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Arabidopsis Trithorax histone methyltransferases are redundant in regulating development and DNA methylation

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Journal of Integrative Plant Biology 2022年第12期64卷 2438-2454页

作者： Ji-Yun Shang Xue-Wei Cai Yin-Na Su Zhao-Chen Zhang xin Wang Nan Zhao xin-jian he National Institute of Biological Sciences Beijing 102206China Tsinghua Institute of Multidisciplinary Biomedical Research Tsinghua UniversityBeijing 100084China

Although the Trithorax histone methyltransferases ATX1-5 are known to regulate development and stress responses by catalyzing histone H3 K4 methylation in Arabidopsis thaliana,it is unknown whether and how these histone methyltransferases affect DNA methylation.here,we found that the redundant ATX1-5 proteins are not only required for plant development and viability but also for the regulation of DNA methylation.The expression and H3 K4 me3 levels of both RNAdirected DNA methylation(RdDM)genes(NRPE1,DCL3,IDN2,and IDP2)and active DNA demethylation genes(ROS1,DML2,and DML3)were downregulated in the atx1/2/4/5 mutant.Consistent with the facts that the active DNA demethylation pathway mediates DNA demethylation mainly at CG and CHG sites,and that the RdDM pathway mediates DNA methylation mainly at CHH sites,whole-genome DNA methylation analyses showed that hyper-CG and CHG DMRs in atx1/2/4/5 significantly overlapped with those in the DNA demethylation pathway mutant ros1 dml2 dml3(rdd),and that hypo-CHH DMRs in atx1/2/4/5 significantly overlapped with those in the RdDM mutant nrpe1,suggesting that the ATX paralogues function redundantly to regulate DNA methylation by promoting H3 K4 me3 levels and expression levels of both RdDM genes and active DNA demethylation genes.Given that the ATX proteins function as catalytic subunits of COMPASS histone methyltransferase complexes,we also demonstrated that the COMPASS complex components function as a whole to regulate DNA methylation.This study reveals a previously uncharacterized mechanism underlying the regulation of DNA methylation.

关键词： development DNA demethylation DNA methylation histone methylation NRPE1 ROS1

The Arabidopsis NuA4 histone acetyltransferase complex is required for chlorophyll biosynthesis and photosynthesis

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Journal of Integrative Plant Biology 2022年第4期64卷 901-914页

作者： Jin-xing Zhou Xiao-Min Su Si-Yao Zheng Chan-Juan Wu Yin-Na Su Zhaodi jiang Lin Li She Chen xin-jian he College of Life Sciences Beijing Normal UniversityBeijing 100091China National Institute of Biological Sciences Beijing 102206China Tsinghua Institute of Multidisciplinary Biomedical Research Tsinghua UniversityBeijing 100084China

Although two Enhancer of Polycomb-like proteins,EPL1 A and EPL1 B(EPL1 A/B),are known to be conserved and characteristic subunits of the Nu A4-type histone acetyltransferase complex in Arabidopsis thaliana,the biological function of EPL1 A/B and the mechanism by which EPL1 A/B function in the complex remain unknown.here,we report that EPL1 A/B are required for the histone acetyltransferase activity of the Nu A4 complex on the nucleosomal histone H4 in vitro and for the enrichment of histone H4 K5 acetylation at thousands of protein-coding genes in vivo.Our results suggest that EPL1 A/B are required for linking the Nu A4 catalytic subunits HISTONE ACETYLTRANSFERASE OF The MYST FAMILY 1(HAM1)and HAM2 with accessory subunits in the Nu A4 complex.EPL1 A/B function redundantly in regulating plant development especially in chlorophyll biosynthesis and de-etiolation.The EPL1 A/B-dependent transcription and H4 K5 Ac are enriched at genes involved in chlorophyll biosynthesis and photosynthesis.We also find that EAF6,another characteristic subunit of the Nu A4 complex,contributes to de-etiolation.These results suggest that the Arabidopsis Nu A4 complex components function as a whole to mediate histone acetylation and transcriptional activation specifically at light-responsive genes and are critical for photomorphogenesis.

关键词： chlorophyll EPL1A HAM1 histone acetyltransferase NuA4 photosynthesis transcription

Dual roles of the Arabidopsis PEAT complex in histone H2A deubiquitination and H4K5 acetylation

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Molecular Plant 2023年第11期16卷 1847-1865页

作者： Si-Yao Zheng Bin-Bin Guan Dan-Yang Yuan Qiang-Qiang Zhao Weiran Ge Lian-Mei Tan Shan-Shan Chen Lin Li She Chen Rui-Ming Xu xin-jian he College of Life Sciences Beijing Normal UniversityBeijingChina National Institute of Biological Sciences BejingChina National Laboratory of Biomacromolecules Institute of BiophysicsChinese Academy of SciencesBeijingChina School of Life Sciences University of Chinese Academy of SciencesBeijingChina Tsinghua Institute of Multidisciplinary Biomedical Research Tsinghua UniversityBeilingChina

Histone H2A monoubiquitination is associated with transcriptional repression and needs to be removed by deubiquitinases to facilitate gene transcription in eukaryotes.However,the deubiquitinase responsible for genome-wide H2A deubiquitination in plants has yet to be identified.In this study,we found that the previously identified PWWP-EPCR-ARID-TRB(PEAT)complex components interact with both the ubiquitin-specific protease UBP5 and the redundant histone acetyltransferases HAM1 and HAM2(HAM1/2)to form a larger version of PEAT complex in Arabidopsis thaliana.UBP5 functions as an H2A deubiquitinase in a nucleosome substrate-dependent manner in vitro and mediates H2A deubiquitination at the whole-genome level in vivo.HAM1/2 are shared subunits of the PEAT complex and the conserved NuA4 histone acetyltransferase com-plex,and are responsible for histone H4K5 acetylation.Within the PEAT complex,the PWWP components(PWWP1,PWWP2,and PWWP3)directly interact with UBP5 and are necessary for UBP5-mediated H2A deu-biquitination,while the EPCR components(EPCR1 and EPCR2)directly interact with HAM1/2 and are required for HAM1/2-mediated H4K5acetylation.Collectively,our study not onlyidentifies dual roles of thePEAT com-plex in H2A deubiquitination and H4K5 acetylation but also illustrates how these processes collaborate at the whole-genome level to regulate the transcription and development in plants.

关键词： histone H2A deubiquitination H4K5 acetylation UBP5 HAM1 NuA4 PEAT

A methylated-DNA-binding complex required for plant development mediates transcriptional activation of promoter methylated genes

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Journal of Integrative Plant Biology 2019年第2期61卷 120-139页

作者： Qiang-Qiang Zhao Rong-Nan Lin Lin Li She Chen xin-jian he National Institute of Biological Sciences Graduate School of Peking Union Medical College

Although the mechanism of DNA methylationmediated 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 SUVHSDJ 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.

关键词： A methylated-DNA-binding complex required for plant development mediates transcriptional activation of promoter methylated genes Figure DNA

Arabidopsis RPD3-like histone deacetylases form multiple complexes involved in stress response

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Journal of Genetics and Genomics 2021年第5期48卷 369-383页

作者： Chao Feng Xue-Wei Cai Yin-Na Su Lin Li She Chen xin-jian he College of Life Sciences Beijing Normal UniversityBeijing 100875China National Institute of Biological Sciences Beijing 102206China Tsinghua Institute of Multidisciplinary Biomedical Research Tsinghua UniversityBeijing 10084China

The Arabidopsis thaliana RPD3-type histone deacetylases have been known to form conserved SIN3-type histone deacetylase complexes,but whether they form other types of complexes is unknown.here,we perform affinity purification followed by mass spectrometry and demonstrate that the Arabidopsis RPD3-type histone deacetylases HDA6 and HDA19 interact with several previously uncharacterized proteins,thereby forming three types of plant-specific histone deacetylase complexes,which we named SANT,ESANT,and ARID.RNA-seq indicates that the newly identified components function together with HDA6 and HDA19 and coregulate the expression of a number of genes.HDA6 and HDA19 were previously thought to repress gene transcription by histone deacetylation.We find that the histone deacetylase complexes can repress gene expression via both histone deacetylation-dependent and-independent mechanisms.In the mutants of histone deacetylase complexes,the expression of a number of stressinduced genes is up-regulated,and several mutants of the histone deacetylase complexes show severe retardation in growth.Considering that growth retardation is thought to be a trade-off for an increase in stress tolerance,we infer that the histone deacetylase complexes identified in this study prevent overexpression of stress-induced genes and thereby ensure normal growth of plants under nonstress conditions.

关键词： Histone deacetylase Complex Transcription Development Stress response HDA6 HDA19

A histone H3K27me3 reader cooperates with a family of PHD finger-containing proteins to regulate flowering time in Arabidopsis

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Journal of Integrative Plant Biology 2021年第4期63卷 787-801页

作者： Feng Qian Qiu-Yuan Zhao Tie-Nan Zhang Yu-Lu Li Yin-Na Su Lin Li jian-Hua Sui She Chen xin-jian he National Institute of Biological Sciences Beijing 102206China Tsinghua Institute of Multidisciplinary Biomedical Research Tsinghua UniversityBeijing 100084China

Trimethylated histone H3 lysine 27(H3 K27 me3)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 H3 K27 me3 is recognized to regulate transcription.here,we identified BAH domain-containing transcriptional regulator 1(BDT1)as an H3 K27 me3 reader.BDT1 is responsible for preventing flowering by suppressing the expression of flowering genes.Mutation of the H3 K27 me3 recognition sites in the BAH domain disrupted the binding of BDT1 to H3 K27 me3,leading to de-repression of H3 K27 me3-enriched flowering genes and an earlyflowering 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 H3 K27 me3 peptide.Mutations in all of the PHD genes caused increased expression of flowering genes and an earlyflowering phenotype.This study suggests that the binding of BDT1 to the H3 K27 me3 peptide,which is enhanced by PHD proteins,is critical for preventing early flowering.

关键词： BAH development flowering histone H3K27me3 PHD transcriptional repression

The Splicing Factor PRP31 Is Involved in Transcriptional Gene Silencing and Stress Response in Arabidopsis

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Molecular Plant 2015年第7期8卷 1053-1068页

作者： Jin-Lu Du Su-Wei Zhang Huan-Wei Huang Tao Cai Lin Li She Chen xin-jian he College of Life Sciences Beijing Normal University Beijing 100875 China National Institute of Biological Sciences Beijing 102206 China

Although DNA methylation is known to play an important role in the silencing of transposable elements （TEs） and introduced transgenes, the mechanisms that generate DNA methylation-independent transcrip- tional silencing are poorly understood. Previous studies suggest that RNA-directed DNA methylation （RdDM） is required for the silencing of the RD29A-LUC transgene in the Arabidopsis rosl mutant back- ground with defective DNA demethylase. Loss of function of ARGONAUTE 4 （AGO4） gene, which encodes a core RdDM component, partially released the silencing of RD29A-LUC in the rosl/ago4 double mutant plants. A forward genetic screen was performed to identify the mutants with elevated RD29A-LUC trans- gene expression in the rosl/ago4 mutant background. We identified a mutation in the homologous gene of PRP31, which encodes a conserved pre-mRNA splicing factor that regulates the formation of the U4/ U6.U5 snRNP complex in fungi and animals. We previously demonstrated that the splicing factors ZOP1 and STA1 contribute to transcriptional gene silencing. here, we reveal that Arabidopsis PRP31 associates with ZOP1, STA1, and several other splicing-related proteins, suggesting that these splicing factors are both physically and functionally connected. We show that Arabidopsis PRP31 participates in transcrip- tional gene silencing. Moreover, we report that PRP31, STA1, and ZOP1 are required for development and stress response. Under cold stress, PRP31 is not only necessary for pre-mRNA splicing but also for regulation of cold-responsive gene expression. Our results suggest that the splicing machinery has multiple functions including pre-mRNA splicing, gene regulation, transcriptional gene silencing, and stress response.

关键词： PRP31 splicing factor DNA methylation transcriptional gene silencing stress response

FHA2 is a plant-specific ISWI subunit responsible for stamen development and plant fertility^FA

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Journal of Integrative Plant Biology 2020年第11期62卷 1703-1716页

作者： Bo-Wen Gu Lian-Mei Tan Cui-Jun Zhang Xiao-Mei Hou Xue-Wei Cai She Chen xin-jian he College of Life Sciences Beijing Normal UniversityBeijing 100875China National Institute of Biological Sciences Beijing 102206China Tsinghu a Institute of Multidisciplinary Biom edical Research Tsinghua UniversityBeijing 10084China

Imitation Switch(ISWI)chromatin remodelers are known to function in diverse multi-subunit complexes in yeast and animals.However,the constitution and function of ISWI complexes in Arabidopsis thaliana remain unclear.In this study,we identified forkheadassociated domain 2(FHA2)as a plant-specific subunit of an ISWI chromatin-remodeling complex in Arabidopsis.By in vivo and in vitro analyses,we demonstrated that FHA2 directly binds to RLT1 and RLT2,two redundant subunits of the ISWI complex in Arabidopsis.The stamen filament is shorter in the fha2 and rlti/2 mutants than in the wild type,whereas their pistil lengths are comparable.The shorter filament,which is due to reduced cell size,results in insufficient pollination and reduced fertility.The rlt1/2 mutant shows an early-floweringphenotype,whereas the phenotype is not shared bythe fha2 mutant.Consistent with the functional specif-icity of FHA2,our RNA-seq analysis indicated that thefha2 mutant affects a subset of RLT1/2-regulated genesthat does not include genes involved in the regulation offlowering time.This study demonstrates that FHA2functions as a previously uncharacterized subunit of theArabidopsis ISwI complex and is exclusively involved inregulating stamen development and plant fertility.

关键词： plant Arabidopsis shorter

The CBP/p300 histone acetyltransferases function as plant-specific MEDIATOR subunits in Arabidopsis

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Journal of Integrative Plant Biology 2021年第4期63卷 755-771页

作者： Jing Guo Long Wei Shan-Shan Chen Xue-Wei Cai Yin-Na Su Lin Li She Chen xin-jian he National Institute of Biological Sciences Beijing 102206China Graduate School of Peking Union Medical College Beijing 100730China Tsinghua Institute of Multidisciplinary Biomedical Research Tsinghua UniversityBeijing 100084China

In eukaryotes,MEDIATOR is a conserved multisubunit 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.

关键词： complex development flowering time histone acetylation MEDIATOR phase separation transcription