Abstract
In plants, CG DNA methylation is prevalent in the transcribed regions of many constitutively expressed genes (gene body methylation; gbM), but the origin and function of gbM remain unknown. Here we report the discovery that Eutrema salsugineum has lost gbM from its genome, to our knowledge the first instance for an angiosperm. Of all known DNA methyltransferases, only CHROMOMETHYLASE 3 (CMT3) is missing from E. salsugineum Identification of an additional angiosperm, Conringia planisiliqua, which independently lost CMT3 and gbM, supports that CMT3 is required for the establishment of gbM. Detailed analyses of gene expression, the histone variant H2A.Z, and various histone modifications in E. salsugineum and in Arabidopsis thaliana epigenetic recombinant inbred lines found no evidence in support of any role for gbM in regulating transcription or affecting the composition and modification of chromatin over evolutionary timescales.
Highlights
In plants, CG DNA methylation is prevalent in the transcribed regions of many constitutively expressed genes, but the origin and function of gbM remain unknown
Cytosine DNA methylation occurs in three sequence contexts: Methylated CG is catalyzed by METHYLTRANSFERASE 1 (MET1), mCHG by CHROMOMETHYLASE 3 (CMT3), and mCHH by DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2) or CHROMOMETHYLASE 2 (CMT2) [1]
We propose that the establishment of gbM might involve the self-reinforcing loop between CMT3 and the histone H3 lysine 9 (H3K9) methyltransferase KRYPTONITE/SUVH4 (KYP) [13, 14] in addition to transcription, similar to a model proposed by Inagaki and Kakutani [15]
Summary
In E. salsugineum the percentage of paired CHG sites that were highly methylated is significantly lower than wild-type A. thaliana and again similar to the cmt mutant, suggesting that the mCHG in E. salsugineum is likely a result of RdDM activity (Fig. 1 E and F). Taken together, these results indicated that E. salsugineum does not have CMT3 activity. RNA-seq analysis showed that E. salsugineum genes predicted to have contained gbM exhibited similar transcription levels to their A. thaliana orthologs (Fig. 4A) These results suggest that gbM may have a limited role in transcriptional regulation. GbM is presumably absent from E. salsugineum for a considerable amount of time, the distribution pattern of H2A.Z remained comparable to that in A. thaliana
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