retrospective and perspective of plant epigenetics in china › hla › sites › zhulab ›...

lable at ScienceDirect

Journal of Genetics and Genomics 45 (2018) 621e638

Contents lists avai

Journal of Genetics and GenomicsJournal homepage: www.journals .e lsevier .com/journal-of -genet ics-

and-genomics/

Review

Retrospective and perspective of plant epigenetics in China

Cheng-Guo Duan a, *, Jian-Kang Zhu a, b, *, Xiaofeng Cao c, *

a Shanghai Center for Plant Stress Biology and Center of Excellence for Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai 200032, Chinab Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USAc State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academy ofSciences, Beijing 100101, China

a r t i c l e i n f o

Article history:Received 15 August 2018Received in revised form25 September 2018Accepted 30 September 2018Available online 6 November 2018

Keywords:Plant epigeneticsDNA methylationHistone modificationsChromatin remodeling

* Corresponding authors.E-mail addresses: [email protected] (C.-G. Duan)

[email protected] (X. Cao).

https://doi.org/10.1016/j.jgg.2018.09.0041673-8527/Copyright © 2018, Institute of Genetics andScience Press. All rights reserved.

a b s t r a c t

Epigenetics refers to the study of heritable changes in gene function that do not involve changes in theDNA sequence. Such effects on cellular and physiological phenotypic traits may result from external orenvironmental factors or be part of normal developmental program. In eukaryotes, DNA wraps on ahistone octamer (two copies of H2A, H2B, H3 and H4) to form nucleosome, the fundamental unit ofchromatin. The structure of chromatin is subjected to a dynamic regulation through multiple epigeneticmechanisms, including DNA methylation, histone posttranslational modifications (PTMs), chromatinremodeling and noncoding RNAs. As conserved regulatory mechanisms in gene expression, epigeneticmechanisms participate in almost all the important biological processes ranging from basal developmentto environmental response. Importantly, all of the major epigenetic mechanisms in mammalians alsooccur in plants. Plant studies have provided numerous important contributions to the epigeneticresearch. For example, gene imprinting, a mechanism of parental allele-specific gene expression, wasfirstly observed in maize; evidence of paramutation, an epigenetic phenomenon that one allele acts in asingle locus to induce a heritable change in the other allele, was firstly reported in maize and tomato.Moreover, some unique epigenetic mechanisms have been evolved in plants. For example, the 24-ntsiRNA-involved RNA-directed DNA methylation (RdDM) pathway is plant-specific because of the in-volvements of two plant-specific DNA-dependent RNA polymerases, Pol IV and Pol V. A thorough studyof epigenetic mechanisms is of great significance to improve crop agronomic traits and environmentaladaptability. In this review, we make a brief summary of important progress achieved in plant epige-netics field in China over the past several decades and give a brief outlook on future research prospects.We focus our review on DNA methylation and histone PTMs, the two most important aspects ofepigenetic mechanisms.Copyright © 2018, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, and

Genetics Society of China. Published by Elsevier Limited and Science Press. All rights reserved.

1. General overview of plant epigenetic research in China

With the continuous improvements of sequencing technologyand the accomplishment of the annotation of Arabidopsis genome,epigenetic studies have experienced explosive growth over the pastseveral decades. Similar situation also occurs in China, one of themajor agricultural countries in the world, especially in the field ofplant genetics benefiting from the growing research funding andthe rich plant resources. Based on the public database from “Web ofScience”, we analyzed the publications in plant epigenetics over the

, [email protected] (J.-K. Zhu),

Developmental Biology, Chinese A

past 40 years ranging from 1978 to 2017, including the fields of DNAmethylation, histone modifications, chromatin remodeling andsmall noncoding RNAs. We compared the total publications peryear in plant epigenetics with that published by Chinese re-searchers or groups. We found that the majority of paperscontributed by China were published after the year 2000 and haveexperienced a dramatical increase since then (Fig. 1A), indicatingepigenetic studies are much active during this period. Consistentwith this trend, total citations per year also experienced rapid in-crease over the past 20 years (Fig. 1B). By contrast, the increase ofpublications from other countries were much slower than China,although there is also a rapid increase after the year 2000 (Fig. 1A).This trend is further supported by a sharp increase in the per-centage of papers published by China over the total publications,

cademy of Sciences, and Genetics Society of China. Published by Elsevier Limited and

mailto:[email protected]



http://crossmark.crossref.org/dialog/?doi=10.1016/j.jgg.2018.09.004&domain=pdf

www.sciencedirect.com/science/journal/16738527

www.journals.elsevier.com/journal-of-genetics-and-genomics/

www.journals.elsevier.com/journal-of-genetics-and-genomics/

https://doi.org/10.1016/j.jgg.2018.09.004



Fig. 1. The comparison of publications contributed by China and other countries over the past 40 years in the field of plant epigenetics. Collection of the publication informationis from the public database of “Web of Science” (https://apps.webofknowledge.com/UA_GeneralSearch_input.do?product¼UA&search_mode¼GeneralSearch&SID¼6C6Gthh4wqMhMnwquYs&preferencesSaved¼ ). For the criteria of publications, only articles and conference papers are included.

C.-G. Duan et al. / Journal of Genetics and Genomics 45 (2018) 621e638622

which arises from 0% (1978) to ~30% (2017). This data stronglysuggests that plant epigenetic studies have been speeding up overthe past 20 years in China. About 53% papers published by China arecontributed by the top 10 research institutions (Fig. 1C). Amongthem, Chinese Academy of Sciences (CAS), Chinese Academy ofAgricultural Sciences (CAAS) and China Agricultural University(CAU) rank the first three (Fig. 1C).

2. Dynamic regulation of DNA methylation pattern in plants

DNA 5-methylcytosine (5mC) modification is a hallmark of

epigenetic gene silencing and heterochromatin in both plants andmammals. DNA methylation is involved in multiple cellular andbiological processes. High level of DNA methylation is required forthe silencing of transposable elements (TEs) which is important forgenome stability (Slotkin and Martienssen, 2007). Proper patternsof DNA methylation are crucial for the precise regulation of growthand development (Zilberman et al., 2007). In mammals, DNAmethylation is closely linked to disease pathogenesis (e.g., cancer)and aging (Bergman and Cedar, 2013; Klutstein et al., 2016). Simi-larly, the dynamically regulated DNA methylation responds toenvironmental changes and contributes to plant stress response

https://apps.webofknowledge.com/UA_GeneralSearch_input.do?product=UA&search_mode=GeneralSearch&SID=6C6Gthh4wqMhMnwquYs&preferencesSaved








C.-G. Duan et al. / Journal of Genetics and Genomics 45 (2018) 621e638 623

(Migicovsky and Kovalchuk, 2013; Deleris et al., 2016). Disruptionof DNA methylation often results in inheritable developmentaldefects and reprograming of gene expression. As an importantaspect of epigenetic mechanisms, DNA methylation studies inChina have made great strides not only in the elucidation of regu-latory mechanisms but also in the discovery of DNA methylation-based novel epigenetic phenomena. With the development ofsequencing technology, more and more crop genomes have beensequenced, the majority of which are completed by Chinese sci-entists, including grain crops like wheat (Jia et al., 2013; Ling et al.,2013, 2018), vegetables like Brassica rapa (Wang et al., 2011), cu-cumber (Cucumis sativus) (Huang et al., 2009), potato (Solanumtuberosum) (Potato Genome Sequencing et al., 2011), Carica papayaLinnaeus (Ming et al., 2008), fruit trees like pear (Pyrus bretsch-neideri) (Wu et al., 2013b), and some stress resistant crops likequinoa (Zou et al., 2017). The elucidation of these crop genomeshelps to investigate their epigenomes. Up to now, high resolutionDNA methylomes have been sequenced in multiple plant species inChina. These plants include food crops like maize (Zea mays) andpotato (S. tuberosum), vegetables like tomato (S. lycopersicum) andcucumber (C. sativus L.), fruit trees like apple (Malus x domestica),and cash crops like cotton and B. napus (Zhang et al., 2014a, 2016a;Song et al., 2015a; Li et al., 2016a; Lai et al., 2017; Lang et al., 2017;Liu et al., 2017a, 2017c; Lu et al., 2017; Xu et al., 2017; Wang et al.,2018).

2.1. Establishment of DNA methylation pattern in Arabidopsis

Different from mammals in which 5mC is mainly found at CGsites, DNA cytosine methylation in plants can occur in three cyto-sine contexts, CG, CHG and CHH (H represents A, T or C), which arecatalyzed by different DNA methyltransferases (DNMTs) (Law andJacobsen, 2010). Early in 2000, Dr. Xiaofeng Cao and her col-leagues described DNMT genes in model plant Arabidopsis and cropplant maize and confirmed the presence of mammalian DNMT3orthologues in plants (Cao et al., 2000). In Arabidopsis, symmetricCG methylation is maintained by METHYLTRANSFERASE 1 (MET1),an orthologue of the mammalian DNMT1, which recognizes hemi-methylated CG double-stranded DNA and methylates unmodifiedcytosine with the help of several cofactors during DNA replication(Kankel et al., 2003; Law and Jacobsen, 2010). Symmetric CHGmethylation is mainly maintained by CHROMOMETHYLASE 3(CMT3) which binds to repressive H3K9me2 mark and methylatesunmodified CHG (Cao and Jacobsen, 2002). Methylated CHG in turnrecruits specific histone lysine methyltransferases, includingSU(VAR)3-9 homolog 4 (SUVH4), SUVH5 and SUVH6, to carry outH3K9 methylation. Therefore, H3K9me2 and methylated CHGreinforce each other to form a positive feedback loop. Dysfunctionsof H3K9 methyltransferases lead to genome-wide loss of CHGmethylation (Jackson et al., 2002; Johnson et al., 2002; Ebbs et al.,2005; Ebbs and Bender, 2006). Consistently, knocking out histoneH3K9me2 demethylase IBM1 leads to dramatic increase of genebody CHG methylation (Saze et al., 2008).

In plants, asymmetric de novo DNA methylation (CHH methyl-ation) is established through a plant-specific mechanism, 24-ntsiRNA-dependent RNA-directed DNA methylation (RdDM)pathway (Law and Jacobsen, 2010). RdDM has been the focus ofplant epigenetics over the past 15 years. Chinese researchers havemade outstanding contributions in both the discovery of novelcomponents and the deciphering of molecular mechanisms ofRdDM pathway. According to a widely accepted canonical model(Fig. 2), Pol IV, a plant-specific multisubunit RNA polymerase,produces noncoding transcript P4RNA at heterochromatic regionwhich is immediately amplified into double-stranded RNA (dsRNA)by RNA-DEPENDENT RNA POLYMERASE 2 (RDR2). dsRNA is

processed by DICER-LIKE PROTEIN 3 (DCL3) into 24-nt siRNAs,which are then loaded onto ARGONAUTE 4 (AGO4) proteins. ThesiRNA-AGO4 complex is recruited by another nascent noncodingRNA transcript P5RNA, a product of Pol V which is the other plant-specific RNA polymerase, via sequence complementary pairing.Finally, AGO4 interacts with DOMAINS REARRANGED METHYLASE2 (DRM2) to catalyze de novo DNA methylation (Cao et al., 2003;Law and Jacobsen, 2010; Zhong et al., 2014). Pol IV and Pol V areeach composed of twelve subunits. He et al. from Dr. Jian-KangZhu's group identified NRPD4/RNA-DIRECTED DNA METHYL-ATION 2 (RDM2), a subunit of Pol IV, as a new component in RdDMpathway using an efficient forward genetic screen (He et al., 2009a).

In canonical RdDMmodel, how Pol IV is recruited to target loci iscritical for the initiation of 24-nt siRNA biogenesis and downstreamRdDM reactions. Zhang et al. (2013b) and Law et al. (2013) inde-pendently reported that the heterochromatic mark H3K9me2 couldbe bound by DNABINDING TRANSCRIPTION FACTOR 1 (DTF1)/SAWADEE HOMEODOMAIN HOMOLOG 1 (SHH1), which directlyinteracts with the chromatin remodeling protein CLASSY 1 (CLSY1)and Pol IV in vivo, thereby assisting the recruitment of Pol IV toRdDM target loci. RDM4 (He et al., 2009b)/DEFECTIVE IN MERI-STEM SILENCING 4 (DMS4) (Kanno et al., 2010), which is firstlyidentified by Dr. Jian-Kang Zhu's group, has been shown to interactwith NRPE1 and NRPB1 to serve as a transcriptional regulator of PolV and Pol II (He et al., 2009b). A study further revealed that RDM4 isalso associated with NRPD1, CLSY1, RDR2 and SHH1 in vivo (Lawet al., 2011), suggesting that RDM4 also participates in the initia-tion of siRNA biogenesis. For the recruitment of Pol V, Liu et al. fromDr. Xin-Jian He's group and Johnson et al. from Dr. Jacobsen's groupindependently reported that two SET (Su(var)3-9, E(Z) and Tri-thorax) domain proteins, SUVH2 and SUVH9, are required for theoccupancy of Pol V to RdDM loci (Johnson et al., 2014; Liu et al.,2014b). SUVH2 and SUVH9 lack histone methyltransferase activ-ity but are capable of binding methylated DNA and directly interactwith the chromatin remodeling complex DMS3-DRD1-RDM1(DDR) (Law et al., 2010) and the Microrchidia (MORC) complex,thereby recruiting Pol V to chromatin for DNA methylation(Johnson et al., 2014). In the DDR complex, DRD1 is an ATP-dependent DNA translocase. RDM1 (also known as DMS7), whichis firstly identified by Dr. Jian-Kang Zhu's group, has the single-stranded DNA-binding activity and directly interacts with AGO4and DRM2 in vivo, thereby facilitating the recruitment of DRM2 tothe chromatin (Gao et al., 2010b; Law et al., 2010). In the MOCRcomplex, MORC1, MORC2 and MORC6 have been shown to interactwith SUVH2/9 and are required for heterochromatin condensation(Liu et al., 2014b; Jing et al., 2016). He et al. from Dr. Jian-Kang Zhu'sgroup reported that KOW DOMAIN-CONTAINING TRANSCRIPTIONFACTOR 1 (KTF1)/RDM3, a member of the nuclear SPT5 RNA poly-merase elongation factor family, recruits siRNA-AGO4 to nascentP5RNA by directly binding AGO4 and P5RNA transcript indepen-dent of siRNA biogenesis to form an RdDM effector complex (Heet al., 2009c).

Argonaute (AGO) proteins play essential roles in RdDM andposttranscriptional gene silencing (PTGS) pathways by recruitingsmall RNAs to form the core RNA silencing complex. However, howdifferent small RNAs are sorted into specific AGO complex remainslargely unknown. Arabidopsis genome encodes ten AGOs whichplay different roles in specific silencing pathways. Dr. Yijun Qi'sgroup revealed the importance of the 50 terminal nucleotide of thesmall RNA in the sorting process in Arabidopsis (Mi et al., 2008).They revealed that AGO1 mainly harbors microRNAs which favor a50 terminal uridine, and AGO2 and AGO4 preferentially recruitsmall RNAs with a 50 terminal adenosine, whereas AGO5 predom-inantly binds small RNAs that initiate with cytosine (Mi et al.,2008). The 50 end-recognition model at least partially explains

Fig. 2. A canonical model of RNA-directed DNA methylation (RdDM) in Arabidopsis. A canonical RdDM has three major steps: Pol IV RNA transcription, de novo DNA methylation andheterochromatin formation. CG methylation maintenance with MET1 and the histone deacetylase HDA6 facilitates histone H3 lysine 9 methylation (H3K9me2). DTF1/SHH1 bindsthe H3K9me2 mark and recruits Pol IV to the chromatin to initiate transcription. The generated short transcript P4RNA is amplified into double-stranded RNA (dsRNA) by RDR2 withthe help of RDM4, or directly bound by AGO4. dsRNA is diced into 24-nt siRNAs which are loaded onto AGO4 in the cytoplasm after methylated by HEN1. The siRNA-AGO4 complexis then imported into the nucleus. SUVH2 and SUVH9 bind methylated DNA and recruit Pol V to the chromatin with the help of chromatin remodeling DDR and MORC complexes.KTF1 as a scaffold protein binds the nascent Pol V transcript P5RNA and siRNA-AGO4/6 complex to recruit DRM2 methyltransferase with the help of RDM1 for catalyzing de novoDNA methylation. The IDN2-IDP complex binds to P5RNA and interacts with SWI/SNF complex to adjust nucleosome positioning (Zhu et al., 2013). DNA methylation is amplified bySUVH4/5/6 to deposit H3K9me2 in the chromatin and form heterochromatin with the help of HDA6. The underlined RdDM components are independently identified by Chineseresearchers or groups.


how different small RNA-AGO complexes mediate diverse regula-tion pathways. In canonical RdDM model, AGO4 protein plays avery critical role through its siRNA-binding activity and interactionwith methyltransferase DRM2 and other factors (Zilberman et al.,2003). Although RdDM is a nuclear process, evidence from Dr.Yijun Qi's group indicated that AGO4 is loaded with 24-nt siRNAs inthe cytoplasm and siRNA binding facilitates the translocation ofAGO4 into the nucleus. Moreover, they also revealed that the for-mation of siRNA-AGO4 complex requires HSP90 and the cleavageactivity of AGO4 (Ye et al., 2012). AGO6, a paralogue protein of AGO4in Arabidopsis, has been considered functionally redundant withAGO4. Contrary to this notion, AGO6 was identified from the for-ward genetic screen (Zheng et al., 2007) (Fig. 2), suggesting thatAGO6 bears nonredundant function with AGO4 in regulatingRdDM. This conclusion is further confirmed by recent studies (Duanet al., 2015b; McCue et al., 2015).

It has been known that DCL3-dependent production of 24-ntsiRNAs is a unique feature in the initiation of RdDM. Recent dis-coveries from Dr. Jian-Kang Zhu's, Dr. Yijun Qi's and Dr. Jacobsen'sgroups updated our understanding about this process. Surprisingly,recent studies revealed that of all the Pol IV- and/or Pol V-depen-dent RdDM loci, only 16% are fully dependent on the slicing of Dicer.Thousands of RdDM loci were identified in dcl1234 tetraploidmutant, suggesting that a Dicer-independent Pol IV-RdDM mech-anism may be present (Zhai et al., 2015; Yang et al., 2016a; Ye et al.,2016). How this Dicer-independent RdDM pathway controls DNAmethylation should be clarified in the future study.

Besides the canonical components in RdDM, several RNAsplicing-related proteins have also been identified by Chinese re-searchers to be directly/indirectly involved in the regulation ofRdDM. Dr. Xinjian He's group revealed that STA1, a PRP6-likesplicing factor, facilitates the production of Pol V transcripts (Douet al., 2013) and ZOP1, a Zinc-finger and OCRE domain-containingpre-mRNA splicing factor, promotes Pol IV-dependent siRNAaccumulation (Zhang et al., 2013a). Consistently, Dr. Jian-Kang Zhu'sgroup also identified a pre-mRNA-splicing factor RDM16, acomponent of U4/U6 snRNP, functioning in regulating DNAmethylation by influencing Pol V transcript level instead of small

RNAs, although the detailed mechanism remains unclear (Huanget al., 2013). These findings suggest that RNA splicing machineryis involved in promoting RdDM and transcriptional gene silencing(TGS) (Huang and Zhu, 2014).

2.2. Removal of DNA methylation: DNA demethylation

A specific DNA methylation state is dynamically determined byDNA methylation and demethylation, two reverse biological pro-cesses. In plants, removal of methylated cytosine can be achievedthrough two ways: passive demethylation which loses DNAmethylation during DNA replication, and active demethylationwhich is catalyzed by a family of DNA glycosylase/lyase proteins(Zhu, 2009). Arabidopsis genome encodes four DNA demethylases:DEMETER (DME), ROS1 (DME LIKE PROTEIN 1, DML1), DML2 andDML3. The first evidence was reported by Dr. Jian-Kang Zhu's lab-oratory from a genetic screen for suppressor of transgene silencing(Gong et al., 2002). ROS1 dysfunction causes transgene silencingand increases DNA methylation levels in transgene promoter andthousands of endogenous loci. Compared to ROS1 which is mainlyexpressed in vegetable tissues, DME is preferentially expressed incompanion cells of the female and male gametes and affects allele-specific expression of imprinted genes through DNA demethylation(Choi et al., 2002; Gehring et al., 2006). Different from DNAmethylation which is catalyzed by single methyltransferase, thecleavage of methylated cytosine by DNA demethylase is followed bya sequential DNA repair reactions called base excision repair (BER)(Zhu, 2009). Most of the components involved in BER have beenidentified by Dr. Jian-Kang Zhu's group. Among them, the apurinic/apyrimidinic endonuclease DNA-(APURINIC OR APYRIMIDINICSITE) LYASE (APE1L) and the ZINC FINGER 30-PHOSPHATASE (ZDP)function downstream of ROS1-mediated cleavage to remove theblocking of 30 b-unsaturated aldehyde (30-PUA) and 30 phosphate,respectively, allowing subsequent DNA polymerization and ligation(Martinez-Macias et al., 2012; Li et al., 2015b). AtLIG1, one of the sixDNA ligases in Arabidopsis, has been shown to be the major DNAligase functioning at the last step of BER to complete the DNA repairreaction (Li et al., 2015c). All the mutants of APE1L, ZDP and AtLIG1


genes display defects in seed development due to disrupted geneimprinting, suggesting that these factors are also required for DME-triggered DNA repair reactions in seeds.

ROS1-dependent DNA demethylation displays target specificity.TEs near protein-coding genes, especially RdDM-dependent DNAhypermethylation loci, are preferentially targeted by ROS1 (Tanget al., 2016), suggesting a potential role of ROS1 in preventing thespreading of DNA methylation to protect the proper expression ofprotein-coding genes. Qian et al. (2012) reported that a histoneacetyltransferase INCREASED DNA METHYLATION1 (IDM1) isrequired for ROS1-dependent active DNA demethylation. IDM1binds to methylated DNA at chromatin sites lacking histone H3K4di-/tri-methylation and acetylates H3 at K18 and K23 sites to createa chromatin environment for the accessibility of ROS1 to target loci.A substantial subset of ROS1 target loci depends on the acetyl-transferase activity of IDM1 on histones (Qian et al., 2012). IDM1,also known as ROS4, was also identified by Dr. Zhizhong Gong'slaboratory using a 35S-NPTII-based forward genetic screen (Li et al.,2012). To uncover more factors functioning upstream of ROS1during target recognition, an efficient forward genetic screen sys-temwas established in Dr. Jian-Kang Zhu's laboratory in which theexpression of 35S promoter-driven SUC2 transgene causes a short-root phenotype on sucrose medium. Mutations in DNA demethy-lation and anti-silencing factors will lead to increase of DNAmethylation level in transgene promoter and silencing of SUC2transgene, and the corresponding mutants grow normally in su-crose medium (Wang et al., 2013b; Lei et al., 2015). Multiple anti-silencing/DNA demethylation factors have been identified fromthis screen system, including IDM2 (Qian et al., 2014), IDM3 (Langet al., 2015), MET18 (Duan et al., 2015a), METHYL-CPG-BINDINGDOMAIN 7 (MBD7) (Lang et al., 2015), HARBINGER TRANSPOSON-DERIVED PROTEIN 1 (HDP1) and HDP2 (Duan et al., 2017a). Zhaoet al. from Dr. Zhizhong Gong's group also identified IDM2 in the35S-NPTII-based screen in which it was named as ROS5 (Zhao et al.,2014). Among these novel DNA demethylation regulators, IDM2,IDM3, MBD7, HDP1 and HDP2 associate with histone acetyl-transferase IDM1 in vivo to form a protein complex and function inROS1-dependent active DNA demethylation (Duan et al., 2017a). Inthis complex, MBD7 is a methylated DNA-binding protein whichshows high binding affinity to DNA regionwith highmethylated CGdensity (Lang et al., 2015). HDP2 is a member of trihelix tran-scription factor family with conserved MYB-like DNA-bindingdomain (Duan et al., 2017a). MBD7 and HDP2 associate with IDM1through interactionwith HSP20-like chaperon proteins IDM2/3 andscaffold protein HDP1, respectively. So, in IDM complex, DNA-binding proteins MBD7 and HDP2 jointly determine the targetspecificity of IDM1-mediated histone acetylation modification,thereby recruiting DNA demethylase ROS1 to specific target loci(Lang et al., 2015; Duan et al., 2017a), although the underlyingrecruitingmechanism is still unclear. Moreover, IDM1 only targets asmall part of ROS1-mediated demethylation loci. Alternativemechanisms for ROS1 recruitment are supposed to be present andshould be clarified in the future study.

Epigenetic inheritance is coupled with DNA replication. How-ever, epigenetic marks are not always precisely copied from theparental cells in each cell cycle which leads to epigenomic change-dependent cell differentiation or different cell responses to envi-ronmental stresses. Recently, more and more evidences haverevealed that DNA replication-related factors are involved in theregulation of TGS. Evidence from Dr. Zhizhong Gong's laboratoryreveals that TOUSLED protein kinase, is required for the mainte-nance of DNA methylation-independent TGS in Arabidopsis (Wanget al., 2007). They provided further evidence to show that DNApolymerase a, which has been shown to interact with LIKE HET-EROCHROMATIN PROTEIN 1 (LHP1) (Barrero et al., 2007), is

involved in chromatin-mediated inheritance during DNA replica-tion. A mutation in DNA polymerase a in Arabidopsis results in therelease of TGS (Liu et al., 2010b). Moreover, Dr. Zhizhong Gong'slaboratory also found that several core DNA replication proteinsand DNA replication-related proteins, including DNA replicationprotein A2A (RPA2A), Replication Factor C1 (RFC1) and DNA poly-merase ε, are directly involved in TGS and chromatin maintenance(Kapoor et al., 2005; Xia et al., 2006; Yin et al., 2009; Liu et al.,2010c). Among them, RPA2A physically interacts with DNA deme-thylase ROS1, suggesting that DNA methylation is dynamicallymaintained during DNA replication (Kapoor et al., 2005; Xia et al.,2006).

2.3. DNA methylation-dependent posttranscriptional regulation ofgene expression

In principal, DNAmethylation often exerts deleterious effects ongene expression at the transcriptional level due to the formation ofheterochromatin in hypermethylated regions. For example, ROS1dysfunction leads to a spread of hypermethylation to the promoterregion of EPF2 gene, which causes transcriptional silencing of EPF2(Fig. 3A) (Yamamuro et al., 2014). However, DNA methylation isfound not only in intergenic regions and gene promoters, but also intranscribed regions, including the introns. In most cases this iscaused by the insertion of TEs or repetitive elements (To et al.,2015). Although it is not clear about the biological functions ofgene body DNA methylation, recent studies have provided impor-tant hints for answering this question. ANTI-SILENCING 1 (ASI1), anRNA-binding protein, was firstly identified from a forward geneticscreen for the factors preventing transgene silencing (Wang et al.,2013b). Wang et al. (2013b), a Japanese group (Saze et al., 2013)and a France group (Coustham et al., 2014) uncovered a unique roleof ASI1, also named as INCREASE BONSAI METHYLATION 2 (IBM2)and SHOOT GROWTH1 (SG1), in RNA processing and gene bodyCHG methylation through an uncharacterized mechanism. In thismechanism, ASI1 is required for the expression of full-lengthtranscripts of the intronic heterochromatin-containing genesthrough affecting the selection of proximal and distal poly-adenylation sites, an RNA processing mechanism called alternativepolyadenylation (APA). In asi1 mutant, truncated short transcriptsare excessive accumulated whereas functional full-length tran-scripts are dramatically reduced, even completely repressed (Wanget al., 2013b). The histone H3K9me2 demethylase gene IBM1 is adirect target of ASI1. Hence, asi1 mutant phenocopies ibm1 mutantin gene body CHG methylation due to the increased levels ofH3K9me2. Moreover, recent studies from Chinese and Americangroups revealed the involvement of two new players in thismechanism, ENHANCED DOWNY MILDEW 2 (EDM2) and ASI1-IMMUNOPRECIPITATED PROTEIN1 (AIPP1) (Tsuchiya and Eulgem,2013; Lei et al., 2014; Duan et al., 2017b). These three compo-nents form a protein complex in vivo, ASI1-AIPP1-EDM2 (AAE)complex, in which AIPP1 serves as a bridge protein to interact withASI1 and EDM2, respectively (Duan et al., 2017b) (Fig. 3B). Althoughthe detailed molecular mechanism remains unclear, current evi-dence has shown that AAE complex is specifically recruited totarget genes through the unique chromatin structure of the intronicheterochromatin in gene body. EDM2 bears three copies of planthomeodomains (PHDs) and displays H3K4me3- and H3K9me2-binding affinity in vitro (Lei et al., 2015). Therefore, in this case,the epigenetic marks, including DNA methylation and histonemodifications, may serve as a functional module to recruit AAEcomplex to target loci for proper RNA processing. Consistent withthis notion, depletion of intronic heterochromatin represses theRNA processing defects caused by asi1 and edm2 mutations (Wanget al., 2013b; Lei et al., 2014). Moreover, Rigal et al. (2012) and our

Fig. 3. DNA methylation-dependent transcriptional gene silencing and posttranscriptional RNA processing. A: Intergenic DNA methylation spreads to promoter regions to result intranscriptional gene silencing. DNA methylation is dynamically regulated by DNA methylation and demethylation, and DNA methylation can affect DNA demethylation by regulatingthe transcription of DNA demethylase gene ROS1. Dysfunction of DNA demethylation will lead to the spread of DNA hypermethylation to promoter regions which represses theexpression of downstream genes. Red and grey rectangles represent TEs and exons, respectively. Black arrows represent transcriptional direction. B: Posttranscriptional RNAprocessing mediated by intronic DNA methylation. When intronic TE is methylated, the intragenic heterochromatin will recruit ASI1-AIPP1-EDM2 (AAE) complex to this region topromote distal polyadenylation. When DNA methylation is lost in the intronic TE, failure of AAE complex recruitment will result in proximal polyadenylation.


unpublished data showed that DNA methyltransferases MET1 andCMT3 and histone H3K9 methyltransferases SUVH4, SUVH5 andSUVH6 are required for the accumulation of full-length IBM1transcript. These evidences suggest that DNA methylation canaffect gene expression at both transcriptional and post-transcriptional levels (Fig. 3).

AAE complex-mediated heterochromatin-dependent RNA pro-cessing is involved in multiple biological processes. Besides theregulation of CHG methylation through IBM1, fungal diseaseresistance gene RPP7 is the direct target of AAE complex. edm2mutant displays similar sensitive phenotype to rpp7 mutant uponfungal infection (Eulgem et al., 2007). Moreover, similar phenom-enon has been reported in oil palm in which the processing of oilgene DEF1 is subjected to the DNA methylation levels of Karma, anintronic LINE retrotransposon embedded in DEF1 gene body (Ong-Abdullah et al., 2015). Although AAE complex-encoding genes havenot been characterized in other species, our unpublished data alsoproved the presence of orthologue protein of Arabidopsis ASI1 in oilpalm and the majority of plant species but not in mammalians,suggesting that ASI1 is a plant-specific protein and ASI1-mediatedRNA processing as a novel epigenetic mechanism is conservedacross different plant species.

3. N6-adenosine methylation

In addition to the most extensively studied DNA cytosinemethylation, N6-adenosine methylation (6mA), which can occur inRNA and DNA strands, is gaining more and more attentionsrecently. The importance of RNA methylation at N6-adenosine isconstantly being clarified and Chinese researchers have achievedgreat achievements in this field. 6mA plays crucial roles in multiplebiological processes. Pattern and function of 6mA methylation are

determined by RNA methyltransferase, 6mA-binding protein anddemethylase (Fu et al., 2014). Dr. Chuan He's laboratory investi-gated the genome-wide profile of 6mA methylation in Arabidopsisand revealed some plant-specific features of 6mA distribution (Luoet al., 2014), revealing the conservation of RNA methylation inplants. In the 6mAmodifiers, Shen et al. (2016) proved that FIP37 isa core component of 6mA methyltransferase complex and plays acritical role in the regulation of shoot stem cell fate in Arabidopsis.Dr. Guifang Jia's laboratory revealed that ALKBH10B can reverse6mAmethylation in Arabidopsis and is required for floral transition,demonstrating that ALKBH10B is a 6mA RNA demethylase (Duanet al., 2017c). Recently, Dr. Guifang Jia’ laboratory and the othertwo groups characterized the YTH-domain family protein ECT2 asthe 6mA reader functioning in the regulation of trichome branchingand developmental timing in Arabidopsis (Arribas-Hernandez et al.,2018; Scutenaire et al., 2018; Wei et al., 2018). In addition to 6mARNA methylation, 6mA DNA methylation has recently been shownto be an important epigenetic mark in eukaryotes. Liang et al.(2018) characterized the genome-wide profile of 6mA DNAmethylation in Arabidopsis. They found that DNA 6mA methylationis enriched in gene bodies and pericentromeric heterochromatinregions, and is potentially associated with actively expressed genes,suggesting an important regulatory role of 6mA DNA methylationin plants. Interestingly, 5mC modification as a well-known DNAmethylation is also present in RNAs in both prokaryotes and eu-karyotes. Cui et al. (2017) characterized the dynamic pattern of 5mCRNA methylation in Arabidopsis. They revealed that 5mC RNAmethylation is enriched in coding sequences and a tRNA-specificmethyltransferase 4B (TRM4B) shows the 5mC RNA methyl-transferase activity. TRM4B is required for root development, sug-gesting that 5mC RNA methylation as a new epigenetic mark playscritical roles in plant development. The researches in RNA


epigenetics field, including RNA 6mA and 5mCmethylation, are stillat an early stage, and largely is unknown about the underlyingmolecular mechanism, such as the establishment, recognition andremove of this RNA epigenetic mark. The identification of newcomponents involved in the dynamic process and the discovery ofits biological functions would be an important focus in the futureepigenetic research.

4. Histone modifications

Histone modifications refer to the posttranslational covalentmodifications on the amino-terminal tails of the core histones.Histone posttranslational modifications (PTMs) serve as histonecode to constitute the other layer of epigenetic mechanism. ThesePTMs include acetylation, methylation, ubiquitination, sumoyla-tion, and phosphorylation. Regulation of histone modifications hasbeen extensively investigated. Among different histone modifica-tions, histone methylation, which not only occurs at different res-idues (lysine and arginine) and different sites but also differs in thenumber of added methyl groups, plays an essential role in multiplebiological processes, including transcriptional regulation of TEs andprotein-coding genes during plant development and stressresponse (Liu et al., 2010a). Among different histone methylations,histone lysine methylation is widely investigated due to itsimportant roles in both transcriptional activation and repression. Inplants, histone H3 lysine methylation occurs at four sites, 4, 9, 27and 36. The function of histone methylation is dependent of thesites of methylated lysine residues and the number of methylgroups. For example, H3K9 and H3K27 methylations are generallyconsidered as repressive marks which are often associated withsilenced regions, while H3K4 and H3K36methylations are enrichedin actively expressed genes. H3K9me2 is enriched in chromocen-ters, where TEs and repeated sequences are enriched and DNAmaintains hypermethylated. Loss of H3K9me1/2 results in reducednon-CG DNA methylation and released silencing of TEs. In theseloci, H3K9 methylation interplays with DNA methylation to rein-force each other. Similar to DNA methylation, histone methylationpattern is dynamically regulated by histone methylase (writer) anddemethylase (eraser)-mediated enzymatic reactions. Differenthistone methylation modifications can be bound by reader proteinto recruit downstream factors. To better understanding the

Table 1Characterized modifiers of histone lysine methylation (HKM) in Arabidopsis and rice.

HKM Species Writer Reader

H3K4 Arabidopsis ATX1 (Pien et al., 2008)ATX2/SDG30 (Saleh et al., 2008)ATX3/4/5 (Chen et al., 2017)SDG4/ASHR3 (Cartagena et al., 2008)ATXR3/SDG2 (Guo et al., 2010)ATXR7/SDG25 (Tamada et al., 2009)

SDG8 (HoppmannALs (Lee et al., 200AtING (Lee et al., 2WDR5a (Jiang et aSHL (Lopez-GonzaEBS (Lopez-Gonza

Rice SDG701 (Liu et al., 2017b) SDG725 (Liu and HCHR729/CHD3 (Hu

H3K9 Arabidopsis KYP/SUVH4 (Jackson et al., 2002)SUVH5 (Ebbs and Bender, 2006)SUVH6 (Ebbs et al., 2005)SUVR4 (Thorstensen et al., 2006)

EDM2 (Tsuchiya aCMT2/3 (Du et al.,SHH1/DTF1 (Law e

Rice SDG714 (Ding et al., 2007)H3K27 Arabidopsis ATXR5, ATXR6 (Jacob et al., 2009)

CLF/SDG1 (Schonrock et al., 2006; Schubertet al., 2006)MEA (Grossniklaus et al., 1998)SWN (Chanvivattana et al., 2004)

LHP1 (Turck et al.,et al., 2009)SHL (Qian et al., 2CYP71 (Li et al., 20

Rice CHR729/CHD3 (HuH3K36 Arabidopsis SDG8/ASHH2 (Xu et al., 2008)

SDG4/ASHR3 (Cartagena et al., 2008)MRG1/2 (Bu et al.

Rice SDG725 (Sui et al., 2012)

Bold literatures represent publications contributed by Chinese researchers or groups.

biological functions of these histone marks, it is important to un-cover and characterize the factors involved in the establishment,recognition and removal of these epigenetic information. Table 1summarizes the known histone lysine methylation modifiers inArabidopsis and rice.

Writers: Most of the histone lysinemethylation is catalyzed by afamily of SET domain-containing proteins in Arabidopsis and rice(Zhao and Shen, 2004; Liu et al., 2010a). There are 49 SET domain-containing proteins in Arabidopsis, known as the SET DOMAINGROUP (SDG) proteins, which can be classified into five groupsbased on their activity and domain architecture (Zhao and Shen,2004). Among them, H3K9 methylation is achieved by SUVH pro-teins. KRYPTONITE (KYP; also known as SUVH4) functions partiallyredundant with SUVH5 and SUVH6 to catalyze H3K9 methylation.Genome-wide loss of DNA methylation at all cytosine contextswere observed in the suvh4/5/6 triple mutant. In 2001, Shen iden-tified the SET domain-containing proteins in tobacco and Arabi-dopsis which show highest homologies with the DrosophilaSU(VAR)3-9 protein (Shen, 2001). Liu et al. from Dr. Wen-HuiShen's laboratory and Ding et al. from Dr. Xiaofeng Cao's labora-tory identified NtSET1 in tobacco and SDG714 in rice as H3K9methyltransferases functioning in heterochromatin formation(Ding et al., 2007; Liu et al., 2007b).

As another repressive histone mark, H3K27 can be mono-, di- ortri-methylated in Arabidopsis. Similar to H3K9me1/2, H3K27me1 isenriched at constitutively silenced heterochromatin regions,whereas H3K27me3 is enriched in euchromatin regions in plants(Fuchs et al., 2006). In Arabidopsis, H3K27me1 is catalyzed byARABIDOPSIS TRITHORAX-RELATED PROTEIN5 (ATXR5) and ATXR6(Jacob et al., 2009). Different from H3K9me2 which affects DNAmethylation, H3K27me1 is DNA methylation-independent and itsdeposition is not affected by the depletion of H3K9me2. Zhang et al.(2007a) investigated the genome-wide distribution of H3K27me3and found that H3K27me3 is preferentially enriched in the tran-scribed region of coding genes, indicating amajor repressive role ongene expression in Arabidopsis. H3K27me3-dependent genesilencing is achieved mainly through two polycomb group (PcG)repressive complexes (PRCs), PRC2 and PRC1. PRC2 is a H3K27me3methylation complex in which CLF, MEA and SWN are believed tobe H3K27me3 methyltransferases in Arabidopsis (Luo et al., 1999;Wang et al., 2006; Kim and Sung, 2014). The deposition of

Eraser

et al., 2011)9)009)l., 2009)lez et al., 2014; Qian et al., 2018)lez et al., 2014)

LDL1 (Spedaletti et al., 2008)JMJ14 (Lu et al., 2010)JMJ18 (Yang et al., 2012a)JMJ15/MEE27 (Liu et al., 2010a; Yang et al.,2012b)

uang, 2018)et al., 2012)

JMJ703 (Cui et al., 2013)

nd Eulgem, 2013; Lei et al., 2014)2012; Stroud et al., 2014)t al., 2013; Zhang et al., 2013b)

IBM1/JMJ25 (Saze et al., 2008)JMJ27 (Dutta et al., 2017)

JMJ706 (Sun and Zhou, 2008)2007; Zhang et al., 2007b; Exner

018)07)

JMJ12/REF6 (Lu et al., 2011)

et al., 2012) JMJ705 (Li et al., 2013), 2014)


repressive H3K27me3 recruits PRC1 complex to the target chro-matin to catalyze mono-ubiquitination of H2A (H2Aub1) (Kim andSung, 2014). Liang et al. (2003) and Luo et al. (2009) characterizedthe homologs of PcG genes in rice and revealed important regula-tory roles of H3K27me3 in multiple developmental processes inrice.

Compared to repressive H3K9 and H3K27 methylation marks,H3K4methylation is widely believed to be involved in transcriptionactivation. H3K4me1/2/3 are highly enriched in genic regions butdepleted in TEs, among which H3K4me3 is present exclusively onactive genes and H3K4me1/2 occur on both active and inactivegenes (Liu et al., 2010a). Methylation of H3K4 is catalyzed by thehighly evolutionarily conserved COMPASS or COMPASS-like H3K4methyltransferase complexes, in which a Trithorax group (TrxG)H3K4 methyltransferase and a core structural subcomplex areincluded (He, 2012). In Arabidopsis, there are five ARABIDOPSISTRITHORAX proteins (named ATX1‒5) and seven ATX-relatedproteins (named ATXR1‒7). ATX1/SDG27, ATX2/SDG30 andATXR7/SDG25 have been shown to display H3K4methyltransferaseactivity (Chen et al., 2017). Dr. Xiaoyu Zhang's laboratory identifiedATXR3/SDG2 as a specific H3K4me3 methyltransferase (Guo et al.,2010). Dysfunction of ATXR3 leads to a dramatic reduction ofH3K4me3 in vivo and severe developmental defects. Recently, Chenet al. from Dr. Yan He's laboratory revealed that ATX3, ATX4 andATX5 function redundantly to methylate H3K4 (Chen et al., 2017).Song et al. from Dr. Jian-Xiang Liu's laboratory identified that basicleucine zipper (bZIP) transcription factors bZIP28 and bZIP60interact with COMPASS-like components to regulate the depositionof H3K4me3 at specific gene promoters (Song et al., 2015b). In rice,SDG701 has been characterized to catalyze H3K4 methylation andfunctions in regulation of flowering and development (Liu et al.,2017b).

For H3K36methylation, Dr.Wen-Hui Shen's laboratory providedexperimental evidence that SDG8 is a major methyltransferasespecific for di- and tri-methylation of H3K36 (Xu et al., 2008). Liet al. from Dr. Yuehui He's laboratory revealed that the evolution-arily conserved nuclear mRNA cap-binding complex (CBC) interactswith COMPASS-like complex and a histone H3K36 methyl-transferase to form a multi-protein complex and functions in theco-transcriptional mRNA processing and cap preservation. In thismechanism, histone methyltransferases are required for CBC-mediated mRNA cap preservation and proper RNA splicing, there-fore revealing a novel role for active histone marks in RNA pro-cessing (Li et al., 2016b). In rice, Sui et al. (2012) reported SDG725 asa H3K36 methyltransferase.

Readers: The epigenetic information of different histone markscan be translated by reader proteins to direct downstream func-tions. To a certain extent, it is the readers/effectors which ulti-mately determine the biological outcome of certain histone PTMs.Different reader proteins exhibit distinct binding specificity tohistone marks. According to current knowledge, the known readerscan be classified into three groups. The first group is the royalfamily domain group proteins which share a conserved structuralcore and have been shown to be readers of methylated histones,including chromodomain, Tudor domain (also known as Agenetdomain in plants), MBT (malignant brain tumour) domain andPWWP (Pro-Trp-Trp-Pro) domain (Liu et al., 2010a; Liu and Min,2016). The second group is the plant homeodomain (PHD) fingergroup proteins. WD40 repeat-containing WDR5 group belongs tothe third group (Liu et al., 2010a). In the first group of chromodo-main proteins, the chromodomain-containing protein LHP1 as acomponent of PRC1-like complex in Arabidopsis shows bindingspecificity to H3K27me3 in vivo (Turck et al., 2007; Zhang et al.,2007b). Interestingly, HP1, the mammalian counterpart of Arabi-dopsis LHP1, is a H3K9me2/3 reader and shows much weaker

interaction with H3K27me3 (Liu and Min, 2016). Biochemical andstructural evidence has revealed that both the chromodomains andbromo-adjacent homology (BAH) domains of CMT2/3 DNA meth-yltransferases bind to H3K9me2 (Du et al., 2012; Stroud et al., 2014).PHD domain is a zinc-binding domain and one major function ofPHD domain is histone binding. A lot of PHD domain-containinghistone readers have been identified in Arabidopsis, such as theH3K4me2/3 readers INHIBITOR OF GROWTH 1/2 (ING1/2) andAlfin1-like (AL) family proteins (Liu and Min, 2016). The biochem-ical and ChIP data fromDr. Jian-Kang Zhu's laboratory and the othergroup revealed that the chromatin regulator EDM2, which bearsthree copies of PHD domains, binds to H3K9me2 and functions inAPA regulation (Lei et al., 2014; Tsuchiya and Eulgem, 2013).

CHD (chromodomain, helicase/ATPase and DNA bindingdomain) and MRG (morf-related gene) proteins also belong to thechromodomain proteins. It has been reported that some readerproteins are capable of recognizing two or more histone marks(Wang and Patel, 2011). Dr. Ai-Wu Dong's laboratory revealed thatthe MRG group proteins MRG1 and MRG2 act as the readers ofH3K4me3/H3K36me3 dual marks and function in photoperiod-dependent flowering time regulation (Bu et al., 2014). In rice,CHR729/CHD3 interacts with H3K4me2 and H3K27me3 through itschromodomain and PHD domains, respectively (Hu et al., 2012),suggesting that CHR729 is a bifunctional chromatin regulatorcapable of recognizing and modulating H3K4 and H3K27 methyl-ation dual marks. More recently, Qian et al. (2018) identified aplant-specific histone modification reader SHORT LIFE (SHL) inArabidopsis which recognizes dual marks, H3K4me3 andH3K27me3. SHL bears BAH and PHD domains, and the PHD domainhas been shown to bind to H3K4me2/3 in vitro (Lopez-Gonzalezet al., 2014). Qian et al. (2018) provided structural and biochem-ical evidence that the BAH domain of SHL is capable of binding toH3K27me3. They further proved that SHL-bound genes colocalizewith H3K4me3 and H3K27me3, suggesting that SHL modulatesgene expression through the recognition of antagonistic histonemarks. EARLY BOLTING IN SHORT DAYS (EBS), the paralogue of SHLin Arabidopsis, also bears both BAH and PHD domains. In vitro pull-down assay has proved that the PHD domain of EBS binds toH3K4me2/3, although the binding specificity of its BAH domain hasnot been determined (Lopez-Gonzalez et al., 2014). These findingssuggest that dual recognition of different histone marks may be ageneral epigenetic mechanism in the fine-tuning regulation of theirassociated genes.

The Tudor domain is a reader of lysine or arginine methylationmarks. Arabidopsis genome encodes 32 Tudor domain-containingproteins, and most of them have not been characterized. Recently,a SAWADEE domain protein SHH1 has been shown as a H3K9methylation reader functioning in RdDM through its interactionwith Pol IV (Law et al., 2011; Zhang et al., 2013b). Structural studieshave revealed that the SAWADEE domain of SHH1 adopts a tandemTudor-like fold with a unique zinc finger embedded in the secondTudor-like domain (Law et al., 2013; Zhang et al., 2013b).

Arabidopsis genome encodes two WDR5 homologues, WDR5aand WDR5b. However, only WDR5a has been shown to bind toH3K4me2 mark and interact with H3K4 methyltransferase ATX1(Jiang et al., 2009). WDR5a is required for the recruitment ofCOMPASS-like complex and promotes the expression of floweringrepressor FLOWERING LOCUS C (FLC). Dr. Sheng Luan's laboratoryrevealed that a WD40 protein CYP71 interacts with H3K27me3through its WD40 domain (Li et al., 2007).

The CW (Cys-Trp) domain is a zinc-binding domain which iscomposed of approximately 50e60 residues. Recently, CW proteinhas been shown to be a H3K4 methylation reader (He et al., 2010;Hoppmann et al., 2011; Liu et al., 2016b). The CW domain displaysdifferent preference for the degree of H3K4 methylation.


Arabidopsis genome encodes 11 CW domain-containing proteins.The histone H3K36 writer SDG8/ASHH2 has been proved to bind toH3K4me1 mark (Hoppmann et al., 2011; Liu and Huang, 2018).Consistently, Liu and Huang (2018) reported that SDG725, the ho-molog of SDG8 in rice, displays similar preference for H3K4me1.

Erasers: Histone demethylation is catalyzed by two types oferasers (demethylases) with different mechanisms, amine oxida-tion by lysine-specific demethylase 1 (LSD1) family proteins andhydroxylation by JumonjiC (JmjC) domain-containing proteins(JMJs) (Liu et al., 2010a). LSD1 family demethylases act on di- andmono-methylation, whereas JMJ demethylases act on all threekinds of lysine methylation (Klose and Zhang, 2007). Four homo-logs of LSD1 are encoded by Arabidopsis genome, includingFLOWERING LOCUS D (FLD), LSD1-LIKE1 (LDL1), LDL2 and LDL3.Among them, LDL1 and FLD have been shown to bear H3K4demethylase activity (Jiang et al., 2007; Liu et al., 2007a). Arabi-dopsis and rice genomes encode 21 and 20 JMJs, respectively (Luet al., 2008a). These JMJs can be classified into five groups ac-cording to sequence similarities, KDM3, KDM4, KDM5, KDM6 andJmjC domain-only groups. Among them, several members havebeen identified as histone demethylases by Chinese researchers. Luet al. from Dr. Xiaofeng Cao's laboratory proved that JMJ14, one ofthe six homologs of KDM5 group, is an active histone H3K4demethylase involved in flowering time regulation through therepression of floral integrators (Lu et al., 2010). Recently, the crystalstructure of JMJ14 catalytic domain revealed by two Chinese groupsindicated that the critical acidic residues are conserved in plantsand animals, suggesting a common substrate recognition mecha-nism for KDM5 group histone demethylases (Yang et al., 2018).JMJ18, another KDM5 group protein, has been identified as a his-tone H3K4 demethylase in Arabidopsis. JMJ18 is predominantlyexpressed in phloem companion cells and promotes the floraltransition by directly binding FLC chromatin for H3K4 demethyla-tion (Yang et al., 2012a). JMJ11/ELF6 and JMJ12/REF6 are twomembers of KDM4 group. Dysfunctions of JMJ11 and JMJ12 displayearly and late flowering phenotypes, respectively (Yu et al., 2008).Dr. Xiaofeng Cao's laboratory revealed that JMJ12/REF6 is a histoneH3K27me2/3 demethylase (Lu et al., 2011), which is the first his-tone H3K27 demethylase identified in plants and fills a major gap ofthe dynamic regulation of H3K27me3. In rice, Dr. Xiaofeng Cao'slaboratory reported that OsJMJ703 is an active H3K4-specificdemethylase which is required for TE silencing, suggesting a roleof histone demethylase in the right control of TE (Cui et al., 2013).Dr. Dao-Xiu Zhou's laboratory revealed that the rice JMJ706, one ofthe JMJD2 family proteins, specifically reverses di- and tri-methylation of H3K9 (Sun and Zhou, 2008). Loss-of-function mu-tations of JMJ706 gene result in severe development defects, sug-gesting that histone demethylases are involved in thedevelopmental regulation in rice. Li et al. from the same laboratoryalso revealed that JMJ705 catalyzes the removal of tri-methylationof H3K27 and functions in defense-related gene activation in rice (Liet al., 2013).

5. Epigenetic mechanisms in flowering time regulation

The floral transition is a major developmental switch in angio-sperms. This biological process is tightly controlled by multiplemechanisms, including environmental (temperature, photoperiodand vernalization) and genetic (autonomous pathway, gibberellin(GA) pathway and FRIGIDA (FRI) pathway) factors. In Arabidopsis,the flowering repressor FLC is a convergent point of several flow-ering pathways. The expression of FLC is promoted by FRI andrepressed by autonomous pathway and vernalization (He, 2012).The expression of FLOWERING LOCUS T (FT), which encodes themajor component of florigen, is repressed by FLC but promoted by

long-day photoperiod and GA pathway (He, 2015). In FRI-mediatedactivation of FLC, multiple active histone modifications arerecruited to FLC locus, including H3K4me3, H3K36me3 and histoneacetylation marks. H3K4me3 is mainly enriched in the regionaround the transcription start site (TSS) of FLC. The deposition ofH3K4m3 on FLC chromatin requires a COMPASS-like H3K4 meth-yltransferase complex. Dr. Yuehui He's laboratory revealed thatCOMPASS-like complex in Arabidopsis contains at least four sub-units, a SET domain-containing H3K4 methyltransferase and threestructural components including WDR5a, RBBP5 LIKE (RBL) andARABIDOPSIS ASH2 RELATIVE (ASH2R) (Jiang et al., 2009, 2011).H3K4me3 writer ATX1 has been shown to be associated withWDR5a in the COMPASS-like complex (Jiang et al., 2009). BesidesCOMPASS-like complex-dependent H3K4me3, the activation of FLCexpression in plants encoding FRI also requires the depositions ofH3K36me3 and histone variant H2A.Z (Choi et al., 2007; Xu et al.,2008). H3K36me2/3 are catalyzed by SDG8/EFS, a homolog of theyeast SET2 histone methyltransferase, in FLC locus (Xu et al., 2008).Zhao et al. (2005) reported that loss-of-function mutant of SDG8displays attenuated expression of FLC due to reduced H3K36me2accumulation.

For the flowering of winter annual plants, vernalization isrequired to silence FLC expression, which is achieved by longnoncoding RNAs (lncRNAs) and PRC complex-mediated depositionof H3K27me3 mark at FLC locus. The silencing of FLC is stablymaintained during the subsequent growth and development uponreturn to warm temperature. It is still not fully understood abouthow PcG complex is recruited to FLC locus and the spreading ofrepression. Polycomb response elements (PREs) have been shownto function in PcG complex recruitment in Drosophila melanogasterby directly interacting with PcG factors, which have not been foundin other species. Recently, Dr. Yuehhui He's laboratory identified a47-bp FLC silencing element which could be recognized bysequence-specific readers VIVIPAROUS1/ABI3-LIKE1 (VAL1) andVAL2. VAL1 and VAL2 bind this cis-element and H3K27me2/3marks and recruit PcG complex to the nucleation region of FLC locusby directly interacting with LHP1 (Yuan et al., 2016). In the dynamicregulation of FLC during lifecycle, another remaining question ishow FLC silencing is reset during each generation. Evidence fromthe same group revealed that a seed-specific transcription factorLEAFY COTYLEDON1 (LEC1) could reverse the silencing of FLCinherited from gametes by promoting the initial establishment ofan active chromatin state at FLC, leading to transmission of theembryonic memory of FLC activation to post-embryonic stages (Taoet al., 2017). This finding reveals a mechanism for the reprogram-ming of embryonic chromatin states in plants and provides insightsinto the epigenetic memory of embryonic active gene expression inpost-embryonic phases.

Through the photoperiod pathway, inductive day lengthspromote flowering by triggering the production of florigen. Inlong-day plant Arabidopsis, the expression of major florigen FT isrhythmically activated by CONSTANS (CO), the output of thephotoperiod pathway, specifically at the end of long days. Gu et al.(2013) reported a periodic histone deacetylation mechanism forthe photoperiodic regulation of FT expression. They found that ahistone deacetylase (HDAC) complex, which includes SAP30FUNCTION-RELATED 1 (AFR1) and AFR2, is recruited by theMADS-domain transcription factor AGAMOUS LIKE 18 (AGL18) to FTchromatin specifically at the end of long days, resulting in histonedeacetylation and attenuated expression of FT (Gu et al., 2013).Moreover, during this regulation, the activity of CO is required forthe recruitment of this HDAC complex (Gu et al., 2013), suggestingthat CO bears two different mechanisms to achieve a preciseregulation of flowering time in response to the inductive long-daycondition. Moreover, Dr. Ai-Wu Dong's laboratory revealed that


the H3K4me3/H3K36me3 readers MRG1 and MRG2 physicallyinteract with CO to activate FT expression, thereby promotingflowering in long-day photoperiod (Bu et al., 2014). In the regu-lation of photoperiod-dependent CO, recent studies revealed thatnuclear factor Y (NF-Y), a heterotrimeric transcription factorcomplex which binds to the CCAAT motif, is also involved. Houet al. (2014) reported that NF-Y in Arabidopsis interacts with COin the photoperiod pathway and DELLAs in the GA pathway toregulate the transcription of floral pathway integrator SUPPRES-SOR OF OVEREXPRESSION OF CO1 (SOC1) by directing binding to aunique cis-element within its promoter. They further revealedthat NF-Y protein NF-YC counteracts the deposition of H3K27me3in FT by temporal interaction with CLF, thereby attenuating theassociation of CLF with FT chromatin under long-day condition(Liu et al., 2018a).

Besides histonemethylation of H3K4, H3K36 and H3K27, severalother histone modifications also participate in the regulation offloral transition in Arabidopsis. For example, Luo et al. (2015) re-ported that histone deacetylase HDA5 interacts with FVE, FLD, andHDA6 and binds to FLC, therefore negatively regulating its expres-sion. Therefore, hda5 mutant displays a late flowering phenotype.Su et al. (2017) reported that a plant-specific histone H2A phos-phorylation on serine 95 (H2AS95) catalyzed by MUT9P-LIKE-KINASE (MLK4) is involved in photoperiod-dependent regulationof flowering time in Arabidopsis. mlk4 mutant displays late flow-ering phenotype under long-day but not short-day conditions. Theyrevealed thatMLK4 interacts with CIRCADIAN CLOCK ASSOCIATED1(CCA1) which interacts with SWI2/SNF2-RELATED 1 (SWR1) com-plex. This interaction allows MLK4 to bind to the GIGANTEA (GI)promoter, thereby promoting the deposition of H2A.Z and histoneacetyltransferase activity and resulting in reduced expression of GI(Su et al., 2017).

In rice (Oryza sativa), similar epigenetic mechanisms are pre-sent in the regulation of heading date. There is also a COMPASS-like complex required for promoting flowering (Jiang et al.,2018a). In this complex, OsTrx1/SDG723 interacts with OsW-DR5a and a transcription factor SDG723/OsTrx1/OsSET33 INTER-ACTION PROTEIN 1 (SIP1), allowing OsTrx1 to bind to Earlyheading date 1 (Ehd1) which encodes a positive regulator of FT-like protein in rice (Jiang et al., 2018a, 2018b). Liu et al. (2017b)revealed that the H3K4 methyltransferase SDG701 in rice pro-motes photoperiod-independent flowering through enhancingthe expression of Heading date 3a (Hd3a) and RICE FLOWERINGLOCUS T1 (RFT1) florigens. Similarly, Liu et al. (2016a) identifiedSDG708 as an H3K36 methyltransferase in rice. Knocking downSDG708 causes photoperiod-independent late flowering in ricedue to the down-regulation of H3K36me3 levels on several keyflowering genes, including Hd3a, RFT1 and Ehd1. Different fromArabidopsis, evidence from Dr. Hong-Wei Xue's laboratoryrevealed that PRC2 is involved in photoperiod-dependent flow-ering regulation (Wang et al., 2013a). They found that theexpression of VERNALIZATION INSENSITIVE 3-LIKE 3 (OsVIL3) andOsVIL2, the putative components of PRC2 complex in rice, isinduced by short-day photoperiod. LC2 and OsVIL2 promoteflowering by depositing H3K27me3 mark on floral repressor geneOsLFwhich encodes a repressor of Hd1. Evidence from Dr. Dao-XiuZhou's laboratory further revealed that SDG711 and SDG718, theother two PRC2 components in rice, are required for photoperiod-dependent regulation of key flowering genes (Liu et al., 2014a).The expression of SDG711 and SDG718 is induced by long-day andshort-day photoperiods, respectively. SDG711 and SDG718 repressthe expression of floral repressor gene OsLF through mediatingH3K27me3 deposition in long-day and short-day photoperiods,respectively, leading to higher expression of Hd1 thus late flow-ering in long-day photoperiod and early flowering in short-day

photoperiod. This finding suggests that PRC2-dependentsilencing of gene expression plays important roles in the accu-rate photoperiod control of rice flowering.

6. Epigenetic regulation in plant development

6.1. DNA methylation and plant development

Although there is no clear evidence of resetting of DNAmethylation during plant development, recent studies revealed atight control of DNA methylation levels in different tissues and celltypes during plant development. Gene imprinting, a mechanism ofparental allele-specific expression which plays key roles in seeddevelopment, is closely associated with DME-dependent DNAdemethylation and siRNA-dependent RdDM pathway (Gehringet al., 2004, 2006; Kinoshita et al., 2004). Dr. Jinsheng Lai's grouprevealed that gene imprinting inmaize is tightly controlled throughcomplex interactions between multiple epigenetic mechanisms,including small RNAs, nucleosome positioning, DNA and histonemethylation (Zhang et al., 2011, 2014a; Dong et al., 2017, 2018).Besides gene imprinting in seed, lots of efforts have been made toinvestigate the tissue-specific DNA methylation patterns in plants,includingmajor crops maize, rice and soybean (Xiong et al., 1999; Liet al., 2008; Lu et al., 2008b; Xu et al., 2009; Gao et al., 2010a; Heet al., 2011). In rice, Zhang et al. (2015) revealed a role of DNAmethylation in the regulation of rice RELATED TO ABI3/VP1 6 (RAV6)gene which encodes a B3 DNA-binding protein and controls mul-tiple agronomical traits. These studies demonstrate a close rela-tionship between DNA methylation levels and tissue-specific geneexpression.

Benefiting from the elucidation of more andmore crop genomesand the development of CRISPR/Cas9-mediated gene editing tech-nology, generation of loss-of-function mutants in crop plants be-comes possible. Although most of the DNA methylation-relatedmutants in Arabidopsis grow normal or display mild developmentaldefects, disruption of DNA methylation often results in severedevelopmental abnormalities in crops, and some are even lethal,suggesting more important roles of DNA methylation in cropdevelopment. In tomato, Zhong et al. (2013) characterized the DNAmethylome of fruit and found a strong correlation between DNAmethylation level and fruit development. Consistent with thisnotion, Lang et al. (2017) reported that tomato SlDML2, one of theorthologous proteins of Arabidopsis DNA demethylase ROS1, isrequired for the fine-tuned expression of ripening-induced and-repressed genes. Expression of SlDML2 is dramatically increased inripening tomato fruits, which promotes active DNA demethylationand modulates the expression of ripening-induced or -repressedgenes. Besides fruit ripening, Zhang et al. (2016a) reported thatchilling-induced tomato flavor loss is associated with reducedaccumulation of key volatile synthesis enzyme-coding genesaccompanied with dramatical changes of DNA methylation statusin the promoters of these genes. The involvements of DNAmethylation-dependent regulation in fruit are also observed inother fruits. Strong correlations were observed between DNAmethylation pattern and the fruit size of apple and tomato (Teliaset al., 2011; Liu et al., 2012a; Daccord et al., 2017). These evi-dences suggest that specific DNAmethylation patterns are requiredfor the development of fruits.

6.2. Histone modifications, chromatin remodeling and plantdevelopment

Epigenetic mechanisms not only participate in the regulationof heading date in rice but also is required for floral development.The floral meristem (FM), which develops from inflorescence


meristem (IM) upon completion of the floral transition, termi-nates after producing a defined number of floral organs.WUSCHEL(WUS) encodes a homeodomain-containing protein and plays acritical role in the establishment and maintenance of shoot apicalmeristem (SAM), IM, and FM as well as FM determinacy. Theexpression of WUS is dynamically regulated by multiple epige-netic mechanisms, including DNA methylation, H3K9 and H3K4methylation as well as histone acetylation (Li et al., 2011). TheWUS-related homeobox 11 (WOX11) directly interacts withH3K27me3 demethylase JMJ705 to activate gene expression dur-ing shoot development in rice (Cheng et al., 2018). Moreover, inArabidopsis, MET1-mediated DNA methylation is involved in theregulation of AUXIN RESPONSE FACTOR3 (ARF3) expression,suggesting a role of DNA methylation in auxin signaling-dependent de novo shoot regeneration (Li et al., 2011). In rice,Dr. Jianmin Wan's group identified DEFORMED FLORAL ORGAN1(DFO1) gene which functions in the regulation of floral organidentity (Zheng et al., 2015). They revealed that DFO1 interactswith the rice PcG proteins MULTICOPY SUPPRESSOR OF IRA1(OsMSI1) and ENHANCER OF ZESTE (E(Z)) 1 (OsiEZ1) to mediateH3K27me3 deposition in the chromatin of OsMADS58, one of theMADS-box genes which control floral organ specification. Evi-dence from Dr. Zuhua He's laboratory revealed that CURVEDCHIMERIC PALEA 1 (CCP1), the Arabidopsis EMBRYONIC FLOWER1(EMF1)-like protein in rice, functions in palea developmentthrough mediating the deposition of H3K27me3 on the chromatinof OsMADS58 (Yan et al., 2015). Liu et al. (2015) reported thatSDG711-mediated H3K27me3 deposition and JMJ703-mediateddemethylation of H3K4me3 have agonistic functions in theregulation of rice IM development. Different from Arabidopsis inwhich H3K27me3 and DNA methylation are generally mutuallyexclusive, Zhou et al. (2016) reported that SDG711-mediatedH3K27me3 mark cooperates with DRM2-mediated non-CG DNAmethylation to regulate the expression of developmental genesthrough direct interaction between SDG711 and DRM2 in rice(Zhou et al., 2016). Knockout of OsDRM2 disrupts the binding ofSDG711 to target genes and leads to loss of H3K27me3, suggestinga different functioning mode of H3K27me3 in rice. In antherdevelopment, Cao et al. (2015) reported that H2B mono-ubiquitination (H2Bub1) is involved in late anther development inrice. O. sativa HISTONE MONOUBIQUITINATION1 (OsHUB1) andOsHUB2-mediated H2Bub1 acts together with H3K4me2 in thechromatins of tapetum degradation-related genes, therebymodulating the transcriptional regulation of anther developmentin rice.

Before the reproductive phase, plants first transit from a juvenilevegetative phase of development to an adult vegetative phase ofdevelopment, and miR156 plays crucial roles in this process. Arecent study demonstrated that the expression of miR156 is regu-lated by a SWI2/SNF2 chromatin remodeling ATPase BRAHMA(BRM) (Li et al., 2015a), suggesting an important involvement ofATPase-based chromatin remodeling in floral transition.

In phytohormone-mediated plant growth and development, Suiet al. (2012) reported that the H3K36 methyltransferase SDG725modulates the expression of brassinosteroid (BR)-related genes,including DWARF11 (D11), BRASSINOSTEROID INSENSITIVE 1 (BRI1)and BRASSINOSTEROID UPREGULATED 1 (BU1), through mediatingthe deposition of H3K36me2/3 on these genes. Li et al. (2018) re-ported that OsINO80, a conserved ATP-dependent chromatin-remodeling factor in rice, functions in the regulation of GAbiosynthesis.

Recent studies also indicated that histone modifications areinvolved in the modulation of seed gene expression. Interest-ingly, although PcG complex and TrxG factors function antago-nistically in flowering, a recent study reported that the PcG

complex protein EMF1 and the TrxG factors ATX1 and ULTRA-PETALA1 (ULT1) are able to bind the chromatin of seed genes,and ULT1 physically interacts with EMF1 and ATX1, suggestingthat they function together to modulate the expression of seedgenes (Xu et al., 2018). In the process of plant germ-line speci-fication, Zhao et al. (2018) reported that histone variant H2A.Zdeposition mediated by SWR1 chromatin remodeling complex isrequired for the expression of WRKY28 which functions throughrepressing hypodermal somatic cells from acquiring megasporemother cell-like cell identify.

In PRC complex-mediated gene suppression, although it isknown that PRC1-mediated H2Aub1 is a key epigenetic mark inPolycomb silencing, how H2Aub1 is read to direct downstreamfunctions remains unclear. The human ZUOTIN-RELATED FACTOR 1(ZRF1) has been shown to bind H2Aub1 via UBIQUITIN-BINDINGDOMAIN (UBD) and favor H2Aub1 deubiquitination, leading tothe switch from repressive to active chromatin state. Dr. Wen-HuiShen's laboratory revealed that AtZRF1a and AtZRF1b, the Arabi-dopsis homologs of animal ZRF1, participate in multiple develop-mental processes, including seed germination, plant growth, floraldevelopment and embryogenesis (Feng et al., 2016). They furtherproved that the developmental regulation is achieved by AtZRF1a/b-mediated H2Aub1 and H3K27me3 deposition in gene suppres-sion, suggesting that AtZRF1a/b may serve as a reader of H2Aub1 indevelopmental regulation.

Besides DNA methylation, histone modifications and chromatinremodeling, recent studies revealed that some lncRNAs also playimportant roles in plant development. Systematic analysis oflncRNAs in Arabidopsis and rice has been conducted in Dr. Xing-Wang Deng's laboratory (Liu et al., 2013; Wang et al., 2014c). Oneof regulatory mechanisms of lncRNAs is to serve as target mimicryof endogenous miRNAs (Wu et al., 2013a). Zhang et al. (2014b) re-ported that some rice lncRNAs serve as competing RNAs tosequester endogenous miRNAs. One lncRNA, XLOC_057324, hasbeen shown to be involved in panicle development (Zhang et al.,2014b). Wang et al. from Dr. Xing-Wang Deng's group revealedthat an Arabidopsis lncRNA, HIDDEN TREASURE 1 (HID1), promotesphotomorphogenesis in continuous red light by interacting withthe transcription factor PIF3 (Wang et al., 2014b). These resultssuggest that lncRNAs are an important aspect of plantdevelopment.

7. Epigenetic regulation of plant stress responses

7.1. Epigenetic regulation in abiotic stress responses

Epigenetic regulation of plant responses to environmentalstresses has been a fascinated research partially due to the conceptof stress memory. In some cases, the transcriptional regulation ofstress response genes is associated with DNA methylation withgeneral or locus-specific manner. Recent studies revealed impor-tant involvements of DNA methylation in high temperature (HT)stress in cotton (Gossypium hirsutum) and Brassica plants (Li et al.,2016a; Liu et al., 2017c; Ma et al., 2018). Ma et al. (2018) foundthat DNA methylation levels, especially 24-nt siRNA-dependentCHH methylation, were significantly reduced under HT stress inHT-sensitive cotton line compared to normal temperature (NT)condition, and experimental removal of DNA methylation led topollen sterility in HT-sensitive line under NT condition. Theyfurther proved that the suppression of DNA methylation affectedthe expression of sugar and reactive oxygen species (ROS) pathwaygenes. Their work revealed a critical role of RdDM pathway in HTstress. During salt stress response, Wang et al. (2014a) demon-strated that induced DNA methylation changes occur in somesalinity-responsive genes in a salinity-tolerant wheat introgression


line. Similarly, Xu et al. (2015) revealed that salt-induced tran-scription factor MYB74 is regulated by RdDM pathway in Arabi-dopsis. These findings suggest that a dynamic regulation of DNAmethylation is present in plant abiotic stress responses.

In plant stress responses, activation or repression of abioticstress-responsive genes is often associated with multiple epige-netic changes. Besides DNA methylation, emerging evidence sug-gests that histone modifications are extensively involved in stress-responsive gene expression and gene priming in plants. Histonemodifier genes are differentially expressed upon exposure toabiotic stresses. For example, ATX1, the main H3K4 methyl-transferase in Arabidopsis, is involved in ABA-dependent and -in-dependent dehydration stress signaling pathways (Ding et al.,2011). Binding of ATX1 to NINE-CIS-EPOXYCAROTENOID DIOXYGE-NASE 3 (NCED3), which encodes a key enzyme functioning in theABA biosynthesis, is increased by dehydration stress, therebyincreasing NCED3 transcription (Ding et al., 2011). Similarly, arecent study reported that ATX4 and ATX5, the other two H3K4methyltransferases in Arabidopsis, function partially redundantly tomodulate plant response to dehydration stress (Liu et al., 2018b).Loss-of-function single and double mutants of ATX4 and ATX5display drought stress-tolerant and ABA-hypersensitive pheno-types. Among the differentially expressed dehydration-responsivegenes caused by ATX4/ATX5 mutations, ABA-HYPERSENSITIVEGERMINATION 3 (AHG3), which encodes a negative regulator of ABAsignaling, is directly bound by ATX4 and ATX5 for H3K4 methyl-ation, and this binding is dramatically increased upon ABA treat-ment, suggesting a direct role of H3K4 methylation in dehydrationstress and ABA response. H3K4me3 demethylase JMJ15 is tissue-specifically expressed in Arabidopsis and its loss-of-functionmutant displays more sensitive phenotype to salt stress (Shenet al., 2014). Ectopic expression of JMJ15 leads to mis-regulationof H3K4me2/3-dependent stress-responsive genes. In rice seed-lings, thousands of genes are differentially H3K4me3 modifiedunder drought stress (Zong et al., 2013).

Histone acetylation as an active histonemark also participates inabiotic stress responses. It has been shown that HDA6- and HD2C-mediated histone deacetylations are involved in ABA and salt stressresponses (Chen et al., 2010; Luo et al., 2012). In maize, histonedeacetylase genes are induced by cold treatment (Hu et al., 2011). Inrice, histone acetyltransferase genes are differently expressed uponexposure to different abiotic stress treatments, including ABA, saltand cold stresses (Liu et al., 2012b). Recent studies revealed aninvolvement of ATP-dependent chromatin remodeling mechanismin abiotic stress responses. Han et al. (2012) reported that the SWI2/SNF2 chromatin remodeling ATPase BRM regulates stress responsesthrough nucleosome stability of ABSCISIC ACID-INSENSITIVE5 (ABI5).In maize, the chromatin remodeler ZmCHB101 functions in osmoticstress response (Yu et al., 2018).

7.2. Epigenetic regulation in plant immunity

In plants, perception of pathogens leads to the activation ofmultiple layers of defense responses which are accompanied withextensive transcriptional reprogramming of defense-responsivegenes. Considering the advantages of rapid, reversible, eventransgenerational changes in gene expression, epigenetic mecha-nisms are very suitable for modulating plant defense responses.However, these mechanisms have only recently attracted moreattentions in plant defense immunity.

The important involvements of DNA methylation in biotic stressresponses were revealed by several recent observations that dys-functions of DNA methyltransferases and demethylases lead todifferent susceptibilities to certain pathogens, including bacterialpathogens (Dowen et al., 2012; Yu et al., 2013) and fungal pathogen

Fusarium oxysporum (Le et al., 2014). In plants, expression ofresistance (R) genes must be tightly controlled to balance plantgrowth and disease resistance. More recently, Dr. Zuhua He's groupidentified a Pigm locus in rice which can confer durable resistanceto the fungus Magnaporthe oryzae without yield penalty (Denget al., 2017). In this locus, PigmR confers broad-spectrum resis-tance, whereas PigmS represses resistance by competitively atten-uating PigmR homodimerization. Two tandem miniaturetransposons (MITEs) are present in the promoter region of PigmS.These two MITEs are targeted by 24-nt siRNA-mediated RdDMpathway and the expression of PigmS is regulated by DNAmethylation level in its promoter region. Silencing of RdDMpathway genes leads to increased PigmS expression. This findingstrongly suggests that DNA methylation mechanism can modulateplant immunity by affecting the expression of innate immunityreceptor.

Besides DNA methylation, recent studies demonstrated a closelink between the transcriptional levels of defense genes and his-tone modifications. Among diverse histone modifications, histoneacetylation, which is dynamically regulated by histone acetyl-transferases and deacetylases, is well-studied in plant immunity(Zhou et al., 2005; Zhu et al., 2011; Ding et al., 2012). Zhou et al.(2005) reported the important involvement of a histone deacety-lase, HDA19, in the transcriptional regulation of genes in jasmonicacid (JA) and ethylene (ET) signaling defense pathways in Arabi-dopsis. In this case, the expression of HDA19 is induced by pathogenAlternaria brassicicola and overexpression of HDA19 results indecreased histone acetylation levels as well as increased resistanceto A. brassicicola. Moreover, HDA19 has also been shown to interactwith two type III WRKY transcription factors, WRKY38 andWRKY62, to repress their transcription in basal defense responses(Kim et al., 2008). Similarly, histone deacetylase HDA6 serves as acorepressor of JASMONATE ZIM-DOMAIN (JAZ) proteins to repressETHYLENE INSENSITIVE 3 (EIN3)/EIN3-LIKE 1 (EIL1)-dependenttranscription, thereby inhibiting JA signaling defense pathway (Zhuet al., 2011). In addition, HDA6 also interacts with an F-box proteinCOI1 to modulate JA signaling defense (Devoto et al., 2002). In rice,evidence from Dr. Guo-Liang Wang's laboratory revealed thatHDT701, a histone deacetylase, negatively regulates plant innateimmunity through modulating H4 acetylation of defense-responsive genes (Ding et al., 2012). In this case, HDT701 directlybinds to defense-related genes. Silencing of HDT701 leads toincreased levels of H4 acetylation, elevated transcription of patternrecognition receptor (PRR) and defense-related genes, as well asenhanced resistance to both M. oryzae and Xanthomonas oryzae pv.oryzae (Xoo). For histone methylation, ATXR7, a H3K4 methyl-transferase, associates with MODIFIER OF SNC1, 9 (MOS9) toregulate the transcriptional expression of R genes RECOGNITION OFPERONOSPORA PARASITICA 4 (RPP4) and SUPPRESSOR OF NPR1-1,CONSTITUTIVE 1 (SNC1), thereby modulating the resistance tofungal pathogen Hyaloperonospora arabidopsidis Emwa1 (Xia et al.,2013). Dr. Dao-Xiu Zhou's laboratory proved that the histonedemethylase JMJ705 is involved in the methyl JA-induced removalof H3K27me3 and gene activation (Li et al., 2013).

8. Perspective

In this review, we summarize the advances in the field of plantepigenetics in China over the past several decades. We focus ourreview on the publications contributed by Chinese researchers andgroups. Epigenetics, as the hotspot in the field of transcriptionalregulation, has been developing rapidly over the past few decades.Benefiting from the growing funding and the importance of agri-cultural sciences, great achievements have beenmade in the field ofplant epigenetics in China and some leading studies have been


emerging. With the constant discovery of novel epigenetic mech-anisms and the elucidation of more and more crop genomes,epigenetic studies will undoubtedly continue to be a major focus ofstudy across biological disciplines. However, compared to theincreasing research publications, the fundamental original discov-eries and revolutionary theoretical innovation to biological sciencewhich is beyond plant epigenetics are still lacking in China. Onepossible reason is that Chinese research foundation in life scienceand genetics is very weak compared to western developed coun-tries. Therefore, sustained scientific funding input is essential forChina to catch up with the developed countries.

In plants, the majority of epigenetic phenomena are reported inthe model plant Arabidopsis. Given the huge difference in genomecomplexity between Arabidopsis and crop plants, the epigeneticmechanisms may be quite different and diverse in crop plants. Theimportance of epigenetic regulation in diverse biological processesmay be only observed in crops. For example, dynamic DNAmethylation regulation is required for fruit ripening and the for-mation of flavor in tomato (Zhang et al., 2016a; Lang et al., 2017).Therefore, it is very necessary to conduct epigenetic studies in cropplants, such as the epigenetic regulation mechanisms in the for-mation of agronomic traits. Moreover, novel epigenetic mecha-nisms may be observed in crop plants given that the larger genomesize.

In addition to keep the sustainable development of basicresearch, promoting the application of epigenetic regulatorymechanisms in crop production practice is another important issue.Recent studies revealed that both genetic and epigenetic compo-nents contribute to the heterosis. Nature epigenetic variations(epialleles) can cause significant heritable variations. Evidencefrom Dr. Xing-Wang Deng's and Dr. Jian-Kang Zhu's laboratoriesrevealed that dramatic epigenetic variations as well as differentialgene expression are observed in the hybrids of different plants(Shen et al., 2012; He et al., 2013; Yang et al., 2016b; Zhang et al.,2016b). These epigenetic variations may be DNA methylation, his-tone modifications or small RNAs. For example, Shen et al. (2012)reported that DNA methylation in all cytosine contexts isincreased in both reciprocal hybrids, and changes in DNA methyl-ation are correlated with altered expression of a subset of genes.These findings make it possible to propagate naturally occurringepialleles which cause heritable superiority in phenotypic traits.However, how the heterosis is established through epigeneticmechanisms remains largely elusive. In the near future, a completeunderstanding of the molecular mechanisms of epigeneticcomponent-dependent heterosis is needed.

Epigenetic mechanisms are involved in both the perception ofpathogens and the repression of robust basal defense. However,compared to the extensively investigation of epigenetic regulationin mammalian disease (e.g., cancer), a deep understanding aboutthe roles of epigenetic mechanisms in the modulation of plantimmunity is still lacking. Only limited plant target genes have beenidentified so far. On the other hand, from the perspective of path-ogens, how epigenetic mechanisms function in pathogenicitydetermination is unclear. China is rich in the resource of plantpathogens. Plant responses to different kinds of pathogens may bequite diverse. In the future, more efforts should be given to inves-tigate how multiple epigenetic mechanisms coordinate in plantimmunity and its interaction with different pathogens.

Acknowledgments

The authors apologize to our colleagues whose work is not citeddue to the space constraints. Work in Cheng-Guo Duan's laboratoryis supported by the Strategic Priority Research Program of theChinese Academy of Sciences (XDB27040203) and the National

Natural Science Foundation of China (No. 31770155).

References

Arribas-Hernandez, L., Bressendorff, S., Hansen, M.H., Poulsen, C., Erdmann, S.,Brodersen, P., 2018. An m(6)A-YTH module controls developmental timing andmorphogenesis in Arabidopsis. Plant Cell 30, 952e967.

Barrero, J.M., Gonzalez-Bayon, R., del Pozo, J.C., Ponce, M.R., Micol, J.L., 2007.INCURVATA2 encodes the catalytic subunit of DNA polymerase alpha and in-teracts with genes involved in chromatin-mediated cellular memory in Arabi-dopsis thaliana. Plant Cell 19, 2822e2838.

Bergman, Y., Cedar, H., 2013. DNA methylation dynamics in health and disease. Nat.Struct. Mol. Biol. 20, 274e281.

Bu, Z., Yu, Y., Li, Z., Liu, Y., Jiang, W., Huang, Y., Dong, A.W., 2014. Regulation ofArabidopsis flowering by the histone mark readers MRG1/2 via interaction withCONSTANS to modulate FT expression. PLoS Genet. 10, e1004617.

Cao, H., Li, X., Wang, Z., Ding, M., Sun, Y., Dong, F., Chen, F., Liu, L., Doughty, J., Li, Y.,Liu, Y.X., 2015. Histone H2B monoubiquitination mediated by HISTONE MON-OUBIQUITINATION1 and HISTONE MONOUBIQUITINATION2 is involved inanther development by regulating tapetum degradation-related genes in rice.Plant Physiol. 168, 1389e1405.

Cao, X., Aufsatz, W., Zilberman, D., Mette, M.F., Huang, M.S., Matzke, M.,Jacobsen, S.E., 2003. Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr. Biol. 13, 2212e2217.

Cao, X., Jacobsen, S.E., 2002. Locus-specific control of asymmetric and CpNpGmethylation by the DRM and CMT3 methyltransferase genes. Proc. Natl. Acad.Sci. U. S. A. 99 (Suppl. 4), 16491e16498.

Cao, X., Springer, N.M., Muszynski, M.G., Phillips, R.L., Kaeppler, S., Jacobsen, S.E.,2000. Conserved plant genes with similarity to mammalian de novo DNAmethyltransferases. Proc. Natl. Acad. Sci. U. S. A. 97, 4979e4984.

Cartagena, J.A., Matsunaga, S., Seki, M., Kurihara, D., Yokoyama, M., Shinozaki, K.,Fujimoto, S., Azumi, Y., Uchiyama, S., Fukui, K., 2008. The Arabidopsis SDG4contributes to the regulation of pollen tube growth by methylation of histoneH3 lysines 4 and 36 in mature pollen. Dev. Biol. 315, 355e368.

Chanvivattana, Y., Bishopp, A., Schubert, D., Stock, C., Moon, Y.H., Sung, Z.R.,Goodrich, J., 2004. Interaction of Polycomb-group proteins controlling flower-ing in Arabidopsis. Development 131, 5263e5276.

Chen, L.Q., Luo, J.H., Cui, Z.H., Xue, M., Wang, L., Zhang, X.Y., Pawlowski, W.P., He, Y.,2017. ATX3, ATX4, and ATX5 encode putative H3K4 methyltransferases and arecritical for plant development. Plant Physiol. 174, 1795e1806.

Chen, L.T., Luo, M., Wang, Y.Y., Wu, K., 2010. Involvement of Arabidopsis histonedeacetylase HDA6 in ABA and salt stress response. J. Exp. Bot. 61, 3345e3353.

Cheng, S., Tan, F., Lu, Y., Liu, X., Li, T., Yuan, W., Zhao, Y., Zhou, D.X., 2018. WOX11recruits a histone H3K27me3 demethylase to promote gene expression duringshoot development in rice. Nucleic Acids Res. 46, 2356e2369.

Choi, K., Park, C., Lee, J., Oh, M., Noh, B., Lee, I., 2007. Arabidopsis homologs ofcomponents of the SWR1 complex regulate flowering and plant development.Development 134, 1931e1941.

Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J.J., Goldberg, R.B.,Jacobsen, S.E., Fischer, R.L., 2002. DEMETER, a DNA glycosylase domain protein,is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell110, 33e42.

Coustham, V., Vlad, D., Deremetz, A., Gy, I., Cubillos, F.A., Kerdaffrec, E., Loudet, O.,Bouche, N., 2014. SHOOT GROWTH1 maintains Arabidopsis epigenomes byregulating IBM1. PLoS One 9, e84687.

Cui, X., Jin, P., Cui, X., Gu, L., Lu, Z., Xue, Y., Wei, L., Qi, J., Song, X., Luo, M., An, G.,Cao, X.F., 2013. Control of transposon activity by a histone H3K4 demethylase inrice. Proc. Natl. Acad. Sci. U. S. A. 110, 1953e1958.

Cui, X., Liang, Z., Shen, L., Zhang, Q., Bao, S., Geng, Y., Zhang, B., Leo, V., Vardy, L.A.,Lu, T., Gu, X., Yu, H., 2017. 5-Methylcytosine RNA methylation in Arabidopsisthaliana. Mol. Plant 10, 1387e1399.

Daccord, N., Celton, J.M., Linsmith, G., Becker, C., Choisne, N., Schijlen, E., van deGeest, H., Bianco, L., Micheletti, D., Velasco, R., Di Pierro, E.A., Gouzy, J.,Rees, D.J.G., Guerif, P., Muranty, H., Durel, C.E., Laurens, F., Lespinasse, Y.,Gaillard, S., Aubourg, S., Quesneville, H., Weigel, D., van de Weg, E., Troggio, M.,Bucher, E., 2017. High-quality de novo assembly of the apple genome andmethylome dynamics of early fruit development. Nat. Cenet. 49, 1099e1106.

Deleris, A., Halter, T., Navarro, L., 2016. DNA methylation and demethylation in plantimmunity. Annu. Rev. Phytopathol. 54, 579e603.

Deng, Y., Zhai, K., Xie, Z., Yang, D., Zhu, X., Liu, J., Wang, X., Qin, P., Yang, Y., Zhang, G.,Li, Q., Zhang, J., Wu, S., Milazzo, J., Mao, B., Wang, E., Xie, H., Tharreau, D., He, Z.,2017. Epigenetic regulation of antagonistic receptors confers rice blast resis-tance with yield balance. Science 355, 962e965.

Devoto, A., Nieto-Rostro, M., Xie, D., Ellis, C., Harmston, R., Patrick, E., Davis, J.,Sherratt, L., Coleman, M., Turner, J.G., 2002. COI1 links jasmonate signalling andfertility to the SCF ubiquitin-ligase complex in Arabidopsis. Plant J. 32, 457e466.

Ding, B., Bellizzi Mdel, R., Ning, Y., Meyers, B.C., Wang, G.L., 2012. HDT701, a histoneH4 deacetylase, negatively regulates plant innate immunity by modulatinghistone H4 acetylation of defense-related genes in rice. Plant Cell 24,3783e3794.

Ding, Y., Avramova, Z., Fromm, M., 2011. The Arabidopsis trithorax-like factor ATX1functions in dehydration stress responses via ABA-dependent and ABA-independent pathways. Plant J. 66, 735e744.

Ding, Y., Wang, X., Su, L., Zhai, J., Cao, S., Zhang, D., Liu, C., Bi, Y., Qian, Q., Cheng, Z.,

http://refhub.elsevier.com/S1673-8527(18)30188-7/sref1







































































































Chu, C.C., Cao, X.F., 2007. SDG714, a histone H3K9 methyltransferase, is involvedin Tos17 DNA methylation and transposition in rice. Plant Cell 19, 9e22.

Dong, X., Chen, J., Li, T., Li, E., Zhang, X., Zhang, M., Song, W., Zhao, H., Lai, J., 2018.Parent-of-origin-dependent nucleosome organization correlates with genomicimprinting in maize. Genome Res. 28, 1020e1028.

Dong, X., Zhang, M., Chen, J., Peng, L., Zhang, N., Wang, X., Lai, J., 2017. Dynamic andantagonistic allele-specific epigenetic modifications controlling the expressionof imprinted genes in maize endosperm. Mol. Plant 10, 442e455.

Dou, K., Huang, C.F., Ma, Z.Y., Zhang, C.J., Zhou, J.X., Huang, H.W., Cai, T., Tang, K.,Zhu, J.K., He, X.J., 2013. The PRP6-like splicing factor STA1 is involved in RNA-directed DNA methylation by facilitating the production of Pol V-dependentscaffold RNAs. Nucleic Acids Res. 41, 8489e8502.

Dowen, R.H., Pelizzola, M., Schmitz, R.J., Lister, R., Dowen, J.M., Nery, J.R., Dixon, J.E.,Ecker, J.R., 2012. Widespread dynamic DNA methylation in response to bioticstress. Proc. Natl. Acad. Sci. U. S. A. 109, E2183eE2191.

Du, J., Zhong, X., Bernatavichute, Y.V., Stroud, H., Feng, S., Caro, E., Vashisht, A.A.,Terragni, J., Chin, H.G., Tu, A., Hetzel, J., Wohlschlegel, J.A., Pradhan, S., Patel, D.J.,Jacobsen, S.E., 2012. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151, 167e180.

Duan, C.G., Wang, X., Tang, K., Zhang, H., Mangrauthia, S.K., Lei, M., Hsu, C.C.,Hou, Y.J., Wang, C., Li, Y., Tao, W.A., Zhu, J.K., 2015a. MET18 connects the cyto-solic iron-sulfur cluster assembly pathway to active DNA demethylation inArabidopsis. PLoS Genet. 11, e1005559.

Duan, C.G., Wang, X., Xie, S., Pan, L., Miki, D., Tang, K., Hsu, C.C., Lei, M., Zhong, Y.,Hou, Y.J., Wang, Z., Zhang, Z., Mangrauthia, S.K., Zhang, H., Dilkes, B., Tao, W.A.,Zhu, J.K., 2017a. A pair of transposon-derived proteins function in a histoneacetyltransferase complex for active DNA demethylation. Cell Res. 27, 226e240.

Duan, C.G., Wang, X., Zhang, L., Xiong, X., Zhang, Z., Tang, K., Pan, L., Hsu, C.C., Xu, H.,Tao, W.A., Zhang, H., Zhu, J.K., 2017b. A protein complex regulates RNA pro-cessing of intronic heterochromatin-containing genes in Arabidopsis. Proc. Natl.Acad. Sci. U. S. A. 114, E7377eE7384.

Duan, C.G., Zhang, H., Tang, K., Zhu, X., Qian, W., Hou, Y.J., Wang, B., Lang, Z., Zhao, Y.,Wang, X., Wang, P., Zhou, j., Liang, G., Liu, N., Wang, C., Zhu, J.K., 2015b. Specificbut interdependent functions for Arabidopsis AGO4 and AGO6 in RNA-directedDNA methylation. EMBO J. 34, 581e592.

Duan, H.C., Wei, L.H., Zhang, C., Wang, Y., Chen, L., Lu, Z., Chen, P.R., He, C., Jia, G.,2017c. ALKBH10B is an RNA N(6)-methyladenosine demethylase affecting Ara-bidopsis floral transition. Plant Cell 29, 2995e3011.

Dutta, A., Choudhary, P., Caruana, J., Raina, R., 2017. JMJ27, an Arabidopsis H3K9histone demethylase, modulates defense against Pseudomonas syringae andflowering time. Plant J. 91, 1015e1028.

Ebbs, M.L., Bartee, L., Bender, J., 2005. H3 lysine 9 methylation is maintained on atranscribed inverted repeat by combined action of SUVH6 and SUVH4 meth-yltransferases. Mol. Cell. Biol. 25, 10507e10515.

Ebbs, M.L., Bender, J., 2006. Locus-specific control of DNA methylation by the Ara-bidopsis SUVH5 histone methyltransferase. Plant Cell 18, 1166e1176.

Eulgem, T., Tsuchiya, T., Wang, X.J., Beasley, B., Cuzick, A., Tor, M., Zhu, T.,McDowell, J.M., Holub, E., Dangl, J.L., 2007. EDM2 is required for RPP7-depen-dent disease resistance in Arabidopsis and affects RPP7 transcript levels. Plant J.49, 829e839.

Exner, V., Aichinger, E., Shu, H., Wildhaber, T., Alfarano, P., Caflisch, A., Gruissem, W.,Kohler, C., Hennig, L., 2009. The chromodomain of LIKE HETEROCHROMATINPROTEIN 1 is essential for H3K27me3 binding and function during Arabidopsisdevelopment. PLoS One 4, e5335.

Feng, J., Chen, D., Berr, A., Shen, W.H., 2016. ZRF1 chromatin regulators have Poly-comb silencing and independent roles in development. Plant Physiol. 172,1746e1759.

Fu, Y., Dominissini, D., Rechavi, G., He, C., 2014. Gene expression regulation medi-ated through reversible m(6)A RNA methylation. Nat. Rev. Genet. 15, 293e306.

Fuchs, J., Demidov, D., Houben, A., Schubert, I., 2006. Chromosomal histone modi-fication patterns-from conservation to diversity. Trends Plant Sci. 11, 199e208.

Gao, L., Geng, Y., Li, B., Chen, J., Yang, J., 2010a. Genome-wide DNA methylationalterations of Alternanthera philoxeroides in natural and manipulated habitats:implications for epigenetic regulation of rapid responses to environmentalfluctuation and phenotypic variation. Plant Cell Environ. 33, 1820e1827.

Gao, Z., Liu, H.L., Daxinger, L., Pontes, O., He, X., Qian, W., Lin, H., Xie, M.,Lorkovic, Z.J., Zhang, S., Miki, D., Zhan, X., Pontier, D., Lagrange, T., Jin, H.,Matzke, A.J., Pikaard, C.S., Zhu, J.K., 2010b. An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465, 106e109.

Gehring, M., Choi, Y., Fischer, R.L., 2004. Imprinting and seed development. PlantCell 16 (Suppl. l), S203eS213.

Gehring, M., Huh, J.H., Hsieh, T.F., Penterman, J., Choi, Y., Harada, J.J., Goldberg, R.B.,Fischer, R.L., 2006. DEMETER DNA glycosylase establishes MEDEA polycombgene self-imprinting by allele-specific demethylation. Cell 124, 495e506.

Gong, Z., Morales-Ruiz, T., Ariza, R.R., Roldan-Arjona, T., David, L., Zhu, J.K., 2002.ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNAglycosylase/lyase. Cell 111, 803e814.

Grossniklaus, U., Vielle-Calzada, J.P., Hoeppner, M.A., Gagliano, W.B., 1998. Maternalcontrol of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis.Science 280, 446e450.

Gu, X., Wang, Y., He, Y., 2013. Photoperiodic regulation of flowering time throughperiodic histone deacetylation of the florigen gene FT. PLoS Biol. 11, e1001649.

Guo, L., Yu, Y., Law, J.A., Zhang, X., 2010. SET DOMAIN GROUP2 is the major histoneH3 lysine 4 trimethyltransferase in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 107,18557e18562.

Han, S.K., Sang, Y., Rodrigues, A., Biol, F., Wu, M.F., Rodriguez, P.L., Wagner, D., 2012.The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acidresponses in the absence of the stress stimulus in Arabidopsis. Plant Cell 24,4892e4906.

He, F., Umehara, T., Saito, K., Harada, T., Watanabe, S., Yabuki, T., Kigawa, T.,Takahashi, M., Kuwasako, K., Tsuda, K., Matsuda, T., Aoki, M., Seki, E.,Kobayashi, N., Guntert, P., Yokoyama, S., Muto, Y., 2010. Structural insight intothe zinc finger CW domain as a histone modification reader. Structure 18,1127e1139.

He, G., Chen, B., Wang, X., Li, X., Li, J., He, H., Yang, M., Lu, L., Qi, Y., Wang, X.,Deng, X.W., 2013. Conservation and divergence of transcriptomic and epi-genomic variation in maize hybrids. Genome Biol. 14, R57.

He, G., Elling, A.A., Deng, X.W., 2011. The epigenome and plant development. Annu.Rev. Plant Biol. 62, 411e435.

He, X.J., Hsu, Y.F., Pontes, O., Zhu, J., Lu, J., Bressan, R.A., Pikaard, C., Wang, C.S.,Zhu, J.K., 2009a. NRPD4, a protein related to the RPB4 subunit of RNA poly-merase II, is a component of RNA polymerases IV and V and is required for RNA-directed DNA methylation. Genes Dev. 23, 318e330.

He, X.J., Hsu, Y.F., Zhu, S., Liu, H.L., Pontes, O., Zhu, J., Cui, X., Wang, C.S., Zhu, J.K.,2009b. A conserved transcriptional regulator is required for RNA-directed DNAmethylation and plant development. Genes Dev. 23, 2717e2722.

He, X.J., Hsu, Y.F., Zhu, S., Wierzbicki, A.T., Pontes, O., Pikaard, C.S., Liu, H.L.,Wang, C.S., Jin, H., Zhu, J.K., 2009c. An effector of RNA-directed DNA methyl-ation in Arabidopsis is an ARGONAUTE 4- and RNA-binding protein. Cell 137,498e508.

He, Y., 2012. Chromatin regulation of flowering. Trends Plant Sci. 17, 556e562.He, Y., 2015. Enabling photoperiodic control of flowering by timely chromatin

silencing of the florigen gene. Nucleus 6, 179e182.Hoppmann, V., Thorstensen, T., Kristiansen, P.E., Veiseth, S.V., Rahman, M.A.,

Finne, K., Aalen, R.B., Aasland, R., 2011. The CW domain, a new histone recog-nition module in chromatin proteins. EMBO J. 30, 1939e1952.

Hou, X., Zhou, J., Liu, C., Liu, L., Shen, L., Yu, H., 2014. Nuclear factor Y-mediatedH3K27me3 demethylation of the SOC1 locus orchestrates flowering responsesof Arabidopsis. Nat. Commun. 5, 4601.

Hu, Y., Liu, D., Zhong, X., Zhang, C., Zhang, Q., Zhou, D.X., 2012. CHD3 protein rec-ognizes and regulates methylated histone H3 lysines 4 and 27 over a subset oftargets in the rice genome. Proc. Natl. Acad. Sci. U. S. A. 109, 5773e5778.

Hu, Y., Zhang, L., Zhao, L., Li, J., He, S., Zhou, K., Yang, F., Huang, M., Jiang, L., Li, L.,2011. Trichostatin A selectively suppresses the cold-induced transcription of theZmDREB1 gene in maize. PLoS One 6, e22132.

Huang, C.F., Miki, D., Tang, K., Zhou, H.R., Zheng, Z., Chen, W., Ma, Z.Y., Yang, L.,Zhang, H., Liu, R., He, X.J., Zhu, J.K., 2013. A pre-mRNA-splicing factor is requiredfor RNA-directed DNA methylation in Arabidopsis. PLoS Genet. 9, e1003779.

Huang, C.F., Zhu, J.K., 2014. RNA splicing factors and RNA-directed DNA methylation.Biology 3, 243e254.

Huang, S., Li, R., Zhang, Z., Li, L., Gu, X., Fan, W., Lucas, W.J., Wang, X., Xie, B., Ni, P.,Ren, Y., Zhu, H., Li, J., Lin, K., Jin, W., Fei, Z., Li, G., Staub, J., Kilian, A., van, der,Vossen, E.A., Wu, Y., Guo, J., He, J., Jia, Z., Ren, Y., Tian, G., Lu, Y., Ruan, J., Qian, W.,Wang, M., Huang, Q., Li, B., Xuan, Z., Cao, J., Asan, Wu, Z., Zhang, J., Cai, Q., Bai, Y.,Zhao, B., Han, Y., Li, Y., Li, X., Wang, S., Shi, Q., Liu, S., Cho, W.K., Kim, J.Y., Xu, Y.,Heller-Uszynska, K., Miao, H., Cheng, Z., Zhang, S., Wu, J., Yang, Y., Kang, H.,Li, M., Liang, H., Ren, X., Shi, Z., Wen, M., Jian, M., Yang, H., Zhang, G., Zhang, Y.,Qin, N., Li, Z., Yang, G., Yang, S., Bolund, L., Kristiansen, K., Zheng, H., Li, S.,Zhang, X., Yang, H., Wang, J., Sun, R., Zhang, B., Jiang, S., Wang, J., Du, Y., Li, S.,2009. The genome of the cucumber, Cucumis sativus L. Nat. Cenet. 41,1275e1281.

Jackson, J.P., Lindroth, A.M., Cao, X., Jacobsen, S.E., 2002. Control of CpNpG DNAmethylation by the KRYPTONITE histone H3 methyltransferase. Nature 416,556e560.

Jacob, Y., Feng, S., LeBlanc, C.A., Bernatavichute, Y.V., Stroud, H., Cokus, S.,Johnson, L.M., Pellegrini, M., Jacobsen, S.E., Michaels, S.D., 2009. ATXR5 andATXR6 are H3K27 monomethyltransferases required for chromatin structureand gene silencing. Nat. Struct. Mol. Biol. 16, 763e768.

Jia, J., Zhao, S., Kong, X., Li, Y., Zhao, G., He, W., Appels, R., Pfeifer, M., Tao, Y.,Zhang, X., JING, r., Zhang, C., Ma, Y., Gao, L., Gao, C., Spannagl, M.L., Mayer, K.F.,Li, D., Pan, S., Zheng, F., Hu, Q., Xia, X., Li, J., Liang, Q., Chen, J., Wicker, T.,Gou, C.L., Kuang, H., He, G., Luo, Y., Keller, B., Xia, Q., Lu, P., Wang, J., Zou, H.,Zhang, R., Xu, J., Gao, J., Middleton, C., Quan, Z., Liu, G., Wang, J., InternationalWheat Genome Sequencing Consortium, Yang, H., Liu, X., He, Z., Mao, L.,Wang, J., 2013. Aegilops tauschii draft genome sequence reveals a gene reper-toire for wheat adaptation. Nature 496, 91e95.

Jiang, D., Gu, X., He, Y., 2009. Establishment of the winter-annual growth habit viaFRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis.Plant Cell 21, 1733e1746.

Jiang, D., Kong, N.C., Gu, X., Li, Z., He, Y., 2011. Arabidopsis COMPASS-like complexesmediate histone H3 lysine-4 trimethylation to control floral transition and plantdevelopment. PLoS Genet. 7, e1001330.

Jiang, D., Yang, W., He, Y., Amasino, R.M., 2007. Arabidopsis relatives of the humanlysine-specific Demethylase1 repress the expression of FWA and FLOWERINGLOCUS C and thus promote the floral transition. Plant Cell 19, 2975e2987.

Jiang, P., Wang, S., Jiang, H., Cheng, B., Wu, K., Ding, Y., 2018a. The COMPASS-likecomplex promotes flowering and panicle branching in rice. Plant Physiol. 176,2761e2771.

Jiang, P., Wang, S., Zheng, H., Li, H., Zhang, F., Su, Y., Xu, Z., Lin, H., Qian, Q., Ding, Y.,2018b. SIP1 participates in regulation of flowering time in rice by recruiting






















































































































































































































OsTrx1 to Ehd1. New Phytol. 219, 422e435.Jing, Y., Sun, H., Yuan, W., Wang, Y., Li, Q., Liu, Y., Li, Y., Qian, W., 2016. SUVH2 and

SUVH9 couple two essential steps for transcriptional gene silencing in Arabi-dopsis. Mol. Plant 9, 1156e1167.

Johnson, L., Cao, X., Jacobsen, S., 2002. Interplay between two epigenetic marks.DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12,1360e1367.

Johnson, L.M., Du, J., Hale, C.J., Bischof, S., Feng, S., Chodavarapu, R.K., Zhong, X.,Marson, G., Pellegrini, M., Segal, D.J., Patel, D.J., Jacobsen, S.E., 2014. SRA- andSET-domain-containing proteins link RNA polymerase V occupancy to DNAmethylation. Nature 507, 124e128.

Kankel, M.W., Ramsey, D.E., Stokes, T.L., Flowers, S.K., Haag, J.R., Jeddeloh, J.A.,Riddle, N.C., Verbsky, M.L., Richards, E.J., 2003. Arabidopsis MET1 cytosinemethyltransferase mutants. Genetics 163, 1109e1122.

Kanno, T., Bucher, E., Daxinger, L., Huettel, B., Kreil, D.P., Breinig, F., Lind, M.,Schmitt, M.J., Simon, S.A., Gurazada, S.G., Meyers, B.C., Lorkovic, Z.J., Matzke, A.J.,Matzke, M., 2010. RNA-directed DNA methylation and plant developmentrequire an IWR1-type transcription factor. EMBO Rep. 11, 65e71.

Kapoor, A., Agarwal, M., Andreucci, A., Zheng, X., Gong, Z., Hasegawa, P.M.,Bressan, R.A., Zhu, J.K., 2005. Mutations in a conserved replication proteinsuppress transcriptional gene silencing in a DNA-methylation-independentmanner in Arabidopsis. Curr. Biol. 15, 1912e1918.

Kim, D.H., Sung, S., 2014. Polycomb-mediated gene silencing in Arabidopsis thaliana.Mol. Cell 37, 841e850.

Kim, K.C., Lai, Z., Fan, B., Chen, Z., 2008. Arabidopsis WRKY38 and WRKY62 tran-scription factors interact with histone deacetylase 19 in basal defense. Plant Cell20, 2357e2371.

Kinoshita, T., Miura, A., Choi, Y., Kinoshita, Y., Cao, X., Jacobsen, S.E., Fischer, R.L.,Kakutani, T., 2004. One-way control of FWA imprinting in Arabidopsis endo-sperm by DNA methylation. Science 303, 521e523.

Klose, R.J., Zhang, Y., 2007. Regulation of histone methylation by demethyliminationand demethylation. Nat. Rev. Mol. Cell Biol. 8, 307e318.

Klutstein, M., Nejman, D., Greenfield, R., Cedar, H., 2016. DNA methylation in cancerand aging. Cancer Res. 76, 3446e3450.

Lai, Y.S., Zhang, X., Zhang, W., Shen, D., Wang, H., Xia, Y., Qiu, Y., Song, J., Wang, C.,Li, X., 2017. The association of changes in DNA methylation with temperature-dependent sex determination in cucumber. J. Exp. Bot. 68, 2899e2912.

Lang, Z., Lei, M., Wang, X., Tang, K., Miki, D., Zhang, H., Mangrauthia, S.K., Liu, W.,Nie, W., Ma, G., Yan, J., Duan, C.G., Hsu, C.C., Wang, C., Tao, W.A., Gong, Z.,Zhu, J.K., 2015. The methyl-CpG-binding protein MBD7 facilitates active DNAdemethylation to limit DNA hyper-methylation and transcriptional genesilencing. Mol. Cell 57, 971e983.

Lang, Z., Wang, Y., Tang, K., Tang, D., Datsenka, T., Cheng, J., Zhang, Y., Handa, A.K.,Zhu, J.K., 2017. Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. Proc.Natl. Acad. Sci. U. S. A. 114, E4511eE4519.

Law, J.A., Ausin, I., Johnson, L.M., Vashisht, A.A., Zhu, J.K., Wohlschlegel, J.A.,Jacobsen, S.E., 2010. A protein complex required for polymerase V transcriptsand RNA- directed DNA methylation in Arabidopsis. Curr. Biol. 20, 951e956.

Law, J.A., Du, J., Hale, C.J., Feng, S., Krajewski, K., Palanca, A.M., Strahl, B.D., Patel, D.J.,Jacobsen, S.E., 2013. Polymerase IV occupancy at RNA-directed DNA methyl-ation sites requires SHH1. Nature 498, 385e389.

Law, J.A., Jacobsen, S.E., 2010. Establishing, maintaining and modifying DNAmethylation patterns in plants and animals. Nat. Rev. Genet. 11, 204e220.

Law, J.A., Vashisht, A.A., Wohlschlegel, J.A., Jacobsen, S.E., 2011. SHH1, a homeo-domain protein required for DNA methylation, as well as RDR2, RDM4, andchromatin remodeling factors, associate with RNA polymerase IV. PLoS Genet. 7,e1002195.

Le, T.N., Schumann, U., Smith, N.A., Tiwari, S., Au, P.C., Zhu, Q.H., Taylor, J.M.,Kazan, K., Llewellyn, D.J., Zhang, R., Dennis, E.S., Wang, M.B., 2014. DNAdemethylases target promoter transposable elements to positively regulatestress responsive genes in Arabidopsis. Genome Biol. 15, 458.

Lee, W.Y., Lee, D., Chung, W.I., Kwon, C.S., 2009. Arabidopsis ING and Alfin1-likeprotein families localize to the nucleus and bind to H3K4me3/2 via planthomeodomain fingers. Plant J. 58, 511e524.

Lei, M., La, H., Lu, K., Wang, P., Miki, D., Ren, Z., Duan, C.G., Wang, X., Tang, K.,Zeng, L., Yang, L., Zhang, H., Nie, W., Liu, P., Zhou, J., Liu, R., Zhong, Y., Liu, D.,Zhu, J.K., 2014. Arabidopsis EDM2 promotes IBM1 distal polyadenylation andregulates genome DNA methylation patterns. Proc. Natl. Acad. Sci. U. S. A. 111,527e532.

Lei, M., Zhang, H., Julian, R., Tang, K., Xie, S., Zhu, J.K., 2015. Regulatory link betweenDNA methylation and active demethylation in Arabidopsis. Proc. Natl. Acad. Sci.U. S. A. 112, 3553e3557.

Li, C., Chen, C., Gao, L., Yang, S., Nguyen, V., Shi, X., Siminovitch, K., Kohalmi, S.E.,Huang, S., Wu, K., Chen, X., Cui, Y., 2015a. The Arabidopsis SWI2/SNF2 chromatinremodeler BRAHMA regulates polycomb function during vegetative develop-ment and directly activates the flowering repressor gene SVP. PLoS Genet. 11,e1004944.

Li, C., Liu, Y., Shen, W.H., Yu, Y., Dong, A., 2018. Chromatin-remodeling factorOsINO80 is involved in regulation of gibberellin biosynthesis and is crucial forrice plant growth and development. J. Integr. Plant Biol. 60, 144e159.

Li, H., He, Z., Lu, G., Lee, S.C., Alonso, J., Ecker, J.R., Luan, S., 2007. A WD40 domaincyclophilin interacts with histone H3 and functions in gene repression andorganogenesis in Arabidopsis. Plant Cell 19, 2403e2416.

Li, J., Huang, Q., Sun, M., Zhang, T., Li, H., Chen, B., Xu, K., Gao, G., Li, F., Yan, G.,

Qiao, J., Cai, Y., Wu, X., 2016a. Global DNA methylation variations after short-term heat shock treatment in cultured microspores of Brassica napus cv.Topas. Sci. Rep. 6, 38401.

Li, T., Chen, X., Zhong, X., Zhao, Y., Liu, X., Zhou, S., Cheng, S., Zhou, D.X., 2013.Jumonji C domain protein JMJ705-mediated removal of histone H3 lysine 27trimethylation is involved in defense-related gene activation in rice. Plant Cell25, 4725e4736.

Li, W., Liu, H., Cheng, Z.J., Su, Y.H., Han, H.N., Zhang, Y., Zhang, X.S., 2011. DNAmethylation and histone modifications regulate de novo shoot regeneration inArabidopsis by modulating WUSCHEL expression and auxin signaling. PLoSGenet. 7, e1002243.

Li, X., Qian, W., Zhao, Y., Wang, C., Shen, J., Zhu, J.K., Gong, Z., 2012. Antisilencing roleof the RNA-directed DNA methylation pathway and a histone acetyltransferasein Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 109, 11425e11430.

Li, X., Wang, X., He, K., Ma, Y., Su, N., He, H., Stolc, V., Tongprasit, W., Jin, W., Jiang, J.,Terzaghi, W., Li, S., Deng, X.W., 2008. High-resolution mapping of epigeneticmodifications of the rice genome uncovers interplay between DNA methylation,histone methylation, and gene expression. Plant Cell 20, 259e276.

Li, Y., Cordoba-Canero, D., Qian, W., Zhu, X., Tang, K., Zhang, H., Ariza, R.R., Roldan-Arjona, T., Zhu, J.K., 2015b. An AP endonuclease functions in active DNAdemethylation and gene imprinting in Arabidopsis [corrected]. PLoS Genet. 11,e1004905.

Li, Y., Duan, C.G., Zhu, X., Qian, W., Zhu, J.K., 2015c. A DNA ligase required for activeDNA demethylation and genomic imprinting in Arabidopsis. Cell Res. 25,757e760.

Li, Z., Jiang, D., Fu, X., Luo, X., Liu, R., He, Y., 2016b. Coupling of histone methylationand RNA processing by the nuclear mRNA cap-binding complex. Nat. Plants 2,16015.

Liang, Y.K., Wang, Y., Zhang, Y., Li, S.G., Lu, X.C., Li, H., Zou, C., Xu, Z.H., Bai, S.N., 2003.OsSET1, a novel SET-domain-containing gene from rice. J. Exp. Bot. 54,1995e1996.

Liang, Z., Shen, L., Cui, X., Bao, S., Geng, Y., Yu, G., Liang, F., Xie, S., Lu, T., Gu, X., Yu, H.,2018. DNA N(6)-adenine methylation in Arabidopsis thaliana. Dev. Cell 45,406e416 e403.

Ling, H.Q., Ma, B., Shi, X., Liu, H., Dong, L., Sun, H., Cao, Y., Gao, Q., Zheng, S., Li, Y.,Yu, Y., Du, H., Qi, M., Li, Y., Lu, H., Yu, H., Cui, Y., Wang, N., Chen, C., Wu, H.,Zhao, Y., Zhang, J., Li, Y., Zhou, W., Zhang, B., Hu, W., van, Eijk, M.J.T., Tang, J.,Witsenboer, H.M.A., Zhao, S., Li, Z., Zhang, A., Wang, D., Liang, C., 2018. Genomesequence of the progenitor of wheat A subgenome Triticum urartu. Nature 557,424e428.

Ling, H.Q., Zhao, S., Liu, D., Wang, J., Sun, H., Zhang, C., Fan, H., Li, D., Dong, L., Tao, Y.,Gao, C., Wu, H., Li, Y., Cui, Y., Guo, X., Zheng, S., Wang, B., Yu, K., Liang, Q.,Yang, W., Lou, X., Chen, J., Feng, M., Jian, J., Zhang, X., Luo, G., Jiang, Y., Liu, J.,Wang, Z., Sha, Y., Zhang, B., Wu, H., Tang, D., Shen, Q., Xue, P., Zou, S., Wang, X.,Liu, X., Wang, F., Yang, Y., An, X., Dong, Z., Zhang, K., Zhang, X., Luo, M.C.,Dvorak, J., Tong, Y., Wang, J., Yang, H., Li, Z., Wang, D., Zhang, A., Wang, J., 2013.Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496,87e90.

Liu, B., Wei, G., Shi, J., Jin, J., Shen, T., Ni, T., Shen, W.H., Yu, Y., Dong, A., 2016a. SETDOMAIN GROUP 708, a histone H3 lysine 36-specific methyltransferase, con-trols flowering time in rice (Oryza sativa). New Phytol. 210, 577e588.

Liu, C., Lu, F., Cui, X., Cao, X., 2010a. Histone methylation in higher plants. Annu. Rev.Plant Biol. 61, 395e420.

Liu, F., Quesada, V., Crevillen, P., Baurle, I., Swiezewski, S., Dean, C., 2007a. TheArabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1homolog to downregulate FLC. Mol. Cell 28, 398e407.

Liu, H., Ma, L., Yang, X., Zhang, L., Zeng, X., Xie, S., Peng, H., Gao, S., Lin, H., Pan, G.,Wu, Y., Shen, Y., 2017a. Integrative analysis of DNA methylation, mRNAs, andsmall RNAs during maize embryo dedifferentiation. BMC Plant Biol. 17, 105.

Liu, J., Ren, X., Yin, H., Wang, Y., Xia, R., Wang, Y., Gong, Z., 2010b. Mutation in thecatalytic subunit of DNA polymerase alpha influences transcriptional genesilencing and homologous recombination in Arabidopsis. Plant J. 61, 36e45.

Liu, J., Tang, X., Gao, L., Gao, Y., Li, Y., Huang, S., Sun, X., Miao, M., Zeng, H., Tian, X.,Niu, X., Zheng, L., Giovannoni, J., Xiao, F., Liu, Y., 2012a. A role of tomato UV-damaged DNA binding protein 1 (DDB1) in organ size control via an epige-netic manner. PLoS One 7, e42621.

Liu, K., Yu, Y., Dong, A., Shen, W.H., 2017b. SET DOMAIN GROUP701 encodes a H3K4-methytransferase and regulates multiple key processes of rice plant develop-ment. New Phytol. 215, 609e623.

Liu, Q., Wang, J., Miki, D., Xia, R., Yu, W., He, J., Zheng, Z., Zhu, J.K., Gong, Z., 2010c.DNA replication factor C1 mediates genomic stability and transcriptional genesilencing in Arabidopsis. Plant Cell 22, 2336e2352.

Liu, S., Yu, Y., Ruan, Y., Meyer, D., Wolff, M., Xu, L., Wang, N., Steinmetz, A.,Shen, W.H., 2007b. Plant SET- and RING-associated domain proteins in heter-ochromatinization. Plant J. 52, 914e926.

Liu, T., Li, Y., Duan, W., Huang, F., Hou, X., 2017c. Cold acclimation alters DNAmethylation patterns and confers tolerance to heat and increases growth rate inBrassica rapa. J. Exp. Bot. 68, 1213e1224.

Liu, T.T., Zhu, D., Chen, W., Deng, W., He, H., He, G., Bai, B., Qi, Y., Chen, R., Deng, X.W.,2013. A global identification and analysis of small nucleolar RNAs and possibleintermediate-sized non-coding RNAs in Oryza sativa. Mol. Plant 6, 830e846.

Liu, X., Luo, M., Zhang, W., Zhao, J., Zhang, J., Wu, K., Tian, L., Duan, J., 2012b. Histoneacetyltransferases in rice (Oryza sativa L.): phylogenetic analysis, subcellularlocalization and expression. BMC Plant Biol. 12, 145.

Liu, X., Yang, Y., Hu, Y., Zhou, L., Li, Y., Hou, X., 2018a. Temporal-specific interaction of




















































































































































































































NF-YC and CURLY LEAF during the floral transition regulates flowering. PlantPhysiol. 177, 105e114.

Liu, X., Zhou, C., Zhao, Y., Zhou, S., Wang, W., Zhou, D.X., 2014a. The rice enhancer ofzeste [E(z)] genes SDG711 and SDG718 are respectively involved in long day andshort day signaling to mediate the accurate photoperiod control of floweringtime. Front. Plant Sci. 5, 591.

Liu, X., Zhou, S., Wang, W., Ye, Y., Zhao, Y., Xu, Q., Zhou, C., Tan, F., Cheng, S.,Zhou, D.X., 2015. Regulation of histone methylation and reprogramming of geneexpression in the rice inflorescence meristem. Plant Cell 27, 1428e1444.

Liu, Y., Huang, Y., 2018. Uncovering the mechanistic basis for specific recognition ofmonomethylated H3K4 by the CW domain of Arabidopsis histone methyl-transferase SDG8. J. Biol. Chem. 293, 6470e6481.

Liu, Y., Min, J., 2016. Structure and function of histone methylation-binding proteinsin plants. Biochem. J. 473, 1663e1680.

Liu, Y., Tempel, W., Zhang, Q., Liang, X., Loppnau, P., Qin, S., Min, J., 2016b. Family-wide characterization of histone binding abilities of human CW domain-containing proteins. J. Biol. Chem. 291, 9000e9013.

Liu, Y., Zhang, A., Yin, H., Meng, Q., Yu, X., Huang, S., Wang, J., Ahmad, R., Liu, B.,Xu, Z.Y., 2018b. Trithorax-group proteins ARABIDOPSIS TRITHORAX4 (ATX4)and ATX5 function in abscisic acid and dehydration stress responses. NewPhytol. 217, 1582e1597.

Liu, Z.W., Shao, C.R., Zhang, C.J., Zhou, J.X., Zhang, S.W., Li, L., Chen, S., Huang, H.W.,Cai, T., He, X.J., 2014b. The SET domain proteins SUVH2 and SUVH9 are requiredfor Pol V occupancy at RNA-directed DNA methylation loci. PLoS Genet. 10,e1003948.

Lopez-Gonzalez, L., Mouriz, A., Narro-Diego, L., Bustos, R., Martinez-Zapater, J.M.,Jarillo, J.A., Pineiro, M., 2014. Chromatin-dependent repression of the Arabi-dopsis floral integrator genes involves plant specific PHD-containing proteins.Plant Cell 26, 3922e3938.

Lu, F., Cui, X., Zhang, S., Jenuwein, T., Cao, X., 2011. Arabidopsis REF6 is a histone H3lysine 27 demethylase. Nat. Cenet. 43, 715e719.

Lu, F., Cui, X., Zhang, S., Liu, C., Cao, X., 2010. JMJ14 is an H3K4 demethylase regu-lating flowering time in Arabidopsis. Cell Res. 20, 387e390.

Lu, F., Li, G., Cui, X., Liu, C., Wang, X.J., Cao, X., 2008a. Comparative analysis of JmjCdomain-containing proteins reveals the potential histone demethylases inArabidopsis and rice. J. Integr. Plant Biol. 50, 886e896.

Lu, X., Wang, X., Chen, X., Shu, N., Wang, J., Wang, D., Wang, S., Fan, W., Guo, L.,Guo, X., Ye, W., 2017. Single-base resolution methylomes of upland cotton(Gossypium hirsutum L.) reveal epigenome modifications in response to droughtstress. BMC Genomics 18, 297.

Lu, Y., Rong, T., Cao, M., 2008b. Analysis of DNA methylation in different maizetissues. J. Genet. Genomics 35, 41e48.

Luo, G.Z., MacQueen, A., Zheng, G., Duan, H., Dore, L.C., Lu, Z., Liu, J., Chen, K., Jia, G.,Bergelson, J., He, C., 2014. Unique features of the m6A methylome in Arabidopsisthaliana. Nat. Commun. 5, 5630.

Luo, M., Bilodeau, P., Koltunow, A., Dennis, E.S., Peacock, W.J., Chaudhury, A.M., 1999.Genes controlling fertilization-independent seed development in Arabidopsisthaliana. Proc. Natl. Acad. Sci. U. S. A. 96, 296e301.

Luo, M., Platten, D., Chaudhury, A., Peacock, W.J., Dennis, E.S., 2009. Expression,imprinting, and evolution of rice homologs of the polycomb group genes. Mol.Plant 2, 711e723.

Luo, M., Tai, R., Yu, C.W., Yang, S., Chen, C.Y., Lin, W.D., Schmidt, W., Wu, K., 2015.Regulation of flowering time by the histone deacetylase HDA5 in Arabidopsis.Plant J. 82, 925e936.

Luo, M., Wang, Y.Y., Liu, X., Yang, S., Lu, Q., Cui, Y., Wu, K., 2012. HD2C interacts withHDA6 and is involved in ABA and salt stress response in Arabidopsis. J. Exp. Bot.63, 3297e3306.

Ma, Y., Min, L., Wang, M., Wang, C., Zhao, Y., Li, Y., Fang, Q., Wu, Y., Xie, S., Ding, Y.,Su, X., Hu, Q., Zhang, Q., Li, X., Zhang, X., 2018. Disrupted genome methylation inresponse to high temperature has distinct affects on microspore abortion andanther indehiscence. Plant Cell 30, 1387e1403.

Martinez-Macias, M.I., Qian, W., Miki, D., Pontes, O., Liu, Y., Tang, K., Liu, R., Morales-Ruiz, T., Ariza, R.R., Roldan-Arjona, T., Zhu, J.K., 2012. A DNA 3' phosphatasefunctions in active DNA demethylation in Arabidopsis. Mol. Cell 45, 357e370.

McCue, A.D., Panda, K., Nuthikattu, S., Choudury, S.G., Thomas, E.N., Slotkin, R.K.,2015. ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to theestablishment of DNA methylation. EMBO J. 34, 20e35.

Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., Ni, F., Wu, L., Li, S., Zhou, H., Long, C.,Chen, S., Hannon, G.J., Qi, Y., 2008. Sorting of small RNAs into Arabidopsisargonaute complexes is directed by the 50 terminal nucleotide. Cell 133,116e127.

Migicovsky, Z., Kovalchuk, I., 2013. Changes to DNA methylation and homologousrecombination frequency in the progeny of stressed plants. Biochem. Cell Biol.91, 1e5.

Ming, R., Hou, S., Feng, Y., Yu, Q., Dionne-Laporte, A., Saw, J.H., Senin, P., Wang, W.,Ly, B.V., Lewis, K.L., Salzberg, S.L., Feng, L., Jones, M.R., Skelton, R.L., Murray, J.E.,Chen, C., Qian, W., Shen, J., Du, P., Eustice, M., Tong, E., Tang, H., Lyons, E.,Paull, R.E., Michael, T.P., Wall, K., Rice, D.W., Albert, H., Wang, M.L., Zhu, Y.J.,Schatz, M., Nagarajan, N., Acob, R.A., Guan, P., Blas, A., Wai, C.M.,Ackerman, C.M., Ren, Y., Liu, C., Wang, J., Na, J.K., Shakirov, E.V., Haas, B.,Thimmapuram, J., Nelson, D., Wang, X., Bowers, J.E., Gschwend, A.R.,Delcher, A.L., Singh, R., Suzuki, J.Y., Tripathi, S., Neupane, K., Wei, H., Irikura, B.,Paidi, M., Jiang, N., Zhang, W., Presting, G., Windsor, A., Navajas-Perez, R.,Torres, M.J., Feltus, F.A., Porter, B., Li, Y., Burroughs, A.M., Luo, M.C., Liu, L.,Christopher, D.A., Mount, S.M., Moore, P.H., Sugimura, T., Jiang, J., Schuler, M.A.,

Friedman, V., Mitchell-Olds, T., Shippen, D.E., dePamphilis, C.W., Palmer, J.D.,Freeling, M., Paterson, A.H., Gonsalves, D., Wang, L., Alam, M., 2008. The draftgenome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus).Nature 452, 991e996.

Ong-Abdullah, M., Ordway, J.M., Jiang, N., Ooi, S.E., Kok, S.Y., Sarpan, N., Azimi, N.,Hashim, A.T., Ishak, Z., Rosli, S.K., Malike, F.A., Bakar, N.A., Marjuni, M.,Abdullah, N., Yaakub, Z., Amiruddin, M.D., Nookiah, R., Singh, R., Low, E.T.,Chan, K.L., Azizi, N., Smith, S.W., Bacher, B., Budiman, M.A., Van Brunt, A.,Wischmeyer, C., Beil, M., Hogan, M., Lakey, N., Lim, C.C., Arulandoo, X.,Wong, C.K., Choo, C.N., Wong, W.C., Kwan, Y.Y., Alwee, S.S.,Sambanthamurthi, R., Martienssen, R.A., 2015. Loss of Karma transposonmethylation underlies the mantled somaclonal variant of oil palm. Nature 525,533e537.

Pien, S., Fleury, D., Mylne, J.S., Crevillen, P., Inze, D., Avramova, Z., Dean, C.,Grossniklaus, U., 2008. ARABIDOPSIS TRITHORAX1 dynamically regulatesFLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell20, 580e588.

Potato Genome Sequencing, C., Xu, X., Pan, S., Cheng, S., Zhang, B., Mu, D., Ni, P.,Zhang, G., Yang, S., Li, R., Wang, J., Orjeda, G., Guzman, F., Torres, M., Lozano, R.,Ponce, O., Martinez, D., De, la, Cruz, G., Chakrabarti, S.K., Patil, V.U.,Skryabin, K.G., Kuznetsov, B.B., Ravin, N.V., Kolganova, T.V., Beletsky, A.V.,Mardanov, A.V., Di, Genova, A., Bolser, D.M., Martin, D.M., Li, G., Yang, Y.,Kuang, H., Hu, Q., Xiong, X., Bishop, G.J., Sagredo, B., Mejía, N., Zagorski, W.,Gromadka, R., Gawor, J., Szczesny, P., Huang, S., Zhang, Z., Liang, C., He, J., Li, Y.,He, Y., Xu, J., Zhang, Y., Xie, B., Du, Y., Qu, D., Bonierbale, M., Ghislain, M., Herrera,Mdel, R., Giuliano, G., Pietrella, M., Perrotta, G., Facella, P., O'Brien, K.,Feingold, S.E., Barreiro, L.E., Massa, G.A., Diambra, L., Whitty, B.R.,Vaillancourt, B., Lin, H., Massa, A.N., Geoffroy, M., Lundback, S., DellaPenna, D.,Buell, C.R., Sharma, S.K., Marshall, D.F., Waugh, R., Bryan, G.J., Destefanis, M.,Nagy, I., Milbourne, D., Thomson, S.J., Fiers, M., Jacobs, J.M., Nielsen, K.L.,Sønderkær, M., Iovene, M., Torres, G.A., Jiang, J., Veilleux, R.E., Bachem, C.W., de,Boer, J., Borm, T., Kloosterman, B., van, Eck, H., Datema, E., Hekkert, Bt,Goverse, A., van, Ham, R.C., Visser, R.G., 2011. Genome sequence and analysis ofthe tuber crop potato. Nature 475, 189e195.

Qian, S., Lv, X., Scheid, R.N., Lu, L., Yang, Z., Chen, W., Liu, R., Boersma, M.D.,Denu, J.M., Zhong, X., Du, J., 2018. Dual recognition of H3K4me3 and H3K27me3by a plant histone reader SHL. Nat. Commun. 9, 2425.

Qian, W., Miki, D., Lei, M., Zhu, X., Zhang, H., Liu, Y., Li, Y., Lang, Z., Wang, J., Tang, K.,Liu, R., Zhu, J.K., 2014. Regulation of active DNA demethylation by an alpha-crystallin domain protein in Arabidopsis. Mol. Cell 55, 361e371.

Qian, W., Miki, D., Zhang, H., Liu, Y., Zhang, X., Tang, K., Kan, Y., La, H., Li, X., Li, S.,Zhu, X., Shi, X., Zhang, K., Pontes, O., Chen, X., Liu, R., Gong, Z., Zhu, J.K., 2012.A histone acetyltransferase regulates active DNA demethylation in Arabidopsis.Science 336, 1445e1448.

Rigal, M., Kevei, Z., Pelissier, T., Mathieu, O., 2012. DNA methylation in an intron ofthe IBM1 histone demethylase gene stabilizes chromatin modification patterns.EMBO J. 31, 2981e2993.

Saleh, A., Alvarez-Venegas, R., Yilmaz, M., Le, O., Hou, G., Sadder, M., Al-Abdallat, A.,Xia, Y., Lu, G., Ladunga, I., Avramova, Z., 2008. The highly similar Arabidopsishomologs of trithorax ATX1 and ATX2 encode proteins with divergentbiochemical functions. Plant Cell 20, 568e579.

Saze, H., Kitayama, J., Takashima, K., Miura, S., Harukawa, Y., Ito, T., Kakutani, T.,2013. Mechanism for full-length RNA processing of Arabidopsis genes contain-ing intragenic heterochromatin. Nat. Commun. 4, 2301.

Saze, H., Shiraishi, A., Miura, A., Kakutani, T., 2008. Control of genic DNA methyl-ation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319,462e465.

Schonrock, N., Bouveret, R., Leroy, O., Borghi, L., Kohler, C., Gruissem, W., Hennig, L.,2006. Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Dev. 20, 1667e1678.

Schubert, D., Primavesi, L., Bishopp, A., Roberts, G., Doonan, J., Jenuwein, T.,Goodrich, J., 2006. Silencing by plant Polycomb-group genes requires dispersedtrimethylation of histone H3 at lysine 27. EMBO J. 25, 4638e4649.

Scutenaire, J., Deragon, J.M., Jean, V., Benhamed, M., Raynaud, C., Favory, J.J.,Merret, R., Bousquet-Antonelli, C., 2018. The YTH domain protein ECT2 is anm(6)A reader required for normal trichome branching in Arabidopsis. Plant Cell30, 986e1005.

Shen, H., He, H., Li, J., Chen, W., Wang, X., Guo, L., Peng, Z., He, G., Zhong, S., Qi, Y.,Terzaghi, W., Deng, X.W., 2012. Genome-wide analysis of DNA methylation andgene expression changes in two Arabidopsis ecotypes and their reciprocal hy-brids. Plant Cell 24, 875e892.

Shen, L., Liang, Z., Gu, X., Chen, Y., Teo, Z.W., Hou, X., Cai, W.M., Dedon, P.C., Liu, L.,Yu, H., 2016. N(6)-methyladenosine RNA modification regulates shoot stem cellfate in Arabidopsis. Dev. Cell 38, 186e200.

Shen, W.H., 2001. NtSET1, a member of a newly identified subgroup of plant SET-domain-containing proteins, is chromatin-associated and its ectopic over-expression inhibits tobacco plant growth. Plant J. 28, 371e383.

Shen, Y., Conde, E.S.N., Audonnet, L., Servet, C., Wei, W., Zhou, D.X., 2014. Over-expression of histone H3K4 demethylase gene JMJ15 enhances salt tolerance inArabidopsis. Front. Plant Sci. 5, 290.

Slotkin, R.K., Martienssen, R., 2007. Transposable elements and the epigeneticregulation of the genome. Nat. Rev. Genet. 8, 272e285.

Song, Q., Guan, X., Chen, Z.J., 2015a. Dynamic roles for small RNAs and DNAmethylation during ovule and fiber development in allotetraploid cotton. PLoSGenet. 11, e1005724.


















































































































































































































Song, Z.T., Sun, L., Lu, S.J., Tian, Y., Ding, Y., Liu, J.X., 2015b. Transcription factorinteraction with COMPASS-like complex regulates histone H3K4 trimethylationfor specific gene expression in plants. Proc. Natl. Acad. Sci. U. S. A. 112,2900e2905.

Spedaletti, V., Polticelli, F., Capodaglio, V., Schinina, M.E., Stano, P., Federico, R.,Tavladoraki, P., 2008. Characterization of a lysine-specific histone demethylasefrom Arabidopsis thaliana. Biochemistry 47, 4936e4947.

Stroud, H., Do, T., Du, J., Zhong, X., Feng, S., Johnson, L., Patel, D.J., Jacobsen, S.E.,2014. Non-CG methylation patterns shape the epigenetic landscape in Arabi-dopsis. Nat. Struct. Mol. Biol. 21, 64e72.

Su, Y., Wang, S., Zhang, F., Zheng, H., Liu, Y., Huang, T., Ding, Y., 2017. Phosphory-lation of histone H2A at serine 95: a plant-specific mark involved in floweringtime regulation and H2A.Z deposition. Plant Cell 29, 2197e2213.

Sui, P., Jin, J., Ye, S., Mu, C., Gao, J., Feng, H., Shen, W.H., Yu, Y., Dong, A., 2012. H3K36methylation is critical for brassinosteroid-regulated plant growth and devel-opment in rice. Plant J. 70, 340e347.

Sun, Q., Zhou, D.X., 2008. Rice jmjC domain-containing gene JMJ706 encodes H3K9demethylase required for floral organ development. Proc. Natl. Acad. Sci. U. S. A.105, 13679e13684.

Tamada, Y., Yun, J.Y., Woo, S.C., Amasino, R.M., 2009. ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for tran-scriptional activation of FLOWERING LOCUS C. Plant Cell 21, 3257e3269.

Tang, K., Lang, Z., Zhang, H., Zhu, J.K., 2016. The DNA demethylase ROS1 targetsgenomic regions with distinct chromatin modifications. Nat. Plants 2, 16169.

Tao, Z., Shen, L., Gu, X., Wang, Y., Yu, H., He, Y., 2017. Embryonic epigeneticreprogramming by a pioneer transcription factor in plants. Nature 551,124e128.

Telias, A., Lin-Wang, K., Stevenson, D.E., Cooney, J.M., Hellens, R.P., Allan, A.C.,Hoover, E.E., Bradeen, J.M., 2011. Apple skin patterning is associated with dif-ferential expression of MYB10. BMC Plant Biol. 11, 93.

Thorstensen, T., Fischer, A., Sandvik, S.V., Johnsen, S.S., Grini, P.E., Reuter, G.,Aalen, R.B., 2006. The Arabidopsis SUVR4 protein is a nucleolar histone meth-yltransferase with preference for monomethylated H3K9. Nucleic Acids Res. 34,5461e5470.

To, T.K., Saze, H., Kakutani, T., 2015. DNA methylation within transcribed regions.Plant Physiol. 168, 1219e1225.

Tsuchiya, T., Eulgem, T., 2013. An alternative polyadenylation mechanism coopted tothe Arabidopsis RPP7 gene through intronic retrotransposon domestication.Proc. Natl. Acad. Sci. U. S. A. 110, E3535eE3543.

Turck, F., Roudier, F., Farrona, S., Martin-Magniette, M.L., Guillaume, E., Buisine, N.,Gagnot, S., Martienssen, R.A., Coupland, G., Colot, V., 2007. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3lysine 27. PLoS Genet. 3, e86.

Wang, D., Tyson, M.D., Jackson, S.S., Yadegari, R., 2006. Partially redundant functionsof two SET-domain polycomb-group proteins in controlling initiation of seeddevelopment in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 103, 13244e13249.

Wang, J., Hu, J., Qian, Q., Xue, H.W., 2013a. LC2 and OsVIL2 promote rice floweringby photoperoid-induced epigenetic silencing of OsLF. Mol. Plant 6, 514e527.

Wang, L., Xie, J., Hu, J., Lan, B., You, C., Li, F., Wang, Z., Wang, H., 2018. Comparativeepigenomics reveals evolution of duplicated genes in potato and tomato. Plant J.93, 460e471.

Wang, M., Qin, L., Xie, C., Li, W., Yuan, J., Kong, L., Yu, W., Xia, G., Liu, S., 2014a.Induced and constitutive DNA methylation in a salinity-tolerant wheat intro-gression line. Plant Cell Physiol. 55, 1354e1365.

Wang, X., Duan, C.G., Tang, K., Wang, B., Zhang, H., Lei, M., Lu, K., Mangrauthia, S.K.,Wang, P., Zhu, G., Zhao, Y., Zhu, J.K., 2013b. RNA-binding protein regulates plantDNA methylation by controlling mRNA processing at the intronicheterochromatin-containing gene IBM1. Proc. Natl. Acad. Sci. U. S. A. 110,15467e15472.

Wang, X., Wang, H., Wang, J., Sun, R., Wu, J., Liu, S., Bai, Y., Mun, J.H., Bancroft, I.,Cheng, F., Huang, S., Li, X., Hua, W., Wang, J., Wang, X., Freeling, M., Pires, J.C.,Paterson, A.H., Chalhoub, B., Wang, B., Hayward, A., Sharpe, A.G., Park, B.S.,Weisshaar, B., Liu, B., Li, B., Liu, B., Tong, C., Song, C., Duran, C., Peng, C., Geng, C.,Koh, C., Lin, C., Edwards, D., Mu, D., Shen, D., Soumpourou, E., Li, F., Fraser, F.,Conant, G., Lassalle, G., King, G.J., Bonnema, G., Tang, H., Wang, H., Belcram, H.,Zhou, H., Hirakawa, H., Abe, H., Guo, H., Wang, H., Jin, H., Parkin, I.A., Batley, J.,Kim, J.S., Just, J., Li, J., Xu, J., Deng, J., Kim, J.A., Li, J., Yu, J., Meng, J., Wang, J.,Min, J., Poulain, J., Wang, J., Hatakeyama, K., Wu, K., Wang, L., Fang, L., Trick, M.,Links, M.G., Zhao, M., Jin, M., Ramchiary, N., Drou, N., Berkman, P.J., Cai, Q.,Huang, Q., Li, R., Tabata, S., Cheng, S., Zhang, S., Zhang, S., Huang, S., Sato, S.,Sun, S., Kwon, S.J., Choi, S.R., Lee, T.H., Fan, W., Zhao, X., Tan, X., Xu, X., Wang, Y.,Qiu, Y., Yin, Y., Li, Y., Du, Y., Liao, Y., Lim, Y., Narusaka, Y., Wang, Y., Wang, Z., Li, Z.,Wang, Z., Xiong, Z., Zhang, Z., Brassica rapa Genome Sequencing Project Con-sortium, 2011. The genome of the mesopolyploid crop species Brassica rapa. Nat.Cenet. 43, 1035e1039.

Wang, Y., Fan, X., Lin, F., He, G., Terzaghi, W., Zhu, D., Deng, X.W., 2014b. Arabidopsisnoncoding RNA mediates control of photomorphogenesis by red light. Proc.Natl. Acad. Sci. U. S. A. 111, 10359e10364.

Wang, Y., Liu, J., Xia, R., Wang, J., Shen, J., Cao, R., Hong, X., Zhu, J.K., Gong, Z., 2007.The protein kinase TOUSLED is required for maintenance of transcriptional genesilencing in Arabidopsis. EMBO Rep. 8, 77e83.

Wang, Y., Wang, X., Deng, W., Fan, X., Liu, T.T., He, G., Chen, R., Terzaghi, W., Zhu, D.,Deng, X.W., 2014c. Genomic features and regulatory roles of intermediate-sizednon-coding RNAs in Arabidopsis. Mol. Plant 7, 514e527.

Wang, Z., Patel, D.J., 2011. Combinatorial readout of dual histone modifications by

paired chromatin-associated modules. J. Biol. Chem. 286, 18363e18368.Wei, L.H., Song, P., Wang, Y., Lu, Z., Tang, Q., Yu, Q., Xiao, Y., Zhang, X., Duan, H.C.,

Jia, G., 2018. The m(6)A reader ECT2 controls trichome morphology by affectingmRNA stability in Arabidopsis. Plant Cell 30, 968e985.

Wu, H.J., Wang, Z.M., Wang, M., Wang, X.J., 2013a. Widespread long noncodingRNAs as endogenous target mimics for microRNAs in plants. Plant Physiol. 161,1875e1884.

Wu, J., Wang, Z., Shi, Z., Zhang, S., Ming, R., Zhu, S., Khan, M.A., Tao, S., Korban, S.S.,Wang, H., Chen, N.J., Nishio, T., Xu, X., Cong, L., Qi, K., Huang, X., Wang, Y.,Zhao, X., Wu, J., Deng, C., Gou, C., Zhou, W., Yin, H., Qin, G., Sha, Y., Tao, Y.,Chen, H., Yang, Y., Song, Y., Zhan, D., Wang, J., Li, L., Dai, M., Gu, C., Wang, Y.,Shi, D., Wang, X., Zhang, H., Zeng, L., Zheng, D., Wang, C., Chen, M., Wang, G.,Xie, L., Sovero, V., Sha, S., Huang, W., Zhang, S., Zhang, M., Sun, J., Xu, L., Li, Y.,Liu, X., Li, Q., Shen, J., Wang, J., Paull, R.E., Bennetzen, J.L., Wang, J., Zhang, S.,2013b. The genome of the pear (Pyrus bretschneideri Rehd.). Genome Res. 23,396e408.

Xia, R., Wang, J., Liu, C., Wang, Y., Wang, Y., Zhai, J., Liu, J., Hong, X., Cao, X., Zhu, J.K.,Gong, Z., 2006. ROR1/RPA2A, a putative replication protein A2, functions inepigenetic gene silencing and in regulation of meristem development in Ara-bidopsis. Plant Cell 18, 85e103.

Xia, S., Cheng, Y.T., Huang, S., Win, J., Soards, A., Jinn, T.L., Jones, J.D., Kamoun, S.,Chen, S., Zhang, Y., Li, X., 2013. Regulation of transcription of nucleotide-bindingleucine-rich repeat-encoding genes SNC1 and RPP4 via H3K4 trimethylation.Plant Physiol. 162, 1694e1705.

Xiong, L.Z., Xu, C.G., Saghai Maroof, M.A., Zhang, Q., 1999. Patterns of cytosinemethylation in an elite rice hybrid and its parental lines, detected by amethylation-sensitive amplification polymorphism technique. Mol. Gen. Genet.261, 439e446.

Xu, F., Kuo, T., Rosli, Y., Liu, M.S., Wu, L., Chen, L.O., Fletcher, J.C., Sung, Z.R., Pu, L.,2018. Trithorax group proteins act together with a polycomb group protein tomaintain chromatin integrity for epigenetic silencing during seed germinationin Arabidopsis. Mol. Plant 11, 659e677.

Xu, J., Wang, X., Cao, H., Xu, H., Xu, Q., Deng, X., 2017. Dynamic changes in meth-ylome and transcriptome patterns in response to methyltransferase inhibitor 5-azacytidine treatment in citrus. DNA Res. 24, 509e522.

Xu, L., Zhao, Z., Dong, A., Soubigou-Taconnat, L., Renou, J.P., Steinmetz, A.,Shen, W.H., 2008. Di- and tri- but not monomethylation on histone H3 lysine 36marks active transcription of genes involved in flowering time regulation andother processes in Arabidopsis thaliana. Mol. Cell. Biol. 28, 1348e1360.

Xu, R., Wang, Y., Zheng, H., Lu, W., Wu, C., Huang, J., Yan, K., Yang, G., Zheng, C., 2015.Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNAmethylation pathway in Arabidopsis. J. Exp. Bot. 66, 5997e6008.

Xu, Y., Zhong, L., Wu, X., Fang, X., Wang, J., 2009. Rapid alterations of geneexpression and cytosine methylation in newly synthesized Brassica napus al-lopolyploids. Planta 229, 471e483.

Yamamuro, C., Miki, D., Zheng, Z., Ma, J., Wang, J., Yang, Z., Dong, J., Zhu, J.K., 2014.Overproduction of stomatal lineage cells in Arabidopsis mutants defective inactive DNA demethylation. Nat. Commun. 5, 4062.

Yan, D., Zhang, X., Zhang, L., Ye, S., Zeng, L., Liu, J., Li, Q., He, Z., 2015. CURVEDCHIMERIC PALEA 1 encoding an EMF1-like protein maintains epigeneticrepression of OsMADS58 in rice palea development. Plant J. 82, 12e24.

Yang, D.L., Zhang, G., Tang, K., Li, J., Yang, L., Huang, H., Zhang, H., Zhu, J.K., 2016a.Dicer-independent RNA-directed DNA methylation in Arabidopsis. Cell Res. 26,66e82.

Yang, H., Han, Z., Cao, Y., Fan, D., Li, H., Mo, H., Feng, Y., Liu, L., Wang, Z., Yue, Y.,Cui, S., Chen, S., Chai, J., Ma, L., 2012a. A companion cell-dominant and devel-opmentally regulated H3K4 demethylase controls flowering time in Arabidopsisvia the repression of FLC expression. PLoS Genet. 8, e1002664.

Yang, H., Mo, H., Fan, D., Cao, Y., Cui, S., Ma, L., 2012b. Overexpression of a histoneH3K4 demethylase, JMJ15, accelerates flowering time in Arabidopsis. Plant CellRep. 31, 1297e1308.

Yang, M., Wang, X., Huang, H., Ren, D., Su, Y., Zhu, P., Zhu, D., Fan, L., Chen, L., He, G.,Deng, X.W., 2016b. Natural variation of H3K27me3 modification in two Arabi-dopsis accessions and their hybrid. J. Integr. Plant Biol. 58, 466e474.

Yang, Z., Qiu, Q., Chen, W., Jia, B., Chen, X., Hu, H., He, K., Deng, X., Li, S., Tao, W.A.,Cao, X., Du, J., 2018. Structure of the Arabidopsis JMJ14-H3K4me3 complexprovides insight into the substrate specificity of KDM5 subfamily histonedemethylases. Plant Cell 30, 167e177.

Ye, R., Chen, Z., Lian, B., Rowley, M.J., Xia, N., Chai, J., Li, Y., He, X.J., Wierzbicki, A.T.,Qi, Y., 2016. A dicer-independent route for biogenesis of siRNAs that direct DNAmethylation in Arabidopsis. Mol. Cell 61, 222e235.

Ye, R., Wang, W., Iki, T., Liu, C., Wu, Y., Ishikawa, M., Zhou, X., Qi, Y., 2012. Cyto-plasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNAcomplexes. Mol. Cell 46, 859e870.

Yin, H., Zhang, X., Liu, J., Wang, Y., He, J., Yang, T., Hong, X., Yang, Q., Gong, Z., 2009.Epigenetic regulation, somatic homologous recombination, and abscisic acidsignaling are influenced by DNA polymerase epsilon mutation in Arabidopsis.Plant Cell 21, 386e402.

Yu, A., Lepere, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., Abraham, A.L.,Penterman, J., Fischer, R.L., Voinnet, O., Navarro, L., 2013. Dynamics and bio-logical relevance of DNA demethylation in Arabidopsis antibacterial defense.Proc. Natl. Acad. Sci. U. S. A. 110, 2389e2394.

Yu, X., Li, L., Li, L., Guo, M., Chory, J., Yin, Y., 2008. Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 andREF6 in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 105, 7618e7623.






















































































































































































































Yu, X., Meng, X., Liu, Y., Li, N., Zhang, A., Wang, T.J., Jiang, L., Pang, J., Zhao, X., Qi, X.,Zhang, M., Wang, S., Liu, B., Xu, Z.Y., 2018. The chromatin remodeler ZmCHB101impacts expression of osmotic stress-responsive genes in maize. Plant Mol. Biol.97, 451e465.

Yuan, W., Luo, X., Li, Z., Yang, W., Wang, Y., Liu, R., Du, J., He, Y., 2016. A cis coldmemory element and a trans epigenome reader mediate Polycomb silencing ofFLC by vernalization in Arabidopsis. Nat. Cenet. 48, 1527e1534.

Zhai, J., Bischof, S., Wang, H., Feng, S., Lee, T.F., Teng, C., Chen, X., Park, S.Y., Liu, L.,Gallego-Bartolome, J., Liu, W., Henderson, I.R., Meyers, B.C., Ausin, I.,Jacobsen, S.E., 2015. A one precursor one siRNA model for Pol IV-dependentsiRNA biogenesis. Cell 163, 445e455.

Zhang, B., Tieman, D.M., Jiao, C., Xu, Y., Chen, K., Fei, Z., Giovannoni, J.J., Klee, H.J.,2016a. Chilling-induced tomato flavor loss is associated with altered volatilesynthesis and transient changes in DNA methylation. Proc. Natl. Acad. Sci. U. S.A. 113, 12580e12585.

Zhang, C.J., Zhou, J.X., Liu, J., Ma, Z.Y., Zhang, S.W., Dou, K., Huang, H.W., Cai, T.,Liu, R., Zhu, J.K., He, X.J., 2013a. The splicing machinery promotes RNA-directedDNA methylation and transcriptional silencing in Arabidopsis. EMBO J. 32,1128e1140.

Zhang, H., Ma, Z.Y., Zeng, L., Tanaka, K., Zhang, C.J., Ma, J., Bai, G., Wang, P.,Zhang, S.W., Liu, Z.W., Cai, T., Tang, K., Liu, R., Shi, X., He, X.J., Zhu, J.K., 2013b.DTF1 is a core component of RNA-directed DNA methylation and may assist inthe recruitment of Pol IV. Proc. Natl. Acad. Sci. U. S. A. 110, 8290e8295.

Zhang, M., Xie, S., Dong, X., Zhao, X., Zeng, B., Chen, J., Li, H., Yang, W., Zhao, H.,Wang, G., Chen, Z., Sun, S., Hauck, A., Jin, W., Lai, J., 2014a. Genome-wide highresolution parental-specific DNA and histone methylation maps uncover pat-terns of imprinting regulation in maize. Genome Res. 24, 167e176.

Zhang, M., Zhao, H., Xie, S., Chen, J., Xu, Y., Wang, K., Zhao, H., Guan, H., Hu, X.,Jiao, Y., Song, W., Lai, J., 2011. Extensive, clustered parental imprinting ofprotein-coding and noncoding RNAs in developing maize endosperm. Proc.Natl. Acad. Sci. U. S. A. 108, 20042e20047.

Zhang, Q., Wang, D., Lang, Z., He, L., Yang, L., Zeng, L., Li, Y., Zhao, C., Huang, H.,Zhang, H., Zhu, J.K., 2016b. Methylation interactions in Arabidopsis hybridsrequire RNA-directed DNA methylation and are influenced by genetic variation.Proc. Natl. Acad. Sci. U. S. A. 113, E4248eE4256.

Zhang, X., Clarenz, O., Cokus, S., Bernatavichute, Y.V., Pellegrini, M., Goodrich, J.,Jacobsen, S.E., 2007a. Whole-genome analysis of histone H3 lysine 27 trime-thylation in Arabidopsis. PLoS Biol. 5, e129.

Zhang, X., Germann, S., Blus, B.J., Khorasanizadeh, S., Gaudin, V., Jacobsen, S.E.,2007b. The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trime-thylation. Nat. Struct. Mol. Biol. 14, 869e871.

Zhang, X., Sun, J., Cao, X., Song, X., 2015. Epigenetic mutation of RAV6 affects leafangle and seed size in rice. Plant Physiol. 169, 2118e2128.

Zhang, Y.C., Liao, J.Y., Li, Z.Y., Yu, Y., Zhang, J.P., Li, Q.F., Qu, L.H., Shu, W.S., Chen, Y.Q.,2014b. Genome-wide screening and functional analysis identify a large numberof long noncoding RNAs involved in the sexual reproduction of rice. GenomeBiol. 15, 512.

Zhao, L., Cai, H., Su, Z., Wang, L., Huang, X., Zhang, M., Chen, P., Dai, X., Zhao, H.,Palanivelu, R., Chen, X., Qin, Y., 2018. KLU suppresses megasporocyte cell fatethrough SWR1-mediated activation of WRKY28 expression in Arabidopsis. Proc.Natl. Acad. Sci. U. S. A. 115, E526eE535.

Zhao, Y., Xie, S., Li, X., Wang, C., Chen, Z., Lai, J., Gong, Z., 2014. REPRESSOR OF

SILENCING5 encodes a member of the small heat shock protein family and isrequired for DNA demethylation in Arabidopsis. Plant Cell 26, 2660e2675.

Zhao, Z., Shen, W.H., 2004. Plants contain a high number of proteins showingsequence similarity to the animal SUV39H family of histone methyltransferases.Ann. N. Y. Acad. Sci. 1030, 661e669.

Zhao, Z., Yu, Y., Meyer, D., Wu, C., Shen, W.H., 2005. Prevention of early flowering byexpression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat.Cell Biol. 7, 1256e1260.

Zheng, M., Wang, Y., Wang, Y., Wang, C., Ren, Y., Lv, J., Peng, C., Wu, T., Liu, K.,Zhao, S., Liu, X., Guo, X., Jiang, L., Terzaghi, W., Wan, J., 2015. DEFORMED FLORALORGAN1 (DFO1) regulates floral organ identity by epigenetically repressing theexpression of OsMADS58 in rice (Oryza sativa). New Phytol. 206, 1476e1490.

Zheng, X., Zhu, J., Kapoor, A., Zhu, J.K., 2007. Role of Arabidopsis AGO6 in siRNAaccumulation, DNA methylation and transcriptional gene silencing. EMBO J. 26,1691e1701.

Zhong, S., Fei, Z., Chen, Y.R., Zheng, Y., Huang, M., Vrebalov, J., McQuinn, R.,Gapper, N., Liu, B., Xiang, J., Shao, Y., Giovannoni, J.J., 2013. Single-base resolu-tion methylomes of tomato fruit development reveal epigenome modificationsassociated with ripening. Nat. Biotechnol. 31, 154e159.

Zhong, X., Du, J., Hale, C.J., Gallego-Bartolome, J., Feng, S., Vashisht, A.A., Chory, J.,Wohlschlegel, J.A., Patel, D.J., Jacobsen, S.E., 2014. Molecular mechanism of ac-tion of plant DRM de novo DNA methyltransferases. Cell 157, 1050e1060.

Zhou, C., Zhang, L., Duan, J., Miki, B., Wu, K., 2005. HISTONE DEACETYLASE19 isinvolved in jasmonic acid and ethylene signaling of pathogen response inArabidopsis. Plant Cell 17, 1196e1204.

Zhou, S., Liu, X., Zhou, C., Zhou, Q., Zhao, Y., Li, G., Zhou, D.X., 2016. Cooperationbetween the H3K27me3 chromatin mark and non-CG methylation in epigeneticregulation. Plant Physiol. 172, 1131e1141.

Zhu, J.K., 2009. Active DNA demethylation mediated by DNA glycosylases. Annu.Rev. Genet. 43, 143e166.

Zhu, Y., Rowley, M.J., Bohmdorfer, G., Wierzbicki, A.T., 2013. A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing.Mol. Cell 49, 298e309.

Zhu, Z., An, F., Feng, Y., Li, P., Xue, L., M, A., Jiang, Z., Kim, J.M., To, T.K., Li, W.,Zhang, X., Yu, Q., Dong, Z., Chen, W.Q., Seki, M., Zhou, J.M., Guo, H., 2011.Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediatesjasmonate and ethylene signaling synergy in Arabidopsis. Proc. Natl. Acad. Sci. U.S. A. 108, 12539e12544.

Zilberman, D., Cao, X., Jacobsen, S.E., 2003. ARGONAUTE4 control of locus-specificsiRNA accumulation and DNA and histone methylation. Science 299, 716e719.

Zilberman, D., Gehring, M., Tran, R.K., Ballinger, T., Henikoff, S., 2007. Genome-wideanalysis of Arabidopsis thaliana DNA methylation uncovers an interdependencebetween methylation and transcription. Nat. Genet. 39, 61e69.

Zong, W., Zhong, X., You, J., Xiong, L., 2013. Genome-wide profiling of histone H3K4-tri-methylation and gene expression in rice under drought stress. Plant Mol.Biol. 81, 175e188.

Zou, C., Chen, A., Xiao, L., Muller, H.M., Ache, P., Haberer, G., Zhang, M., Jia, W.,Deng, P., Huang, R., Lang, D., Li, F., Zhan, D., Wu, X., Zhang, H., Bohm, J., Liu, R.,Shabala, S., Hedrich, R., Zhu, J.K., Zhang, H., 2017. A high-quality genome as-sembly of quinoa provides insights into the molecular basis of salt bladder-based salinity tolerance and the exceptional nutritional value. Cell Res. 27,1327e1340.





































































































































retrospective and perspective of plant epigenetics in china › hla › sites › zhulab ›...

Documents