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    The mechanism and function of active DNA demethylation in plants
    Ruie Liu and Zhaobo Lang
    J Integr Plant Biol 2020, 62 (1): 148-159.  
    doi: 10.1111/jipb.12879
    Abstract (Browse 1274)  |   Save

    DNA methylation is a conserved and important epigenetic mark in both mammals and plants. DNA methylation can be dynamically established, maintained, and removed through different pathways. In plants, active DNA demethylation is initiated by the RELEASE OF SILENCING 1 (ROS1) family of bifunctional DNA glycosylases/lyases. Accumulating evidence suggests that DNA demethylation is important in many processes in plants. In this review, we summarize recent studies on the enzymes and regulatory factors that have been identified in the DNA demethylation pathway. We also review the functions of active DNA demethylation in plant development as well as biotic and abiotic stress responses. Finally, we highlight those aspects of DNA demethylation that require additional research.

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    Genome editing for plant research and crop improvement
    Xiangqiang Zhan, Yuming Lu, Jian-Kang Zhu and Jose Ramon Botella
    J Integr Plant Biol 2021, 63 (1): 3-33.  
    doi: 10.1111/jipb.13063
    Abstract (Browse 779)  |   Save
    The advent of clustered regularly interspaced short palindromic repeat (CRISPR) has had a profound impact on plant biology, and crop improvement. In this review, we summarize the state‐of‐the‐art development of CRISPR technologies and their applications in plants, from the initial introduction of random small indel (insertion or deletion) mutations at target genomic loci to precision editing such as base editing, prime editing and gene targeting. We describe advances in the use of class 2, types II, V, and VI systems for gene disruption as well as for precise sequence alterations, gene transcription, and epigenome control.
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    A methylated-DNA-binding complex required for plant development mediates transcriptional activation of promoter methylated genes
    Qiang-Qiang Zhao, Rong-Nan Lin, Lin Li, She Chen and Xin-Jian He
    J Integr Plant Biol 2019, 61 (2): 120-139.  
    doi: 10.1111/jipb.12767
    Abstract (Browse 771)  |   Save
    Although the mechanism of DNA methylation-mediated gene silencing is extensively studied, relatively little is known about how promoter methylated genes are protected from transcriptional silencing. SUVH1, an Arabidopsis Su(var)3‐9 homolog, was previously shown to be required for the expression of a few promoter methylated genes. By chromatin immunoprecipitation combined with sequencing, we demonstrate that SUVH1 binds to methylated genomic loci targeted by RNA-directed DNA methylation. SUVH1 and its homolog SUVH3 function partially redundantly and interact with three DNAJ domain-containing homologs, SDJ1, SDJ2, and SDJ3, thus forming a complex which we named SUVH-SDJ. The SUVH-SDJ complex components are co-localized in a large number of methylated promoters and are required for the expression of a subset of promoter methylated genes. We demonstrate that the SUVH-SDJ complex components have transcriptional activation activity. SUVH1 and SUVH3 function synergistically with SDJ1, SDJ2, and SDJ3 and are required for plant viability. This study reveals how the SUVH-SDJ complex protects promoter methylated genes from transcriptional silencing and suggests that the transcriptional activation of promoter methylated genes mediated by the SUVH-SDJ complex may play a critical role in plant growth and development.
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    Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions
    Nai-Qian Dong and Hong-Xuan Lin
    J Integr Plant Biol 2021, 63 (1): 180-209.  
    doi: 10.1111/jipb.13054
    Abstract (Browse 739)  |   Save
    Phenylpropanoid metabolism is one of the most important metabolisms in plants, yielding more than 8,000 metabolites contributing to plant development and plant–environment interplay. Phenylpropanoid metabolism materialized during the evolution of early freshwater algae that were initiating terrestrialization and land plants have evolved multiple branches of this pathway, which give rise to metabolites including lignin, flavonoids, lignans, phenylpropanoid esters, hydroxycinnamic acid amides, and sporopollenin. Recent studies have revealed that many factors participate in the regulation of phenylpropanoid metabolism, and modulate phenylpropanoid homeostasis when plants undergo successive developmental processes and are subjected to stressful environments. In this review, we summarize recent progress on elucidating the contribution of phenylpropanoid metabolism to the coordination of plant development and plant–environment interaction, and metabolic flux redirection among diverse metabolic routes. In addition, our review focuses on the regulation of phenylpropanoid metabolism at the transcriptional, post‐transcriptional, post‐translational, and epigenetic levels, and in response to phytohormones and biotic and abiotic stresses.
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    Histone deacetylase HDA710 controls salt tolerance by regulating ABA signaling in rice
    Farhan Ullah, Qiutao Xu, Yu Zhao and Dao‐Xiu Zhou
    J Integr Plant Biol 2021, 63 (3): 451-467.  
    doi: 10.1111/jipb.13042
    Abstract (Browse 675)  |   Save
    Plants have evolved numerous mechanisms that assist them in withstanding environmental stresses. Histone deacetylases (HDACs) play crucial roles in plant stress responses; however, their regulatory mechanisms remain poorly understood. Here, we explored the function of HDA710/OsHDAC2, a member of the HDAC RPD3/HDA1 family, in stress tolerance in rice (Oryza sativa). We established that HDA710 localizes to both the nucleus and cytoplasm and is involved in regulating the acetylation of histone H3 and H4, specifically targeting H4K5 and H4K16 under normal conditions. HDA710 transcript accumulation levels were strongly induced by abiotic stresses including drought and salinity, as well as by the phytohormones jasmonic acid (JA) and abscisic acid (ABA). hda710 knockout mutant plants showed enhanced salinity tolerance and reduced ABA sensitivity, whereas transgenic plants overexpressing HDA710 displayed the opposite phenotypes. Moreover, ABA‐ and salt‐stress‐responsive genes, such as OsLEA3, OsABI5, OsbZIP72, and OsNHX1, were upregulated in hda710 compared with wild‐type plants. These expression differences corresponded with higher levels of histone H4 acetylation in gene promoter regions in hda710 compared with the wild type under ABA and salt‐stress treatment. Collectively, these results suggest that HDA710 is involved in regulating ABA‐ and salt‐stress‐responsive genes by altering H4 acetylation levels in their promoters.
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    Tissue‐specific Hi‐C analyses of rice, foxtail millet and maize suggest non‐canonical function of plant chromatin domains
    Pengfei Dong, Xiaoyu Tu, Haoxuan Li, Jianhua Zhang, Donald Grierson, Pinghua Li and Silin Zhong
    J Integr Plant Biol 2020, 62 (2): 201-217.  
    DOI: 10.1111/jipb.12809
    Abstract (Browse 576)  |   Save
    Chromatins are not randomly packaged in the nucleus and their organization plays important roles in transcription regulation, which is best studied in the mammalian models. Using in situ Hi-C, we have compared the 3D chromatin architectures of rice mesophyll and endosperm, foxtail millet bundle sheath and mesophyll, and maize bundle sheath, mesophyll and endosperm tissues. We found that their global A/B compartment partitions are stable across tissues, while local A/B compartment has tissue-specific dynamic associated with differential gene expression. Plant domains are largely stable across tissues, while new domain border formations are often associated with transcriptional activation in the region. Genes inside plant domains are not conserved across species, and lack significant co-expression behavior unlike those in mammalian TADs. Although we only observed chromatin loops between gene islands in the large genomes, the maize loop gene pairs’ syntenic orthologs have shorter physical distances in small genome monocots, suggesting that loops instead of domains might have conserved biological function. Our study showed that plants’ chromatin features might not have conserved biological functions as the mammalian ones.
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    A histone H3K27me3 reader cooperates with a family of PHD finger‐containing proteins to regulate flowering time in Arabidopsis
    Feng Qian, Qiu‐Yuan Zhao, Tie‐Nan Zhang, Yu‐Lu Li, Yin‐Na Su, Lin Li, Jian‐Hua Sui, She Chen and Xin‐Jian He
    J Integr Plant Biol 2021, 63 (4): 787-802.  
    DOI: 10.1111/jipb.13067
    Abstract (Browse 541)  |   Save
    Trimethylated histone H3 lysine 27 (H3K27me3) is a repressive histone marker that regulates a variety of developmental processes, including those that determine flowering time. However, relatively little is known about the mechanism of how H3K27me3 is recognized to regulate transcription. Here, we identified BAH domain‐containing transcriptional regulator 1 (BDT1) as an H3K27me3 reader. BDT1 is responsible for preventing flowering by suppressing the expression of flowering genes. Mutation of the H3K27me3 recognition sites in the BAH domain disrupted the binding of BDT1 to H3K27me3, leading to de‐repression of H3K27me3‐enriched flowering genes and an early‐flowering phenotype. We also found that BDT1 interacts with a family of PHD finger‐containing proteins, which we named PHD1–6, and with CPL2, a Pol II carboxyl terminal domain (CTD) phosphatase responsible for transcriptional repression. Pull‐down assays showed that the PHD finger‐containing proteins can enhance the binding of BDT1 to the H3K27me3 peptide. Mutations in all of the PHD genes caused increased expression of flowering genes and an early‐flowering phenotype. This study suggests that the binding of BDT1 to the H3K27me3 peptide, which is enhanced by PHD proteins, is critical for preventing early flowering.
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    RNA-directed DNA methylation has an important developmental function in Arabidopsis that is masked by the chromatin remodeler PICKLE
    Rong Yang, Li He, Huan Huang, Jian-Kang Zhu, Rosa Lozano-Duran and Heng Zhang
    J Integr Plant Biol 2020, 62 (11): 1647-1652.  
    doi: 10.1111/jipb.12979
    Abstract (Browse 480)  |   Save
    In Arabidopsis, RNA‐directed DNA methylation (RdDM) is required for the maintenance of CHH methylation, and for de novo methylation in all (CG, CHG, and CHH) contexts, but no obvious effect of RdDM deficiency on plant development has been found to date. We show that the combination of mutations in the chromatin remodeler PKL and RdDM components results in developmental alterations, which appear in a SUPPRESSOR OF DRM1 DRM2 CMT3 (SDC)‐dependent manner.
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    A group of SUVH methyl-DNA binding proteins regulate expression of the DNA demethylase ROS1 in Arabidopsis
    Xinlong Xiao, Jieqiong Zhang, Tao Li, Xing Fu, Viswanathan Satheesh, Qingfeng Niu, Zhaobo Lang, Jian-Kang Zhu and Mingguang Lei
    J Integr Plant Biol 2019, 61 (2): 110-119.  
    doi: 10.1111/jipb.12768
    Abstract (Browse 476)  |   Save
    DNA methylation is typically regarded as a repressive epigenetic marker for gene expression. Genome-wide DNA methylation patterns in plants are dynamically regulated by the opposing activities of DNA methylation and demethylation reactions. In Arabidopsis, a DNA methylation monitoring sequence (MEMS) in the promoter of the DNA demethylase gene ROS1 functions as a methylstat that senses these opposing activities and regulates genome DNA methylation levels by adjusting ROS1 expression. How DNA methylation in the MEMS region promotes ROS1 expression is not known. Here, we show that several Su(var)3‐9 homologs (SUVHs) can sense DNA methylation levels at the MEMS region and function redundantly to promote ROS1 expression. The SUVHs bind to the MEMS region, and the extent of binding is correlated with the methylation level of the MEMS. Mutations in the SUVHs lead to decreased ROS1 expression, causing DNA hypermethylation at more than 1,000 genomic regions. Thus, the SUVHs function to mediate the activation of gene transcription by DNA methylation.
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    The Class III peroxidase gene OsPrx30, transcriptionally modulated by the AT‐hook protein OsATH1, mediates rice bacterial blight‐induced ROS accumulation
    Hao Liu, Shuangyu Dong, Ming Li, Fengwei Gu, Guili Yang, Tao Guo, Zhiqiang Chen and Jiafeng Wang
    J Integr Plant Biol 2021, 63 (2): 393-408.  
    doi: 10.1111/jipb.13040
    Abstract (Browse 436)  |   Save
    Class III peroxidases (CIII Prxs) play critical roles in plant immunity by scavenging reactive oxygen species (ROS). However, the functions of CIII Prxs in rice (Oryza sativa L.) immunity are largely unexplored. Here, we report a Prx precursor, OsPrx30, that is responsive to the bacterial blight Xanthomonas oryzae pv. oryzae (Xoo). OsPrx30 was primarily expressed in rice roots, leaves, and stems, and its protein product was mainly localized at the endoplasmic reticulum. Overexpression of OsPrx30 enhanced the plant's susceptibility to Xoo by maintaining a high level of peroxidase (POD) activity and reducing the content of H2O2, whereas depletion of OsPrx30 had the opposite effects. Furthermore, we identified an AT‐hook transcription factor, OsATH1, that is specifically bound to the OsPrx30 promoter. As observed in plants overexpressing OsPrx30, depletion of OsATH1 enhanced susceptibility to Xoo. Finally, we demonstrated that depletion of OsATH1 increased histone H3 acetylation at the AT‐rich region of the OsPrx30 promoter. Taken together, these results reveal a mechanism underlying the POD‐induced natural resistance to bacterial diseases and suggest a model for transcription regulation of Prx genes in rice.
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    Chromatin remodeling factors regulate environmental stress responses in plants
    Ze‐Ting Song, Jian‐Xiang Liu and Jia‐Jia Han
    J Integr Plant Biol 2021, 63 (3): 438-450.  
    doi: 10.1111/jipb.13064
    Abstract (Browse 419)  |   Save
    Environmental stress from climate change and agricultural activity threatens global plant biodiversity as well as crop yield and quality. As sessile organisms, plants must maintain the integrity of their genomes and adjust gene expression to adapt to various environmental changes. In eukaryotes, nucleosomes are the basic unit of chromatin around which genomic DNA is packaged by condensation. To enable dynamic access to packaged DNA, eukaryotes have evolved Snf2 (sucrose nonfermenting 2) family proteins as chromatin remodeling factors (CHRs) that modulate the position of nucleosomes on chromatin. During plant stress responses, CHRs are recruited to specific genomic loci, where they regulate the distribution or composition of nucleosomes, which in turn alters the accessibility of these loci to general transcription or DNA damage repair machinery. Moreover, CHRs interplay with other epigenetic mechanisms, including DNA methylation, histone modifications, and deposition of histone variants. CHRs are also involved in RNA processing at the post‐transcriptional level. In this review, we discuss major advances in our understanding of the mechanisms by which CHRs function during plants’ response to environmental stress.
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    Synergistic regulation of drought-responsive genes by transcription factor OsbZIP23 and histone modification in rice
    Wei Zong, Jun Yang, Jie Fu and Lizhong Xiong
    J Integr Plant Biol 2020, 62 (6): 723-729.  
    doi: 10.1111/jipb.12850
    Abstract (Browse 407)  |   Save

    Thousands of differentially expressed genes (DEGs) have been identified in rice under drought stress conditions. However, the regulatory mechanism of these DEGs remains largely unclear. Here, we report an interplay between histone H3K4me3 modification and transcription factor OsbZIP23 in the regulation of a dehydrin gene cluster under drought stress conditions in rice. When the H3K4me3 modification level was increased, the dehydrin gene expression levels were increased, and the binding levels of OsbZIP23 to the promoter of the dehydrin genes were also enhanced. Conversely, the H3K4me3 modification and dehydrin gene expression levels were downregulated in the osbzip23 mutant under drought stress conditions. Our study uncovers a collaboration between transcription factor and H3K4me3 modification in the regulation of drought‐responsive genes, which will help us to further understand the gene regulation mechanism under stress conditions in plants.

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    Experiencing winter for spring flowering: A molecular epigenetic perspective on vernalization
    Xiao Luo and Yuehui He
    J Integr Plant Biol 2020, 62 (1): 104-117.  
    doi: 10.1111/jipb.12896
    Abstract (Browse 373)  |   Save

    Many over‐wintering plants, through vernalization, overcome a block to flowering and thus acquire competence to flower in the following spring after experiencing prolonged cold exposure or winter cold. The vernalization pathways in different angiosperm lineages appear to have convergently evolved to adapt to temperate climates. Molecular and epigenetic mechanisms for vernalization regulation have been well studied in the crucifer model plant Arabidopsis thaliana. Here, we review recent progresses on the vernalization pathway in Arabidopsis. In addition, we summarize current molecular and genetic understandings of vernalization regulation in temperate grasses including wheat and Brachypodium, two monocots from Pooideae, followed by a brief discussion on divergence of the vernalization pathways between Brassicaceae and Pooideae.

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    H3K36me2 is highly correlated with m6A modifications in plants
    Sangrea Shim, Hong Gil Lee, Hongwoo Lee, and Pil Joon Seo
    J Integr Plant Biol 2020, 62 (10): 1455-1460.  
    doi: 10.1111/jipb.12917
    Abstract (Browse 367)  |   Save

    The intimate linkage between H3K36me3 and m6A modifications has been demonstrated in mammals. In this issue, Shim et al. (2020) show that similar crosstalk between histone modification and mRNA methylation is conserved in plants, but H3K36me2 is more important for m6A deposition in plants.

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    SIZ1 negatively regulates aluminum resistance by mediating the STOP1–ALMT1 pathway in Arabidopsis
    Jiameng Xu, Jiayong Zhu, Jiajia Liu, Junxia Wang, Zhaojun Ding and Huiyu Tian
    J Integr Plant Biol 2021, 63 (6): 1147-1160.  
    DOI: 10.1111/jipb.13091
    Abstract (Browse 365)  |   Save
    Sensitive to proton rhizotoxicity 1 (STOP1) functions as a crucial regulator of root growth during aluminum (Al) stress. However, how this transcription factor is regulated by Al stress to affect downstream genes expression is not well understood. To explore the underlying mechanisms of the function and regulation of STOP1, we employed a yeast two hybrid screen to identify STOP1-interacting proteins. The SUMO E3 ligase SIZ1, was found to interact with STOP1 and mainly facilitate its SUMO modification at K40 and K212 residues. Simultaneous introduction of K40R and K212R substitutions in STOP1 enhances its transactivation activity to upregulate the expression of aluminum-activated malate transporter 1 (ALMT1) via increasing the association with mediator 16 (MED16) transcriptional co-activator. Loss of function of SIZ1 causes highly increased expression of ALMT1, thus enhancing Al-induced malate exudation and Al tolerance. Also, we found that the protein level of SIZ1 is reduced in response to Al stress. Genetic evidence demonstrates that STOP1/ALMT1 is epistatic to SIZ1 in regulating root growth response to Al stress. This study suggests a mechanism about how the SIZ1–STOP1–ALMT1 signaling module is involved in root growth response to Al stress.
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    A novel protein complex that regulates active DNA demethylation in Arabidopsis
    Pan Liu, Wen‐Feng Nie, Xiansong Xiong, Yuhua Wang, Yuwei Jiang, Pei Huang, Xueqiang Lin, Guochen Qin, Huan Huang, Qingfeng Niu, Jiamu Du, Zhaobo Lang, Rosa Lozano‐Duran and Jian‐Kang Zhu
    J Integr Plant Biol 2021, 63 (4): 772-786.  
    doi: 10.1111/jipb.13045
    Abstract (Browse 361)  |   Save
    Active DNA demethylation is critical for altering DNA methylation patterns and regulating gene expression. The 5‐methylcytosine DNA glycosylase/lyase ROS1 initiates a base‐excision repair pathway for active DNA demethylation and is required for the prevention of DNA hypermethylation at 1 000s of genomic regions in Arabidopsis. How ROS1 is regulated and targeted to specific genomic regions is not well understood. Here, we report the discovery of an Arabidopsis protein complex that contains ROS1, regulates ROS1 gene expression, and likely targets the ROS1 protein to specific genomic regions. ROS1 physically interacts with a WD40 domain protein (RWD40), which in turn interacts with a methyl‐DNA binding protein (RMB1) as well as with a zinc finger and homeobox domain protein (RHD1). RMB1 binds to DNA that is methylated in any sequence context, and this binding is necessary for its function in vivo. Loss‐of‐function mutations in RWD40, RMB1, or RHD1 cause DNA hypermethylation at several tested genomic regions independently of the known ROS1 regulator IDM1. Because the hypermethylated genomic regions include the DNA methylation monitoring sequence in the ROS1 promoter, plants mutated in RWD40, RMB1, or RHD1 show increased ROS1 expression. Importantly, ROS1 binding to the ROS1 promoter requires RWD40, RMB1, and RHD1, suggesting that this complex dictates ROS1 targeting to this locus. Our results demonstrate that ROS1 forms a protein complex with RWD40, RMB1, and RHD1, and that this novel complex regulates active DNA demethylation at several endogenous loci in Arabidopsis.
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    EXPORTIN 1A prevents transgene silencing in Arabidopsis by modulating nucleo-cytoplasmic partitioning of HDA6
    Guohui Zhu, Yanan Chang, Xuezhong Xu, Kai Tang, Chunxiang Chen, Mingguang Lei, Jian-Kang Zhu and Cheng-Guo Duan
    J Integr Plant Biol 2019, 61 (12): 1243-1254.  
    doi: 10.1111/jipb.12787
    Abstract (Browse 343)  |   Save
    In eukaryotic cells, transport of macromolecules across the nuclear envelope is an essential process that ensures rapid exchange of cellular components, including protein and RNA molecules. Chromatin regulators involved in epigenetic control are among the molecules exported across the nuclear envelope, but the significance of this nucleo‐cytoplasmic trafficking is not well understood. Here, we use a forward screen to isolate XPO1A (a nuclear export receptor in Arabidopsis) as an anti‐silencing factor that protects transgenes from transcriptional silencing. Loss‐of‐function of XPO1A leads to locus‐specific DNA hypermethylation at transgene promoters and some endogenous loci. We found that XPO1A directly interacts with histone deacetylase HDA6 in vivo and that the xpo1a mutation causes increased nuclear retention of HDA6 protein and results in reduced histone acetylation and enhanced transgene silencing. Our results reveal a new mechanism of epigenetic regulation through the modulation of XPO1A‐dependent nucleo‐cytoplasm partitioning of a chromatin regulator.
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    The E3 ligase XBAT35 mediates thermoresponsive hypocotyl growth by targeting ELF3 for degradation in Arabidopsis
    Lin‐Lin Zhang, Wei Li, Ying‐Ying Tian, Seth Jon Davis and Jian‐Xiang Liu
    J Integr Plant Biol 2021, 63 (6): 1097-1103.  
    doi: 10.1111/jipb.13107
    Abstract (Browse 334)  |   Save
    Plants are capable of coordination of their growth and development with ambient temperatures. EARLY FLOWERING3 (ELF3), an essential component of the plant circadian clock, is also involved in ambient temperature sensing, as well as in inhibiting the expression and protein activity of the thermoresponsive regulator phytochrome interacting factor 4 (PIF4). The ELF3 activity is subjected to attenuation in response to warm temperature; however, how the protein level of ELF3 is regulated at warm temperature remains less understood. Here, we report that the E3 ligase XB3 ORTHOLOG 5 IN ARABIDOPSIS THALIANA, XBAT35, mediates ELF3 degradation. XBAT35 interacts with ELF3 and ubiquitinates ELF3. Loss-of-function mutation of XBAT35 increases the protein level of ELF3 and confers a short-hypocotyl phenotype under warm temperature conditions. Thus, our findings establish that XBAT35 mediates ELF3 degradation to lift the inhibition of ELF3 on PIF4 for promoting thermoresponsive hypocotyl growth in plants.
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    N4‐methylcytidine ribosomal RNA methylation in chloroplasts is crucial for chloroplast function, development, and abscisic acid response in Arabidopsis
    Le Nguyen Tieu Ngoc, Su Jung Park, Trinh Thi Huong, Kwang Ho Lee and Hunseung Kang
    J Integr Plant Biol 2021, 63 (3): 570-582.  
    doi: 10.1111/jipb.13009
    Abstract (Browse 309)  |   Save
    Although the essential role of messenger RNA methylation in the nucleus is increasingly understood, the nature of ribosomal RNA (rRNA) methyltransferases and the role of rRNA methylation in chloroplasts remain largely unknown. A recent study revealed that CMAL (for Chloroplast mr aW‐ Like) is a chloroplast‐localized rRNA methyltransferase that is responsible for N4‐methylcytidine (m4C) in 16S chloroplast rRNA in Arabidopsis thaliana. In this study, we further examined the role of CMAL in chloroplast biogenesis and function, development, and hormone response. The cmal mutant showed reduced chlorophyll biosynthesis, photosynthetic activity, and growth‐defect phenotypes, including severely stunted stems, fewer siliques, and lower seed yield. The cmal mutant was hypersensitive to chloroplast translation inhibitors, such as lincomycin and erythromycin, indicating that the m4C‐methylation defect in the 16S rRNA leads to a reduced translational activity in chloroplasts. Importantly, the stunted stem of the cmal mutant was partially rescued by exogenous gibberellic acid or auxin. The cmal mutant grew poorer than wild type, whereas the CMAL‐overexpressing transgenic Arabidopsis plants grew better than wild type in the presence of abscisic acid. Altogether, these results indicate that CMAL is an indispensable rRNA methyltransferase in chloroplasts and is crucial for chloroplast biogenesis and function, photosynthesis, and hormone response during plant growth and development.
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    Roles of DEMETER in regulating DNA methylation in vegetative tissues and pathogen resistance
    Wenjie Zeng, Huan Huang, Xueqiang Lin, Chen Zhu, Ken‐ichi Kosami, Chaofeng Huang, Huiming Zhang, Cheng‐Guo Duan, Jian‐Kang Zhu and Daisuke Miki
    J Integr Plant Biol 2021, 63 (4): 691-706.  
    doi: 10.1111/jipb.13037
    Abstract (Browse 299)  |   Save
    DNA methylation is an epigenetic mark important for genome stability and gene expression. In Arabidopsis thaliana, the 5‐methylcytosine DNA glycosylase/demethylase DEMETER (DME) controls active DNA demethylation during the reproductive stage; however, the lethality of loss‐of‐function dme mutations has made it difficult to assess DME function in vegetative tissues. Here, we edited DME using clustered regularly interspaced short palindromic repeats (CRISPR) /CRISPR‐associated protein 9 and created three weak dme mutants that produced a few viable seeds. We also performed central cell‐specific complementation in a strong dme mutant and combined this line with mutations in the other three Arabidopsis demethylase genes to generate the dme ros1 dml2 dml3 (drdd) quadruple mutant. A DNA methylome analysis showed that DME is required for DNA demethylation at hundreds of genomic regions in vegetative tissues. A transcriptome analysis of the drdd mutant revealed that DME and the other three demethylases are important for plant responses to biotic and abiotic stresses in vegetative tissues. Despite the limited role of DME in regulating DNA methylation in vegetative tissues, the dme mutants showed increased susceptibility to bacterial and fungal pathogens. Our study highlights the important functions of DME in vegetative tissues and provides valuable genetic tools for future investigations of DNA demethylation in plants.
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    The CBP/p300 histone acetyltransferases function as plant‐specific MEDIATOR subunits in Arabidopsis
    Jing Guo, Long Wei, Shan‐Shan Chen, Xue‐Wei Cai, Yin‐Na Su, Lin Li, She Chen and Xin‐Jian He
    J Integr Plant Biol 2021, 63 (4): 755-771.  
    DOI: 10.1111/jipb.13052
    Abstract (Browse 289)  |   Save
    In eukaryotes, MEDIATOR is a conserved multi‐subunit complex that links transcription factors and RNA polymerase II and that thereby facilitates transcriptional initiation. Although the composition of MEDIATOR has been well studied in yeast and mammals, relatively little is known about the composition of MEDIATOR in plants. By affinity purification followed by mass spectrometry, we identified 28 conserved MEDIATOR subunits in Arabidopsis thaliana, including putative MEDIATOR subunits that were not previously validated. Our results indicated that MED34, MED35, MED36, and MED37 are not Arabidopsis MEDIATOR subunits, as previously proposed. Our results also revealed that two homologous CBP/p300 histone acetyltransferases, HAC1 and HAC5 (HAC1/5) are in fact plant‐specific MEDIATOR subunits. The MEDIATOR subunits MED8 and MED25 (MED8/25) are partially responsible for the association of MEDIATOR with HAC1/5, MED8/25 and HAC1/5 co‐regulate gene expression and thereby affect flowering time and floral development. Our in vitro observations indicated that MED8 and HAC1 form liquid‐like droplets by phase separation, and our in vivo observations indicated that these droplets co‐localize in the nuclear bodies at a subset of nuclei. The formation of liquid‐like droplets is required for MED8 to interact with RNA polymerase II. In summary, we have identified all of the components of Arabidopsis MEDIATOR and revealed the mechanism underlying the link of histone acetylation and transcriptional regulation.
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    Critical function of DNA methyltransferase 1 in tomato development and regulation of the DNA methylome and transcriptome
    Yu Yang, Kai Tang, Tatsiana U Datsenka, Wenshan Liu, Suhui Lv, Zhaobo Lang, Xingang Wang, Jinghui Gao, Wei Wang, Wenfeng Nie, Zhaoqing Chu, Heng Zhang, Avtar K Handa, Jian-Kang Zhu and Huiming Zhang
    J Integr Plant Biol 2019, 61 (12): 1224-1242.  
    DOI: 10.1111/jipb.12778
    Abstract (Browse 283)  |   Save
    DNA methylation confers epigenetic regulation on gene expression and thereby on various biological processes. Tomato has emerged as an excellent system to study the function of DNA methylation in plant development. To date, regulation and function of DNA methylation maintenance remains unclear in tomato plants. Here, we report the critical function of tomato (Solanum lycopersicum) Methyltransferase 1 (SlMET1) in plant development and DNA methylome and transcriptome regulation. Using CRISPR‐Cas9 gene editing, we generated slmet1 mutants and observed severe developmental defects with a frame‐shift mutation, including small and curly leaves, defective inflorescence, and parthenocarpy. In leaf tissues, mutations in SlMET1 caused CG hypomethylation and CHH hypermethylation on a whole‐genome scale, leading to a disturbed transcriptome including ectopic expression of many RIN target genes such as ACC2 in leaf tissues, which are normally expressed in fruits. Neither the CG hypomethylation nor CHH hypermethylation in the slmet1 mutants is related to tissue culture. Meanwhile, tissue culture induces non‐CG hypomethylation, which occurs more frequently at gene regions than at TE regions. Our results depict SlMET1‐ and tissue culture‐dependent tomato DNA methylomes, and that SlMET1 is required for maintaining a normal transcriptome and normal development of tomato.
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    Recognition of H3K9me1 by maize RNA-directed DNA methylation factor SHH2
    Yuhua Wang, Xuelin Zhou, Jinyan Luo, Suhui Lv, Rui Liu, Xuan Du, Bei Jia, Fengtong Yuan, Heng Zhang and Jiamu Du
    J Integr Plant Biol 2021, 63 (6): 1091-1096.  
    doi: 10.1111/jipb.13103
    Abstract (Browse 269)  |   Save
    RNA-directed DNA methylation (RdDM) is a plant-specific de novo DNA methylation pathway, which has extensive cross-talk with histone modifications. Here, we report that the maize RdDM regulator SAWADEE HOMEODOMAIN HOMOLOG 2 (SHH2) is an H3K9me1 reader. Our structural studies reveal that H3K9me1 recognition is achieved by recognition of the methyl group via a classic aromatic cage and hydrogen-bonding and salt-bridge interactions with the free protons of the mono-methyllysine. The di- and tri-methylation states disrupt the polar interactions, decreasing the binding affinity. Our study reveals a mono-methyllysine recognition mechanism which potentially links RdDM to H3K9me1 in maize.
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    Decrease in DNA methylation 1 (DDM1) is required for the formation of mCHH islands in maize
    Jin Cheng Long, Ai Ai Xia, Jing Han Liu, Ju Li Jing, Ya Zhong Wang, Chuang Ye Qi and Yan He
    J Integr Plant Biol 2019, 61 (6): 749-764.  
    doi: 10.1111/jipb.12733
    Abstract (Browse 268)  |   Save
    DNA methylation plays a crucial role in suppressing mobilization of transposable elements and regulation of gene expression. A number of studies have indicated that DNA methylation pathways and patterns exhibit distinct properties in different species, including Arabidopsis, rice, and maize. Here, we characterized the function of DDM1 in regulating genome-wide DNA methylation in maize. Two homologs of ZmDDM1 are abundantly expressed in the embryo and their simultaneous disruption caused embryo lethality with abnormalities in cell proliferation from the early stage of kernel development. We establish that ZmDDM1 is critical for DNA methylation, at CHG sites, and to a lesser extent at CG sites, in heterochromatic regions, and unexpectedly, it is required for the formation of mCHH islands. In addition, ZmDDM1 is indispensable for the presence of 24-nt siRNA, suggesting its involvement in the RdDM pathway. Our results provide novel insight into the role of ZmDDM1 in regulating the formation of mCHH islands, via the RdDM pathway maize, suggesting that, in comparison to Arabidopsis, maize may have adopted distinct mechanisms for regulating mCHH.
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    Phytochrome B interacts with SWC6 and ARP6 to regulate H2A.Z deposition and photomorphogensis in Arabidopsis
    Xuxu Wei, Wanting Wang, Peng Xu, Wenxiu Wang, Tongtong Guo, Shuang Kou, Minqing Liu, Yake Niu, Hong‐Quan Yang and Zhilei Mao
    J Integr Plant Biol 2021, 63 (6): 1133-1146.  
    DOI: 10.1111/jipb.13111
    Abstract (Browse 268)  |   Save
    Light serves as a crucial environmental cue which modulates plant growth and development, and which is controlled by multiple photoreceptors including the primary red light photoreceptor, phytochrome B (phyB). The signaling mechanism of phyB involves direct interactions with a group of basic helix-loop-helix (bHLH) transcription factors, PHYTOCHROME-INTERACTING FACTORS (PIFs), and the negative regulators of photomorphogenesis, COP1 and SPAs. H2A.Z is an evolutionarily conserved H2A variant which plays essential roles in transcriptional regulation. The replacement of H2A with H2A.Z is catalyzed by the SWR1 complex. Here, we show that the Pfr form of phyB physically interacts with the SWR1 complex subunits SWC6 and ARP6. phyB and ARP6 co-regulate numerous genes in the same direction, some of which are associated with auxin biosynthesis and response including YUC9, which encodes a rate-limiting enzyme in the tryptophan-dependent auxin biosynthesis pathway. Moreover, phyB and HY5/HYH act to inhibit hypocotyl elongation partially through repression of auxin biosynthesis. Based on our findings and previous studies, we propose that phyB promotes H2A.Z deposition at YUC9 to inhibit its expression through direct phyB-SWC6/ARP6 interactions, leading to repression of auxin biosynthesis, and thus inhibition of hypocotyl elongation in red light.
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    A domesticated Harbinger transposase forms a complex with HDA6 and promotes histone H3 deacetylation at genes but not TEs in Arabidopsis
    Xishi Zhou, Junna He, Christos N. Velanis, Yiwang Zhu, Yuhan He, Kai Tang, Mingku Zhu, Lisa Graser, Erica deLeau, Xingang Wang, Lingrui Zhang, W. Andy Tao, Justin Goodrich, Jian‐Kang Zhu and Cui‐Jun Zhang
    J Integr Plant Biol 2021, 63 (8): 1462-1474.  
    doi: 10.1111/jipb.13108
    Abstract (Browse 267)  |   Save
    In eukaryotes, histone acetylation is a major modification on histone N-terminal tails that is tightly connected to transcriptional activation. HDA6 is a histone deacetylase involved in the transcriptional regulation of genes and transposable elements (TEs) in Arabidopsis thaliana. HDA6 has been shown to participate in several complexes in plants, including a conserved SIN3 complex. Here, we uncover a novel protein complex containing HDA6, several Harbinger transposon-derived proteins (HHP1, SANT1, SANT2, SANT3, and SANT4), and MBD domain-containing proteins (MBD1, MBD2, and MBD4). We show that mutations of all four SANT genes in the sant-null mutant cause increased expression of the flowering repressors FLC, MAF4, and MAF5, resulting in a late flowering phenotype. Transcriptome deep sequencing reveals that while the SANT proteins and HDA6 regulate the expression of largely overlapping sets of genes, TE silencing is unaffected in sant-null mutants. Our global histone H3 acetylation profiling shows that SANT proteins and HDA6 modulate gene expression through deacetylation. Collectively, our findings suggest that Harbinger transposon-derived SANT domain-containing proteins are required for histone deacetylation and flowering time control in plants.
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    Cytosine methylation of the FWA promoter promotes direct in vitro shoot regeneration in Arabidopsis thaliana
    Xuehuan Dai, Jing Wang, Yuguang Song, Zhenhua Liu, Tao Xue, Meng Qiao, Yanchong Yu, Wei Xin and Fengning Xiang
    J Integr Plant Biol 2021, 63 (8): 1491-1504.  
    doi: 10.1111/jipb.13156
    Abstract (Browse 238)  |   Save
    Epigenetic modifications within promoter sequences can act as regulators of gene expression. Shoot regeneration is influenced by both DNA methylation and histone methylation, but the mechanistic basis of this regulation is obscure. Here, we identified 218 genes related to the regeneration capacity of callus that were differentially transcribed between regenerable calli (RC) and non-regenerable calli (NRC) in Arabidopsis thaliana. An analysis of the promoters of five of the differentially expressed genes (FWA, ACC1, TFL1, MAX3, and GRP3) pointed to an inverse relationship between cytosine methylation and transcription. The FWA promoter was demethylated and highly expressed in NRC, whereas it was methylated and expressed at low levels in RC. Explants of the hypomethylation mutants fwa-1 and fwa-2 showed strong levels of FWA expression and regenerated less readily than the wild type, suggesting that FWA inhibits direct in vitro shoot regeneration. WUSCHEL-RELATED HOMEOBOX 9 (WOX9), which is required for shoot apical meristem formation, was directly repressed by FWA. Overexpressing WOX9 partly rescued the shoot regeneration defect of fwa-2 plants. These findings suggest that cytosine methylation of the FWA promoter forms part of the regulatory system governing callus regenerability and direct in vitro shoot regeneration.
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    NF-YCs modulate histone variant H2A.Z deposition to regulate photomorphogenic growth in Arabidopsis
    Chunyu Zhang, Qian Qian, Xiang Huang, Wenbin Zhang, Xu Liu and Xingliang Hou
    J Integr Plant Biol 2021, 63 (6): 1120-1132.  
    DOI: 10.1111/jipb.13109
    Abstract (Browse 214)  |   Save
    In plants, light signals trigger a photomorphogenic program involving transcriptome changes, epigenetic regulation, and inhibited hypocotyl elongation. The evolutionarily conserved histone variant H2A.Z, which functions in transcriptional regulation, is deposited in chromatin by the SWI2/SNF2-RELATED 1 complex (SWR1c). However, the role of H2A.Z in photomorphogenesis and its deposition mechanism remain unclear. Here, we show that in Arabidopsis thaliana, H2A.Z deposition at its target loci is induced by light irradiation via NUCLEAR FACTOR-Y, subunit C (NF-YC) proteins, thereby inhibiting photomorphogenic growth. NF-YCs physically interact with ACTIN-RELATED PROTEIN6 (ARP6), a key component of the SWR1c that is essential for depositing H2A.Z, in a light-dependent manner. NF-YCs and ARP6 function together as negative regulators of hypocotyl growth by depositing H2A.Z at their target genes during photomorphogenesis. Our findings reveal an important role for the histone variant H2A.Z in photomorphogenic growth and provide insights into a novel transcription regulatory node that mediates H2A.Z deposition to control plant growth in response to changing light conditions.
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    Genome‐wide distribution and functions of the AAE complex in epigenetic regulation in Arabidopsis
    Yi‐Zhe Zhang, Juncheng Lin, Zhizhong Ren, Chun‐Xiang Chen, Daisuke Miki, Si‐Si Xie, Jian Zhang, Ya‐Nan Chang, Jing Jiang, Jun Yan, Qingshun Q. Li, Jian‐Kang Zhu and Cheng‐Guo Duan
    J Integr Plant Biol 2021, 63 (4): 707-722.  
    DOI: 10.1111/jipb.13068
    Abstract (Browse 205)  |   Save
    Heterochromatin is widespread in eukaryotic genomes and has diverse impacts depending on its genomic context. Previous studies have shown that a protein complex, the ASI1‐AIPP1‐EDM2 (AAE) complex, participates in polyadenylation regulation of several intronic heterochromatin‐containing genes. However, the genome‐wide functions of AAE are still unknown. Here, we show that the ASI1 and EDM2 mostly target the common genomic regions on a genome‐wide level and preferentially interacts with genetic heterochromatin. Polyadenylation (poly(A) sequencing reveals that AAE complex has a substantial influence on poly(A) site usage of heterochromatin‐containing genes, including not only intronic heterochromatin‐containing genes but also the genes showing overlap with heterochromatin. Intriguingly, AAE is also involved in the alternative splicing regulation of a number of heterochromatin‐overlapping genes, such as the disease resistance gene RPP4. We provided evidence that genic heterochromatin is indispensable for the recruitment of AAE in polyadenylation and splicing regulation. In addition to conferring RNA processing regulation at genic heterochromatin‐containing genes, AAE also targets some transposable elements (TEs) outside of genes (including TEs sandwiched by genes and island TEs) for epigenetic silencing. Our results reveal new functions of AAE in RNA processing and epigenetic silencing, and thus represent important advances in epigenetic regulation.
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