scholarly journals Unusual predominance of maintenance DNA methylation in Spirodela polyrhiza

2020 ◽  
Author(s):  
Alex Harkess ◽  
Adam J. Bewick ◽  
Zefu Lu ◽  
Paul Fourounjian ◽  
Joachim Messing ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Plant Species ◽  
Repetitive Dna ◽  
Small Rnas ◽  
Small Interfering Rnas ◽  
Gene Body Methylation ◽  
Spirodela Polyrhiza ◽  
Genome Wide ◽  
Low Levels ◽  
Maintenance Methylation

Abstract5-methylcytosine (5mC) is a modified base often described as necessary for the proper regulation of genes and transposons and for the maintenance of genome integrity in plants. However, the extent of this dogma is limited by the current phylogenetic sampling of land plant species diversity. Here, we report that a monocot plant, Spirodela polyrhiza, has lost CG gene body methylation, genome-wide CHH methylation, and the presence or expression of several genes in the highly conserved RNA-directed DNA methylation (RdDM) pathway. It has also lost the CHH methyltransferase CHROMOMETHYLASE 2. Consequently, the transcriptome is depleted of 24-nucleotide, heterochromatic, small interfering RNAs that act as guides for the deposition of 5mC to RdDM-targeted loci in all other currently sampled angiosperm genomes. Although the genome displays low levels of genome-wide 5mC primarily at LTR retrotransposons, CG maintenance methylation is still functional. In contrast, CHG methylation is weakly maintained even though H3K9me2 is present at loci dispersed throughout the euchromatin and highly enriched at regions likely demarcating pericentromeric regions. Collectively, these results illustrate that S. polyrhiza is maintaining CG and CHG methylation mostly at repeats in the absence of small RNAs. S. polyrhiza reproduces rapidly through clonal propagation in aquatic environments, which we hypothesize may enable low levels of maintenance methylation to persist in large populations.Significance StatementDNA methylation is a widespread chromatin modification that is regularly found in all plant species. By examining one aquatic duckweed species, Spirodela polyrhiza, we find that it has lost highly conserved genes involved in methylation of DNA at sites often associated with repetitive DNA, and within genes, however DNA methylation and heterochromatin is maintained during cell division at other sites. Consequently, small RNAs that normally guide methylation to silence repetitive DNA like retrotransposons are diminished. Despite the loss of a highly conserved methylation pathway, and the reduction of small RNAs that normally target repetitive DNA, transposons have not proliferated in the genome, perhaps due in part to the rapid, clonal growth lifestyle of duckweeds.

scholarly journals Epimutations are associated with CHROMOMETHYLASE 3-induced de novo DNA methylation

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Jered M Wendte ◽  
Yinwen Zhang ◽  
Lexiang Ji ◽  
Xiuling Shi ◽  
Rashmi R Hazarika ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Plant Species ◽  
Dna Methyltransferase ◽  
Constitutive Heterochromatin ◽  
De Novo ◽  
Flowering Plant ◽  
Gene Body ◽  
Gene Body Methylation ◽  
Mechanistic Basis ◽  
Flowering Plant Species

In many plant species, a subset of transcribed genes are characterized by strictly CG-context DNA methylation, referred to as gene body methylation (gbM). The mechanisms that establish gbM are unclear, yet flowering plant species naturally without gbM lack the DNA methyltransferase, CMT3, which maintains CHG (H = A, C, or T) and not CG methylation at constitutive heterochromatin. Here, we identify the mechanistic basis for gbM establishment by expressing CMT3 in a species naturally lacking CMT3. CMT3 expression reconstituted gbM through a progression of de novo CHG methylation on expressed genes, followed by the accumulation of CG methylation that could be inherited even following loss of the CMT3 transgene. Thus, gbM likely originates from the simultaneous targeting of loci by pathways that promote euchromatin and heterochromatin, which primes genes for the formation of stably inherited epimutations in the form of CG DNA methylation.

scholarly journals Regulation of genome-wide DNA methylation by mobile small RNAs

2017 ◽  
Vol 217 (2) ◽  
pp. 540-546 ◽  
Author(s):  
Muluneh Tamiru ◽  
Thomas J. Hardcastle ◽  
Mathew G. Lewsey
Keyword(s):  
Dna Methylation ◽  
Small Rnas ◽  
Genome Wide

scholarly journals Phylogenetic Shifts in Gene Body Methylation Correlate with Gene Expression and Reflect Trait Conservation

2019 ◽  
Vol 37 (1) ◽  
pp. 31-43 ◽  
Author(s):  
Danelle K Seymour ◽  
Brandon S Gaut
Keyword(s):  
Gene Expression ◽  
Dna Methylation ◽  
Molecular Evolution ◽  
Methylation Status ◽  
Evolutionary Constraint ◽  
Gene Body ◽  
Gene Body Methylation ◽  
Plant Genomes ◽  
Genome Wide ◽  
Rates Of Molecular Evolution

Abstract A subset of genes in plant genomes are labeled with DNA methylation specifically at CG residues. These genes, known as gene-body methylated (gbM), have a number of associated characteristics. They tend to have longer sequences, to be enriched for intermediate expression levels, and to be associated with slower rates of molecular evolution. Most importantly, gbM genes tend to maintain their level of DNA methylation between species, suggesting that this trait is under evolutionary constraint. Given the degree of conservation in gbM, we still know surprisingly little about its function in plant genomes or whether gbM is itself a target of selection. To address these questions, we surveyed DNA methylation across eight grass (Poaceae) species that span a gradient of genome sizes. We first established that genome size correlates with genome-wide DNA methylation levels, but less so for genic levels. We then leveraged genomic data to identify a set of 2,982 putative orthologs among the eight species and examined shifts of methylation status for each ortholog in a phylogenetic context. A total of 55% of orthologs exhibited a shift in gbM, but these shifts occurred predominantly on terminal branches, indicating that shifts in gbM are rarely conveyed over time. Finally, we found that the degree of conservation of gbM across species is associated with increased gene length, reduced rates of molecular evolution, and increased gene expression level, but reduced gene expression variation across species. Overall, these observations suggest a basis for evolutionary pressure to maintain gbM status over evolutionary time.

scholarly journals The stem rust fungus Puccinia graminis f. sp. tritici induces centromeric small RNAs during late infection that direct genome-wide DNA methylation

2018 ◽  
Author(s):  
Jana Sperschneider ◽  
Ashley W. Jones ◽  
Jamila Nasim ◽  
Bo Xu ◽  
Silke Jacques ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Stem Rust ◽  
Small Rnas ◽  
Genome Stability ◽  
Cytosine Methylation ◽  
Rust Fungus ◽  
Epigenetic Silencing ◽  
Puccinia Graminis ◽  
Genome Wide ◽  
Late Wave

AbstractBackgroundSilencing of transposable elements (TEs) is essential for maintaining genome stability. Plants use small RNAs (sRNAs) to direct DNA methylation to TEs (RNA-directed DNA methylation; RdDM). Similar mechanisms of epigenetic silencing in the fungal kingdom have remained elusive.ResultsWe use sRNA sequencing and methylation data to gain insight into epigenetics in the dikaryotic fungus Puccinia graminis f. sp. tritici (Pgt), which causes the devastating stem rust disease on wheat. We use Hi-C data to define the Pgt centromeres and show that they are repeat-rich regions (∼250 kb) that are highly diverse in sequence between haplotypes and, like in plants, are enriched for young TEs. DNA cytosine methylation is particularly active at centromeres but also associated with genome-wide control of young TE insertions. Strikingly, over 90% of Pgt sRNAs and several RNAi genes are differentially expressed during infection. Pgt induces waves of functionally diversified sRNAs during infection. The early wave sRNAs are predominantly 21 nts with a 5’ uracil derived from genes. In contrast, the late wave sRNAs are mainly 22 nt sRNAs with a 5’ adenine and are strongly induced from centromeric regions. TEs that overlap with late wave sRNAs are more likely to be methylated, both inside and outside the centromeres, and methylated TEs exhibit a silencing effect on nearby genes.ConclusionsWe conclude that rust fungi use an epigenetic silencing pathway that resembles RdDM in plants. The Pgt RNAi machinery and sRNAs are under tight temporal control throughout infection and might ensure genome stability during sporulation.

scholarly journals Phylogenetic shifts in gene body methylation correlate with gene expression and reflect trait conservation

2019 ◽  
Author(s):  
Danelle K. Seymour ◽  
Brandon S. Gaut
Keyword(s):  
Gene Expression ◽  
Dna Methylation ◽  
Molecular Evolution ◽  
Methylation Status ◽  
Evolutionary Constraint ◽  
Gene Body ◽  
Gene Body Methylation ◽  
Plant Genomes ◽  
Genome Wide ◽  
Rates Of Molecular Evolution

ABSTRACTA subset of genes in plant genomes are labeled with DNA methylation specifically at CG residues. These genes, known as gene-body methylated (gbM), have a number of associated characteristics. They tend to have longer sequences, to be enriched for intermediate expression levels, and to be associated with slower rates of molecular evolution. Most importantly, gbM genes tend to maintain their level of DNA methylation between species, suggesting that this trait is under evolutionary constraint. Given the degree of conservation in gbM, we still know surprisingly little about its function in plant genomes or whether gbM is itself a target of selection. To address these questions, we surveyed DNA methylation across eight grass (Poaceae) species that span a gradient of genome sizes. We first established that genome size correlates with genome-wide DNA methylation levels, but less so for genic levels. We then leveraged genomic data to identify a set of 2,982 putative orthologs among the eight species and examined shifts of methylation status for each ortholog in a phylogenetic context. A total of 55% of orthologs exhibited a shift in gbM, but these shifts occurred predominantly on terminal branches, indicating that shifts in gbM are rarely conveyed over time. Finally, we found that the degree of conservation of gbM across species is associated with increased gene length, reduced rates of molecular evolution, and increased gene expression level, but reduced gene expression variation across species. Overall, these observations suggest a basis for evolutionary pressure to maintain gbM status over evolutionary time.

scholarly journals DNA Methylation Explains a Subset of Placental Gene Expression Differences Based on Ancestry and Altitude

2018 ◽  
Author(s):  
William E. Gundling ◽  
Priyadarshini Pantham ◽  
Nicholas P Illsley ◽  
Lourdes Echalar ◽  
Stacy Zamudio ◽  
...  
Keyword(s):  
Gene Expression ◽  
Dna Methylation ◽  
Birth Weight ◽  
Native Americans ◽  
High Altitude ◽  
Mrna Expression ◽  
European Ancestry ◽  
Gene Body Methylation ◽  
Genome Wide ◽  
Or Gene

Abstract:Objectives: The most pronounced effect of high altitude (>2700m) on reproductive outcomes is reduced birth weight. Indigenous Bolivians (Andean Native Americans) residing for generations at high altitudes have higher birth weights relative to more recent migrants of primarily European ancestry. Previous research demonstrated that the placenta is a key contributor to the preservation of Andean birth weight at high altitude. Our current research investigated how gene expression and epigenetics contributes to the conservation of birth weight at high altitude by examining mRNA expression and DNA methylation differences between placentas of Andeans and those of European ancestry residing at high and low altitude.Methods: Genome-wide mRNA expression and DNA methylation of villous placenta tissue was quantified utilizing microarray technology. Subjects were of Andean and European ancestry and resident at high (3600m) or low (400m) altitudes. Differentially expressed genes (DEGs) associated with altitude or ancestry were identified (FDR<0.1, |fold change|>1.25). To predict which DEGs could be regulated by methylation we tested for correlation between gene expression and methylation values.Results: 69 DEGs associated with altitude (n=36) or ancestry (n=34) were identified. Altitude-associated DEGs included members of the AP-1 transcription factor family. Ancestry-associated DEGs were implicated in inflammatory pathways and associated with pro-angiogenic macrophages. More ancestry-associated DEGs correlated significantly (n=17) (FDR<0.1) with promoter or gene body methylation (p=0.0242) when compared to altitude associated DEGs (n=8).Conclusions:Compared to altitude-associated DEGs, methylation regulates more ancestry-associated DEGs, potentially allowing for rapid modification in the expression of inflammatory genes to attract pro-angiogenic macrophages as a means of promoting placental capillary growth in Andeans, regardless of altitude.

scholarly journals H3K9me3 is Required for Inheritance of Small RNAs that Target a Unique Subset of Newly Evolved Genes

2018 ◽  
Author(s):  
Itamar Lev ◽  
Hila Gingold ◽  
Oded Rechavi
Keyword(s):  
Rna Interference ◽  
Caenorhabditis Elegans ◽  
Small Rnas ◽  
Foreign Gene ◽  
Small Interfering Rnas ◽  
Endogenous Gene ◽  
C Elegans ◽  
Histone 3 ◽  
Repressive Chromatin ◽  
Genome Wide

AbstractIn Caenorhabditis elegans, RNA interference (RNAi) responses can transmit across generations via small RNAs. RNAi inheritance is associated with Histone-3-Lysine-9 tri-methylation (H3K9me3) of the targeted genes. In other organisms, maintenance of silencing requires a feed-forward loop between H3K9me3 and small RNAs. Here we show that in C. elegans not only is H3K9me3 unnecessary for inheritance, the modification’s function depends on the identity of the RNAi-targeted gene. We found an asymmetry in the requirement for H3K9me3 and the main worm H3K9me3 methyltransferases, SET-25 and SET-32. Both methyltransferases promote heritable silencing of the foreign gene gfp, but are dispensable for silencing of the endogenous gene oma-1. Genome-wide examination of heritable endogenous small interfering RNAs (endo-siRNAs) revealed that the SET-25-dependent heritable endo-siRNAs target newly acquired and highly H3K9me3 marked genes. Thus, “repressive” chromatin marks could be important specifically for heritable silencing of genes which are flagged as “foreign”, such as gfp.

scholarly journals Global reinforcement of DNA methylation through enhancement of RNA-directed DNA methylation ensures sexual reproduction in rice

2020 ◽  
Author(s):  
Lili Wang ◽  
Longjun Zeng ◽  
Kezhi Zheng ◽  
Tianxin Zhu ◽  
Yumeng Yin ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Sexual Reproduction ◽  
De Novo ◽  
Rice Genome ◽  
Biological Significance ◽  
Reproductive Organs ◽  
Epigenetic Mark ◽  
Small Interfering Rnas ◽  
Genome Wide ◽  
Global Increase

AbstractDNA methylation is an important epigenetic mark that regulates the expression of genes and transposons. RNA-directed DNA methylation (RdDM) is the main molecular pathway responsible for de novo DNA methylation in plants. In Arabidopsis, however, mutations in RdDM genes cause no visible developmental defects, which raising the question of the biological significance of RdDM in plant development. Here, we isolated and cloned Five Elements Mountain 1 (FEM1), which encodes an RNA-dependent RNA polymerase. Mutation in FEM1 substantially decreased genome-wide CHH methylation levels and abolished the accumulation of 24-nt small interfering RNAs. Moreover, male and female reproductive development was disturbed, which led to the sterility of fem1 mutants. In wild-type (WT) plants but not in fem1 mutants, genome-wide CHH DNA methylation levels were greater in panicles, stamens, and pistils than in seedlings. The global increase of methylation in reproductive organs of the WT was attributed to enhancement of RdDM activity including FEM1 activity. More than half of all encoding genes in the rice genome overlapped with hypermethylated regions in the sexual organs of the WT, and many of them appear to be directly regulated by an increase in DNA methylation.Our results demonstrate that a global increase of DNA methylation through enhancement of RdDM activity in reproductive organs ensures sexual reproduction of rice.

scholarly journals piRNAs prevent runaway amplification of siRNAs from ribosomal RNAs and histone mRNAs

2020 ◽  
Author(s):  
Brooke E. Montgomery ◽  
Tarah Vijayasarathy ◽  
Taylor N. Marks ◽  
Kailee J. Reed ◽  
Taiowa A. Montgomery
Keyword(s):  
Rna Interference ◽  
Small Rnas ◽  
Rnai Pathway ◽  
Specific Class ◽  
Biological Processes ◽  
Small Interfering Rnas ◽  
Ribosomal Rnas ◽  
Feed Forward ◽  
Histone Mrnas ◽  
Low Levels

ABSTRACTPiwi-interacting RNAs (piRNAs) are a largely germline-specific class of small RNAs found in animals. Although piRNAs are best known for silencing transposons, they regulate many different biological processes. Here we identify a role for piRNAs in preventing runaway amplification of small interfering RNAs (siRNAs) from certain genes, including ribosomal RNAs (rRNAs) and histone mRNAs. In Caenorhabditis elegans, rRNAs and some histone mRNAs are heavily targeted by piRNAs, which facilitates their entry into an endogenous RNA interference (RNAi) pathway involving a class of siRNAs called 22G-RNAs. Under normal conditions, rRNAs and histone mRNAs produce relatively low levels of 22G-RNAs. But if piRNAs are lost, 22G-RNA production is highly elevated. We show that 22G-RNAs produced downstream of piRNAs likely function in a feed-forward amplification circuit. Thus, our results suggest that piRNAs facilitate low-level 22G-RNA production while simultaneously obstructing the 22G-RNA machinery to prevent runaway amplification from certain RNAs. Histone mRNAs and rRNAs are unique from other cellular RNAs in lacking polyA tails, which may promote feed-forward amplification of 22G-RNAs. In support of this, we show that the subset of histone mRNAs that contain polyA tails are largely resistant to silencing in piRNA mutants.

scholarly journals DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Manu J Dubin ◽  
Pei Zhang ◽  
Dazhe Meng ◽  
Marie-Stanislas Remigereau ◽  
Edward J Osborne ◽  
...  
Keyword(s):  
Dna Methylation ◽  
Local Adaptation ◽  
Dna Methyltransferase ◽  
Association Studies ◽  
Genome Wide Association Studies ◽  
Gene Body Methylation ◽  
Genome Wide ◽  
Different Temperatures ◽  
Cis And Trans ◽  
Methylation Variation

Epigenome modulation potentially provides a mechanism for organisms to adapt, within and between generations. However, neither the extent to which this occurs, nor the mechanisms involved are known. Here we investigate DNA methylation variation in Swedish Arabidopsis thaliana accessions grown at two different temperatures. Environmental effects were limited to transposons, where CHH methylation was found to increase with temperature. Genome-wide association studies (GWAS) revealed that the extensive CHH methylation variation was strongly associated with genetic variants in both cis and trans, including a major trans-association close to the DNA methyltransferase CMT2. Unlike CHH methylation, CpG gene body methylation (GBM) was not affected by growth temperature, but was instead correlated with the latitude of origin. Accessions from colder regions had higher levels of GBM for a significant fraction of the genome, and this was associated with increased transcription for the genes affected. GWAS revealed that this effect was largely due to trans-acting loci, many of which showed evidence of local adaptation.

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