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A position effect on the heritability of epigenetic silencing.

Singh J, Freeling M, Lisch D - PLoS Genet. (2008)

Bottom Line: In animals and yeast, position effects have been well documented.In contrast, there are few examples of position effects in plants, and there are no documented examples in either plants or animals for positions that are associated with the reversal of previously established silenced states.To our knowledge, this is the first documented example of a position effect that is associated with the reversal of epigenetic silencing.

View Article: PubMed Central - PubMed

Affiliation: Plant Science Department, McGill University, Macdonald Campus, Ste Anne de Bellevue, Quebec, Canada.

ABSTRACT
In animals and yeast, position effects have been well documented. In animals, the best example of this process is Position Effect Variegation (PEV) in Drosophila melanogaster. In PEV, when genes are moved into close proximity to constitutive heterochromatin, their expression can become unstable, resulting in variegated patches of gene expression. This process is regulated by a variety of proteins implicated in both chromatin remodeling and RNAi-based silencing. A similar phenomenon is observed when transgenes are inserted into heterochromatic regions in fission yeast. In contrast, there are few examples of position effects in plants, and there are no documented examples in either plants or animals for positions that are associated with the reversal of previously established silenced states. MuDR transposons in maize can be heritably silenced by a naturally occurring rearranged version of MuDR. This element, Muk, produces a long hairpin RNA molecule that can trigger DNA methylation and heritable silencing of one or many MuDR elements. In most cases, MuDR elements remain inactive even after Muk segregates away. Thus, Muk-induced silencing involves a directed and heritable change in gene activity in the absence of changes in DNA sequence. Using classical genetic analysis, we have identified an exceptional position at which MuDR element silencing is unstable. Muk effectively silences the MuDR element at this position. However, after Muk is segregated away, element activity is restored. This restoration is accompanied by a reversal of DNA methylation. To our knowledge, this is the first documented example of a position effect that is associated with the reversal of epigenetic silencing. This observation suggests that there are cis-acting sequences that alter the propensity of an epigenetically silenced gene to remain inactive. This raises the interesting possibility that an important feature of local chromatin environments may be the capacity to erase previously established epigenetic marks.

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Related in: MedlinePlus

A graphic representation of a lineage in which MuDR(p5) and a duplicate copy of that element were crossed to a Muk heterozygote.Percent figures refer to the summarized frequency of spotted progeny kernels derived from each cross.
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pgen-1000216-g009: A graphic representation of a lineage in which MuDR(p5) and a duplicate copy of that element were crossed to a Muk heterozygote.Percent figures refer to the summarized frequency of spotted progeny kernels derived from each cross.

Mentions: If the reactivation effect we observe for MuDR(p5) were a function of position, then we would expect that, if this element transposed to a new position, it would exhibit a more typical heritable response to Muk. To test this hypothesis, plants carrying MuDR(p5), a transposed copy of this element at a second unlinked position and Muk were test crossed (Figure 9). Resulting progeny plants grown from spotted kernels were genotyped for MuDR(p5) and Muk and test crossed a second time (Table 7). Plants carrying MuDR(p5) that lacked Muk gave rise to ears that segregated for one or more active MuDR elements and averaged 55% spotted progeny kernels. In contrast, siblings that inherited only the second MuDR element and not MuDR(p5) gave rise to a much lower frequency of spotted kernels (5%), consistent with the kind of heritable silencing that is typical for MuDR elements after having been exposed to Muk. These results suggest that, while MuDR(p5) reactivates once Muk is segregated away, the duplicate copy of this element remained heritably silenced. These data strongly suggest that the reduction of heritable silencing at MuDR(p5) is a function of chromosomal position and not sequence, since this effect can be reversed following transposition.


A position effect on the heritability of epigenetic silencing.

Singh J, Freeling M, Lisch D - PLoS Genet. (2008)

A graphic representation of a lineage in which MuDR(p5) and a duplicate copy of that element were crossed to a Muk heterozygote.Percent figures refer to the summarized frequency of spotted progeny kernels derived from each cross.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2563033&req=5

pgen-1000216-g009: A graphic representation of a lineage in which MuDR(p5) and a duplicate copy of that element were crossed to a Muk heterozygote.Percent figures refer to the summarized frequency of spotted progeny kernels derived from each cross.
Mentions: If the reactivation effect we observe for MuDR(p5) were a function of position, then we would expect that, if this element transposed to a new position, it would exhibit a more typical heritable response to Muk. To test this hypothesis, plants carrying MuDR(p5), a transposed copy of this element at a second unlinked position and Muk were test crossed (Figure 9). Resulting progeny plants grown from spotted kernels were genotyped for MuDR(p5) and Muk and test crossed a second time (Table 7). Plants carrying MuDR(p5) that lacked Muk gave rise to ears that segregated for one or more active MuDR elements and averaged 55% spotted progeny kernels. In contrast, siblings that inherited only the second MuDR element and not MuDR(p5) gave rise to a much lower frequency of spotted kernels (5%), consistent with the kind of heritable silencing that is typical for MuDR elements after having been exposed to Muk. These results suggest that, while MuDR(p5) reactivates once Muk is segregated away, the duplicate copy of this element remained heritably silenced. These data strongly suggest that the reduction of heritable silencing at MuDR(p5) is a function of chromosomal position and not sequence, since this effect can be reversed following transposition.

Bottom Line: In animals and yeast, position effects have been well documented.In contrast, there are few examples of position effects in plants, and there are no documented examples in either plants or animals for positions that are associated with the reversal of previously established silenced states.To our knowledge, this is the first documented example of a position effect that is associated with the reversal of epigenetic silencing.

View Article: PubMed Central - PubMed

Affiliation: Plant Science Department, McGill University, Macdonald Campus, Ste Anne de Bellevue, Quebec, Canada.

ABSTRACT
In animals and yeast, position effects have been well documented. In animals, the best example of this process is Position Effect Variegation (PEV) in Drosophila melanogaster. In PEV, when genes are moved into close proximity to constitutive heterochromatin, their expression can become unstable, resulting in variegated patches of gene expression. This process is regulated by a variety of proteins implicated in both chromatin remodeling and RNAi-based silencing. A similar phenomenon is observed when transgenes are inserted into heterochromatic regions in fission yeast. In contrast, there are few examples of position effects in plants, and there are no documented examples in either plants or animals for positions that are associated with the reversal of previously established silenced states. MuDR transposons in maize can be heritably silenced by a naturally occurring rearranged version of MuDR. This element, Muk, produces a long hairpin RNA molecule that can trigger DNA methylation and heritable silencing of one or many MuDR elements. In most cases, MuDR elements remain inactive even after Muk segregates away. Thus, Muk-induced silencing involves a directed and heritable change in gene activity in the absence of changes in DNA sequence. Using classical genetic analysis, we have identified an exceptional position at which MuDR element silencing is unstable. Muk effectively silences the MuDR element at this position. However, after Muk is segregated away, element activity is restored. This restoration is accompanied by a reversal of DNA methylation. To our knowledge, this is the first documented example of a position effect that is associated with the reversal of epigenetic silencing. This observation suggests that there are cis-acting sequences that alter the propensity of an epigenetically silenced gene to remain inactive. This raises the interesting possibility that an important feature of local chromatin environments may be the capacity to erase previously established epigenetic marks.

Show MeSH
Related in: MedlinePlus