scholarly journals Nurse cell-derived small RNAs define paternal epigenetic inheritance in Arabidopsis

2021 ◽  
Author(s):  
Jincheng Long ◽  
James Walker ◽  
Wenjing She ◽  
Billy Aldridge ◽  
Hongbo Gao ◽  
...  

AbstractThe plant male germline undergoes DNA methylation reprogramming, which methylates genes de novo and thereby alters gene expression and facilitates meiosis. Why reprogramming is limited to the germline and how specific genes are chosen is unknown. Here, we demonstrate that genic methylation in the male germline, from meiocytes to sperm, is established by germline-specific siRNAs transcribed from transposons with imperfect sequence homology. These siRNAs are synthesized by meiocyte nurse cells (tapetum) via activity of the tapetum-specific chromatin remodeler CLASSY3. Remarkably, tapetal siRNAs govern germline methylation throughout the genome, including the inherited methylation patterns in sperm. Finally, we demonstrate that these nurse cell-derived siRNAs (niRNAs) silence germline transposons, thereby safeguarding genome integrity. Our results reveal that tapetal niRNAs are sufficient to reconstitute germline methylation patterns and drive extensive, functional methylation reprogramming analogous to piRNA-mediated reprogramming in animal germlines.

Science ◽  
2021 ◽  
Vol 373 (6550) ◽  
pp. eabh0556 ◽  
Author(s):  
Jincheng Long ◽  
James Walker ◽  
Wenjing She ◽  
Billy Aldridge ◽  
Hongbo Gao ◽  
...  

The plant male germline undergoes DNA methylation reprogramming, which methylates genes de novo and thereby alters gene expression and regulates meiosis. Here, we reveal the molecular mechanism underlying this reprogramming. We demonstrate that genic methylation in the male germline, from meiocytes to sperm, is established by 24-nucleotide small interfering RNAs (siRNAs) transcribed from transposons with imperfect sequence homology. These siRNAs are synthesized by meiocyte nurse cells (tapetum) through activity of CLSY3, a chromatin remodeler absent in other anther cells. Tapetal siRNAs govern germline methylation throughout the genome, including the inherited methylation patterns in sperm. Tapetum-derived siRNAs also silence germline transposons, safeguarding genome integrity. Our results reveal that tapetal siRNAs are sufficient to reconstitute germline methylation patterns and drive functional methylation reprogramming throughout the male germline.


Author(s):  
Adil Altaf ◽  
Ahmad Zada

Common DNA methylation controls gene expression and preserves genomic integrity. Mal methylation can cause developmental abnormalities in the plants. Multiple enzymes carrying out de novo methylation, methylation maintenance, and active demethylation culminate in a particular DNA methylation state. Next-generation sequencing advances and computational methods to analyze the data. The model plant Arabidopsis thaliana was used to study DNA methylation patterns, epigenetic inheritance, and plant methylation. Plant DNA methylation research reveals methylation patterns and describing variations in plant tissues. Determining the kinetics of DNA methylation in diverse plant tissues is also a new field. However, it is vital to understand regulatory and developmental decisions and use plant model species to develop new commercial crops; that are more resistant to stress and yield more. There are several methods available for assessing DNA methylation data. The performance of several techniques is assessed in A. thaliana, which has a smaller genome than hexaploid bread wheat. Keywords: DNA methylation, plants, process, use and benefits


Genetics ◽  
2020 ◽  
Vol 215 (2) ◽  
pp. 379-391 ◽  
Author(s):  
Diane Burgess ◽  
Hong Li ◽  
Meixia Zhao ◽  
Sang Yeol Kim ◽  
Damon Lisch

Transposable elements (TEs) are a ubiquitous feature of plant genomes. Because of the threat they post to genome integrity, most TEs are epigenetically silenced. However, even closely related plant species often have dramatically different populations of TEs, suggesting periodic rounds of activity and silencing. Here, we show that the process of de novo methylation of an active element in maize involves two distinct pathways, one of which is directly implicated in causing epigenetic silencing and one of which is the result of that silencing. Epigenetic changes involve changes in gene expression that can be heritably transmitted to daughter cells in the absence of changes in DNA sequence. Epigenetics has been implicated in phenomena as diverse as development, stress response, and carcinogenesis. A significant challenge facing those interested in investigating epigenetic phenomena is determining causal relationships between DNA methylation, specific classes of small RNAs, and associated changes in gene expression. Because they are the primary targets of epigenetic silencing in plants and, when active, are often targeted for de novo silencing, TEs represent a valuable source of information about these relationships. We use a naturally occurring system in which a single TE can be heritably silenced by a single derivative of that TE. By using this system it is possible to unravel causal relationships between different size classes of small RNAs, patterns of DNA methylation, and heritable silencing. Here, we show that the long terminal inverted repeats within Zea mays MuDR transposons are targeted by distinct classes of small RNAs during epigenetic silencing that are dependent on distinct silencing pathways, only one of which is associated with transcriptional silencing of the transposon. Further, these small RNAs target distinct regions of the terminal inverted repeats, resulting in different patterns of cytosine methylation with different functional consequences with respect to epigenetic silencing and the heritability of that silencing.


Changing DNA methylation patterns during embryonic development are discussed in relation to differential gene expression, changes in X-chromosome activity and genomic imprinting. Sperm DNA is more methylated than oocyte DNA, both overall and for specific sequences. The methylation difference between the gametes could be one of the mechanisms (along with chromatin structure) regulating initial differences in expression of parental alleles in early development. There is a loss of methylation during development from the morula to the blastocyst and a marked decrease in methylase activity. De novo methylation becomes apparent around the time of implantation and occurs to a lesser extent in extra-embryonic tissue DNA. In embryonic DNA, de novo methylation begins at the time of random X-chromosome inactivation but it continues to occur after X-chromosome inactivation and may be a mechanism that irreversibly fixes specific patterns of gene expression and X-chromosome inactivity in the female. The germ line is probably delineated before extensive de novo methylation and hence escapes this process. The marked undermethylation of the germ line DNA may be a prerequisite for X-chromosome reactivation. The process underlying reactivation and removal of parent-specific patterns of gene expression may be changes in chromatin configuration associated with meiosis and a general reprogramming of the germ line to developmental totipotency.


2018 ◽  
Author(s):  
Komivi Dossa ◽  
Marie Ali Mmadi ◽  
Rong Zhou ◽  
Qi Zhou ◽  
Mei Yang ◽  
...  

AbstractDNA methylation is a heritable epigenetic mechanism that participates in gene regulation under abiotic stresses in plants. Sesame (Sesamum indicum L.) is typically considered a drought-tolerant crop but highly susceptible to waterlogging, a property attributed to its presumed origin in Africa or India. Understanding DNA methylation patterns in sesame under drought and waterlogging conditions can provide insights into the regulatory mechanisms underlying its contrasting responses to these principal abiotic stresses. Here, we combined Methylation-Sensitive Amplified Polymorphism and transcriptome analyses to profile cytosine methylation patterns, gene expression alteration, and their interplay in drought-tolerant and waterlogging-tolerant sesame genotypes under control, stress and recovery conditions. Our data showed that drought stress strongly induced de novo methylation (DNM) whereas most of the loci were demethylated (DM) during the recovery phase. In contrast, waterlogging decreased the level of methylation under stress but during the recovery phase, both DM and DNM were concomitantly deployed. In both stresses, the differentially expressed genes (DEGs) were highly correlated with the methylation patterns. We observed that DM was associated with the up-regulation of the DEGs while DNM was correlated with the down-regulation of the DEGs. In addition, we sequenced 44 differentially methylated regions of which 90% overlapped with the promoters and coding sequences of the DEGs. Altogether, we demonstrated that sesame has divergent epigenetic programs that respond to drought and waterlogging stresses. Our results also highlighted the possible interplay among DNA methylation and gene expression, which may modulate the contrasting responses to drought and waterlogging in sesame.


2014 ◽  
Vol 1 (2) ◽  
pp. 219-229 ◽  
Author(s):  
Yuanyuan Zhao ◽  
Xuemei Chen

Abstract Cytosine DNA methylation is an epigenetic modification in eukaryotes that maintains genome integrity and regulates gene expression. The DNA methylation patterns in plants are more complex than those in animals, and plants and animals have common as well as distinct pathways in regulating DNA methylation. Recent studies involving genetic, molecular, biochemical and genomic approaches have greatly expanded our knowledge of DNA methylation in plants. The roles of many proteins as well as non-coding RNAs in DNA methylation have been uncovered.


2021 ◽  
Vol 9 (3) ◽  
pp. 109-114
Author(s):  
Adil Altaf ◽  
Ahmad Zada

Common DNA methylation controls gene expression and preserves genomic integrity. Mal methylation can cause developmental abnormalities in the plants. Multiple enzymes carrying out de novo methylation, methylation maintenance, and active demethylation culminate in a particular DNA methylation state. Next-generation sequencing advances and computational methods to analyze the data. The model plant Arabidopsis thaliana was used to study DNA methylation patterns, epigenetic inheritance, and plant methylation. Plant DNA methylation research reveals methylation patterns and describing variations in plant tissues. Determining the kinetics of DNA methylation in diverse plant tissues is also a new field. However, it is vital to understand regulatory and developmental decisions and use plant model species to develop new commercial crops; that are more resistant to stress and yield more. There are several methods available for assessing DNA methylation data. The performance of several techniques is assessed in A. thaliana, which has a smaller genome than hexaploid bread wheat. Keywords: DNA methylation, plants, process, use and benefits.


2020 ◽  
Author(s):  
Diane Burgess ◽  
Meixia Zhao ◽  
Sang Yeol Kim ◽  
Damon Lisch

Epigenetic changes involve changes in gene expression that can be heritably transmitted to daughter cells in the absence of changes in DNA sequence. Epigenetics has been implicated in phenomena as diverse as development, stress response and carcinogenesis. A significant challenge facing those interested in investigating epigenetic phenomena is determining causal relationships between DNA methylation, specific classes of small RNAs and associated changes in gene expression. Because they are the primary targets of epigenetic silencing in plants and, when active, are often targeted for de novo silencing, transposable elements (TEs) represent a valuable source of information about these relationships. We use a naturally occurring system in which a single TE can be heritably silenced by a single derivative of that TE. By using this system it is possible to unravel causal relationships between different size classes of small RNAs, patterns of DNA methylation and heritable silencing. Here, we show that the long terminal inverted repeats (TIRs) within Zea mays MuDR transposons are targeted by distinct classes of small RNAs during epigenetic silencing that are dependent on distinct silencing pathways. Further, these small RNAs target distinct regions of the TIRs, resulting in different patterns of cytosine methylation with different functional consequences with respect to epigenetic silencing and heritability of that silencing.


2021 ◽  
Author(s):  
Roza Berhanu Lemma ◽  
Thomas Fleischer ◽  
Emily Martinsen ◽  
Vessela N Kristensen ◽  
Ragnhild Eskeland ◽  
...  

Methylation of cytosines on DNA is a prominent modification associated with gene expression regulation. Aberrant DNA methylation patterns have recurrently been linked to dysregulation of the regulatory program in cancer cells. To shed light on the underlying molecular mechanism driving this process, we hypothesized that aberrant methylation patterns could be controlled by the binding of specific transcription factors (TFs) across cancer types. By combining DNA methylation arrays and gene expression data with TF binding sites (TFBSs), we explored the interplay between TF binding and DNA methylation in 19 cancer cohorts. We performed emQTL (expression-methylation quantitative trait loci) analyses in each cohort and identified 13 TFs whose expression levels are correlated with local DNA methylation patterns around their binding site in at least 2 cancer types. The 13 TFs are mainly associated with local demethylation and are enriched for pioneer function, suggesting a specific role for these TFs in modulating chromatin structure and transcription in cancer patients. Furthermore, we confirmed that de novo methylation is precluded across cancers at CpGs lying in genomic regions enriched for TF-binding signatures associated with SP1, CTCF, NRF1, GABPA, KLF9, and/or YY1. The modulation of DNA methylation associated with TF binding was observed at cis-regulatory regions controlling immune- and cancer-associated pathways, corroborating that the emQTL signals were derived from both cancer and tumour-infiltrating cells. As a case example, we experimentally confirmed that FOXA1 knock-down is associated with higher methylation in regions bound by FOXA1 in breast cancer MCF-7 cells. Finally, we reported physical interactions between FOXA1 with TET1 and TET2 at physiological levels in MCF-7 cells, adding further support for FOXA1 attracting TET1 and TET2 to induce local demethylation in cancer.


2018 ◽  
Author(s):  
Tanja Božić ◽  
Joana Frobel ◽  
Annamarija Raic ◽  
Fabio Ticconi ◽  
Chao-Chung Kuo ◽  
...  

AbstractThede novoDNA methyltransferase 3A (DNMT3A) plays pivotal roles in hematopoietic differentiation. In this study, we followed the hypothesis that alternative splicing ofDNMT3Ahas characteristic epigenetic and functional sequels. SpecificDNMT3Atranscripts were either downregulated or overexpressed in human hematopoietic stem and progenitor cells and this resulted in complementary and transcript-specific DNA methylation and gene expression changes. Functional analysis indicated that particularly transcript 2 (coding for DNMT3A2) activates proliferation and induces loss of a primitive immunophenotype, whereas transcript 4 interferes with colony formation of the erythroid lineage. Notably, in acute myeloid leukemia (AML) expression of transcript 2 correlates with itsin vitroDNA methylation and gene expression signatures and is associated with overall survival, indicating thatDNMT3Avariants impact also on malignancies. Our results demonstrate that specificDNMT3Avariants have distinct epigenetic and functional impact. Particularly DNMT3A2 triggers hematopoietic differentiation and the corresponding signatures are reflected in AML.


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