The role of DNA methylation, nucleosome occupancy and histone modifications in paramutation

Haring, Max; Bader, Rechien; Louwers, Marieke; Schwabe, Anne; Driel, Roel van; Stam, Maike

doi:10.1111/j.1365-313x.2010.04245.x

Cited by 58 publications

(82 citation statements)

References 70 publications

(106 reference statements)

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“…The current model for the transcriptional regulation involves changes in chromatin conformation and chromatin looping events that bring the enhancer repeats in proximity with the b1 promoter (Louwers et al 2009). This is consistent with observed changes in chromatin structure, nucleosome occupancy, posttranslational histone modifications, and DNA methylation at the b1 enhancer repeats associated with the differential transcriptional regulation of B9 and B-I (Haring et al 2010). …”

supporting

confidence: 72%

Diverse Gene-Silencing Mechanisms with Distinct Requirements for RNA Polymerase Subunits in Zea mays

2014

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In Zea mays, transcriptional regulation of the b1 (booster1) gene requires a distal enhancer and MEDIATOR OF PARA-MUTATION1 (MOP1), MOP2, and MOP3 proteins orthologous to Arabidopsis components of the RNA-dependent DNA methylation pathway. We compared the genetic requirements for MOP1, MOP2, and MOP3 for endogenous gene silencing by two hairpin transgenes with inverted repeats of the a1 (anthocyaninless1) gene promoter (a1pIR) and the b1 gene enhancer (b1IR), respectively. The a1pIR transgene induced silencing of endogenous A1 in mop1-1 and mop3-1, but not in Mop2-1 homozygous plants. This finding suggests that transgene-derived small interfering RNAs (siRNAs) circumvented the requirement for MOP1, a predicted RNA-dependent RNA polymerase, and MOP3, the predicted largest subunit of RNA polymerase IV (Pol IV). Because the Arabidopsis protein orthologous to MOP2 is the second largest subunit of Pol IV and V, our results may indicate that hairpin-induced siRNAs cannot bypass the requirement for the predicted scaffolding activity of Pol V. In contrast to a1pIR, the b1IR transgene silenced endogenous B1 in all three homozygous mutant genotypes-mop1-1, Mop2-1, and mop3-1-suggesting that transgene mediated b1 silencing did not involve MOP2-containing Pol V complexes. Based on the combined results for a1, b1, and three previously described loci, we propose a speculative hypothesis of locus-specific deployment of Pol II, MOP2-containing Pol V, or alternative versions of Pol V with second largest subunits other than MOP2 to explain the mechanistic differences in silencing at specific loci, including one example associated with paramutation.

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confidence: 72%

Diverse Gene-Silencing Mechanisms with Distinct Requirements for RNA Polymerase Subunits in Zea mays

2014

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“…Only one of the four loci we examined, At5g26345, had TCM-generated levels of m C early in the hybrid life cycle (3 DAS). Similar patterns occur in the maize paramutation locus BOOSTER1 and in Arabidopsis at the PHOSPHORIBOSYLANTHRANILATE ISOMERASE (PAI) locus (25,26). The m C level at the booster1 locus increases during early development and peaks when the plant has 10 leaves (26).…”

Section: Discussionmentioning

confidence: 69%

Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

Greaves

Eichten

Groszmann

et al. 2016

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

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Hybrid Arabidopsis plants undergo epigenetic reprogramming producing decreased levels of 24-nt siRNAs and altered patterns of DNA methylation that can affect gene expression. Driving the changes in methylation are the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM). In TCM/TCdM the methylation state of one allele is altered to resemble the other allele. We show that Pol IV-dependent sRNAs are required to establish TCM events. The changes in DNA methylation and the associated changes in sRNA levels in the F1 hybrid can be maintained in subsequent generations and affect hundreds of regions in the F2 epigenome. The inheritance of these altered epigenetic states varies in F2 individuals, resulting in individuals with genetically identical loci displaying different epigenetic states and gene expression profiles. The change in methylation at these regions is associated with the presence of sRNAs. Loci without any sRNA activity can have altered methylation states, suggesting that a sRNA-independent mechanism may also contribute to the altered methylation state of the F1 and F2 generations.H ybrid vigor, heterosis, is important in agriculture due to the increased performance of hybrid plants over parental lines. The increase in performance is attributable to changes in gene expression (1, 2) but how these changes result in the increased performance of the hybrid is still not known. The level of hybrid vigor is believed to correlate with the genetic distance between parental lines; however, hybrid vigor can occur in progeny derived from crosses of genetically similar parents. An example is found in intraspecific crosses between Arabidopsis thaliana accessions. In crosses between C24 and Landsberg erecta (Ler), up to a 100% increase in plant biomass and seed yield is observed (3). The different epigenomes of the two parental accessions could provide the diversity required to initiate gene expression changes and vigor-related characteristics. A number of laboratories have investigated whether there are epigenetic changes in Arabidopsis hybrids, whether they affect gene expression, and whether they contribute to the hybrid vigor phenotype (1, 3-6).We have previously established that F1 hybrids between Arabidopsis accessions undergo some epigenetic reprogramming. We found that the abundance of 24-nt siRNAs is reduced in F1 hybrids and that a second epigenetic system, DNA methylation ( m C), is also altered in the hybrid genome (1, 3, 5). The altered m C patterns in the hybrids involve the processes trans-chromosomal methylation (TCM) and trans-chromosomal demethylation (TCdM), where the m C state of one parental allele is altered to resemble the other allele (reviewed in ref. 7). Due to the presence of siRNAs at regions that undergo TCM/TCdM, we have suggested that siRNAs are the initiating molecules that establish these TCM/TCdM events (reviewed in ref. 8). In the hybrid nucleus, the complement of 24-nt siRNAs can interact with homologous sequences from either parent.The TCM and TCdM...

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“…29,30). Both At3g43340/50 and the booster1 locus in maize involve a donor segment suppressing a recipient segment through siRNA activity, m C, and histone modification (31)(32)(33). The late onset of TCM at At3g43340/50 is paralleled by the m C associated with the B locus, where the m C level increases up until the 10 leaf stage (33).…”

Section: Discussionmentioning

confidence: 98%

“…Both At3g43340/50 and the booster1 locus in maize involve a donor segment suppressing a recipient segment through siRNA activity, m C, and histone modification (31)(32)(33). The late onset of TCM at At3g43340/50 is paralleled by the m C associated with the B locus, where the m C level increases up until the 10 leaf stage (33). Paramutation can be sequence specific, with the B K55 and B-peru alleles being "immune" to paramutation (31), similar to our observations that the unmethylated At3g43340/50 locus of Cvi is not able to be involved in TCM.…”

Section: Discussionmentioning

confidence: 99%

Inheritance of Trans Chromosomal Methylation patterns from Arabidopsis F1 hybrids

Greaves

Groszmann

Wang

et al. 2014

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

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Hybridization in plants leads to transinteractions between the parental genomes and epigenomes that can result in changes to both 24 nt siRNA and cytosine methylation ( m C) levels in the hybrid. In Arabidopsis the principle processes altering the hybrid methylome are Trans Chromosomal Methylation (TCM) and Trans Chromosomal deMethylation (TCdM) in which the m C pattern of a genomic segment attains the same m C pattern of the corresponding segment on the other parental chromosome. We examined two loci that undergo TCM/TCdM in the Arabidopsis C24/Landsberg erecta (Ler) F1 hybrids, which show patterns of inheritance dependent on the properties of the particular donor and recipient chromosomal segments. At At1g64790 the TCM-and TCdMderived m C patterns are maintained in the F2 generation but are transmitted in outcrosses or backcrosses only by the C24 genomic segment. At a region between and adjacent to At3g43340 and At3g43350, the originally unmethylated Ler genomic segment receives the C24 m C pattern in the F1, which is then maintained in backcross plants independent of the presence of the parental C24 segment. In backcrosses to an unmethylated Ler allele, the newly methylated F1 Ler segment may act as a TCM source in a process comparable to paramutation in maize. TCM-derived m C patterns are associated with reduced expression of both At3g43340 and At3g43350 in F1 and F2 plants, providing support for such events influencing the transcriptome. The inheritance of the F1 m C patterns and the segregation of other genetic and epigenetic determinants may contribute to the reduced hybrid vigor in the F2 and subsequent generations.heterosis | chromatin | histones | RdDM

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The role of DNA methylation, nucleosome occupancy and histone modifications in paramutation

Cited by 58 publications

References 70 publications

Diverse Gene-Silencing Mechanisms with Distinct Requirements for RNA Polymerase Subunits in Zea mays

Diverse Gene-Silencing Mechanisms with Distinct Requirements for RNA Polymerase Subunits in Zea mays

Twenty-four–nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids

Inheritance of Trans Chromosomal Methylation patterns from Arabidopsis F1 hybrids

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