Limits...
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.

Show MeSH

Related in: MedlinePlus

A graphic representation of a lineage in which a plant carrying active MuDR(p5) and MuDR(p4) was crossed to a Muk homozygote, and resulting progeny plants were subsequently test crossed.Percent figures refer to the summarized frequency of spotted progeny kernels derived from each cross.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2563033&req=5

pgen-1000216-g008: A graphic representation of a lineage in which a plant carrying active MuDR(p5) and MuDR(p4) was crossed to a Muk homozygote, and resulting progeny plants were subsequently test crossed.Percent figures refer to the summarized frequency of spotted progeny kernels derived from each cross.

Mentions: In order to replicate the “rescue experiment”, a plant carrying active MuDR(p5) and MuDR(p4) elements was crossed to a Muk homozygote. Progeny plants were genotyped and test crossed (Figure 8). Plants that carried only MuDR(p4) and Muk gave an average ratio of spotted kernels of 6%, consistent with our previous result that MuDR(p4) without MuDR(p5) is heritably silenced by Muk. Plants that carried Muk with MuDR(p5) alone or with MuDR(p4) gave an average frequency of spotted progeny of 48%, consistent with reactivation of MuDR(p5) following the loss of Muk. Progeny of this cross that carried both MuDR(p5) and MuDR(p4) but that lacked Muk were test crossed again. One individual gave rise to a ratio of spotted kernels of 68%, consistent with the independent segregation of two active elements. In the next generation, somatic activity segregated with both elements; plants carrying both MuDR(p4) and MuDR(p5) gave rise to a 75% ratio, and those with either MuDR(p4) or MuDR(p5) by itself gave rise to roughly 50% ratios (Table 6). These data strongly support the hypothesis that, although MuDR(p4) is invariably silenced in the absence of MuDR(p5), a reactivated MuDR(p5) element can cause MuDR(p4) to reactivate as well.


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 a plant carrying active MuDR(p5) and MuDR(p4) was crossed to a Muk homozygote, and resulting progeny plants were subsequently test crossed.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-g008: A graphic representation of a lineage in which a plant carrying active MuDR(p5) and MuDR(p4) was crossed to a Muk homozygote, and resulting progeny plants were subsequently test crossed.Percent figures refer to the summarized frequency of spotted progeny kernels derived from each cross.
Mentions: In order to replicate the “rescue experiment”, a plant carrying active MuDR(p5) and MuDR(p4) elements was crossed to a Muk homozygote. Progeny plants were genotyped and test crossed (Figure 8). Plants that carried only MuDR(p4) and Muk gave an average ratio of spotted kernels of 6%, consistent with our previous result that MuDR(p4) without MuDR(p5) is heritably silenced by Muk. Plants that carried Muk with MuDR(p5) alone or with MuDR(p4) gave an average frequency of spotted progeny of 48%, consistent with reactivation of MuDR(p5) following the loss of Muk. Progeny of this cross that carried both MuDR(p5) and MuDR(p4) but that lacked Muk were test crossed again. One individual gave rise to a ratio of spotted kernels of 68%, consistent with the independent segregation of two active elements. In the next generation, somatic activity segregated with both elements; plants carrying both MuDR(p4) and MuDR(p5) gave rise to a 75% ratio, and those with either MuDR(p4) or MuDR(p5) by itself gave rise to roughly 50% ratios (Table 6). These data strongly support the hypothesis that, although MuDR(p4) is invariably silenced in the absence of MuDR(p5), a reactivated MuDR(p5) element can cause MuDR(p4) to reactivate as well.

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