Paramutagenicity of a p1 epiallele in maize
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ORIGINAL PAPER
Paramutagenicity of a p1 epiallele in maize Wolfgang Goettel • Joachim Messing
Received: 28 June 2012 / Accepted: 16 August 2012 / Published online: 18 September 2012 Ó Springer-Verlag 2012
Abstract Complex silencing mechanisms in plants and other kingdoms target transposons, repeat sequences, invasive viral nucleic acids and transgenes, but also endogenous genes and genes involved in paramutation. Paramutation occurs in a heterozygote when a transcriptionally active allele heritably adopts the epigenetic state of a transcriptionally and/or post-transcriptionally repressed allele. P1-rr and its silenced epiallele P1-pr, which encode a Myb-like transcription factor mediating pigmentation in floral organs of Zea mays, differ in their cytosine methylation pattern and chromatin structure at a complex enhancer site. Here, we tested whether P1-pr is able to heritably silence its transcriptionally active P1-rr allele in a heterozygote and whether DNA methylation is associated with the establishment and maintenance of P1-rr silencing. We found that P1-pr participates in paramutation as the repressing allele and P1-rr as the sensitive allele. Silencing of P1-rr is highly variable compared to the inducing P1-pr resulting in a wide range of gene expression. Whereas cytosine methylation at P1-rr is negatively correlated with transcription and pigment levels after segregation of P1-pr, methylation lags behind the establishment of the repressed p1 gene expression. We propose a model in which P1-pr paramutation is triggered by changing epigenetic states of
Communicated by B. Friebe.
Electronic supplementary material The online version of this article (doi:10.1007/s00122-012-1970-z) contains supplementary material, which is available to authorized users. W. Goettel J. Messing (&) Waksman Institute of Microbiology, Rutgers University, 190 Frelinghuysen Road, Piscataway, NJ 08854, USA e-mail: [email protected]
transposons immediately adjacent to a P1-rr enhancer sequence. Considering the vast amount of transposable elements in the maize genome close to regulatory elements of genes, numerous loci could undergo paramutationinduced allele silencing, which could also have a significant impact on breeding agronomically important traits.
Introduction Paramutation is an epigenetic silencing phenomenon that occurs between homologous or allelic sequences (ArteagaVazquez and Chandler 2010; Chandler 2010; Chandler and Stam 2004; Erhard and Hollick 2011; Hollick 2010). Several epialleles—alleles that share an identical nucleotide sequence but differ in their epigenetic state—have been shown to participate in paramutation. Paramutation or paramutation-like silencing events have also been reported between two transgenes, and between transgenes and endogenous genes. Paramutation is defined as the interaction of two alleles in a heterozygote where one allele is able to reduce heritably the expression status of another allele. Consequently, paramutation is a violation of Mendel’s First Law, stating that genes leave a
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