Abstract
Paramutation is a well-studied epigenetic phenomenon in which trans communication between two different alleles leads to meiotically heritable transcriptional silencing of one of the alleles. Paramutation at the b1 locus involves RNA-mediated transcriptional silencing and requires specific tandem repeats that generate siRNAs. This study addressed three important questions: 1) are the tandem repeats sufficient for paramutation, 2) do they need to be in an allelic position to mediate paramutation, and 3) is there an association between the ability to mediate paramutation and repeat DNA methylation levels? Paramutation was achieved using multiple transgenes containing the b1 tandem repeats, including events with tandem repeats of only one half of the repeat unit (413 bp), demonstrating that these sequences are sufficient for paramutation and an allelic position is not required for the repeats to communicate. Furthermore, the transgenic tandem repeats increased the expression of a reporter gene in maize, demonstrating the repeats contain transcriptional regulatory sequences. Transgene-mediated paramutation required the mediator of paramutation1 gene, which is necessary for endogenous paramutation, suggesting endogenous and transgene-mediated paramutation both require an RNA-mediated transcriptional silencing pathway. While all tested repeat transgenes produced small interfering RNAs (siRNAs), not all transgenes induced paramutation suggesting that, as with endogenous alleles, siRNA production is not sufficient for paramutation. The repeat transgene-induced silencing was less efficiently transmitted than silencing induced by the repeats of endogenous b1 alleles, which is always 100% efficient. The variability in the strength of the repeat transgene-induced silencing enabled testing whether the extent of DNA methylation within the repeats correlated with differences in efficiency of paramutation. Transgene-induced paramutation does not require extensive DNA methylation within the transgene. However, increased DNA methylation within the endogenous b1 repeats after transgene-induced paramutation was associated with stronger silencing of the endogenous allele.
Highlights
Paramutation is a trans-interaction between specific alleles or transgenes that leads to a meiotically heritable change in the expression of one of the participating alleles or transgenes
While paramutation was first described in the 1950s and extensively studied through the 1960s, its underlying mechanism remained mysterious for many years
Scoring of plant pigment of the B’ allele. Nontransgenic sibling plants (B-I/b-N) progeny carrying transgene loci (TG/-) revealed that four out of ten pB, and five out of nine pBD transgene loci induced silencing of B-I (Figure 2B)
Summary
Paramutation is a trans-interaction between specific alleles or transgenes that leads to a meiotically heritable change in the expression of one of the participating alleles or transgenes. Alterations of b1 expression lead to a visual change in plant pigmentation, and the amount of pigment is a read-out of the b1 transcription level [3]. The two b1 alleles that participate in paramutation are B-I (BIntense) and B’; B-I is highly expressed and specifies dark purple pigmentation of the husk, sheath and tassel of the maize plant, while B’ is expressed at a much lower level and specifies light streaky pigmentation in the same plant tissues as B-I [3,13]. The high expressing B-I allele is unstable and can spontaneously change to B’ at variable frequencies (can be up to 10%; [13]). Alleles that do not participate in paramutation are referred to as neutral [14]
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