A pair of transposon-derived proteins function in a histone acetyltransferase complex for active DNA demethylation

Abstract

Transposons are generally kept silent by epigenetic mechanisms including DNA methylation. Here, we identified a pair of Harbinger transposon-derived proteins (HDPs), HDP1 and HDP2, as anti-silencing factors in Arabidopsis. hdp1 and hdp2 mutants displayed an enhanced silencing of transgenes and some transposons. Phylogenetic analyses revealed that HDP1 and HDP2 were co-domesticated from the Harbinger transposon-encoded transposase and DNA-binding protein, respectively. HDP1 interacts with HDP2 in the nucleus, analogous to their transposon counterparts. Moreover, HDP1 and HDP2 are associated with IDM1, IDM2, IDM3 and MBD7 that constitute a histone acetyltransferase complex functioning in DNA demethylation. HDP2 and the methyl-DNA-binding protein MBD7 share a large set of common genomic binding sites, indicating that they jointly determine the target specificity of the histone acetyltransferase complex. Thus, our data revealed that HDP1 and HDP2 constitute a functional module that has been recruited to a histone acetyltransferase complex to prevent DNA hypermethylation and epigenetic silencing.

The MBD7 complex promotes expression of methylated transgenes without significantly altering their methylation status

“…The number of cytosines in each sequence context within the quantified regions in ( D ) is indicated in parentheses. Note that the two d35S promoters driving LUC and NPTII are 94% identical in sequences, thus the DNA methylation data shown includes both multi-mapping and unique reads. DOI: http://dx.doi.org/10.7554/eLife.19893.019

10.7554/eLife.19893.020Figure 6—figure supplement 4.Gene expression at previously characterized loci in mbd7 and lil mutants.( A ) Normalized expression values (FPKM; fragments per kilobase mapped) of control and mutant RNA-seq samples at genes previously shown to be associated with hyper DMRs and to display reduced expression by qPCR in mutants of the MBD7 complex (Lang et al, 2015; Li et al, 2015b; Qian et al, 2014; Duan et al, 2017; Qian et al, 2012). Genes marked by an ‘a’ were assessed in Lang et al (2015), ‘b’ in Qian et al (2014), ‘c’ in Qian et al (2012), ‘d’ in Duan et al (2017) and ‘e’ in Li et al (2015b) and the two genes marked by a ‘^' were assayed under heat stress conditions in Lang et al (2015).

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“…Genes marked by an ‘a’ were assessed in Lang et al (2015), ‘b’ in Qian et al (2014), ‘c’ in Qian et al (2012), ‘d’ in Duan et al (2017) and ‘e’ in Li et al (2015b) and the two genes marked by a ‘^' were assayed under heat stress conditions in Lang et al (2015). The asterisk (*) marks the only gene consistently down-regulated (>2x) in any of the mutants tested. DOI: http://dx.doi.org/10.7554/eLife.19893.020…”

A methylated‐DNA‐binding complex required for plant development mediates transcriptional activation of promoter methylated genes

“…The DNA glycosylases tend to target transposable elements adjacent to genes and thus prevent spreading of DNA methylation and transcriptional silencing from transposable elements to nearby genes (Penterman et al ; Gehring et al ; Hsieh et al ; Tang et al ). An anti‐silencing protein complex, IDM, was thought to target ROS1, resulting in DNA demethylation at specific genomic loci (Qian et al ; Lang et al ; Wang et al ; Duan et al ; Li et al ). The active DNA demethylation mechanism is involved in diverse biological processes including seed development and dormancy (Gehring et al ; Zhu et al ), fruit ripening (Liu et al ; Lang et al ), stomata formation (Yamamuro et al ), and nodule development (Satge et al ), suggesting biological significance of the active DNA demethylation mechanism.…”

A group of SUVH methyl‐DNA binding proteins regulate expression of the DNA demethylase ROS1 in Arabidopsis

“…The transgenic plants with SUC2 expression would take up sucrose in excess from sucrose‐containing media, resulting in severe growth inhibition; mutants with silenced 35S‐SUC2 do not show such growth inhibition. Using this genetic system, we identified a number of cellular factors that regulate the active DNA demethylation pathway, including components of the RdDM pathway (Lei et al ; Qian et al ; Duan et al ; Lei et al ; Duan et al ). Mutations in SUVH1 resulted in a partial reduction in the growth inhibition on sucrose‐containing media (Figure A).…”