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Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication

Abstract

It has been suggested that gene silencing evolved as a defense against genomic parasites such as transposons1. This idea is based on analysis of mutations that reactivate transposons that are stably silenced2,3,4,5,6,7,8,9: they affect maintenance rather than initiation of silencing. Here we describe the cloning and characterization of a naturally occurring locus able to heritably silence the otherwise highly active MuDR transposon in maize. This locus, Mu killer (Muk), results from the inverted duplication of a partially deleted autonomous MuDR element located at the breakpoint of a genomic deletion. Muk produces a hybrid hairpin transcript that is processed into small RNAs, which are amplified when the target MuDR transcript is present. Muk provides the first example of a naturally occurring transposon derivative capable of initiating the heritable silencing of an active transposon family. Further, transposon-generated inverted duplications may be important for the generation of double-stranded RNAs used in gene silencing.

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Figure 1: Structures of MuDR and Muk.
Figure 2: Characterization of the Muk transcript.
Figure 3: Readthrough of the Mutator inverted duplication creates a hairpin transcript.
Figure 4: Muk produces small RNAs homologous to mudrA, which are amplified when both Muk and MuDR are present.

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Acknowledgements

The authors thank M. Roth-Woodhouse and C. Hale for critical review of the manuscript. Research was supported by grant DBI-0321726 from the US National Science Foundation.

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Correspondence to Damon Lisch.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Structure of the genomic deletion around the Muk inverted duplication. (PDF 578 kb)

Supplementary Fig. 2

Detection of a transcript that cosegregates with Muk. (PDF 917 kb)

Supplementary Fig. 3

No transitive silencing of mudrB is detected. (PDF 934 kb)

Supplementary Table 1

Sequences of primers used in the letter. (PDF 24 kb)

Supplementary Methods (PDF 32 kb)

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Slotkin, R., Freeling, M. & Lisch, D. Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37, 641–644 (2005). https://doi.org/10.1038/ng1576

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