Transcription-coupled and epigenome-encoded mechanisms direct H3K4 methylation

Oya, Satoyo; Takáhashi, Mayumí; Takashima, Kazuya; Kakutani, Tetsuji; Inagaki, Soichi

doi:10.1101/2021.06.03.446702

Cited by 6 publications

(17 citation statements)

References 100 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The current study indicated that five ATX proteins function redundantly and are required for plant viability, suggesting that the ATX proteins play a critical role in plant growth and development. Although the effect of atx mutations on H3K4me1 was not detected in the current study, the H3K4me1 level was significantly reduced in the atx1/2 mutant as reported by a recent study (Oya et al, 2022). Of note, the atx1 mutant allele (SAIL_409_A10) used in the current study is different from the atx1 allele (SALK_149002C) used in the previous study, which may cause different effects on H3K4me1.…”

Section: Discussionsupporting

confidence: 70%

“…In Arabidopsis , histone H3K4 methylation was found to be catalyzed by different histone methyltransferases, including ATX1–5 (Alvarez‐Venegas et al, 2003; Saleh et al, 2008; Chen et al, 2017; Oya et al, 2022), SDG2/ATXR3 (Berr et al, 2010; Guo et al, 2010), and ATXR7 (Berr et al, 2009; Tamada et al, 2009; Oya et al, 2022). However, how different types of histone methyltransferases cooperate to regulate histone H3K4 methylation was largely unknown.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

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

Shang

Cai

et al. 2022

JIPB

View full text Add to dashboard Cite

Although the Trithorax histone methyltransferases ATX1–5 are known to regulate development and stress responses by catalyzing histone H3K4 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 H3K4me3 levels of both RNA‐directed 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 H3K4me3 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.

show abstract

Section: Discussionsupporting

confidence: 70%

Section: Discussionmentioning

confidence: 99%

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

Shang

Cai

et al. 2022

JIPB

View full text Add to dashboard Cite

show abstract

“…ATX1, ATX2, ATXR7 are responsible for the enrichment of H3K4me1 in the gene bodies of active genes (Oya et al 2021). Tudor domain of PDS5C binds H3K4me1 and facilitates homology directed repair (HDR) (Niu et al 2021).…”

Section: Discussionmentioning

confidence: 99%

“…Unlike in humans, in plants, H3K4me1 (rather than H3K36me3) marks the gene bodies of active genes. Recent work has demonstrated that H3K4me1 enrichment is mediated by a combination of transcription-coupled (ATXR7) and epigenome-encoded (ATX1, ATX2) methyltransferases (Oya et al, 2021). Once established, H3K4me1 reading can then occur by proteins containing histone-reader domains such as “Royal family” Tudor domains, which bind methylated lysine residues on H3 histone tails (Kim et al, 2006; Lu and Wang, 2013; Maurer-Stroh et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

The H3K4me1 histone mark recruits DNA repair to functionally constrained genomic regions in plants

Quiroz

Zhao

Carbonell‐Bejerano

et al. 2022

Preprint

View full text Add to dashboard Cite

Mutation is the ultimate source of genetic variation in natural populations and crops. To study mechanisms determining mutation rate variation within plant genomes, we analyzed 43,483 de novo germline single base substitutions in 1,504 fast neutron mutation lines of the model rice cultivar Kitaake (Oryza sativa ssp japonica) (from Li et al. 2017). We find that, like previously observed for de novo germline mutations in Arabidopsis. thaliana, mutation rates are significantly lower in genomic regions marked by H3K4me1, a histone modification found in the gene bodies of actively expressed genes in plants. We also observed conservation in rice for PDS5C, a cohesion cofactor involved in the homology-directed repair pathway that in A. thaliana binds to H3K4me1 via its Tudor domain. By examining existing ChIP-seq data for PDS5C in A. thaliana, we find that it localizes to genome regions marked by H3K4me1: regions of low mutation rates, coding regions, essential genes, constitutively expressed genes, and genes under stronger purifying selection, mirroring mutation biases observed in rice as well. We searched the A. thaliana proteome for genes containing similar Tudor domains and found that they are significantly enriched for DNA repair functions (p<1×10-11), including the mismatch repair MSH6 gene (in both rice and A. thaliana ), suggesting the potential for multiple DNA repair pathways to specifically target gene bodies and essential genes through H3K4me1 reading. These findings inspire further research to characterize mechanisms that localize DNA repair via histone interactions, leading to hypomutation in functionally constrained regions and potentially tuning the evolutionary trajectories of plant genomes.

show abstract

“…A consortium that included a subset of the authors of the current study (J.G.M., P.C.-B., C.B.F., D.W.) recently reported a link between mutation rates and local epigenomic features enriched in gene bodies and evolutionarily constrained genes [1], with variation in mutation rate probability paralleling patterns of neutral and functional polymorphism in natural populations of Arabidopsis thaliana. The epigenomic feature most strongly associated with lower mutation rate was H3K4me1, whose deposition in plants is coupled to transcription and which is enriched in gene bodies and functionally constrained genes [2]. We demonstrated with simulations how epigenomic features that are characteristic for broad genomic regions, such as constitutively expressed genes, and which simultaneously affect mutation rate, could yield a solution to Lynch’s equations for the barrier imposed by genetic drift on the evolution of targeted hypomutation [3–5].…”

Section: Introductionmentioning

confidence: 99%

Report of mutation biases mirroring selection in Arabidopsis thaliana unlikely to be entirely due to variant calling errors

Monroe

Murray

Xian

et al. 2022

Preprint

View full text Add to dashboard Cite

It has recently been proposed that the uneven distribution of epigenomic features might facilitate reduced mutation rate in constrained regions of the Arabidopsis thaliana genome, even though previous work had shown that it would be difficult for reduced mutation rates to evolve on a gene-by-gene basis. A solution to Lynch's equations for the barrier imposed by genetic drift on the evolution of targeted hypomutation can, however, come from epigenomic features that are enriched in certain portions of the genome, for example, coding regions of essential genes, and which simultaneously affect mutation rate. Such theoretical considerations draw on what is known about DNA repair guided by epigenomic features. A recent publication challenged these conclusions, because several mutation data sets that support a lower mutation rate in constrained regions suffered from variant calling errors. Here we show that neither homopolymer errors nor elevated mutation rates at transposable elements are likely to entirely explain reported mutation rate biases. Observed mutation biases are also supported by a meta-analysis of several independent germline mutation data sets, with complementary experimental data providing a mechanistic basis for reduced mutation rate in genes and specifically in essential genes. Finally, models derived from the drift-barrier hypothesis demonstrate that mechanisms linking DNA repair to chromatin marks and other epigenomic features can evolve in response to second-order selection on emergent mutation biases.

show abstract

Transcription-coupled and epigenome-encoded mechanisms direct H3K4 methylation

Cited by 6 publications

References 100 publications

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

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

The H3K4me1 histone mark recruits DNA repair to functionally constrained genomic regions in plants

Report of mutation biases mirroring selection in Arabidopsis thaliana unlikely to be entirely due to variant calling errors

Contact Info

Product

Resources

About