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Extensive demethylation of repetitive elements during seed development underlies gene imprinting.

ABSTRACT: DNA methylation is an epigenetic mark associated with transposable element silencing and gene imprinting in flowering plants and mammals. In plants, imprinting occurs in the endosperm, which nourishes the embryo during seed development. We have profiled Arabidopsis DNA methylation genome-wide in the embryo and endosperm and found that large-scale methylation changes accompany endosperm development and endosperm-specific gene expression. Transposable element fragments are extensively demethylated in the endosperm. We discovered new imprinted genes by the identification of candidates associated with regions of reduced endosperm methylation and preferential expression in endosperm relative to other parts of the plant. These data suggest that imprinting in plants evolved from targeted methylation of transposable element insertions near genic regulatory elements followed by positive selection when the resulting expression change was advantageous.

SUBMITTER: Gehring M

PROVIDER: S-EPMC2886585 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Extensive demethylation of repetitive elements during seed development underlies gene imprinting.

Gehring Mary M Bubb Kerry L KL Henikoff Steven S

Science (New York, N.Y.) 20090601 5933

DNA methylation is an epigenetic mark associated with transposable element silencing and gene imprinting in flowering plants and mammals. In plants, imprinting occurs in the endosperm, which nourishes the embryo during seed development. We have profiled Arabidopsis DNA methylation genome-wide in the embryo and endosperm and found that large-scale methylation changes accompany endosperm development and endosperm-specific gene expression. Transposable element fragments are extensively demethylated ...[more]

PMID: 19520961

Similar Datasets

Extensive demethylation of repetitive elements during seed development underlies gene imprinting

Project description:DNA methylation is an epigenetic mark associated with transposable element silencing and gene imprinting in flowering plants and mammals. In plants, imprinting occurs in the endosperm, which nourishes the embryo during seed development. We have profiled Arabidopsis DNA methylation genome-wide in the embryo and endosperm. Large-scale methylation changes accompany endosperm development and endosperm-specific gene expression. Transposable element fragments are extensively demethylated in the endosperm. We discovered new imprinted genes by identifying candidate genes associated with the top differentially methylated regions. Our data suggest that imprinting in plants evolved from genome defense against transposable elements. Keywords: Affinity-purification on microarray All experiments were done using two channels per chip. Immunoprecipitated methylated DNA (IP) was compared to control genomic DNA (input). Both the IP and input represent Cy5 and Cy3 labeled Illumina GA libraries.

2009-06-12 | E-GEOD-14570 | biostudies-arrayexpress

Extensive demethylation of repetitive elements during seed development underlies gene imprinting

2009-06-12 | GSE14570 | GEO

Dormancy-specific imprinting underlies maternal inheritance of seed dormancy in Arabidopsis thaliana.

Project description:Mature seed dormancy is a vital plant trait that prevents germination out of season. In Arabidopsis, the trait can be maternally regulated but the underlying mechanisms sustaining this regulation, its general occurrence and its biological significance among accessions are poorly understood. Upon seed imbibition, the endosperm is essential to repress the germination of dormant seeds. Investigation of genomic imprinting in the mature seed endosperm led us to identify a novel set of imprinted genes that are expressed upon seed imbibition. Remarkably, programs of imprinted gene expression are adapted according to the dormancy status of the seed. We provide direct evidence that imprinted genes play a role in regulating germination processes and that preferential maternal allelic expression can implement maternal inheritance of seed dormancy levels.

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Sequential gene activation and extensive gene imprinting during early embryo development in maize

Project description:The embryo is responsible for transmitting genetic information to the next generation. However, the underlying gene expression and gene imprinting during early embryo development remain largely elusive in maize. Using high-throughput RNA sequencing, we analyzed the allelic gene expression patterns of maize embryos from reciprocal crosses between inbred lines B73 and Mo17 at six time points (3 to 13 days after pollination). A total of 9532 genes were found to be differentially expressed in developmental stage, 3512 of 9532 genes were affected by cross direction. Co-expression analysis uncovered the sequential gene activations during maize embryo development. Further, we found 64 embryo strongly imprinted genes, including 57 maternally expressed imprinted genes (MEG) and 7 paternally expressed imprinted genes (PEG) in the maize embryo. Among them, 20 genes were continuously imprinted and 36 imprinted genes were newly identified. By applying In situ hybridization, we verified that six of the differentially expressed genes showed enriched transcription in the embryo. In addition, mutant analyses indicated that three of the imprinted genes displayed reduced embryo size. Therefore, our data shed new light on our understanding of the gene expression and gene imprinting in early maize embryo development, and suggested that imprinted genes are important for proper embryo development.

2017-12-05 | GSE95399 | GEO

Maternal small RNAs mediate spatial-temporal regulation of gene expression, imprinting, and seed development in Arabidopsis.

Project description:Arabidopsis seed development involves maternal small interfering RNAs (siRNAs) that induce RNA-directed DNA methylation (RdDM) through the NRPD1-mediated pathway. To investigate their biological functions, we characterized siRNAs in the endosperm and seed coat that were separated by laser-capture microdissection (LCM) in reciprocal genetic crosses with an nrpd1 mutant. We also monitored the spatial-temporal activity of the NRPD1-mediated pathway on seed development using the AGO4:GFP::AGO4 (promoter:GFP::protein) reporter and promoter:GUS sensors of siRNA-mediated silencing. From these approaches, we identified four distinct groups of siRNA loci dependent on or independent of the maternal NRPD1 allele in the endosperm or seed coat. A group of maternally expressed NRPD1-siRNA loci targets endosperm-preferred genes, including those encoding AGAMOUS-LIKE (AGL) transcription factors. Using translational promoter:AGL::GUS constructs as sensors, we demonstrate that spatial and temporal expression patterns of these genes in the endosperm are regulated by the NRPD1-mediated pathway irrespective of complete silencing (AGL91) or incomplete silencing (AGL40) of these target genes. Moreover, altered expression of these siRNA-targeted genes affects seed size. We propose that the corresponding maternal siRNAs could account for parent-of-origin effects on the endosperm in interploidy and hybrid crosses. These analyses reconcile previous studies on siRNAs and imprinted gene expression during seed development.

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A full-length transcriptome and gene expression analysis reveal genes and molecular elements expressed during seed development in Gnetum luofuense.

Project description:BACKGROUND:Gnetum is an economically important tropical and subtropical gymnosperm genus with various dietary, industrial and medicinal uses. Many carbohydrates, proteins and fibers accumulate during the ripening of Gnetum seeds. However, the molecular mechanisms related to this process remain unknown. RESULTS:We therefore assembled a full-length transcriptome from immature and mature G. luofuense seeds using PacBio sequencing reads. We identified a total of 5726 novel genes, 9061 alternative splicing events, 3551 lncRNAs, 2160 transcription factors, and we found that 8512 genes possessed at least one poly(A) site. In addition, gene expression comparisons of six transcriptomes generated by Illumina sequencing showed that 14,323 genes were differentially expressed from an immature stage to a mature stage with 7891 genes upregulated and 6432 genes downregulated. The expression of 14 differentially expressed transcription factors from the MADS-box, Aux/IAA and bHLH families was validated by qRT-PCR, suggesting that they may have important roles in seed ripening of G. luofuense. CONCLUSIONS:These findings provide a valuable molecular resource for understanding seed development of gymnosperms.

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DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation.

Project description:MEDEA (MEA) is an Arabidopsis Polycomb group gene that is imprinted in the endosperm. The maternal allele is expressed and the paternal allele is silent. MEA is controlled by DEMETER (DME), a DNA glycosylase required to activate MEA expression, and METHYLTRANSFERASE I (MET1), which maintains CG methylation at the MEA locus. Here we show that DME is responsible for endosperm maternal-allele-specific hypomethylation at the MEA gene. DME can excise 5-methylcytosine in vitro and when expressed in E. coli. Abasic sites opposite 5-methylcytosine inhibit DME activity and might prevent DME from generating double-stranded DNA breaks. Unexpectedly, paternal-allele silencing is not controlled by DNA methylation. Rather, Polycomb group proteins that are expressed from the maternal genome, including MEA, control paternal MEA silencing. Thus, DME establishes MEA imprinting by removing 5-methylcytosine to activate the maternal allele. MEA imprinting is subsequently maintained in the endosperm by maternal MEA silencing the paternal allele.

| S-EPMC4106368 | biostudies-literature

A Genomic View of Alternative Splicing of Long Non-coding RNAs during Rice Seed Development Reveals Extensive Splicing and lncRNA Gene Families.

Project description:Alternative splicing (AS) is a key modulator of development in many eukaryotic organisms. In plants, alternative splice forms of non-coding RNAs (ncRNAs) are known to modulate flowering time in Arabidopsis and fertility in rice. Here we demonstrate that alternative splicing of coding and long non-coding RNAs occurs during rice seed development by comparing AS in immature seeds vs. embryo and endosperm of mature seeds. Based on computational predictions of AS events determined from a Bayesian analysis of junction counts of RNA-seq datasets, differential splicing of protein-coding, and non-coding RNAs was determined. In contrast to roots, leaves, flowers, buds, and reproductive meristems, developing seeds had 5.8-57 times more predicted AS. Primers designed to span introns and exons were used to detect AS events predicted by rMATs in cDNA derived from early (milk) seed, embryo, and endosperm. Comparing milk seed vs. mature embryo and endosperm, AS of MORC7 (a gene implicated in epigenetic gene silencing), was markedly different. Long non-coding RNAs (lncRNAs) also underwent AS during the transition from milk seed to mature embryo and endosperm, with a complex gene structure, and were more extensively processed than predicted by current genome annotation. Exon retention of lncRNAs was enhanced in embryos. Searching all 5,515 lncRNAs in the NCBI genome annotation uncovered gene families based on highly conserved regions shared by groups of 3-35 lncRNAs. The homologies to other lncRNAs, as well as homologies to coding sequences, and the genomic context of lncRNAs provide inroads for functional analysis of multi-exonic lncRNAs that can be extensively processed during seed development.

| S-EPMC5808331 | biostudies-literature

Repetitive DNA elements, nucleosome binding and human gene expression.

Project description:We evaluated the epigenetic contributions of repetitive DNA elements to human gene regulation. Human proximal promoter sequences show distinct distributions of transposable elements (TEs) and simple sequence repeats (SSRs). TEs are enriched distal from transcriptional start sites (TSSs) and their frequency decreases closer to TSSs, being largely absent from the core promoter region. SSRs, on the other hand, are found at low frequency distal to the TSS and then increase in frequency starting approximately 150 bp upstream of the TSS. The peak of SSR density is centered around the -35 bp position where the basal transcriptional machinery assembles. These trends in repetitive sequence distribution are strongly correlated, positively for TEs and negatively for SSRs, with relative nucleosome binding affinities along the promoters. Nucleosomes bind with highest probability distal from the TSS and the nucleosome binding affinity steadily decreases reaching its nadir just upstream of the TSS at the same point where SSR frequency is at its highest. Promoters that are enriched for TEs are more highly and broadly expressed, on average, than promoters that are devoid of TEs. In addition, promoters that have similar repetitive DNA profiles regulate genes that have more similar expression patterns and encode proteins with more similar functions than promoters that differ with respect to their repetitive DNA. Furthermore, distinct repetitive DNA promoter profiles are correlated with tissue-specific patterns of expression. These observations indicate that repetitive DNA elements mediate chromatin accessibility in proximal promoter regions and the repeat content of promoters is relevant to both gene expression and function.

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An AP endonuclease functions in active DNA demethylation and gene imprinting in Arabidopsis [corrected].

Project description:Active DNA demethylation in plants occurs through base excision repair, beginning with removal of methylated cytosine by the ROS1/DME subfamily of 5-methylcytosine DNA glycosylases. Active DNA demethylation in animals requires the DNA glycosylase TDG or MBD4, which functions after oxidation or deamination of 5-methylcytosine, respectively. However, little is known about the steps following DNA glycosylase action in the active DNA demethylation pathways in plants and animals. We show here that the Arabidopsis APE1L protein has apurinic/apyrimidinic endonuclease activities and functions downstream of ROS1 and DME. APE1L and ROS1 interact in vitro and co-localize in vivo. Whole genome bisulfite sequencing of ape1l mutant plants revealed widespread alterations in DNA methylation. We show that the ape1l/zdp double mutant displays embryonic lethality. Notably, the ape1l+/-zdp-/- mutant shows a maternal-effect lethality phenotype. APE1L and the DNA phosphatase ZDP are required for FWA and MEA gene imprinting in the endosperm and are important for seed development. Thus, APE1L is a new component of the active DNA demethylation pathway and, together with ZDP, regulates gene imprinting in Arabidopsis.

| S-EPMC4287435 | biostudies-literature

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