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Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification.

Lippman Z, May B, Yordan C, Singer T, Martienssen R - PLoS Biol. (2003)

Bottom Line: More recently, transposon silencing has been associated with DNA methylation, histone H3 lysine-9 methylation (H3mK9), and RNA interference (RNAi).According to their pattern of transposon regulation, the mutants can be divided into two groups, which suggests that there are distinct, but interacting, complexes or pathways involved in transposon silencing.Furthermore, different transposons tend to be susceptible to different forms of epigenetic regulation.

View Article: PubMed Central - PubMed

Affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

ABSTRACT
Heritable, but reversible, changes in transposable element activity were first observed in maize by Barbara McClintock in the 1950s. More recently, transposon silencing has been associated with DNA methylation, histone H3 lysine-9 methylation (H3mK9), and RNA interference (RNAi). Using a genetic approach, we have investigated the role of these modifications in the epigenetic regulation and inheritance of six Arabidopsis transposons. Silencing of most of the transposons is relieved in DNA methyltransferase (met1), chromatin remodeling ATPase (ddm1), and histone modification (sil1) mutants. In contrast, only a small subset of the transposons require the H3mK9 methyltransferase KRYPTONITE, the RNAi gene ARGONAUTE1, and the CXG methyltransferase CHROMOMETHYLASE3. In crosses to wild-type plants, epigenetic inheritance of active transposons varied from mutant to mutant, indicating these genes differ in their ability to silence transposons. According to their pattern of transposon regulation, the mutants can be divided into two groups, which suggests that there are distinct, but interacting, complexes or pathways involved in transposon silencing. Furthermore, different transposons tend to be susceptible to different forms of epigenetic regulation.

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Inheritance of Transposon ActivityPollen from homozygous mutant plants (m/m) was crossed onto WT (+/+) to generate backcrossed BC heterozygous seed (m/+). The parents were also self-pollinated as a control. Each class of progeny was then tested for expression of transposon mRNA, loss of DNA methylation, and changes in histone H3 methylation. Accumulation of transposon mRNA (+) or lack thereof (−) in each progeny genotype was used to determine whether the elements were silent (“cryptic”), reversibly activated, or heritably activated (“preset”).
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pbio.0000067-g001: Inheritance of Transposon ActivityPollen from homozygous mutant plants (m/m) was crossed onto WT (+/+) to generate backcrossed BC heterozygous seed (m/+). The parents were also self-pollinated as a control. Each class of progeny was then tested for expression of transposon mRNA, loss of DNA methylation, and changes in histone H3 methylation. Accumulation of transposon mRNA (+) or lack thereof (−) in each progeny genotype was used to determine whether the elements were silent (“cryptic”), reversibly activated, or heritably activated (“preset”).

Mentions: We selected five class I retrotransposons and one class II DNA transposon to assess silencing in the Arabidopsis ecotype Landsberg erecta (Ler) (WT) (Figure 1): the non-long terminal repeat (LTR) retrotransposon ATLINE1-4 (At2g01840); the gypsy-class LTR retroelements ATLANTYS2-1 (located between At4g03760 and At4g03770), ATLANTYS2-2 (located between At3g43680 and At3g43690), and ATGP1 (At4g03650); the copia-like element ATCOPIA4/COPIA-LIKE23 (At4g16870); and the MULE DNA transposon AtMu1 (At4g08680) (Singer et al. 2001). ATLANTYS2-1 and ATLANTYS2-2 were assayed with the same primer pair. In order to assess both activation and inheritance, mutants were backcrossed to WT, and F1 seed was planted and used in each assay alongside samples from selfed mutant and WT parents (Figure 1). By assessing transcript accumulation and association with methylated histone H3 as well as methylated DNA in backcrossed plants heterozygous for each mutation, we could determine whether each transposon remained silent (“cryptic”), was reversibly activated, or was heritably activated (“preset”) in each mutant.


Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification.

Lippman Z, May B, Yordan C, Singer T, Martienssen R - PLoS Biol. (2003)

Inheritance of Transposon ActivityPollen from homozygous mutant plants (m/m) was crossed onto WT (+/+) to generate backcrossed BC heterozygous seed (m/+). The parents were also self-pollinated as a control. Each class of progeny was then tested for expression of transposon mRNA, loss of DNA methylation, and changes in histone H3 methylation. Accumulation of transposon mRNA (+) or lack thereof (−) in each progeny genotype was used to determine whether the elements were silent (“cryptic”), reversibly activated, or heritably activated (“preset”).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC300680&req=5

pbio.0000067-g001: Inheritance of Transposon ActivityPollen from homozygous mutant plants (m/m) was crossed onto WT (+/+) to generate backcrossed BC heterozygous seed (m/+). The parents were also self-pollinated as a control. Each class of progeny was then tested for expression of transposon mRNA, loss of DNA methylation, and changes in histone H3 methylation. Accumulation of transposon mRNA (+) or lack thereof (−) in each progeny genotype was used to determine whether the elements were silent (“cryptic”), reversibly activated, or heritably activated (“preset”).
Mentions: We selected five class I retrotransposons and one class II DNA transposon to assess silencing in the Arabidopsis ecotype Landsberg erecta (Ler) (WT) (Figure 1): the non-long terminal repeat (LTR) retrotransposon ATLINE1-4 (At2g01840); the gypsy-class LTR retroelements ATLANTYS2-1 (located between At4g03760 and At4g03770), ATLANTYS2-2 (located between At3g43680 and At3g43690), and ATGP1 (At4g03650); the copia-like element ATCOPIA4/COPIA-LIKE23 (At4g16870); and the MULE DNA transposon AtMu1 (At4g08680) (Singer et al. 2001). ATLANTYS2-1 and ATLANTYS2-2 were assayed with the same primer pair. In order to assess both activation and inheritance, mutants were backcrossed to WT, and F1 seed was planted and used in each assay alongside samples from selfed mutant and WT parents (Figure 1). By assessing transcript accumulation and association with methylated histone H3 as well as methylated DNA in backcrossed plants heterozygous for each mutation, we could determine whether each transposon remained silent (“cryptic”), was reversibly activated, or was heritably activated (“preset”) in each mutant.

Bottom Line: More recently, transposon silencing has been associated with DNA methylation, histone H3 lysine-9 methylation (H3mK9), and RNA interference (RNAi).According to their pattern of transposon regulation, the mutants can be divided into two groups, which suggests that there are distinct, but interacting, complexes or pathways involved in transposon silencing.Furthermore, different transposons tend to be susceptible to different forms of epigenetic regulation.

View Article: PubMed Central - PubMed

Affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

ABSTRACT
Heritable, but reversible, changes in transposable element activity were first observed in maize by Barbara McClintock in the 1950s. More recently, transposon silencing has been associated with DNA methylation, histone H3 lysine-9 methylation (H3mK9), and RNA interference (RNAi). Using a genetic approach, we have investigated the role of these modifications in the epigenetic regulation and inheritance of six Arabidopsis transposons. Silencing of most of the transposons is relieved in DNA methyltransferase (met1), chromatin remodeling ATPase (ddm1), and histone modification (sil1) mutants. In contrast, only a small subset of the transposons require the H3mK9 methyltransferase KRYPTONITE, the RNAi gene ARGONAUTE1, and the CXG methyltransferase CHROMOMETHYLASE3. In crosses to wild-type plants, epigenetic inheritance of active transposons varied from mutant to mutant, indicating these genes differ in their ability to silence transposons. According to their pattern of transposon regulation, the mutants can be divided into two groups, which suggests that there are distinct, but interacting, complexes or pathways involved in transposon silencing. Furthermore, different transposons tend to be susceptible to different forms of epigenetic regulation.

Show MeSH
Related in: MedlinePlus