DNA Methylation within Transcribed Regions

To, Taiko Kim; Saze, Hidetoshi; Kakutani, Tetsuji

doi:10.1104/pp.15.00543

Cited by 67 publications

(49 citation statements)

References 67 publications

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“…Many TEs are also present in intronic regions especially in large plant genomes [28][29][30][31], likely due to less adverse effects on coding sequences compared to exonic insertions. Enigmatically, intronic TE sequences can also be targeted by repressive chromatin modifications, thus forming heterochromatic structure within transcription permissive chromatin environments [32]. In Arabidopsis thaliana, nuclear proteins, including INCREASE IN BONSAI METHYLATION 2 (IBM2)/ANTI-SILENCING1/SHOOT GROWTH1, are required for proper transcription of heterochromatin-containing genes [33][34][35][36].…”

Section: Introductionmentioning

confidence: 99%

Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

Espinas

Furci

et al. 2020

PLoS Genet

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Intronic regions of eukaryotic genomes accumulate many Transposable Elements (TEs). Intronic TEs often trigger the formation of transcriptionally repressive heterochromatin, even within transcription-permissive chromatin environments. Although TE-bearing introns are widely observed in eukaryotic genomes, their epigenetic states, impacts on gene regulation and function, and their contributions to genetic diversity and evolution, remain poorly understood. In this study, we investigated the genome-wide distribution of intronic TEs and their epigenetic states in the Oryza sativa genome, where TEs comprise 35% of the genome. We found that over 10% of rice genes contain intronic heterochromatin, most of which are associated with TEs and repetitive sequences. These heterochromatic introns are longer and highly enriched in promoter-proximal positions. On the other hand, introns also accumulate hypomethylated short TEs. Genes with heterochromatic introns are implicated in various biological functions. Transcription of genes bearing intronic heterochromatin is regulated by an epigenetic mechanism involving the conserved factor OsIBM2, mutation of which results in severe developmental and reproductive defects. Furthermore, we found that heterochromatic introns evolve rapidly compared to non-heterochromatic introns. Our study demonstrates that heterochromatin is a common epigenetic feature associated with actively transcribed genes in the rice genome.

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Section: Introductionmentioning

confidence: 99%

Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

Espinas

Furci

et al. 2020

PLoS Genet

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“…Thus, intronic TEs are widespread in human and plant genomes. Although the repressive effect of promoter HC-TREs on the expression of downstream genes has been well documented (7,8), the effect of intronic HC-TREs on the expression of their associated genes remains largely unknown (9).…”

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confidence: 99%

A protein complex regulates RNA processing of intronic heterochromatin-containing genes in Arabidopsis

Duan

Wang

Zhang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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In several eukaryotic organisms, heterochromatin (HC) in the introns of genes can regulate RNA processing, including polyadenylation, but the mechanism underlying this regulation is poorly understood. By promoting distal polyadenylation, the bromo-adjacent homology (BAH) domain-containing and RNA recognition motif-containing protein ASI1 and the H3K9me2-binding protein EDM2 are required for the expression of functional full-length transcripts of intronic HC-containing genes in Here we report that ASI1 and EDM2 form a protein complex in vivo via a bridge protein, ASI1-Immunoprecipitated Protein 1 (AIPP1), which is another RNA recognition motif-containing protein. The complex also may contain the Pol II CTD phosphatase CPL2, the plant homeodomain-containing protein AIPP2, and another BAH domain protein, AIPP3. As is the case with dysfunction of ASI1 and EDM2, dysfunction of AIPP1 impedes the use of distal polyadenylation sites at tested intronic HC-containing genes, such as the histone demethylase gene, resulting in a lack of functional full-length transcripts. A mutation in causes silencing of the transgene and genome-wide CHG hypermethylation at gene body regions, consistent with the lack of full-length functional transcripts in the mutant. Interestingly, compared with, , and mutations, mutations in ,, and cause the opposite effects on the expression of intronic HC-containing genes and other genes, suggesting that CPL2, AIPP2, and AIPP3 may form a distinct subcomplex. These results advance our understanding of the interplay between heterochromatic epigenetic modifications and RNA processing in higher eukaryotes.

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“…MITEs are preferentially located within gene regions of many plants and could in uence gene expression (Bureau and Wessler, 1994;Wessler et al, 1995;Casacuberta and Santiago, 2003;Liu et al, 2005;Lu et al, 2012). There is evidence that some MITE insertions located close to gene promoters could also downregulate gene expression (To et al, 2015). MITE3321 was frequently inserted also in the introns of genes of the studied pine species.…”

Section: Discussionmentioning

confidence: 98%

Comparative study of pine reference genomes reveals transposable element interconnected gene networks

Voronova

Rendón-Anaya

Ingvarsson

et al. 2020

Preprint

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Background: Sequencing the giga-genomes of several pine species belonging to the ancient gymnosperm clade has enabled comparative genomic analyses of these widely distributed outcrossing tree species. Initial sequence studies have revealed the wide distribution and extraordinary diversity of transposable elements (TEs) that occupy the large intergenic spaces. Our previous investigations revealed significant variations of class I TEs within pine subpopulations, but inoculation with pathogen induced correlated expression of TE families in pine seedlings, suggesting TE co-localisation with stress-responsive genes. In this study, we analyzed the distribution of TEs in gene regions of the assembled genomes of Pinus taeda and Pinus lambertiana using high-performance computing resources.Results: The quality of draft genomes and the genome annotation have significant consequences for the investigation of TEs and these aspects are discussed. Several TE families were identified in both species genomes frequently inserted into genes or their flanks. The non-autonomous MITE3321 family found in gene flanking regions and provide TATA boxes, several ARR1, DOF, WRKY and GT-binding sites, which are important signals in plant transcription activation and stress-response regulation. Distribution of MITE3321 across gene non-coding regions suggests action of selective pressure on this sequences and formation of gene sub-networks, depending on the location of MITE insertions. DNA TE DTX184 could potentially form microRNAs or provide its target site, thereby connect about 200 important stress-responsive genes in both pine species. Several retrotransposons propagated in gene regions were also identified, such as Copia-1813 containing important light-responsive regulative sequences, however full- length structures of low-copy-number TEs couldn’t be verified in the current genome assemblies. Only rare gene homologs carried similar insertions, indicating that most transposition events occurred after separation of investigated pine species. Node genes that contain many types of interspersed repeats were identified and observed in multiple potential transposable element associated networks.Conclusions: This study demonstrated the increased accumulation of TEs in the introns of stress-responsive genes of pines and the probability of rewiring them in responsive networks and sub-networks interconnected with node genes containing multiple TEs. Many such regulatory influences could lead to the adaptive environmental response clines that are characteristic of naturally spread pine populations.

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DNA Methylation within Transcribed Regions

Abstract: DNA methylation within transcribed genes is commonly found in diverse animals and plants. Here, we provide an overview of recent advances and the remaining mystery regarding intragenic DNA methylation.

Cited by 67 publications

References 67 publications

Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

Transcriptional regulation of genes bearing intronic heterochromatin in the rice genome

A protein complex regulates RNA processing of intronic heterochromatin-containing genes in Arabidopsis

Comparative study of pine reference genomes reveals transposable element interconnected gene networks

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