Journal of Genetics and Genomics 45 (2018) 621e638 Contents lists available at ScienceDirect Journal of Genetics and Genomics Journal homepage: www.journals.elsevier.com/journal-of-genetics- 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, China b Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN 47907, USA c State Key Laboratory of Plant Genomics and National Center for Plant Gene Research, Institute of Genetics and Developmental Biology, Chinese Academyof Sciences, Beijing 100101, China article info abstract Article history: Epigenetics refers to the study of heritable changes in gene function that do not involve changes in the Received 15 August 2018 DNA sequence. Such effects on cellular and physiological phenotypic traits may result from external or Received in revised form environmental factors or be part of normal developmental program. In eukaryotes, DNA wraps on a 25 September 2018 histone octamer (two copies of H2A, H2B, H3 and H4) to form nucleosome, the fundamental unit of Accepted 30 September 2018 chromatin. The structure of chromatin is subjected to a dynamic regulation through multiple epigenetic Available online 6 November 2018 mechanisms, including DNA methylation, histone posttranslational modifications (PTMs), chromatin remodeling and noncoding RNAs. As conserved regulatory mechanisms in gene expression, epigenetic Keywords: Plant epigenetics mechanisms participate in almost all the important biological processes ranging from basal development DNA methylation to environmental response. Importantly, all of the major epigenetic mechanisms in mammalians also Histone modifications occur in plants. Plant studies have provided numerous important contributions to the epigenetic Chromatin remodeling research. For example, gene imprinting, a mechanism of parental allele-specific gene expression, was firstly observed in maize; evidence of paramutation, an epigenetic phenomenon that one allele acts in a single 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-nt siRNA-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 study of epigenetic mechanisms is of great significance to improve crop agronomic traits and environmental adaptability. 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 of epigenetic 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 past 40 years ranging from 1978 to 2017, including the fields of DNA methylation, histone modifications, chromatin remodeling and With the continuous improvements of sequencing technology small noncoding RNAs. We compared the total publications per and the accomplishment of the annotation of Arabidopsis genome, year in plant epigenetics with that published by Chinese re- epigenetic studies have experienced explosive growth over the past searchers or groups. We found that the majority of papers several decades. Similar situation also occurs in China, one of the contributed by China were published after the year 2000 and have major agricultural countries in the world, especially in the field of experienced a dramatical increase since then (Fig. 1A), indicating plant genetics benefiting from the growing research funding and epigenetic studies are much active during this period. Consistent the rich plant resources. Based on the public database from “Web of with this trend, total citations per year also experienced rapid in- Science”, we analyzed the publications in plant epigenetics over the crease over the past 20 years (Fig. 1B). By contrast, the increase of publications from other countries were much slower than China, although there is also a rapid increase after the year 2000 (Fig. 1A). * Corresponding authors. This trend is further supported by a sharp increase in the per- E-mail addresses: [email protected] (C.-G. Duan), [email protected] (J.-K. Zhu), centage of papers published by China over the total publications, [email protected] (X. Cao). https://doi.org/10.1016/j.jgg.2018.09.004 1673-8527/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. 622 C.-G. Duan et al. / Journal of Genetics and Genomics 45 (2018) 621e638 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 information is from the public database of “Web of Science” (https://apps.webofknowledge.com/UA_GeneralSearch_input.do?product¼UA&search_mode¼GeneralSearch&SID¼6C6G thh4wqMhMnwquYs&preferencesSaved ¼ ). For the criteria of publications, only articles and conference papers are included. which arises from 0% (1978) to ~30% (2017). This data strongly epigenetic gene silencing and heterochromatin in both plants and suggests that plant epigenetic studies have been speeding up over mammals. DNA methylation is involved in multiple cellular and the past 20 years in China. About 53% papers published by China are biological processes. High level of DNA methylation is required for contributed by the top 10 research institutions (Fig. 1C). Among the silencing of transposable elements (TEs) which is important for them, Chinese Academy of Sciences (CAS), Chinese Academy of genome stability (Slotkin and Martienssen, 2007). Proper patterns Agricultural Sciences (CAAS) and China Agricultural University of DNA methylation are crucial for the precise regulation of growth (CAU) rank the first three (Fig. 1C). and development (Zilberman et al., 2007). In mammals, DNA methylation is closely linked to disease pathogenesis (e.g., cancer) 2. Dynamic regulation of DNA methylation pattern in plants and aging (Bergman and Cedar, 2013; Klutstein et al., 2016). Simi- larly, the dynamically regulated DNA methylation responds to DNA 5-methylcytosine (5mC) modification is a hallmark of environmental changes and contributes to plant stress response C.-G. Duan et al. / Journal of Genetics and Genomics 45 (2018) 621e638 623 (Migicovsky and Kovalchuk, 2013; Deleris et al., 2016). Disruption processed by DICER-LIKE PROTEIN 3 (DCL3) into 24-nt siRNAs, of DNA methylation often results in inheritable developmental which are then loaded onto ARGONAUTE 4 (AGO4) proteins. The defects and reprograming of gene expression. As an important siRNA-AGO4 complex is recruited by another nascent noncoding aspect of epigenetic mechanisms, DNA methylation studies in RNA transcript P5RNA, a product of Pol V which is the other plant- China have made great strides not only in the elucidation of regu- specific RNA polymerase, via sequence complementary pairing. latory mechanisms but also in the discovery of DNA methylation- Finally, AGO4 interacts with DOMAINS REARRANGED METHYLASE based novel epigenetic phenomena. With the development of 2 (DRM2) to catalyze de novo DNA methylation (Cao et al., 2003; sequencing technology, more and more crop genomes have been Law and Jacobsen, 2010; Zhong et al., 2014). Pol IV and Pol V are sequenced, the majority of which are completed by Chinese sci- each composed of twelve subunits. He et al. from Dr. Jian-Kang entists, including grain crops like wheat (Jia et al., 2013; Ling et al., Zhu's group identified NRPD4/RNA-DIRECTED DNA METHYL- 2013, 2018), vegetables like Brassica rapa (Wang et al., 2011), cu- ATION 2 (RDM2), a subunit of Pol IV, as a new component in RdDM cumber (Cucumis sativus)(Huang et al., 2009), potato (Solanum pathway using an efficient forward genetic screen (He et al., 2009a). tuberosum)(Potato Genome Sequencing et al., 2011), Carica papaya In canonical RdDM model, how Pol IV is recruited to target loci is Linnaeus (Ming et al., 2008), fruit trees like pear (Pyrus bretsch- critical for the initiation of 24-nt siRNA biogenesis and downstream neideri)(Wu et al., 2013b), and some stress resistant crops like RdDM reactions. Zhang et al. (2013b) and Law et al. (2013) inde- quinoa (Zou et al., 2017). The elucidation of these crop genomes pendently reported that the heterochromatic mark H3K9me2 could helps to investigate their epigenomes. Up to now, high resolution be bound by DNABINDING TRANSCRIPTION FACTOR 1 (DTF1)/ DNA methylomes have been sequenced in multiple plant species in SAWADEE HOMEODOMAIN HOMOLOG 1 (SHH1), which directly China. These plants include food crops like maize (Zea mays) and interacts with the chromatin remodeling protein CLASSY 1 (CLSY1) potato (S. tuberosum), vegetables like tomato (S. lycopersicum) and and Pol IV in vivo, thereby assisting the recruitment of Pol IV to cucumber (C. sativus L.), fruit trees like apple (Malus x domestica), RdDM target loci. RDM4