Abstract
Progress in epigenetics has revealed mechanisms that can heritably regulate gene function independent of genetic alterations. Nevertheless, little is known about the role of epigenetics in evolution. This is due in part to scant data on epigenetic variation among natural populations. In plants, small interfering RNA (siRNA) is involved in both the initiation and maintenance of gene silencing by directing DNA methylation and/or histone methylation. Here, we report that, in the model plant Arabidopsis thaliana, a cluster of ∼24 nt siRNAs found at high levels in the ecotype Landsberg erecta (Ler) could direct DNA methylation and heterochromatinization at a hAT element adjacent to the promoter of FLOWERING LOCUS C (FLC), a major repressor of flowering, whereas the same hAT element in ecotype Columbia (Col) with almost identical DNA sequence, generates a set of low abundance siRNAs that do not direct these activities. We have called this hAT element MPF for Methylated region near Promoter of FLC, although de novo methylation triggered by an inverted repeat transgene at this region in Col does not alter its FLC expression. DNA methylation of the Ler allele MPF is dependent on genes in known silencing pathways, and such methylation is transmissible to Col by genetic crosses, although with varying degrees of penetrance. A genome-wide comparison of Ler and Col small RNAs identified at least 68 loci matched by a significant level of ∼24 nt siRNAs present specifically in Ler but not Col, where nearly half of the loci are related to repeat or TE sequences. Methylation analysis revealed that 88% of the examined loci (37 out of 42) were specifically methylated in Ler but not Col, suggesting that small RNA can direct epigenetic differences between two closely related Arabidopsis ecotypes.
Highlights
Epigenetics, defined as the study of heritable alteration in gene expression without changes in DNA sequence, has greatly expanded our understanding of inheritance [1]
From comparisons between Landsberg erecta (Ler) and Col of small RNA data produced by high-throughput sequencing, we identified at least 68 loci that are matched by significant levels of,24 nt small interfering RNA (siRNA), and 88% are methylated in Ler but not Col from a set of 42 loci that were examined
In addition to the previously described Mutator-like transposable element (TE) inserted in the first intron of FLOWERING LOCUS C (FLC) [19] in Ler, we found that a region located adjacent to the promoter of the FLC was methylated in Ler but not in Col (Figure 1A)
Summary
Epigenetics, defined as the study of heritable alteration in gene expression without changes in DNA sequence, has greatly expanded our understanding of inheritance [1]. Epigenetic differences could potentially contribute to evolution [3,4,5], studies of evolution and natural variation have still been focused mainly on sequence variation, and little is known about the role of epigenetic machinery in these processes. This is primarily due to the lack of evidence for epigenetic natural variation between populations. Small interfering RNAs (siRNAs), as a key player in the epigenetic machinery, have been well documented for their general role in gene silencing at both the transcriptional and posttranscriptional levels [6,7].
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