Histone tales: lysine methylation, a protagonist in Arabidopsis development

Cheng, Kai; Yang, Xu; Yang, Chao; Ouellette, Luc; Niu, Longjian; Zhou, Xiaochen; Chu, Liutian; Zhuang, Feng; Jin, Liu; Wu, Hualing; Charron, Jean‐Benoît; Luo, Ming

doi:10.1093/jxb/erz435

Cited by 56 publications

(69 citation statements)

References 155 publications

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“…Taken together, these results indicate that ATX1-drived H3K4me3 methylation of NST1 and SND1 is involved in the dynamic regulation of the secondary wall synthesis during Arabidopsis stem development. Our findings extend the knowledge about epigenetic regulation of reprogramming of chromatin modification states associated with cell differentiation in plant organ development ( 69–71 ).…”

Section: Discussionsupporting

confidence: 79%

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Histone methyltransferase ATX1 dynamically regulates fiber secondary cell wall biosynthesis inArabidopsisinflorescence stem

Wang

et al. 2020

Nucleic Acids Research

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Secondary wall thickening in the sclerenchyma cells is strictly controlled by a complex network of transcription factors in vascular plants. However, little is known about the epigenetic mechanism regulating secondary wall biosynthesis. In this study, we identified that ARABIDOPSIS HOMOLOG of TRITHORAX1 (ATX1), a H3K4-histone methyltransferase, mediates the regulation of fiber cell wall development in inflorescence stems of Arabidopsis thaliana. Genome-wide analysis revealed that the up-regulation of genes involved in secondary wall formation during stem development is largely coordinated by increasing level of H3K4 tri-methylation. Among all histone methyltransferases for H3K4me3 in Arabidopsis, ATX1 is markedly increased during the inflorescence stem development and loss-of-function mutant atx1 was impaired in secondary wall thickening in interfascicular fibers. Genetic analysis showed that ATX1 positively regulates secondary wall deposition through activating the expression of secondary wall NAC master switch genes, SECONDARY WALL-ASSOCIATED NAC DOMAIN PROTEIN1 (SND1) and NAC SECONDARY WALL THICKENING PROMOTING FACTOR1 (NST1). We further identified that ATX1 directly binds the loci of SND1 and NST1, and activates their expression by increasing H3K4me3 levels at these loci. Taken together, our results reveal that ATX1 plays a key role in the regulation of secondary wall biosynthesis in interfascicular fibers during inflorescence stem development of Arabidopsis.

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Section: Discussionsupporting

confidence: 79%

“…As an extensively reported epigenetic mark for transcriptional initiation, H3K4 tri-methylation levels are found to change dynamically during plant growth and development ( 69 ). However, the dynamic changes in H3K4me3 levels during stem development remains elusive.…”

Section: Discussionmentioning

confidence: 99%

Histone methyltransferase ATX1 dynamically regulates fiber secondary cell wall biosynthesis inArabidopsisinflorescence stem

Wang

et al. 2020

Nucleic Acids Research

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“…These modifications were distributed throughout the gene with H3K4me3 enriched at the promoter and 5´ end of the genes [22] and H3K36me2 and H3K36me3 enriched in the transcribed regions [23,24]. Another active mark is H3K4me2, a gene specific histone mark found at the 5ˊ end and promoter of active genes [25,26]. However, the presence of H3K4me2 does not always correlate with active transcription [27][28][29].…”

Section: Introductionmentioning

confidence: 99%

An optimised chromatin immunoprecipitation (ChIP) method for starchy leaves of Nicotiana benthamiana to study histone modifications of an allotetraploid plant

et al. 2020

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All flowering plants have evolved through multiple rounds of polyploidy throughout the evolutionary process. Intergenomic interactions between subgenomes in polyploid plants are predicted to induce chromatin modifications such as histone modifications to regulate expression of gene homoeologs. Nicotiana benthamiana is an ancient allotetraploid plant with ecotypes collected from climatically diverse regions of Australia. Studying the chromatin landscape of this unique collection will likely shed light on the importance of chromatin modifications in gene regulation in polyploids as well its implications in adaptation of plants in environmentally diverse conditions. Generally, chromatin immunoprecipitation and high throughput DNA sequencing (ChIP-seq) is used to study chromatin modifications. However, due to the starchy nature of mature N. benthamiana leaves, previously published protocols were unsuitable. The higher amounts of starch in leaves that co-precipitated with nuclei hindered downstream processing of DNA. Here we present an optimised ChIP protocol for N. benthamiana leaves to facilitate comparison of chromatin modifications in two closely related ecotypes. Several steps of ChIP were optimised including tissue harvesting, nuclei isolation, nuclei storage, DNA shearing and DNA recovery. Commonly available antibodies targeting histone 3 lysine 4 trimethylation (H3K4me3) and histone 3 lysine 9 dimethylation (H3K9me2) histone modifications were used and success of ChIP was confirmed by PCR and next generation sequencing. Collectively, our optimised method is the first comprehensive ChIP method for mature starchy leaves of N. benthamiana to enable studies of chromatin landscape at the genome-wide scale.

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“…These modi cations were distributed throughout the gene with H3K4me3 enriched at the promoter and 5' end of the genes (26) and H3K36me2 and H3K36me3 enriched in the transcribed regions (27,28). Another active mark is H3K4me2, a gene speci c histone mark found at the 5' end and promoter of active genes (29,30). However, the presence of H3K4me2 does not always correlate with active transcription (31)(32)(33).…”

Section: Introductionmentioning

confidence: 99%

An optimised Chromatin Immunoprecipitation (ChIP) method for starchy leaves of Nicotiana benthamiana to study histone modifications of an allotetraploid plant

Ranawaka

Tanurdžić

Waterhouse

et al. 2020

Preprint

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Background All flowering plants have evolved through multiple rounds of polyploidy throughout the evolutionary process. Intergenomic interactions between subgenomes in polyploid plants are predicted to induce chromatin modifications such as histone modifications to regulate expression of gene homoeologs. Nicotiana benthamiana is an ancient allotetraploid plant with ecotypes collected from climatically diverse regions of Australia. Studying the differences in chromatin landscape of this unique collection will shed light on the importance of chromatin modifications in gene regulation in polyploids as well its implications in adaptation of plants in environmentally diverse conditions. N.benthamiana is also an important biotechnological tool and it is widely used in virological research and functional genomics. Chromatin Immunoprecipitation and high throughput DNA sequencing (ChIP-seq) is well established technique used to study histone modifications. However, due to the starchy nature of mature N.benthamiana leaves, previously published protocols were unsuitable. The aim of this study was to optimise ChIP protocol for N.benthamiana leaves to facilitate comparison of chromatin modifications in two closely related ecotypes. Results Several steps of ChIP were optimised including tissue harvesting, nuclei isolation, nuclei storage, DNA shearing and DNA recovery. The higher amounts of starch in mature N.benthamiana leaves that co-precipitated with nuclei using previously published protocols, hindered chromatin shearing and resulted in low recovery of ChIP DNA. The optimised method reduced starch contamination and resulted in isolation of high quality nuclei suitable for next generation sequencing. Commonly available antibodies targeting histone 3 lysine 4 trimethylation (H3K4me3) and histone 3 lysine 9 dimethylation (H3K9me2) histone modifications were used and success of ChIP was confirmed by PCR and next generation sequencing. Conclusions An optimised ChIP method for mature leaves of N.benthamiana is described. It is relatively less laborious than previously published protocols and allows extraction of high quality nuclear genomic DNA from N.benthamiana. It is also the first comprehensive ChIP method for starchy leaves of N.benthamiana suitable for preparation of ChIP libraries for next generation sequencing.

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Histone tales: lysine methylation, a protagonist in Arabidopsis development

Abstract: Recent advances in the regulation of histone lysine methylation in plants and the role of this modification in the developmental programming of Arabidopsis are discussed.

Cited by 56 publications

References 155 publications

Histone methyltransferase ATX1 dynamically regulates fiber secondary cell wall biosynthesis inArabidopsisinflorescence stem

Histone methyltransferase ATX1 dynamically regulates fiber secondary cell wall biosynthesis inArabidopsisinflorescence stem

An optimised chromatin immunoprecipitation (ChIP) method for starchy leaves of Nicotiana benthamiana to study histone modifications of an allotetraploid plant

An optimised Chromatin Immunoprecipitation (ChIP) method for starchy leaves of Nicotiana benthamiana to study histone modifications of an allotetraploid plant

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