.ac.cn (C.-G. Duan) The Author(s) 2023 aBIOTECH homeostasis is essential for the plant immunity histone modification, DNA modification, histone vari- regulation. ants, and ranges of noncoding RNA. In this review, we In addition to the modifications on histone tails, primarily focus on the mechanism of histone modifica- various modifications can also occur on the DNA strand, tion and DNA methylation in plant immunity regulation. among which the most prominent one is the methyla- tion of the carbon-5 of cytosine (5-mC). DNA methyla- Plant immune pathways tion can occur in different sequence contexts, including symmetrical CG, CHG, and asymmetrical CHH (H corre- In nature, plants are generally exposed to a complex sponds to A, T, or C) (Henderson and Jacobsen 2007), environment with a range of organisms and microor- and be present at promoters, introns, and transposable ganisms, including insects, bacteria, fungi, and viruses. elements (TEs). In plants, de novo DNA methylation is All these challenges have important influences on many established by a specific RNA-directed DNA methylation aspects of plant life, including growth, development, (RdDM) pathway. In Arabidopsis, a canonical RdDM crop yield, and adaptability to the environment. To model proposes that single-stranded RNA (ssRNA), adapt to these diverse biotic stresses, plants have produced by RNA POLYMERASE IV (Pol IV), can be evolved intricate mechanisms to recognize the charac- recognized by RNA-DEPENDENT RNA POLYMERASE 2 teristics of insects or microorganism and activate the (RDR2) to generate double-stranded RNA (dsRNA), appropriate immune response. Here, cell surface-local- which is processed into 24 nt small interfering RNAs ized pattern-recognition receptors (PRRs) can recognize (siRNAs) by DICER-LIKE 3 (DCL3). These siRNAs are the pathogen- or microbe-associated molecular patterns then loaded onto an RNA-induced silencing complex (PAMPs or MAMPs), such as bacteria flagellin or fungal (RISC) containing the Argonaute (AGO) protein (AGO4/ chitin, and induce PAMP-triggered immunity (PTI) 6/9). The nascent scaffold RNA produced by Pol V rec- (Bigeard et al. 2015). However, pathogens can gradually ognizes the siRNA–AGO complex through sequence escape from the host’s monitoring systems, due to long- pairing. Subsequently, AGO4 interacts with DOMAINS term coevolution of microorganisms and plants. There- REARRANGED METHYLASE 2 (DRM2), DEFECTIVE IN fore, plants evolved resistance (R) proteins to specifi- RNA-DIRECTED DNA METHYLATION 1 (DRD1), and cally recognize the effectors, delivered from pathogens, RNA-DIRECTED DNA METHYLATION 1 (RDM1) to which activates another immune response called effec- methylate the target DNA (Zhang et al. 2018a). In tor-triggered immunity (ETI) (Jones and Dangl 2006). addition to the de novo establishment of CHH methy- The PTI and ETI use different PRRs and intracellular lation, DNA methylation can also be maintained by dif- nucleotide-binding domain leucine-rich repeat contain- ing receptors (NLRs), respectively. However, they share ferent pathways. The symmetric CG methylation is maintained by METHYLTRANSFERASE1 (MET1) and some downstream effects, such as the activation of CHG methylation by CHROMOMETHYLASE2 and 3 mitogen-activated protein kinase (MAPK) cascades, (CMT2 and CMT3) in Arabidopsis (Zhang et al. 2018a). reactive oxygen species (ROS) generation, hormone The maintenance of asymmetric CHH methylation signaling transduction, and transcriptional reprogram- requires either CMT2 or RdDM (Huettel et al. 2006; Liu ming. Recent studies demonstrate that the influence of et al. 2014). DECRESED DNA METHYLATION 1 (DDM1), PTI and ETI appears to be mutual and the upregulation a chromatin remodeling protein, is also required for the of PTI components is also a feature of ETI (Ngou et al. maintenance of symmetric methylation (Zemach et al. 2021; Yuan et al. 2021). But how ETI can regulate PTI, 2013). DNA methylation is highly correlated with H3K9 or how PTI affects ETI still needs to be further explored. methylation and forms a positive feedback loop. In this Plant hormones are well known as important regu- loop, the H3K9me2-containing nucleosome can be rec- lator of plant growth, development and stress responses ognized by the BAH domain of DNA methyltransferase (Pieterse et al. 2009). In the last two decades, increasing CMT2/3 to confer non-CG methylation of the target evidence has demonstrated that the classical plant DNA. In turn, non-CG methylation can be recognized by hormones, salicylic acid (SA), jasmonic acid (JA), and the SAR domain of SUVH4/5/6 histone methyltrans- ethylene (ET) play key roles in the plant immune ferases to enhance the deposition of H3K9me2 (Duan response. Generally, SA is considered to participate in et al. 2018). In plants, the removal of DNA methylation the defense against biotrophic pathogens, whereas JA/ is mainly catalyzed by a pathway termed active DNA ET usually function in defense against necrotrophic demethylation. In Arabidopsis, four demethylases are pathogens. The biosynthesis and perception pathways encoded, including REPRESSOR OF SILENCING1 (ROS1), of these hormones are quite well studied. In the SA DEMETER (DME), DEMETER-LIKE 2 (DML2), and signaling pathway, accumulation of SA can result in DML3. The ‘‘chromatin codes’’ are generally composed of transformation of the SA receptor, NONEXPRESSOR OF The Author(s) 2023 aBIOTECH PR GENES 1 (NPR1), from an inactive to active form, activation of two transcriptional activator factors, followed by its translocation into the nucleus to facili- ETHYLENE-INSENSITIVE 3 (EIN3) and ETHYLENE- tate expression of the SA-dependent defensive genes, INSENSITIVE3-LIKE 1 (EIL1), thereby promoting such as PATHOGENESIS-RELATED GENE 1 (PR1), during expression of another branch of downstream JA-re- pathogen infection (Ding and Ding 2020) (Fig. 1). SA is sponsive genes, such as ETHYLENE RESPONSE FACTOR 1 also an important regulator of systemic acquired resis- (ERF1), OCTADECANOID-RESPONSIVE ARABIDOPSIS AP2 tance (SAR), which refers to the phenomenon by which 59 (ORA59), and PLANT DEFENSIN 1.2 (PDF1.2) (Li et al. infection of plant aerial tissues, by pathogens, results in 2022; Ruan et al. 2019). the systemic induction of a long-lasting and broad- Under normal conditions, ETHYLENE-INSENSITIVE 1 spectrum disease resistance. Accumulation of SA and (ETR1), the receptor for the gaseous hormone ET, acti- activation of the downstream signaling pathway are vates CONSTITUTIVE TRIPLE RESPONSE 1 (CTR1) to essential for SAR establishment (Kachroo and Robin repress the positive regulator, EIN2, via phosphoryla- 2013). tion. Upon perception of ET, the release of repression In the JA signaling pathway, jasmonoyl-L-isoleucine from CTR1 results in the activation of EIN2, which then (JAIle), the active form, is repressed by jasmonate ZIM- inhibits the degradation of EIN3 and EIL1, and further domain (JAZ) in the resting state. Once JA accumulates, activates downstream ET-responsive genes, such as JAIle can recognize CORONATINE INSENSITIVE 1 (COI1) ERF1 and ORA59 (Li et al. 2019b). COI1 of the SCF complex, leading to the degradation of JAZ The antagonism between the SA and JA signaling by the 26S proteasome. JAIle functions as a transcrip- pathways is well established. In Arabidopsis, NPR1 is tional activator to promote the expression of JA-re- required for the activation of many transcription factors, sponsive genes, such as JASMONATE INSENSITIVE 1 such as the TGACG-binding transcription factors (TGAs) (JIN1/MYC2) and its downstream genes (Fig. 1). More- and WRKYs, which are responsible for the suppression over, release of repression from JAZ leads to the of JA-responsive genes (Zhang et al. 2018b). In addition, Fig. 1 Pathogen-triggered transcriptional reprogramming in the plant immune response. BIK1 is quickly phosphorylated upon PRR 2? recognition of the elicitor, such as flg22, chitin, lectin, etc. Subsequently, several signaling events are activated, such as a Ca burst, ROS production, and MAPK cascade, resulting in transcriptional reprogramming in the nucleus. Epigenetic regulators, such as ATX1 and HAC1, are required for activation of the WRKYs. The PRC2 complex and JAZ promote silencing of the JA-responsive genes, whereas JMJ functions 2? 2? in their activation. In addition, a Ca signal is transduced by Ca binding with CaM, followed by binding to other proteins, such as CBP60g, to facilitate expression of the SA biogenesis gene, ICS1. The SA receptor, NPR1, recognizes SA and is then translocated into the nucleus to recruit the transcriptional activator, TGA, thereby promoting the expression of PR genes. Activation of PR genes can also be mediated by histone modifier genes, JMJ27 and JMJ705 The Author(s) 2023 aBIOTECH some WRKYs, such as WRKY50, WRKY51, and WRKY70, mutants, suggesting that ATX7 and SDG8 function syn- have also been shown to repress the expression of JA- ergistically in the regulation of plant immunity. ATXR7 responsive genes, via NPR1-independent pathways (Gao and SDG8 regulate plant immunity partially through et al. 2011;Li etal. 2004). Moreover, SA can repress the controlling the expression of CAROTENOID AND JA pathway through inhibition of the transcriptional CHLOROPLAST REGULATION 2 (CCR2) and FACELESS activities of MYC2 and ORA59 in Arabidopsis (Aerts et al. POLLEN 1 (FLP1/CER3), two genes that are associated 2021). In turn, the JA pathway can also exert a repres- with the biosynthesis of carotenoids and cuticle integ- sive effect on the SA pathway. For instance, three tran- rity, respectively. Similar with sdg8, atxr7, and the atxr7 scriptional factors ANAC019, ANAC055, and ANAC072, sdg8 double mutant, dysfunction of CCR2 and CER3 which function in suppression of the SA biosynthesis displays increased susceptibility to B. cinerea and A. enzyme, isochorismate synthase 1 (ICS1), need to be brassicicola (Lee et al. 2016). Several SDG8 studies also activated by MYC2 (Gimenez-Ibanez et al. 2017). By reported that SDG8 plays critical roles in plant defense sharing some common regulators, such as EIN3 and against necrotrophic fungal pathogens and hemi-bio- EIL1, the JA and ET pathways are synergistic (Liu and trophic pathogens, via activating JA/ET signaling path- Timko 2021). way marker genes, PDF1.2a, VSP2, MKK3, MKK5, and the R gene, LAZ5, respectively (Berr et al. 2010; Palma et al. 2010). Loss of function of SDG8 results in faster HISTONE MODIFICATIONS IN PLANT IMMUNITY hypersensitive responses (HRs) to Pst DC3000 and Pst REGULATION DC3000 hrpA strains (De-La-Pena et al. 2012). In plants, removal of the histone methyl group is Histone methylation in plant immunity achieved through two classes of demethylases, Jumonji regulation C domain-containing proteins (JMJs) and LSD1-like (LDL) proteins (Jiang et al. 2007;Luetal. 2008). In Generally, histone H3 lysine 4 trimethylation (H3K4me3) Arabidopsis, the H3K4 demethylase, JMJ14, positively and H3K36me2/3 are associated with transcriptionally modulates plant immunity and represses gene expres- active regions, whereas H3K9me2 and H3K27me3 are sion of the negative regulator SUPPRESSOR OF NPR1-1 associated with silenced regions. H3K4me is catalyzed by INDUCIBLE 1 (SNI1), via removing the H3K4me3 from a conserved protein complex (COMPASS-like complex) and the locus. In addition, JMJ14 was also shown to be is mainly located in euchromatin. Seven SET domain pro- required for systematic defense. Loss of function of teins (SDGs), including ARABIDOPSIS TRITHORAX 1 JMJ14 leads to attenuation in the local defense response, (ATX1/SDG27), ATX2 (SDG30), ATX3 (SDG14), ATX4 and reduced Pip accumulation in distal leaves during (SDG16), ATX5 (SDG29), ARABIDOPSIS TRITHORAX- pathogen invasion (Li et al. 2020). RELATED7 (ATXR7/SDG25), and ATXR3 (SDG2), are pro- In Arabidopsis, four LDL genes (LDL1-4) have been posed to mediate the deposition of H3K4 methylation in identified. Among them, LDL4/FLOWERING LOCUS D Arabidopsis. (FLD)/REDUCED SYSTEMIC IMMUNITY1 (RSI1)is A number of H3K4 methyltransferases have been required for the activation of WRKY29 and WRKY6 implicated in plant immunity regulation. ATX1 has been genes, through H3K4me3 dynamics, and differential identified as a ‘master regulator’ in activating expres- influences on the expression of WRKY38, WRKY65 and sion of the transcription factor, WRKY70, by promoting WRKY53 (Singh et al. 2014b). Furthermore, GLU- H3K4me3 deposition (Alvarez-Venegas et al. 2007) TATHIONE S-TRANSFERASE THETA 2 (GSTT2), a mem- (Fig. 1). ATX1 may indirectly activate PR1 and repress ber of the glutathione S-transferase theta class, was THI2.1 expression, thereby contributing to a rapid plant shown to be associated with LDL4 and functions in response to pathogen infection (Alvarez-Venegas et al. activating SAR, probably through influencing H3KAc and 2007). ATXR7, a Set1 class H3K4me methyltransferase, H3K4me2/3 levels at WRKY6 and WRKY29 (Banday and was reported to be implicated in regulation of PTI, ETI, Nandi 2018). Subsequently, it was shown that LDL4 acts and SAR immune pathways, together with a H3K36 as a positive regulator of plant defense against the methyltransferase, SDG8 (Lee et al. 2016). These necrotrophic fungi B. cinerea and Alternaria alternata. authors observed that atxr7 and sdg8 mutants display More importantly, the ldl4 mutants are partially defec- enhanced susceptibility to Botrytis cinerea, Pseu- tive in JA signaling, but hyperactive in ethylene signaling domonas syringae pv tomato DC3000 (Pst DC3000), or (Singh et al. 2019). Recently, the ldl1 ldl2 double mutant Alternaria brassicicola infection. was shown to exhibit resistance to Pst DC3000, which Of importance, the atxr7 sdg8 double mutant showed may be caused, in part, by H3K4me3-dependent additive susceptibility, compared with the single upregulation of WRKY22/40/70 genes (Noh et al. 2021). The Author(s) 2023 aBIOTECH In rice, another H3K4me2/3 demethylase, JMJ704, was H3K9me is a typical heterochromatin marker that shown to be a positive regulator in plant defense against generally associates with DNA methylation. In Ara- Xanthomonas oryzae pv. Oryzae (Xoo). Here, JMJ704 bidopsis, H3K9me2 and H3K9me1 predominantly exist, represses the expression of a subset of negative regu- whereas H3K9me3 is barely detected. KRYPTONITE lators in plant defense, such as NRR, OsWRKY62, and Os- (KYP)/SU(VAR)3–9 homolog 4 (SUVH4) was the first 11N3, by removing H3K4me2/3 and maintaining a identified H3K9 methyltransferase and it functions, transcriptionally inactive state (Hou et al. 2015). partially redundantly with SUVH5 and SUVH6, in cat- In higher plants, Polycomb group (PcG) proteins alyzing H3K9 methylation in plants (Ebbs and Bender associate with different proteins to form multiple pro- 2006; Jackson et al. 2002; Zhang et al. 2023). A recent tein complexes, named Polycomb Repressive Complex 2 study showed that SUVH4/5/6 represses the expression (PRC2) and PRC1, which synergize to maintain gene of PRR/NLR genes and downstream associated defense silencing. The core components of PRC1/2 are con- genes. The suvh4 suvh5 suvh6 triple mutant displays served in animals and plants. Three H3K27 methyl- greater resistance to Pst DC3000 than wild type plants transferases of the PRC2 complexes have been identified (Cambiagno et al. 2021). In addition, SUVH4 was also in Arabidopsis, including MEDEA (MEA), CURLY LEAF shown to be involved in the regulation of pathogen- (CLF), and SWINGER (SWN). Recently, MEA was shown induced programmed cell death (Dvorak Tomastikova to negatively regulate plant immunity. Overexpression et al. 2021). of MEA results in enhanced susceptibility to B. cinerea, The IBM1, a major H3K9 demethylase in Arabidopsis, Pst DC3000 and Pst-AvrRpt2. In addition, MEA is asso- also participates in plant immunity regulation. The ibm1 ciated with a transcription factor, DROUGHT-INDUCED mutants are hyper-susceptible to the bacteria pathogen 19 (DIL9), and is recruited to the promoter of RESIS- Pst DC3000. IBM1 could directly target defense genes TANT TO P. SYRINGAE 2 (RPS2) to repress its expression PR1, PR2, and FLG22-INDUCED RECEPTOR-LIKE KINASE by deposition of H3K27me3, leading to an attenuated 1 (FRK1) and activate their expression during pathogen defense response (Roy et al. 2018). infection (Chan and Zimmerli 2019). However, a very The LIKE HETEROCHROMATIN PROTEIN 1 (LHP1), a recent study showed that the ibm1 mutant displays subunit of PRC1 responsible for H3K27me3 recognition, increased resistance to Pst DC3000 (Lv et al. 2022). The acts as a repressor of the MYC2-dependent immune JMJ27, a H3K9 demethylase, is required for resistance to pathway. The lhp1 mutant displays reduced SA content virulent Pst DC3000. In this case, JMJ27 functions as a and is more susceptible to Pst DC3000 (Ramirez-Prado negative mediator of the defense repressor gene, et al. 2019). A recent study revealed that the histone WRKY25, and a positive regulator of PR genes (Dutta modifications H3K27me3 and H3K4me3 work together et al. 2017). All above studies show histone methyl- to affect expression of stress-responsive genes to transferases and demethylases are widely involved in respond to powdery mildew in hulless barley (Zha et al. plant immune regulation (Fig. 2). 2021). In Arabidopsis, REF6, an H3K27me3 demethy- lase, has been shown to form positive feedback with Histone acetylation in plant immunity regulation HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2) to maintain the activation of HSFA2 and degradation of Histone acetylation also plays vital roles in immunity SUPPRESSOR OF GENE SILENCING 3 (SGS3), during regulation (Fig. 2) and is catalyzed by distinct HAT transgenerational inheritance, and the degradation of families, including GENERAL CONTROL NON- SGS3 could result in reduced trans-acting siRNA DEREPRESSIBLE 5 (GCN5)-RELATED ACETYLTRA (tasiRNA) production. The REF6-HSFA2 loop and NSFERASE (GNAT), p300/CREB (cAMP-RESPONSIVE reduced tasiRNA converge to release HEAT-INDUCED ELEMENT-BINDING PROTEIN)-BINDING PROTEIN TAS1 TARGET 5 (HTT5), which drives early flowering (CBP), TATA-BINDING PROTEIN-ASSOCIATED FACTOR 1 and attenuates immunity (He 2019). In rice, JMJ705 (TAFII250), and MOZ-YBF2/SAS3-SAS2/ TIP60 (MYST) encodes an H3K27me2/3 demethylase, and JMJ705- (Pandey et al. 2002). GCN5, a catalytic subunit of the mediated H3K27me demethylation is required for basal acetylating modification complex, Spt-ADA-Gcn5- and induced expression of disease resistance genes (Li Acetyltransferase (SAGA), was previously shown to et al. 2013). JMJ705 is induced during pathogen infec- influence H3K14ac and H3K9ac level on its targets, but tion, and JMJ705 loss of function results in enhanced is not strictly coupled to transcriptional activation of the susceptibility to Xoo. Moreover, JMJ705 dynamically target genes (Benhamed et al. 2008). A recent study removes H3K27me3 from responsive genes, such as proposed that GCN5 has a dual role in transcriptional JAMYB, PR10, TPS3, and Os07g11739, during MeJA regulation and repression of SA-mediate immunity. induction (Fig. 1). Dysfunction of GCN5 leads to a decrease of H3K14ac in The Author(s) 2023 aBIOTECH Fig. 2 The effects of histone modifiers in plant immune regulation. Histone modifiers are widely implicated in the regulation of an immune response through dynamically modulating the expression of master regulatory genes in hormone (SA, JA/ET) signaling pathways. According to their effects on plant resistance, histone modifiers are divided into two categories: positive and negative regulation. The green icons represent positive regulators, whereas the yellow icons represent negative regulators, in the regulation of disease response the 5’end of down-regulated targets, and an increase in complex can then be recruited to PR genes to facilitate the 3’ ends of up-regulated targets. This suggests that transcription, through deposition of H3Ac, and a GCN5 could either activate or repress gene expression response to SA-triggered immunity (Jin et al. 2018). by controlling H3K14ac distribution on its target genes. Based on their homology to yeast, histone deacety- Moreover, GCN5 functions as a repressor of SA-mediated lases (HDACs) can be divided into three groups: immunity by reducing SA accumulation (Kim et al. REDUCED POTASSIUM DEPENDENCY3 (RPD3), HIS- 2020). An earlier study showed that a Phytophthora TONE DEACETYLASE1 (HDA1), and SIRTUIN2 (Pandey effector, PsAvh23, could affect the assembly of the SAGA et al. 2002; Yang and Seto 2003). In addition, type-II complex by breaking the association of GCN5 and reg- HDAC (HD2) also has histone deacetylation activity, but ulatory subunit Alteration/Deficiency in Activation 2 is plant-specific (Dangl et al. 2001). HDA19, an RPD3 (ADA2) and suppressing the activation of defense genes type histone deacetylase in Arabidopsis, can be induced in soybean (Kong et al. 2017). by JA, ET, wounding, and pathogens. Overexpression of In addition to the GNAT family, a member of the HDA19 causes increased expression of PR genes and p300/CBP family, HISTONE ACETYLTRANSFERASE OF enhanced resistance to Alternaria brassicicola (Zhou THE CBP FAMILY 1 (HAC1) and HAC5 also play impor- et al. 2005). WRKY38 and WRKY62, two members of tant roles in immune response. The HAC1/5 can form a WRKY group III transcription factors, are required for complex with NPR1 and TGAs and this HAC–NPR1–TGA transcriptional activation and SA-mediated suppression The Author(s) 2023 aBIOTECH of JA signaling, with functional redundancy (Kalde et al. rice broad-spectrum resistance against rice pathogens 2003; Mao et al. 2007). HDA19 can interact with (Chen et al. 2022). WRKY38 and WRKY62 to repress their transcriptional SRT2, a NAD -dependent deacetylase of the SIR- activation activity. Moreover, the had19 mutant displays TUIN2 and HD2 family, is able to negatively regulate increased susceptibility to Pst DC3000 (Kim et al. 2008). plant basal defense against Pst DC3000, via suppressing However, it has also been reported that HDA19 loss of SA biosynthesis. The expression of key master regula- function causes increased SA content and increased tors in the SA biosynthesis pathway, including PAD4, expression of a group of genes required for accumula- EDS5, and SID2, was increased in the srt2 mutant and tion of SA and PR genes, such as PR1 and PR2, resulting decreased in SRT2 overexpression plants (Wang et al. in enhanced resistance to Pst DC3000 (Choi et al. 2012). 2010). In rice, the HD2 subfamily histone deacetylase A similar mechanism was also shown in the regulation HDT701 negatively regulates plant innate immunity by of HDA6-mediated plant immunity. HDA6 constitutively modulating histone H4 acetylation of PRR and defense- represses the expression of pathogen-responsive genes, related genes in response to Xoo infection (Ding et al. including PR1 and PR2, through decreasing histone 2012). Additionally, an Arabidopsis HD2 class of H3K9ac acetylation levels at their promoters (Wang et al. 2017). deacetylase, HD2B, was identified to be targeted by MAP The following study showed that this may be caused by kinase MPK3 and plays an important role in bacteria HDA6-mediated suppression of SA biosynthesis. HDA6 defense. In this case, MPK3 directly phosphorylates can directly bind to the promoter regions to repress the HD2B, thereby conferring its relocation to the nucleus to expression of CALMODULIN-BINDING PROTEIN 60 g regulate H3K9 acetylation levels of biotic stress (CBP60g) and SYSTEMIC-ACQUIRED RESISTANCE-DEFI- response genes (Latrasse et al. 2017). Furthermore, CIENT 1 (SARD1) through histone deacetylation (Wu HD2C functions as a positive regulator in defending et al. 2021). A very recent study reported that the against Cauliflower mosaic virus (CaMV) infection. Loss acetylation level of TOPLESS is antagonistically regu- of function of HD2C results in an increased histone lated by GCN5 and HDA6 to respond to the regulation of acetylation level on the viral mini-chromosomes, which JA signaling (An et al. 2022). caused enhanced susceptibility to CaMV. Intriguingly, TOPLESS is a conserved Groucho/thymidine uptake 1 the P6 protein of CaMV could destroy the function of (Gro/Tup1) family corepressor and is required for the HD2C through interfering with the HD2C–HDA6 inter- repression of JA-responsive gene expression (Pauwels action (Li et al. 2021b). et al. 2010). GCN5-mediated acetylation of TOPLESS facilitates TPL–NINJA interaction and recruitment to the Histone ubiquitination and other modifications promoter of MYC2 targets for gene repression. Con- in plant immunity regulation versely, HDA6-mediated deacetylation of TOPLESS weakens the TPL–NINJA interaction and activates Compared to histone methylation and acetylation, the expression of a JA-responsive gene (An et al. 2022). function of histone ubiquitination in regulating plant In wheat, TaHDA6 interacts with TaHOS15 and is immunity has been less explored. However, the limited recruited to defense responsive genes, including TaPR1, studies indicate the important involvement of histone TaPR2, TaPR5, and TaWRKY45, to fine-tune defense ubiquitination in the plant defense response (Fig. 2). responses to powdery mildew (Liu et al. 2019). HDA9 is HISTONE MONOUBIQUITINATION1 (HUB1), a RING E3 also a member of the RPD3-like group and interacts ligase of histone 2B monoubiquitination, was reported with HOS15 to function as a negative regulator of to be an important regulator of plant defense against immunity. Importantly, HOS15 can repress these NLR necrotrophic fungal pathogens (Dhawan et al. 2009). In genes, including SUPPRESSOR OF NPR1-1, CON- addition, HUB1 and another E3 ligase, HUB2, have roles STITUTIVE1 (SNC1), under both pathogen infection and in the depolymerization of cortical microtubules, the resting state. However, HDA9 can only repress the through positively regulating the expression of key NLR genes during pathogen infection (Yang et al. 2020). protein tyrosine phosphatase genes and promoting This suggests that HDA9 is involved in the repression of protein tyrosine phosphorylation during the defense NLR genes during a response to pathogen infection, and response to Verticillium dahliae toxins (Hu et al. 2014). there may be other factors involved in the repression of Additionally, HUB1 and HUB2 can upregulate expres- NLR genes, by HOS15, in the resting state. Interestingly, sion of the R gene, SNC1, by promoting the deposition of pathogens have also developed antagonism strategies H2B monoubiquitination, and are required for autoim- for better infection. A recent study showed that a mune responses in the bon1 mutant (Zou et al. 2014). In secreted fungal effector, UvSec117, can target the rice tomato, SlHUB1 and SlHUB2 can positively regulate histone deacetylase OsHDA701 and negatively regulate plant defense response to B. cinerea through modulating The Author(s) 2023 aBIOTECH the balance between the SA- and JA/ET-mediated sig- geminivirus infection. Consistently, a number of DNA naling pathways (Zhang et al. 2015). methylation- and RdDM-deficient mutants have been In rice, an emerging post-translational modification shown to display enhanced susceptibility to gemi- lysine 2-hydroxyisobutyrylation (K ) has been impli- niviruses (Raja et al. 2008). Loss of function of NRPD2, hib cated in plant immunity. Histone deacetylases, the second largest subunit of Pol IV and Pol V, also leads OsHDA705, OsHDA716, OsSRT1, and OsSRT2, are all to increased susceptibility to the necrotrophic fungal responsible for the removal of K marks. Among them, pathogens B. cinerea and Plectosphaerella cucumerina. hib OsHDA705 was further shown to negatively regulate The other mutants involved in different steps of the rice disease resistance. Dysfunction of OsHDA705 RdDM pathway, such as nrpe1, ago4, drd1, rdr2, and enhanced resistance to Ustilaginoidea virens, the bacte- drm1 drm2, have similar phenotypes with nrdp2 during rial blight pathogen Xoo and the rice blast fungus, M. pathogen infection (Lopez et al. 2011). Through DNA oryzae. Importantly, histone Khib functions as an active methylation sequencing of plants exposed to different marker for gene transcription, and is involved in regu- biotic stresses, Dowen et al. (2012) reported that the lating the expression of R genes (Chen et al. 2021). DNA methylation changes in repetitive sequences, or transposons, could affect the expression of neighboring genes in response to SA stress. The CG methylation DNA METHYLATION IN PLANT IMMUNITY mutant (met1-3, ddm1) and non-CG methylation REGULATION mutants (ddc, drm1-2 drm2-2 cmt3-11, rdr1, rdr2, rdr6, drd1, nrpd1a, and dcl2 dcl3 dcl4) displayed enhanced The important participation of DNA methylation in plant resistance to Pst DC3000. immunity regulation has been well established (Fig. 3). In recent years, whole-genome bisulfite sequencing For example, the methylation level of viral DNA is studies have revealed that DNA hypomethylation is decreased in Arabidopsis 5-mC-deficient mutants after often associated with enhanced resistance during Fig. 3 DNA methylation-dependent regulation of R gene-mediated immunity. Specific pathogens cause plant disease through the secretion of effectors into host cells. In the resting state, the promoter region of R genes is hyper-methylated and silenced by the RdDM pathway. The DNA demethylase, ROS1, can antagonize the silencing of R genes through DNA demethylation, during infection, thereby promoting the expression of R genes. In another case, the intragenic hyper-methylation can recruit the AAE protein complex to promote the production of full-length transcripts of R genes. Impairment of DNA methylation, or the AAE complex, results in mis-splicing or proximal polyadenylation, facilitating the production of intact R protein. Then, the R protein can activate ETI immune responses through recognition of the effectors. The ETI immune response may also have an important effect on the dynamic regulation of the DNA methylation state on R genes The Author(s) 2023 aBIOTECH pathogen infection. For example, in wheat, infection (RLP43) and catalyze DNA demethylation during flg22 with Blumeria graminis f. sp. tritici resulted in a signif- induction, thereby indirectly promoting the binding of icant decrease in CHH methylation and downregulation WRKY transcriptional factors to the W-box motif of of AGO4a (Geng et al. 2019). Consistent with these RLP43 and activating gene expression. findings, in Arabidopsis, infestation with the green peach The gene-for-gene resistance model proposes that aphid leads to DNA hypomethylation in hundreds of loci, one avirulence gene in distinct races of microorganisms particularly transposable elements (Annacondia et al. can be recognized by genetically interacting with the 2021). In addition, upon treatment with nematode-as- corresponding R gene in plants, thereby leading to plant sociated molecular patterns from different nematode disease resistance (Dangl and Jones 2001). The largest species, or the bacterial pathogen-associated molecular class of R genes encodes a nucleotide-binding site plus pattern, flg22, both rice and tomato plants displayed leucine-rich repeat (NB-LRR) class of proteins. R genes global DNA hypomethylation. Intriguingly, hypomethy- are usually clustered in regions enriched for TEs and lation mainly occurred in CHH methylation (Atighi et al. repetitive sequences, wherein 5-mC and H3K9me2 are 2020). Apart from the factors associated with the RdDM densely deposited. These repressive markers can pre- pathway and enzymes that catalyze methylation, Ara- vent TE activation to facilitate the integrity of NB-LRR bidopsis ELONGATOR SUBUNIT 2 (ELP2) was shown to genes and stabilize chromatin structure. be required for pathogen-induced rapid transcriptome DNA hypomethylation may promote the recombina- reprogramming, through altering methylation levels of tion and evolution of R genes (Alvarez et al. 2010). specific methyl cytosines (Wang et al. 2013). In addition, Therefore, DNA methylation homeostasis is essential for MED18, a subunit of mediator, is associated with NRPD2 R gene expression and plant resistance (Fig. 3). PigmS, a to regulate the immune response through modulating rice NLR receptor, was reported to suppress the PigmR- the expression of defense-related genes (Zhang et al. mediated broad resistance to pathogen by interfering 2021a). with the formation of PigmR homodimerization. The It would seem that plants undergo a global PigmS promoter contains two tandem miniature trans- hypomethylation upon perceiving pathogen signals. For posons, MITE1 and MITE2. The expression of PigmS was example, flg22 (bacteria elicitor) can trigger the down- affected by DNA methylation level in MITE1 and MITE2 regulation of a series of RdDM gene expression, mediated by the RdDM pathway. The lower DNA including AGO4, AGO6, NRPD2, NRPD7, Nuclear RNA methylation in MITE1 and MITE2 increased the gene Polymerase E7 (NRPE7), NRPE5, INVOLVED IN DE NOVO expression of PigmS, and further compromised PigmR- 2 (IDN2), KOW DOMAIN-CONTAINING TRANSCRIPTION mediated resistance (Deng et al. 2017). FACTOR 1 (KTF1), DRD1, and MET1. The downregulation It is generally accepted that cytosine methylation of of these genes results in hypomethylation within the the promoter region often plays a repressive role in RdDM loci during flg22 induction. Moreover, DNA modulating expression of the gene. However, an earlier demethylase ROS1 facilitates the demethylation of an study showed that promoter DNA methylation plays a RdDM target (also a disease resistance gene) TNL novel enhancing role in resistance to the pathogen. For RESISTANCE METHYLATED GENE 1 (RMG1) and is example, the fungal pathogen, Magnaporthe grisea, can associated with the activation of a SA-dependent induce the expression of Pib, an NLR gene in rice. defense response (Yu et al. 2013). Consistent with this Notably, the DNA methylation level in the promoter finding, the DNA demethylase triple mutant, rdd (ros1 region (contains heavy CG methylation) of Pib is dml2 dml3), displays increased susceptibility to the increased after infection by this fungal pathogen (Li fungal pathogen, Fusarium oxysporum. In addition, DNA et al. 2011). Furthermore, some studies have shown that demethylases can positively regulate the expression of DNA methylation not only represses gene expression stress response genes enriched with transposon or but also activates gene expression at different targets repeat sequence in their promoter regions for defense (Harris et al. 2018; Shibuya et al. 2009). Collectively, against fungal pathogens (Le et al. 2014). Intriguingly, these studies indicate that DNA methylation is involved among those defense genes mis-expressed by pathogen in the regulation of plant immunity, through balancing infection in a ros1 mutant, only a few were accompanied the transcriptional repression and activation effects to by DNA methylation changes (Sanchez et al. 2016). fine-tune the expression of different defensive genes. Hence, the molecular mechanism of how ROS1 mediates DNA methylation not only regulates the expression of transcriptional reprogramming in immune response has R genes, but also modulates the length of the R gene been a mystery. However, recently, Halter et al. (2021) transcript (Fig. 3). RPP7, which encodes a CC-NB-LRR reported that ROS1 can directly bind to the promoters protein and contains a Ty-1 COPIA-type retrotransposon of RMG1 and ORPHAN RECEPTOR-LIKE PROTEIN 43 (also named COPIA-R7), is specifically enriched with the The Author(s) 2023 aBIOTECH H3K9me2 marker in the sense orientation of the first ASSEMBLY FACTOR 1 (CAF1), a histone chaperone, intron, contributes to disease resistance during mediates the repression of priming of defensive genes, Hyaloperonospora parasitica infection (Eulgem et al. under non-inductive conditions. Consistent with this 2007). ENHANCED DOWNY MILDEW 2 (EDM2), Anti- model, dysfunction of CAF1 resulted in spurious acti- silencing 1 (ASI1) and ASI1 immunoprecipitated protein vation of SA-dependent defense response accompanied 1 (AIPP1) form a protein complex (designated as AAE with low nucleosome occupancy and high H3K4me3 at complex) that recognizes and affects the H3K9me2 at the transcription start sites of defensive genes (Mozgova COPIA-R7 to promote the 3’ distal polyadenylation et al. 2015). (Duan et al. 2017; Lei et al. 2014; Tsuchiya and Eulgem Some studies have provided evidence showing that 2013). The intronic heterochromatin has been shown to DNA methylation is implicated with transgenerational be required for the distal polyadenylation of the RPP7 SAR. An earlier finding showed that the next generation gene. Abnormal expression of the RPP7 transcript of tobacco displays enhanced resistance to TMV, Pseu- occurred in the ddm1 and suvh4 suvh5 suvh6 mutants domonas syringae,or Phytophthora nicotianae, after (Zhang et al. 2021b). Similarly, another R gene, RPP4, infection during the first generation. TMV infection can was also shown to be regulated by the AAE complex enhance homologous recombination frequency and (Deremetz et al. 2019; Zhang et al. 2021b). The RPP4 induce expression of PR1 and promote callose accu- partially overlaps with a COPIA4-like retrotransposon mulation to mediate resistance against the pathogen in (AT4TE42860), at its 3 terminal exon region, and facil- the second generation (Kathiria et al. 2010). A subse- itates disease resistance to Hyaloperonospora parasitica quent study showed that descendants could acquire (Garcia et al. 2010). Dysfunction of this AAE complex resistance after the infection with Pst DC3000, in the leads to the mis-splicing of the RPP4 transcript (Zhang first generation. This transgenerational SAR effect is et al. 2021b). These examples support the notion that regulated by the RdDM pathway and transmitted by intragenic heterochromatin, caused by TE insertions, hypomethylation at CHG sites (Luna and Ton 2012). serve as an important regulatory element in R gene These findings suggest that the inheritance of a specific expression. DNA methylation pattern may contribute to the regu- lation of transgenerational SAR. However, how DNA methylation contributes to transgenerational SAR EPIGENETIC REGULATION IN DEFENSE PRIMING remains to be elucidated. It is possibly that the DNA AND TRANSGENERATIONAL SAR methylation state and the accumulated of effector pro- teins, in the first generation, will be gamete-transmitted Plants can respond faster or show more resistance to to the next generation, or re-established in the second environment challenges when previously exposed to a generation. moderate stress. After suffering from mild environment stress, plants will be primed and form a ‘memory’ to be better equipped to cope with the situation when again APPLICATION OF EPIGENETICS TO PLANT encountering this stimulus. Priming involves changes in IMMUNITY histone modifications, DNA methylation and accumula- tion of inactive MAPKs and transcriptional factors To survive in adverse conditions, plants have evolved (Beckers et al. 2009; Jaskiewicz et al. 2011; Luna and diverse mechanisms to enhance resistance to pathogens. Ton 2012; Singh et al. 2014a). For example, H3 and H4 Epigenetic regulation gradually becomes an efficient acetylation, as well as H3K4 methylation, on the WRKY tool to overcome the challenges from biotic stress. promoter may promote priming of genes during Epigenetic mechanism-mediated crop disease resistance pathogen infection or treatment with the SA synthetic strategies are being employed in crop breeding (Fig. 4). analog, acibenzolar S-methyl (Jaskiewicz et al. 2011). For instance, some chemical agents have been identified Interestingly, abiotic stress could trigger the priming of that enhance plant resistance through an epigenetic biotic stress. For example, the hac1-1 mutant displays mechanism. In rice, application of 5-azadeoxycytidine, a increased susceptibility to Pst DC3000 after repetitive DNA de-methylating agent, enhances plant resistance to stress (cold, salt, and heat), but there was no obvious the bacterial pathogen Xanthomonas (Akimoto et al. distinction, compared to wide type, during nonstress. 2007). Additionally, in plants, the chemical SAR inducer Moreover, the expression of PTI-responsive genes b-aminobutyric acid (BABA) was shown to enhance WRKY53, FRK1, and NHL10 failed to be activated in the resistance to various pathogens, including the hemi- hac1 mutant, after repetitive heat stress (Singh et al. biotrophic bacterium Pst DC3000, the necrotrophic 2014a). It has been reported that CHROMATIN fungus B. cinerea, and the oomycete pathogen P. The Author(s) 2023 aBIOTECH Fig. 4 Epigenetic regulation-based plant disease resistance strategy. Spraying a chemical reagent, BABA, onto pants can induce high expression of defensive genes (such as FRK1, NHL10) through facilitating the deposition of H3K4me3 and H3K36me3. In addition to affecting the expression of immune-related genes, BABA can also induce SAR to enhance plant resistance during a pathogen infection. dCAS9 could be used as a tool for activating or repressing the histone modifiers and further fine-tune plant immune response, via modulating expression of downstream defensive genes. Zinc-finger-fused epigenetic regulators can also be utilized for promoting the establishment of DNA hyper-methylation, through the RdDM pathway, in the promoter regions to repress expression of the susceptibility genes and improve the tolerance to pathogen infection in future. ZFP, zinc finger protein parasitica, through affecting the histone modification initial treatment. After a 48 h treatment, NPR1 was and inducing defensive gene expression (Martinez- repressed by the accumulation of H3K27me3, whereas Aguilat et. 2016; Zimmerli et al. 2000, 2001). Moreover, SNI1, the negative regulator of SAR, was activated by an BABA induces resistance against P. parasitica in trans- increase in H3K4me2 level (Meller et al. 2018). BABA genic NahG (salicylate hydroxylase) plants. Thus, BABA has been widely used to improve the disease resistance mainly activates the SAR pathway downstream of SA in crops, such as common bean, potato, grapes, tomato, accumulation (Zimmerli et al. 2000). Another study pepper, cabbage, and fruits (Hamiduzzaman et al. 2005; showed that BABA treatment induces the deposition of Janotik et al. 2022; Kim et al. 2013;Li etal. callose, stomatal closure, and expression of the defen- 2019a, 2021a; Martinez-Aguilat et. 2016; Meller et al. sive gene, PR1, in the SA pathway and other PTI-re- 2018). These studies also have shown that enhanced sponsive genes, including those that facilitate resistance resistance, induced by chemical agents, depends on the to the necrotrophic bacterium, Pectobacterium caro- regulation of epigenetic markers. tovorum subsp. carotovorum (Pcc), in Arabidopsis (Po- Importantly, DNA methylation and histone modifica- Wen et al. 2013). tion can be manipulated by several approaches. The In common bean, BABA treatment can prime the SUVH2/9 proteins are two inactive histone methyl- expression of many defense genes. Interestingly, the transferase, due to their lack of a post SET domain that levels of several histone modifications, such as is required for cofactor and peptide substrate-binding. H3K4me3 or H3K36me3, are higher in the promoter Johnson et al (2014) used Zinc Finger (ZF) fused with regions for different defense genes, during 24 h after SUVH2/9 to establish DNA methylation, at an BABA treatment, but are not accompanied by obvious unmethylated site, through the RdDM pathway. The fwa- accumulation of defensive gene transcripts. The actual 4, an unmethylated epiallele of FWA, was observed to be activation of defensive genes occurs 24 h after BABA successfully methylated and the ZF–SUVH2/fwa-4 plant treatment (Martinez-Aguilat et. 2016). In potato, histone displayed an early flowering phenotype. Moreover, the lysine methylation, but not acetylation, appears to altered DNA methylation could be stably transmitted to function in BABA-triggered resistance. BABA induces the next generation (Johnson et al. 2014). A synthetic ZF, higher level of H3K4me2 in NPR1, the positive regulator fused to the Arabidopsis DEFECTIVE IN MERISTEM of SAR, to respond to Phytophthora infestans during SILENCING 3 (DMS3), a component of the RdDM The Author(s) 2023 aBIOTECH pathway, was employed to deposit DNA methylation at plant defense and successful infection by pathogens the promoter of a susceptibility (S) gene, MeSWEET10a, depend upon the dynamic regulation of epigenetic in cassava. Methylation in this promoter prevented the markers, to activate or repress, the expression of binding of the transcription activator-like (TAL) effector, defensive genes. In general, the transcriptional repro- TAL20, which prevented transcriptional activation of gramming, mediated by chromatin modifications, acts MeSWEET10a and showed a decrease in bacterial blight downstream of immune signaling pathways. Although symptoms in these cassava plants (Veley et al. 2023). A many chromatin regulators have been identified to play similar approach for selectively targeting epigenetic a role in plant immunity, the reported mechanisms silencing could be developed in future studies to mod- mostly focus on how the specific regulator affects some ified key defensive genes for improvement of disease key defensive genes, through changing the chromatin resistance in other crop species (Fig. 4). modifications. However, how these epigenetic factors In addition, CRISPR/dCas9-mediated manipulation of are recruited by immune factors to defense genes histone modifications has also been reported in plants. remains largely unsolved. Hence, more detailed regula- Interfering (CRISPRi) or activation (CRISPRa) of tar- tory mechanisms need to be further explored in future. geted genes is mediated by genetically fusing effector Some important questions include: what are the proteins to dCas9. CRISPR/dCas9-mediated histone dynamics of epigenetic factors before and after patho- modification regulation has been applied in response to gen infection? how do epigenetic regulators induce the abiotic stress. For example, HAC1-fused dCas9 trans- plant response at the single cell level after infection? genic plants were generated to improve drought stress how do plants achieve their return to a resting state tolerance through the transcriptional activation of the after a period of defense? and how do plants trans- positive regulator, ABSCISIC ACID-RESPONSIVE ELE- mit/maintain the ‘‘stress memory’’ to the next genera- MENT-BINDING FACTOR 2 (ABF2/AREB1) (Roca Paixao tion? Answers to these questions will help us gain a et al. 2019). Therefore, similar strategies could also be deeper understanding of how plants respond to patho- employed to engineer plant disease resistance through gen infection and make corresponding changes at the targeting of key regulators of plant defense. For exam- chromatin level. Such knowledge will facilitate the ple, spraying artificial 24-nt siRNAs may be used to development of more efficient disease resistance induce RdDM pathway-mediated silencing of defense strategies based on epigenetic mechanisms. repressive genes to confer immune activation (Fig. 4). Acknowledgements We apologize to all the colleagues whose This approach deserves further exploration in future. work could not be fully cited in this review due to a space limi- tation. This work was supported by a grant from the National Natural Science Foundation of China (32270200 to CGD). CONCLUSION AND PERSPECTIVE Author contributions SSX and CGD wrote the paper and pre- pared the figures. The world today is facing a severe food crisis and a deteriorating natural environment, which highlights the Data availability Data sharing not applicable to this article as no importance of biological breeding in establishing global datasets were generated or analyzed during the current study. food security. During evolution, plants utilized both Declarations genetic and epigenetic variations to cope with diverse environmental stresses. The growing evidence shows Conflict of interest Both authors declare no conflict of interest. that epigenetic markers could influence and modulate plant disease resistance, and thus epigenetic regulation Open Access This article is licensed under a Creative Commons emerges as an efficient strategy for plant disease Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or for- resistance breeding. In this review, we summarize the mat, as long as you give appropriate credit to the original transcriptional reprogramming of defensive gene, author(s) and the source, provide a link to the Creative Commons mediated by ‘‘writers’’ and ‘‘erasers’’ of histone modifi- licence, and indicate if changes were made. The images or other cations and DNA methylation, in plant defense respon- third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit ses, and the increasing application of epigenetic line to the material. If material is not included in the article’s mechanisms in improvement of crop yield potential, as Creative Commons licence and your intended use is not permitted well as techniques that have potential for future uses in by statutory regulation or exceeds the permitted use, you will crop breeding programs. need to obtain permission directly from the copyright holder. 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Epigenetic regulation of plant immunity: from chromatin codes to plant disease resistance

aBIOTECH , Volume 4 (2) – Jun 1, 2023

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Abstract

aBIOTECH https://doi.org/10.1007/s42994-023-00101-z aBIOTECH REVIEW Epigenetic regulation of plant immunity: from chromatin codes to plant disease resistance 1,2 1,2& Si-Si Xie , Cheng-Guo Duan Shanghai Center for Plant Stress Biology and CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, China University of the Chinese Academy of Sciences, Beijing 100049, China Received: 17 January 2023 / Accepted: 1 March 2023 Abstract Facing a deteriorating natural environment and an increasing serious food crisis, bioengineering-based breeding is increasing in importance. To defend against pathogen infection, plants have evolved mul- tiple defense mechanisms, including pathogen-associated molecular pattern (PAMP)-triggered immu- nity (PTI) and effector-triggered immunity (ETI). A complex regulatory network acts downstream of these PTI and ETI pathways, including hormone signal transduction and transcriptional reprogram- ming. In recent years, increasing lines of evidence show that epigenetic factors act, as key regulators involved in the transcriptional reprogramming, to modulate plant immune responses. Here, we sum- marize current progress on the regulatory mechanism of DNA methylation and histone modifications in plant defense responses. In addition, we also discuss the application of epigenetic mechanism-based resistance strategies in plant disease breeding. Keywords Histone modification, DNA methylation, Transcriptional reprogramming, Plant immunity, Disease resistance INTRODUCTION numbers, including mono-, di-, and tri-methylation (me1/2/3). Histone lysine methylation is a critical and Histone modifications and DNA methylation complex epigenetic marker that dynamically controls the transition between different transcriptional states. In eukaryotes, the genomic information is packaged as Another well-studied histone modification is histone nucleosomes, the basic units of chromatin. Each nucle- acetylation. It is generally assumed that histone acety- osome is composed of a core histone octamer (two lation interferes with the interaction within the nucle- copies of four core histone proteins H2A, H2B, H3, and osome, thereby leading to a more loose chromatin state H4) and 147 bp DNA. The N-terminal tails of these for transcriptional activation (Shahbazian and Grunstein histones are easily accessed and modified with various 2007). These epigenetic marks are dynamically regu- covalent modifications, such as methylation, acetylation, lated by different factors, including the enzymes that ubiquitination, phosphorylation, etc. (Kouzarides 2007), can catalyze/remove (‘‘writers/erasers’’) the modifica- a process called histone post-translational modification tion to/from the histone, and the proteins (‘‘readers’’) (PTM). Among them, histone methylation is a well- that recognize and link the modification with other characterized PTM. Histone methylation usually occurs molecules. Epigenetic modifications are generally able at lysine and arginine residues with different methyl to implement transcriptional and/or posttranscriptional regulation of such marked genes. More importantly, growing evidence shows that histone modification & Correspondence: cgduan@cemps.ac.cn (C.-G. Duan) The Author(s) 2023 aBIOTECH homeostasis is essential for the plant immunity histone modification, DNA modification, histone vari- regulation. ants, and ranges of noncoding RNA. In this review, we In addition to the modifications on histone tails, primarily focus on the mechanism of histone modifica- various modifications can also occur on the DNA strand, tion and DNA methylation in plant immunity regulation. among which the most prominent one is the methyla- tion of the carbon-5 of cytosine (5-mC). DNA methyla- Plant immune pathways tion can occur in different sequence contexts, including symmetrical CG, CHG, and asymmetrical CHH (H corre- In nature, plants are generally exposed to a complex sponds to A, T, or C) (Henderson and Jacobsen 2007), environment with a range of organisms and microor- and be present at promoters, introns, and transposable ganisms, including insects, bacteria, fungi, and viruses. elements (TEs). In plants, de novo DNA methylation is All these challenges have important influences on many established by a specific RNA-directed DNA methylation aspects of plant life, including growth, development, (RdDM) pathway. In Arabidopsis, a canonical RdDM crop yield, and adaptability to the environment. To model proposes that single-stranded RNA (ssRNA), adapt to these diverse biotic stresses, plants have produced by RNA POLYMERASE IV (Pol IV), can be evolved intricate mechanisms to recognize the charac- recognized by RNA-DEPENDENT RNA POLYMERASE 2 teristics of insects or microorganism and activate the (RDR2) to generate double-stranded RNA (dsRNA), appropriate immune response. Here, cell surface-local- which is processed into 24 nt small interfering RNAs ized pattern-recognition receptors (PRRs) can recognize (siRNAs) by DICER-LIKE 3 (DCL3). These siRNAs are the pathogen- or microbe-associated molecular patterns then loaded onto an RNA-induced silencing complex (PAMPs or MAMPs), such as bacteria flagellin or fungal (RISC) containing the Argonaute (AGO) protein (AGO4/ chitin, and induce PAMP-triggered immunity (PTI) 6/9). The nascent scaffold RNA produced by Pol V rec- (Bigeard et al. 2015). However, pathogens can gradually ognizes the siRNA–AGO complex through sequence escape from the host’s monitoring systems, due to long- pairing. Subsequently, AGO4 interacts with DOMAINS term coevolution of microorganisms and plants. There- REARRANGED METHYLASE 2 (DRM2), DEFECTIVE IN fore, plants evolved resistance (R) proteins to specifi- RNA-DIRECTED DNA METHYLATION 1 (DRD1), and cally recognize the effectors, delivered from pathogens, RNA-DIRECTED DNA METHYLATION 1 (RDM1) to which activates another immune response called effec- methylate the target DNA (Zhang et al. 2018a). In tor-triggered immunity (ETI) (Jones and Dangl 2006). addition to the de novo establishment of CHH methy- The PTI and ETI use different PRRs and intracellular lation, DNA methylation can also be maintained by dif- nucleotide-binding domain leucine-rich repeat contain- ing receptors (NLRs), respectively. However, they share ferent pathways. The symmetric CG methylation is maintained by METHYLTRANSFERASE1 (MET1) and some downstream effects, such as the activation of CHG methylation by CHROMOMETHYLASE2 and 3 mitogen-activated protein kinase (MAPK) cascades, (CMT2 and CMT3) in Arabidopsis (Zhang et al. 2018a). reactive oxygen species (ROS) generation, hormone The maintenance of asymmetric CHH methylation signaling transduction, and transcriptional reprogram- requires either CMT2 or RdDM (Huettel et al. 2006; Liu ming. Recent studies demonstrate that the influence of et al. 2014). DECRESED DNA METHYLATION 1 (DDM1), PTI and ETI appears to be mutual and the upregulation a chromatin remodeling protein, is also required for the of PTI components is also a feature of ETI (Ngou et al. maintenance of symmetric methylation (Zemach et al. 2021; Yuan et al. 2021). But how ETI can regulate PTI, 2013). DNA methylation is highly correlated with H3K9 or how PTI affects ETI still needs to be further explored. methylation and forms a positive feedback loop. In this Plant hormones are well known as important regu- loop, the H3K9me2-containing nucleosome can be rec- lator of plant growth, development and stress responses ognized by the BAH domain of DNA methyltransferase (Pieterse et al. 2009). In the last two decades, increasing CMT2/3 to confer non-CG methylation of the target evidence has demonstrated that the classical plant DNA. In turn, non-CG methylation can be recognized by hormones, salicylic acid (SA), jasmonic acid (JA), and the SAR domain of SUVH4/5/6 histone methyltrans- ethylene (ET) play key roles in the plant immune ferases to enhance the deposition of H3K9me2 (Duan response. Generally, SA is considered to participate in et al. 2018). In plants, the removal of DNA methylation the defense against biotrophic pathogens, whereas JA/ is mainly catalyzed by a pathway termed active DNA ET usually function in defense against necrotrophic demethylation. In Arabidopsis, four demethylases are pathogens. The biosynthesis and perception pathways encoded, including REPRESSOR OF SILENCING1 (ROS1), of these hormones are quite well studied. In the SA DEMETER (DME), DEMETER-LIKE 2 (DML2), and signaling pathway, accumulation of SA can result in DML3. The ‘‘chromatin codes’’ are generally composed of transformation of the SA receptor, NONEXPRESSOR OF The Author(s) 2023 aBIOTECH PR GENES 1 (NPR1), from an inactive to active form, activation of two transcriptional activator factors, followed by its translocation into the nucleus to facili- ETHYLENE-INSENSITIVE 3 (EIN3) and ETHYLENE- tate expression of the SA-dependent defensive genes, INSENSITIVE3-LIKE 1 (EIL1), thereby promoting such as PATHOGENESIS-RELATED GENE 1 (PR1), during expression of another branch of downstream JA-re- pathogen infection (Ding and Ding 2020) (Fig. 1). SA is sponsive genes, such as ETHYLENE RESPONSE FACTOR 1 also an important regulator of systemic acquired resis- (ERF1), OCTADECANOID-RESPONSIVE ARABIDOPSIS AP2 tance (SAR), which refers to the phenomenon by which 59 (ORA59), and PLANT DEFENSIN 1.2 (PDF1.2) (Li et al. infection of plant aerial tissues, by pathogens, results in 2022; Ruan et al. 2019). the systemic induction of a long-lasting and broad- Under normal conditions, ETHYLENE-INSENSITIVE 1 spectrum disease resistance. Accumulation of SA and (ETR1), the receptor for the gaseous hormone ET, acti- activation of the downstream signaling pathway are vates CONSTITUTIVE TRIPLE RESPONSE 1 (CTR1) to essential for SAR establishment (Kachroo and Robin repress the positive regulator, EIN2, via phosphoryla- 2013). tion. Upon perception of ET, the release of repression In the JA signaling pathway, jasmonoyl-L-isoleucine from CTR1 results in the activation of EIN2, which then (JAIle), the active form, is repressed by jasmonate ZIM- inhibits the degradation of EIN3 and EIL1, and further domain (JAZ) in the resting state. Once JA accumulates, activates downstream ET-responsive genes, such as JAIle can recognize CORONATINE INSENSITIVE 1 (COI1) ERF1 and ORA59 (Li et al. 2019b). COI1 of the SCF complex, leading to the degradation of JAZ The antagonism between the SA and JA signaling by the 26S proteasome. JAIle functions as a transcrip- pathways is well established. In Arabidopsis, NPR1 is tional activator to promote the expression of JA-re- required for the activation of many transcription factors, sponsive genes, such as JASMONATE INSENSITIVE 1 such as the TGACG-binding transcription factors (TGAs) (JIN1/MYC2) and its downstream genes (Fig. 1). More- and WRKYs, which are responsible for the suppression over, release of repression from JAZ leads to the of JA-responsive genes (Zhang et al. 2018b). In addition, Fig. 1 Pathogen-triggered transcriptional reprogramming in the plant immune response. BIK1 is quickly phosphorylated upon PRR 2? recognition of the elicitor, such as flg22, chitin, lectin, etc. Subsequently, several signaling events are activated, such as a Ca burst, ROS production, and MAPK cascade, resulting in transcriptional reprogramming in the nucleus. Epigenetic regulators, such as ATX1 and HAC1, are required for activation of the WRKYs. The PRC2 complex and JAZ promote silencing of the JA-responsive genes, whereas JMJ functions 2? 2? in their activation. In addition, a Ca signal is transduced by Ca binding with CaM, followed by binding to other proteins, such as CBP60g, to facilitate expression of the SA biogenesis gene, ICS1. The SA receptor, NPR1, recognizes SA and is then translocated into the nucleus to recruit the transcriptional activator, TGA, thereby promoting the expression of PR genes. Activation of PR genes can also be mediated by histone modifier genes, JMJ27 and JMJ705 The Author(s) 2023 aBIOTECH some WRKYs, such as WRKY50, WRKY51, and WRKY70, mutants, suggesting that ATX7 and SDG8 function syn- have also been shown to repress the expression of JA- ergistically in the regulation of plant immunity. ATXR7 responsive genes, via NPR1-independent pathways (Gao and SDG8 regulate plant immunity partially through et al. 2011;Li etal. 2004). Moreover, SA can repress the controlling the expression of CAROTENOID AND JA pathway through inhibition of the transcriptional CHLOROPLAST REGULATION 2 (CCR2) and FACELESS activities of MYC2 and ORA59 in Arabidopsis (Aerts et al. POLLEN 1 (FLP1/CER3), two genes that are associated 2021). In turn, the JA pathway can also exert a repres- with the biosynthesis of carotenoids and cuticle integ- sive effect on the SA pathway. For instance, three tran- rity, respectively. Similar with sdg8, atxr7, and the atxr7 scriptional factors ANAC019, ANAC055, and ANAC072, sdg8 double mutant, dysfunction of CCR2 and CER3 which function in suppression of the SA biosynthesis displays increased susceptibility to B. cinerea and A. enzyme, isochorismate synthase 1 (ICS1), need to be brassicicola (Lee et al. 2016). Several SDG8 studies also activated by MYC2 (Gimenez-Ibanez et al. 2017). By reported that SDG8 plays critical roles in plant defense sharing some common regulators, such as EIN3 and against necrotrophic fungal pathogens and hemi-bio- EIL1, the JA and ET pathways are synergistic (Liu and trophic pathogens, via activating JA/ET signaling path- Timko 2021). way marker genes, PDF1.2a, VSP2, MKK3, MKK5, and the R gene, LAZ5, respectively (Berr et al. 2010; Palma et al. 2010). Loss of function of SDG8 results in faster HISTONE MODIFICATIONS IN PLANT IMMUNITY hypersensitive responses (HRs) to Pst DC3000 and Pst REGULATION DC3000 hrpA strains (De-La-Pena et al. 2012). In plants, removal of the histone methyl group is Histone methylation in plant immunity achieved through two classes of demethylases, Jumonji regulation C domain-containing proteins (JMJs) and LSD1-like (LDL) proteins (Jiang et al. 2007;Luetal. 2008). In Generally, histone H3 lysine 4 trimethylation (H3K4me3) Arabidopsis, the H3K4 demethylase, JMJ14, positively and H3K36me2/3 are associated with transcriptionally modulates plant immunity and represses gene expres- active regions, whereas H3K9me2 and H3K27me3 are sion of the negative regulator SUPPRESSOR OF NPR1-1 associated with silenced regions. H3K4me is catalyzed by INDUCIBLE 1 (SNI1), via removing the H3K4me3 from a conserved protein complex (COMPASS-like complex) and the locus. In addition, JMJ14 was also shown to be is mainly located in euchromatin. Seven SET domain pro- required for systematic defense. Loss of function of teins (SDGs), including ARABIDOPSIS TRITHORAX 1 JMJ14 leads to attenuation in the local defense response, (ATX1/SDG27), ATX2 (SDG30), ATX3 (SDG14), ATX4 and reduced Pip accumulation in distal leaves during (SDG16), ATX5 (SDG29), ARABIDOPSIS TRITHORAX- pathogen invasion (Li et al. 2020). RELATED7 (ATXR7/SDG25), and ATXR3 (SDG2), are pro- In Arabidopsis, four LDL genes (LDL1-4) have been posed to mediate the deposition of H3K4 methylation in identified. Among them, LDL4/FLOWERING LOCUS D Arabidopsis. (FLD)/REDUCED SYSTEMIC IMMUNITY1 (RSI1)is A number of H3K4 methyltransferases have been required for the activation of WRKY29 and WRKY6 implicated in plant immunity regulation. ATX1 has been genes, through H3K4me3 dynamics, and differential identified as a ‘master regulator’ in activating expres- influences on the expression of WRKY38, WRKY65 and sion of the transcription factor, WRKY70, by promoting WRKY53 (Singh et al. 2014b). Furthermore, GLU- H3K4me3 deposition (Alvarez-Venegas et al. 2007) TATHIONE S-TRANSFERASE THETA 2 (GSTT2), a mem- (Fig. 1). ATX1 may indirectly activate PR1 and repress ber of the glutathione S-transferase theta class, was THI2.1 expression, thereby contributing to a rapid plant shown to be associated with LDL4 and functions in response to pathogen infection (Alvarez-Venegas et al. activating SAR, probably through influencing H3KAc and 2007). ATXR7, a Set1 class H3K4me methyltransferase, H3K4me2/3 levels at WRKY6 and WRKY29 (Banday and was reported to be implicated in regulation of PTI, ETI, Nandi 2018). Subsequently, it was shown that LDL4 acts and SAR immune pathways, together with a H3K36 as a positive regulator of plant defense against the methyltransferase, SDG8 (Lee et al. 2016). These necrotrophic fungi B. cinerea and Alternaria alternata. authors observed that atxr7 and sdg8 mutants display More importantly, the ldl4 mutants are partially defec- enhanced susceptibility to Botrytis cinerea, Pseu- tive in JA signaling, but hyperactive in ethylene signaling domonas syringae pv tomato DC3000 (Pst DC3000), or (Singh et al. 2019). Recently, the ldl1 ldl2 double mutant Alternaria brassicicola infection. was shown to exhibit resistance to Pst DC3000, which Of importance, the atxr7 sdg8 double mutant showed may be caused, in part, by H3K4me3-dependent additive susceptibility, compared with the single upregulation of WRKY22/40/70 genes (Noh et al. 2021). The Author(s) 2023 aBIOTECH In rice, another H3K4me2/3 demethylase, JMJ704, was H3K9me is a typical heterochromatin marker that shown to be a positive regulator in plant defense against generally associates with DNA methylation. In Ara- Xanthomonas oryzae pv. Oryzae (Xoo). Here, JMJ704 bidopsis, H3K9me2 and H3K9me1 predominantly exist, represses the expression of a subset of negative regu- whereas H3K9me3 is barely detected. KRYPTONITE lators in plant defense, such as NRR, OsWRKY62, and Os- (KYP)/SU(VAR)3–9 homolog 4 (SUVH4) was the first 11N3, by removing H3K4me2/3 and maintaining a identified H3K9 methyltransferase and it functions, transcriptionally inactive state (Hou et al. 2015). partially redundantly with SUVH5 and SUVH6, in cat- In higher plants, Polycomb group (PcG) proteins alyzing H3K9 methylation in plants (Ebbs and Bender associate with different proteins to form multiple pro- 2006; Jackson et al. 2002; Zhang et al. 2023). A recent tein complexes, named Polycomb Repressive Complex 2 study showed that SUVH4/5/6 represses the expression (PRC2) and PRC1, which synergize to maintain gene of PRR/NLR genes and downstream associated defense silencing. The core components of PRC1/2 are con- genes. The suvh4 suvh5 suvh6 triple mutant displays served in animals and plants. Three H3K27 methyl- greater resistance to Pst DC3000 than wild type plants transferases of the PRC2 complexes have been identified (Cambiagno et al. 2021). In addition, SUVH4 was also in Arabidopsis, including MEDEA (MEA), CURLY LEAF shown to be involved in the regulation of pathogen- (CLF), and SWINGER (SWN). Recently, MEA was shown induced programmed cell death (Dvorak Tomastikova to negatively regulate plant immunity. Overexpression et al. 2021). of MEA results in enhanced susceptibility to B. cinerea, The IBM1, a major H3K9 demethylase in Arabidopsis, Pst DC3000 and Pst-AvrRpt2. In addition, MEA is asso- also participates in plant immunity regulation. The ibm1 ciated with a transcription factor, DROUGHT-INDUCED mutants are hyper-susceptible to the bacteria pathogen 19 (DIL9), and is recruited to the promoter of RESIS- Pst DC3000. IBM1 could directly target defense genes TANT TO P. SYRINGAE 2 (RPS2) to repress its expression PR1, PR2, and FLG22-INDUCED RECEPTOR-LIKE KINASE by deposition of H3K27me3, leading to an attenuated 1 (FRK1) and activate their expression during pathogen defense response (Roy et al. 2018). infection (Chan and Zimmerli 2019). However, a very The LIKE HETEROCHROMATIN PROTEIN 1 (LHP1), a recent study showed that the ibm1 mutant displays subunit of PRC1 responsible for H3K27me3 recognition, increased resistance to Pst DC3000 (Lv et al. 2022). The acts as a repressor of the MYC2-dependent immune JMJ27, a H3K9 demethylase, is required for resistance to pathway. The lhp1 mutant displays reduced SA content virulent Pst DC3000. In this case, JMJ27 functions as a and is more susceptible to Pst DC3000 (Ramirez-Prado negative mediator of the defense repressor gene, et al. 2019). A recent study revealed that the histone WRKY25, and a positive regulator of PR genes (Dutta modifications H3K27me3 and H3K4me3 work together et al. 2017). All above studies show histone methyl- to affect expression of stress-responsive genes to transferases and demethylases are widely involved in respond to powdery mildew in hulless barley (Zha et al. plant immune regulation (Fig. 2). 2021). In Arabidopsis, REF6, an H3K27me3 demethy- lase, has been shown to form positive feedback with Histone acetylation in plant immunity regulation HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2) to maintain the activation of HSFA2 and degradation of Histone acetylation also plays vital roles in immunity SUPPRESSOR OF GENE SILENCING 3 (SGS3), during regulation (Fig. 2) and is catalyzed by distinct HAT transgenerational inheritance, and the degradation of families, including GENERAL CONTROL NON- SGS3 could result in reduced trans-acting siRNA DEREPRESSIBLE 5 (GCN5)-RELATED ACETYLTRA (tasiRNA) production. The REF6-HSFA2 loop and NSFERASE (GNAT), p300/CREB (cAMP-RESPONSIVE reduced tasiRNA converge to release HEAT-INDUCED ELEMENT-BINDING PROTEIN)-BINDING PROTEIN TAS1 TARGET 5 (HTT5), which drives early flowering (CBP), TATA-BINDING PROTEIN-ASSOCIATED FACTOR 1 and attenuates immunity (He 2019). In rice, JMJ705 (TAFII250), and MOZ-YBF2/SAS3-SAS2/ TIP60 (MYST) encodes an H3K27me2/3 demethylase, and JMJ705- (Pandey et al. 2002). GCN5, a catalytic subunit of the mediated H3K27me demethylation is required for basal acetylating modification complex, Spt-ADA-Gcn5- and induced expression of disease resistance genes (Li Acetyltransferase (SAGA), was previously shown to et al. 2013). JMJ705 is induced during pathogen infec- influence H3K14ac and H3K9ac level on its targets, but tion, and JMJ705 loss of function results in enhanced is not strictly coupled to transcriptional activation of the susceptibility to Xoo. Moreover, JMJ705 dynamically target genes (Benhamed et al. 2008). A recent study removes H3K27me3 from responsive genes, such as proposed that GCN5 has a dual role in transcriptional JAMYB, PR10, TPS3, and Os07g11739, during MeJA regulation and repression of SA-mediate immunity. induction (Fig. 1). Dysfunction of GCN5 leads to a decrease of H3K14ac in The Author(s) 2023 aBIOTECH Fig. 2 The effects of histone modifiers in plant immune regulation. Histone modifiers are widely implicated in the regulation of an immune response through dynamically modulating the expression of master regulatory genes in hormone (SA, JA/ET) signaling pathways. According to their effects on plant resistance, histone modifiers are divided into two categories: positive and negative regulation. The green icons represent positive regulators, whereas the yellow icons represent negative regulators, in the regulation of disease response the 5’end of down-regulated targets, and an increase in complex can then be recruited to PR genes to facilitate the 3’ ends of up-regulated targets. This suggests that transcription, through deposition of H3Ac, and a GCN5 could either activate or repress gene expression response to SA-triggered immunity (Jin et al. 2018). by controlling H3K14ac distribution on its target genes. Based on their homology to yeast, histone deacety- Moreover, GCN5 functions as a repressor of SA-mediated lases (HDACs) can be divided into three groups: immunity by reducing SA accumulation (Kim et al. REDUCED POTASSIUM DEPENDENCY3 (RPD3), HIS- 2020). An earlier study showed that a Phytophthora TONE DEACETYLASE1 (HDA1), and SIRTUIN2 (Pandey effector, PsAvh23, could affect the assembly of the SAGA et al. 2002; Yang and Seto 2003). In addition, type-II complex by breaking the association of GCN5 and reg- HDAC (HD2) also has histone deacetylation activity, but ulatory subunit Alteration/Deficiency in Activation 2 is plant-specific (Dangl et al. 2001). HDA19, an RPD3 (ADA2) and suppressing the activation of defense genes type histone deacetylase in Arabidopsis, can be induced in soybean (Kong et al. 2017). by JA, ET, wounding, and pathogens. Overexpression of In addition to the GNAT family, a member of the HDA19 causes increased expression of PR genes and p300/CBP family, HISTONE ACETYLTRANSFERASE OF enhanced resistance to Alternaria brassicicola (Zhou THE CBP FAMILY 1 (HAC1) and HAC5 also play impor- et al. 2005). WRKY38 and WRKY62, two members of tant roles in immune response. The HAC1/5 can form a WRKY group III transcription factors, are required for complex with NPR1 and TGAs and this HAC–NPR1–TGA transcriptional activation and SA-mediated suppression The Author(s) 2023 aBIOTECH of JA signaling, with functional redundancy (Kalde et al. rice broad-spectrum resistance against rice pathogens 2003; Mao et al. 2007). HDA19 can interact with (Chen et al. 2022). WRKY38 and WRKY62 to repress their transcriptional SRT2, a NAD -dependent deacetylase of the SIR- activation activity. Moreover, the had19 mutant displays TUIN2 and HD2 family, is able to negatively regulate increased susceptibility to Pst DC3000 (Kim et al. 2008). plant basal defense against Pst DC3000, via suppressing However, it has also been reported that HDA19 loss of SA biosynthesis. The expression of key master regula- function causes increased SA content and increased tors in the SA biosynthesis pathway, including PAD4, expression of a group of genes required for accumula- EDS5, and SID2, was increased in the srt2 mutant and tion of SA and PR genes, such as PR1 and PR2, resulting decreased in SRT2 overexpression plants (Wang et al. in enhanced resistance to Pst DC3000 (Choi et al. 2012). 2010). In rice, the HD2 subfamily histone deacetylase A similar mechanism was also shown in the regulation HDT701 negatively regulates plant innate immunity by of HDA6-mediated plant immunity. HDA6 constitutively modulating histone H4 acetylation of PRR and defense- represses the expression of pathogen-responsive genes, related genes in response to Xoo infection (Ding et al. including PR1 and PR2, through decreasing histone 2012). Additionally, an Arabidopsis HD2 class of H3K9ac acetylation levels at their promoters (Wang et al. 2017). deacetylase, HD2B, was identified to be targeted by MAP The following study showed that this may be caused by kinase MPK3 and plays an important role in bacteria HDA6-mediated suppression of SA biosynthesis. HDA6 defense. In this case, MPK3 directly phosphorylates can directly bind to the promoter regions to repress the HD2B, thereby conferring its relocation to the nucleus to expression of CALMODULIN-BINDING PROTEIN 60 g regulate H3K9 acetylation levels of biotic stress (CBP60g) and SYSTEMIC-ACQUIRED RESISTANCE-DEFI- response genes (Latrasse et al. 2017). Furthermore, CIENT 1 (SARD1) through histone deacetylation (Wu HD2C functions as a positive regulator in defending et al. 2021). A very recent study reported that the against Cauliflower mosaic virus (CaMV) infection. Loss acetylation level of TOPLESS is antagonistically regu- of function of HD2C results in an increased histone lated by GCN5 and HDA6 to respond to the regulation of acetylation level on the viral mini-chromosomes, which JA signaling (An et al. 2022). caused enhanced susceptibility to CaMV. Intriguingly, TOPLESS is a conserved Groucho/thymidine uptake 1 the P6 protein of CaMV could destroy the function of (Gro/Tup1) family corepressor and is required for the HD2C through interfering with the HD2C–HDA6 inter- repression of JA-responsive gene expression (Pauwels action (Li et al. 2021b). et al. 2010). GCN5-mediated acetylation of TOPLESS facilitates TPL–NINJA interaction and recruitment to the Histone ubiquitination and other modifications promoter of MYC2 targets for gene repression. Con- in plant immunity regulation versely, HDA6-mediated deacetylation of TOPLESS weakens the TPL–NINJA interaction and activates Compared to histone methylation and acetylation, the expression of a JA-responsive gene (An et al. 2022). function of histone ubiquitination in regulating plant In wheat, TaHDA6 interacts with TaHOS15 and is immunity has been less explored. However, the limited recruited to defense responsive genes, including TaPR1, studies indicate the important involvement of histone TaPR2, TaPR5, and TaWRKY45, to fine-tune defense ubiquitination in the plant defense response (Fig. 2). responses to powdery mildew (Liu et al. 2019). HDA9 is HISTONE MONOUBIQUITINATION1 (HUB1), a RING E3 also a member of the RPD3-like group and interacts ligase of histone 2B monoubiquitination, was reported with HOS15 to function as a negative regulator of to be an important regulator of plant defense against immunity. Importantly, HOS15 can repress these NLR necrotrophic fungal pathogens (Dhawan et al. 2009). In genes, including SUPPRESSOR OF NPR1-1, CON- addition, HUB1 and another E3 ligase, HUB2, have roles STITUTIVE1 (SNC1), under both pathogen infection and in the depolymerization of cortical microtubules, the resting state. However, HDA9 can only repress the through positively regulating the expression of key NLR genes during pathogen infection (Yang et al. 2020). protein tyrosine phosphatase genes and promoting This suggests that HDA9 is involved in the repression of protein tyrosine phosphorylation during the defense NLR genes during a response to pathogen infection, and response to Verticillium dahliae toxins (Hu et al. 2014). there may be other factors involved in the repression of Additionally, HUB1 and HUB2 can upregulate expres- NLR genes, by HOS15, in the resting state. Interestingly, sion of the R gene, SNC1, by promoting the deposition of pathogens have also developed antagonism strategies H2B monoubiquitination, and are required for autoim- for better infection. A recent study showed that a mune responses in the bon1 mutant (Zou et al. 2014). In secreted fungal effector, UvSec117, can target the rice tomato, SlHUB1 and SlHUB2 can positively regulate histone deacetylase OsHDA701 and negatively regulate plant defense response to B. cinerea through modulating The Author(s) 2023 aBIOTECH the balance between the SA- and JA/ET-mediated sig- geminivirus infection. Consistently, a number of DNA naling pathways (Zhang et al. 2015). methylation- and RdDM-deficient mutants have been In rice, an emerging post-translational modification shown to display enhanced susceptibility to gemi- lysine 2-hydroxyisobutyrylation (K ) has been impli- niviruses (Raja et al. 2008). Loss of function of NRPD2, hib cated in plant immunity. Histone deacetylases, the second largest subunit of Pol IV and Pol V, also leads OsHDA705, OsHDA716, OsSRT1, and OsSRT2, are all to increased susceptibility to the necrotrophic fungal responsible for the removal of K marks. Among them, pathogens B. cinerea and Plectosphaerella cucumerina. hib OsHDA705 was further shown to negatively regulate The other mutants involved in different steps of the rice disease resistance. Dysfunction of OsHDA705 RdDM pathway, such as nrpe1, ago4, drd1, rdr2, and enhanced resistance to Ustilaginoidea virens, the bacte- drm1 drm2, have similar phenotypes with nrdp2 during rial blight pathogen Xoo and the rice blast fungus, M. pathogen infection (Lopez et al. 2011). Through DNA oryzae. Importantly, histone Khib functions as an active methylation sequencing of plants exposed to different marker for gene transcription, and is involved in regu- biotic stresses, Dowen et al. (2012) reported that the lating the expression of R genes (Chen et al. 2021). DNA methylation changes in repetitive sequences, or transposons, could affect the expression of neighboring genes in response to SA stress. The CG methylation DNA METHYLATION IN PLANT IMMUNITY mutant (met1-3, ddm1) and non-CG methylation REGULATION mutants (ddc, drm1-2 drm2-2 cmt3-11, rdr1, rdr2, rdr6, drd1, nrpd1a, and dcl2 dcl3 dcl4) displayed enhanced The important participation of DNA methylation in plant resistance to Pst DC3000. immunity regulation has been well established (Fig. 3). In recent years, whole-genome bisulfite sequencing For example, the methylation level of viral DNA is studies have revealed that DNA hypomethylation is decreased in Arabidopsis 5-mC-deficient mutants after often associated with enhanced resistance during Fig. 3 DNA methylation-dependent regulation of R gene-mediated immunity. Specific pathogens cause plant disease through the secretion of effectors into host cells. In the resting state, the promoter region of R genes is hyper-methylated and silenced by the RdDM pathway. The DNA demethylase, ROS1, can antagonize the silencing of R genes through DNA demethylation, during infection, thereby promoting the expression of R genes. In another case, the intragenic hyper-methylation can recruit the AAE protein complex to promote the production of full-length transcripts of R genes. Impairment of DNA methylation, or the AAE complex, results in mis-splicing or proximal polyadenylation, facilitating the production of intact R protein. Then, the R protein can activate ETI immune responses through recognition of the effectors. The ETI immune response may also have an important effect on the dynamic regulation of the DNA methylation state on R genes The Author(s) 2023 aBIOTECH pathogen infection. For example, in wheat, infection (RLP43) and catalyze DNA demethylation during flg22 with Blumeria graminis f. sp. tritici resulted in a signif- induction, thereby indirectly promoting the binding of icant decrease in CHH methylation and downregulation WRKY transcriptional factors to the W-box motif of of AGO4a (Geng et al. 2019). Consistent with these RLP43 and activating gene expression. findings, in Arabidopsis, infestation with the green peach The gene-for-gene resistance model proposes that aphid leads to DNA hypomethylation in hundreds of loci, one avirulence gene in distinct races of microorganisms particularly transposable elements (Annacondia et al. can be recognized by genetically interacting with the 2021). In addition, upon treatment with nematode-as- corresponding R gene in plants, thereby leading to plant sociated molecular patterns from different nematode disease resistance (Dangl and Jones 2001). The largest species, or the bacterial pathogen-associated molecular class of R genes encodes a nucleotide-binding site plus pattern, flg22, both rice and tomato plants displayed leucine-rich repeat (NB-LRR) class of proteins. R genes global DNA hypomethylation. Intriguingly, hypomethy- are usually clustered in regions enriched for TEs and lation mainly occurred in CHH methylation (Atighi et al. repetitive sequences, wherein 5-mC and H3K9me2 are 2020). Apart from the factors associated with the RdDM densely deposited. These repressive markers can pre- pathway and enzymes that catalyze methylation, Ara- vent TE activation to facilitate the integrity of NB-LRR bidopsis ELONGATOR SUBUNIT 2 (ELP2) was shown to genes and stabilize chromatin structure. be required for pathogen-induced rapid transcriptome DNA hypomethylation may promote the recombina- reprogramming, through altering methylation levels of tion and evolution of R genes (Alvarez et al. 2010). specific methyl cytosines (Wang et al. 2013). In addition, Therefore, DNA methylation homeostasis is essential for MED18, a subunit of mediator, is associated with NRPD2 R gene expression and plant resistance (Fig. 3). PigmS, a to regulate the immune response through modulating rice NLR receptor, was reported to suppress the PigmR- the expression of defense-related genes (Zhang et al. mediated broad resistance to pathogen by interfering 2021a). with the formation of PigmR homodimerization. The It would seem that plants undergo a global PigmS promoter contains two tandem miniature trans- hypomethylation upon perceiving pathogen signals. For posons, MITE1 and MITE2. The expression of PigmS was example, flg22 (bacteria elicitor) can trigger the down- affected by DNA methylation level in MITE1 and MITE2 regulation of a series of RdDM gene expression, mediated by the RdDM pathway. The lower DNA including AGO4, AGO6, NRPD2, NRPD7, Nuclear RNA methylation in MITE1 and MITE2 increased the gene Polymerase E7 (NRPE7), NRPE5, INVOLVED IN DE NOVO expression of PigmS, and further compromised PigmR- 2 (IDN2), KOW DOMAIN-CONTAINING TRANSCRIPTION mediated resistance (Deng et al. 2017). FACTOR 1 (KTF1), DRD1, and MET1. The downregulation It is generally accepted that cytosine methylation of of these genes results in hypomethylation within the the promoter region often plays a repressive role in RdDM loci during flg22 induction. Moreover, DNA modulating expression of the gene. However, an earlier demethylase ROS1 facilitates the demethylation of an study showed that promoter DNA methylation plays a RdDM target (also a disease resistance gene) TNL novel enhancing role in resistance to the pathogen. For RESISTANCE METHYLATED GENE 1 (RMG1) and is example, the fungal pathogen, Magnaporthe grisea, can associated with the activation of a SA-dependent induce the expression of Pib, an NLR gene in rice. defense response (Yu et al. 2013). Consistent with this Notably, the DNA methylation level in the promoter finding, the DNA demethylase triple mutant, rdd (ros1 region (contains heavy CG methylation) of Pib is dml2 dml3), displays increased susceptibility to the increased after infection by this fungal pathogen (Li fungal pathogen, Fusarium oxysporum. In addition, DNA et al. 2011). Furthermore, some studies have shown that demethylases can positively regulate the expression of DNA methylation not only represses gene expression stress response genes enriched with transposon or but also activates gene expression at different targets repeat sequence in their promoter regions for defense (Harris et al. 2018; Shibuya et al. 2009). Collectively, against fungal pathogens (Le et al. 2014). Intriguingly, these studies indicate that DNA methylation is involved among those defense genes mis-expressed by pathogen in the regulation of plant immunity, through balancing infection in a ros1 mutant, only a few were accompanied the transcriptional repression and activation effects to by DNA methylation changes (Sanchez et al. 2016). fine-tune the expression of different defensive genes. Hence, the molecular mechanism of how ROS1 mediates DNA methylation not only regulates the expression of transcriptional reprogramming in immune response has R genes, but also modulates the length of the R gene been a mystery. However, recently, Halter et al. (2021) transcript (Fig. 3). RPP7, which encodes a CC-NB-LRR reported that ROS1 can directly bind to the promoters protein and contains a Ty-1 COPIA-type retrotransposon of RMG1 and ORPHAN RECEPTOR-LIKE PROTEIN 43 (also named COPIA-R7), is specifically enriched with the The Author(s) 2023 aBIOTECH H3K9me2 marker in the sense orientation of the first ASSEMBLY FACTOR 1 (CAF1), a histone chaperone, intron, contributes to disease resistance during mediates the repression of priming of defensive genes, Hyaloperonospora parasitica infection (Eulgem et al. under non-inductive conditions. Consistent with this 2007). ENHANCED DOWNY MILDEW 2 (EDM2), Anti- model, dysfunction of CAF1 resulted in spurious acti- silencing 1 (ASI1) and ASI1 immunoprecipitated protein vation of SA-dependent defense response accompanied 1 (AIPP1) form a protein complex (designated as AAE with low nucleosome occupancy and high H3K4me3 at complex) that recognizes and affects the H3K9me2 at the transcription start sites of defensive genes (Mozgova COPIA-R7 to promote the 3’ distal polyadenylation et al. 2015). (Duan et al. 2017; Lei et al. 2014; Tsuchiya and Eulgem Some studies have provided evidence showing that 2013). The intronic heterochromatin has been shown to DNA methylation is implicated with transgenerational be required for the distal polyadenylation of the RPP7 SAR. An earlier finding showed that the next generation gene. Abnormal expression of the RPP7 transcript of tobacco displays enhanced resistance to TMV, Pseu- occurred in the ddm1 and suvh4 suvh5 suvh6 mutants domonas syringae,or Phytophthora nicotianae, after (Zhang et al. 2021b). Similarly, another R gene, RPP4, infection during the first generation. TMV infection can was also shown to be regulated by the AAE complex enhance homologous recombination frequency and (Deremetz et al. 2019; Zhang et al. 2021b). The RPP4 induce expression of PR1 and promote callose accu- partially overlaps with a COPIA4-like retrotransposon mulation to mediate resistance against the pathogen in (AT4TE42860), at its 3 terminal exon region, and facil- the second generation (Kathiria et al. 2010). A subse- itates disease resistance to Hyaloperonospora parasitica quent study showed that descendants could acquire (Garcia et al. 2010). Dysfunction of this AAE complex resistance after the infection with Pst DC3000, in the leads to the mis-splicing of the RPP4 transcript (Zhang first generation. This transgenerational SAR effect is et al. 2021b). These examples support the notion that regulated by the RdDM pathway and transmitted by intragenic heterochromatin, caused by TE insertions, hypomethylation at CHG sites (Luna and Ton 2012). serve as an important regulatory element in R gene These findings suggest that the inheritance of a specific expression. DNA methylation pattern may contribute to the regu- lation of transgenerational SAR. However, how DNA methylation contributes to transgenerational SAR EPIGENETIC REGULATION IN DEFENSE PRIMING remains to be elucidated. It is possibly that the DNA AND TRANSGENERATIONAL SAR methylation state and the accumulated of effector pro- teins, in the first generation, will be gamete-transmitted Plants can respond faster or show more resistance to to the next generation, or re-established in the second environment challenges when previously exposed to a generation. moderate stress. After suffering from mild environment stress, plants will be primed and form a ‘memory’ to be better equipped to cope with the situation when again APPLICATION OF EPIGENETICS TO PLANT encountering this stimulus. Priming involves changes in IMMUNITY histone modifications, DNA methylation and accumula- tion of inactive MAPKs and transcriptional factors To survive in adverse conditions, plants have evolved (Beckers et al. 2009; Jaskiewicz et al. 2011; Luna and diverse mechanisms to enhance resistance to pathogens. Ton 2012; Singh et al. 2014a). For example, H3 and H4 Epigenetic regulation gradually becomes an efficient acetylation, as well as H3K4 methylation, on the WRKY tool to overcome the challenges from biotic stress. promoter may promote priming of genes during Epigenetic mechanism-mediated crop disease resistance pathogen infection or treatment with the SA synthetic strategies are being employed in crop breeding (Fig. 4). analog, acibenzolar S-methyl (Jaskiewicz et al. 2011). For instance, some chemical agents have been identified Interestingly, abiotic stress could trigger the priming of that enhance plant resistance through an epigenetic biotic stress. For example, the hac1-1 mutant displays mechanism. In rice, application of 5-azadeoxycytidine, a increased susceptibility to Pst DC3000 after repetitive DNA de-methylating agent, enhances plant resistance to stress (cold, salt, and heat), but there was no obvious the bacterial pathogen Xanthomonas (Akimoto et al. distinction, compared to wide type, during nonstress. 2007). Additionally, in plants, the chemical SAR inducer Moreover, the expression of PTI-responsive genes b-aminobutyric acid (BABA) was shown to enhance WRKY53, FRK1, and NHL10 failed to be activated in the resistance to various pathogens, including the hemi- hac1 mutant, after repetitive heat stress (Singh et al. biotrophic bacterium Pst DC3000, the necrotrophic 2014a). It has been reported that CHROMATIN fungus B. cinerea, and the oomycete pathogen P. The Author(s) 2023 aBIOTECH Fig. 4 Epigenetic regulation-based plant disease resistance strategy. Spraying a chemical reagent, BABA, onto pants can induce high expression of defensive genes (such as FRK1, NHL10) through facilitating the deposition of H3K4me3 and H3K36me3. In addition to affecting the expression of immune-related genes, BABA can also induce SAR to enhance plant resistance during a pathogen infection. dCAS9 could be used as a tool for activating or repressing the histone modifiers and further fine-tune plant immune response, via modulating expression of downstream defensive genes. Zinc-finger-fused epigenetic regulators can also be utilized for promoting the establishment of DNA hyper-methylation, through the RdDM pathway, in the promoter regions to repress expression of the susceptibility genes and improve the tolerance to pathogen infection in future. ZFP, zinc finger protein parasitica, through affecting the histone modification initial treatment. After a 48 h treatment, NPR1 was and inducing defensive gene expression (Martinez- repressed by the accumulation of H3K27me3, whereas Aguilat et. 2016; Zimmerli et al. 2000, 2001). Moreover, SNI1, the negative regulator of SAR, was activated by an BABA induces resistance against P. parasitica in trans- increase in H3K4me2 level (Meller et al. 2018). BABA genic NahG (salicylate hydroxylase) plants. Thus, BABA has been widely used to improve the disease resistance mainly activates the SAR pathway downstream of SA in crops, such as common bean, potato, grapes, tomato, accumulation (Zimmerli et al. 2000). Another study pepper, cabbage, and fruits (Hamiduzzaman et al. 2005; showed that BABA treatment induces the deposition of Janotik et al. 2022; Kim et al. 2013;Li etal. callose, stomatal closure, and expression of the defen- 2019a, 2021a; Martinez-Aguilat et. 2016; Meller et al. sive gene, PR1, in the SA pathway and other PTI-re- 2018). These studies also have shown that enhanced sponsive genes, including those that facilitate resistance resistance, induced by chemical agents, depends on the to the necrotrophic bacterium, Pectobacterium caro- regulation of epigenetic markers. tovorum subsp. carotovorum (Pcc), in Arabidopsis (Po- Importantly, DNA methylation and histone modifica- Wen et al. 2013). tion can be manipulated by several approaches. The In common bean, BABA treatment can prime the SUVH2/9 proteins are two inactive histone methyl- expression of many defense genes. Interestingly, the transferase, due to their lack of a post SET domain that levels of several histone modifications, such as is required for cofactor and peptide substrate-binding. H3K4me3 or H3K36me3, are higher in the promoter Johnson et al (2014) used Zinc Finger (ZF) fused with regions for different defense genes, during 24 h after SUVH2/9 to establish DNA methylation, at an BABA treatment, but are not accompanied by obvious unmethylated site, through the RdDM pathway. The fwa- accumulation of defensive gene transcripts. The actual 4, an unmethylated epiallele of FWA, was observed to be activation of defensive genes occurs 24 h after BABA successfully methylated and the ZF–SUVH2/fwa-4 plant treatment (Martinez-Aguilat et. 2016). In potato, histone displayed an early flowering phenotype. Moreover, the lysine methylation, but not acetylation, appears to altered DNA methylation could be stably transmitted to function in BABA-triggered resistance. BABA induces the next generation (Johnson et al. 2014). A synthetic ZF, higher level of H3K4me2 in NPR1, the positive regulator fused to the Arabidopsis DEFECTIVE IN MERISTEM of SAR, to respond to Phytophthora infestans during SILENCING 3 (DMS3), a component of the RdDM The Author(s) 2023 aBIOTECH pathway, was employed to deposit DNA methylation at plant defense and successful infection by pathogens the promoter of a susceptibility (S) gene, MeSWEET10a, depend upon the dynamic regulation of epigenetic in cassava. Methylation in this promoter prevented the markers, to activate or repress, the expression of binding of the transcription activator-like (TAL) effector, defensive genes. In general, the transcriptional repro- TAL20, which prevented transcriptional activation of gramming, mediated by chromatin modifications, acts MeSWEET10a and showed a decrease in bacterial blight downstream of immune signaling pathways. Although symptoms in these cassava plants (Veley et al. 2023). A many chromatin regulators have been identified to play similar approach for selectively targeting epigenetic a role in plant immunity, the reported mechanisms silencing could be developed in future studies to mod- mostly focus on how the specific regulator affects some ified key defensive genes for improvement of disease key defensive genes, through changing the chromatin resistance in other crop species (Fig. 4). modifications. However, how these epigenetic factors In addition, CRISPR/dCas9-mediated manipulation of are recruited by immune factors to defense genes histone modifications has also been reported in plants. remains largely unsolved. Hence, more detailed regula- Interfering (CRISPRi) or activation (CRISPRa) of tar- tory mechanisms need to be further explored in future. geted genes is mediated by genetically fusing effector Some important questions include: what are the proteins to dCas9. CRISPR/dCas9-mediated histone dynamics of epigenetic factors before and after patho- modification regulation has been applied in response to gen infection? how do epigenetic regulators induce the abiotic stress. For example, HAC1-fused dCas9 trans- plant response at the single cell level after infection? genic plants were generated to improve drought stress how do plants achieve their return to a resting state tolerance through the transcriptional activation of the after a period of defense? and how do plants trans- positive regulator, ABSCISIC ACID-RESPONSIVE ELE- mit/maintain the ‘‘stress memory’’ to the next genera- MENT-BINDING FACTOR 2 (ABF2/AREB1) (Roca Paixao tion? Answers to these questions will help us gain a et al. 2019). Therefore, similar strategies could also be deeper understanding of how plants respond to patho- employed to engineer plant disease resistance through gen infection and make corresponding changes at the targeting of key regulators of plant defense. For exam- chromatin level. Such knowledge will facilitate the ple, spraying artificial 24-nt siRNAs may be used to development of more efficient disease resistance induce RdDM pathway-mediated silencing of defense strategies based on epigenetic mechanisms. repressive genes to confer immune activation (Fig. 4). Acknowledgements We apologize to all the colleagues whose This approach deserves further exploration in future. work could not be fully cited in this review due to a space limi- tation. This work was supported by a grant from the National Natural Science Foundation of China (32270200 to CGD). CONCLUSION AND PERSPECTIVE Author contributions SSX and CGD wrote the paper and pre- pared the figures. The world today is facing a severe food crisis and a deteriorating natural environment, which highlights the Data availability Data sharing not applicable to this article as no importance of biological breeding in establishing global datasets were generated or analyzed during the current study. food security. During evolution, plants utilized both Declarations genetic and epigenetic variations to cope with diverse environmental stresses. The growing evidence shows Conflict of interest Both authors declare no conflict of interest. that epigenetic markers could influence and modulate plant disease resistance, and thus epigenetic regulation Open Access This article is licensed under a Creative Commons emerges as an efficient strategy for plant disease Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or for- resistance breeding. In this review, we summarize the mat, as long as you give appropriate credit to the original transcriptional reprogramming of defensive gene, author(s) and the source, provide a link to the Creative Commons mediated by ‘‘writers’’ and ‘‘erasers’’ of histone modifi- licence, and indicate if changes were made. The images or other cations and DNA methylation, in plant defense respon- third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit ses, and the increasing application of epigenetic line to the material. If material is not included in the article’s mechanisms in improvement of crop yield potential, as Creative Commons licence and your intended use is not permitted well as techniques that have potential for future uses in by statutory regulation or exceeds the permitted use, you will crop breeding programs. need to obtain permission directly from the copyright holder. 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aBIOTECHSpringer Journals

Published: Jun 1, 2023

Keywords: Histone modification; DNA methylation; Transcriptional reprogramming; Plant immunity; Disease resistance

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