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Polyploidy is an important evolutionary force, yet epigenetic mechanisms, such as DNA methylation, that regulate genome‐wide expression of duplicated genes remain largely unknown. Here, we useTragopogon(Asteraceae) as a model system to discover patterns and temporal dynamics of DNA methylation in recently formed polyploids.

The naturally occurring allotetraploidTragopogon miscellusformed in the last 95–100 yr from parental diploidsTragopogon dubiusandT. pratensis. We profiled the DNA methylomes of these three species using whole‐genome bisulfite sequencing.

Genome‐wide methylation levels inT. miscelluswere intermediate between its diploid parents. However, nonadditive CG and CHG methylation occurred in transposable elements (TEs), with variation among TE types. Most differentially methylated regions (DMRs) showed parental legacy, but some novel DMRs were detected in the polyploid. Differentially methylated genes (DMGs) were also identified and characterized.

This study provides the first assessment of both overall and locus‐specific patterns of DNA methylation in a recent natural allopolyploid and shows that novel methylation variants can be generated rapidly after polyploid formation. Together, these results demonstrate that mechanisms to regulate duplicate gene expression may arise soon after allopolyploid formation and that these mechanisms vary among genes.

 

In plants and mammals, DNA methylation plays a critical role in transcriptional silencing by delineating heterochromatin from transcriptionally active euchromatin. A homeostatic balance between heterochromatin and euchromatin is essential to genomic stability. This is evident in many diseases and mutants for heterochromatin maintenance, which are characterized by global losses of DNA methylation coupled with localized ectopic gains of DNA methylation that alter transcription. Furthermore, we have shown that genome-wide methylation patterns inArabidopsis thalianaare highly stable over generations, with the exception of rare epialleles. However, the extent to which natural variation in the robustness of targeting DNA methylation to heterochromatin exists, and the phenotypic consequences of such variation, remain to be fully explored. Here we describe the finding that heterochromatin and genic DNA methylation are highly variable among 725A. thalianaaccessions. We found that genic DNA methylation is inversely correlated with that in heterochromatin, suggesting that certain methylation pathway(s) may be redirected to genes upon the loss of heterochromatin. This redistribution likely involves a feedback loop involving the DNA methyltransferase, CHROMOMETHYLASE 3 (CMT3), H3K9me2, and histone turnover, as highly expressed, long genes with a high density of CMT3-preferred CWG sites are more likely to be methylated. Importantly, although the presence of CG methylation in genes alone may not affect transcription, genes containing CG methylation are more likely to become methylated at non-CG sites and silenced. These findings are consistent with the hypothesis that natural variation in DNA methylation homeostasis may underlie the evolution of epialleles that alter phenotypes.

 

In many plant species, a subset of transcribed genes are characterized by strictly CG-context DNA methylation, referred to as gene body methylation (gbM). The mechanisms that establish gbM are unclear, yet flowering plant species naturally without gbM lack the DNA methyltransferase, CMT3, which maintains CHG (H = A, C, or T) and not CG methylation at constitutive heterochromatin. Here, we identify the mechanistic basis for gbM establishment by expressing CMT3 in a species naturally lacking CMT3. CMT3 expression reconstituted gbM through a progression of de novo CHG methylation on expressed genes, followed by the accumulation of CG methylation that could be inherited even following loss of the CMT3 transgene. Thus, gbM likely originates from the simultaneous targeting of loci by pathways that promote euchromatin and heterochromatin, which primes genes for the formation of stably inherited epimutations in the form of CG DNA methylation.