Epigenetic regulation of spurious transcription initiation in Arabidopsis

Abstract

In plants, epigenetic regulation is critical for silencing transposons and maintaining proper gene expression. However, its impact on the genome-wide transcription initiation landscape remains elusive. By conducting a genome-wide analysis of transcription start sites (TSSs) using cap analysis of gene expression (CAGE) sequencing, we show that thousands of TSSs are exclusively activated in various epigenetic mutants of Arabidopsis thaliana and referred to as cryptic TSSs. Many have not been identified in previous studies, of which up to 65% are contributed by transposons. They possess similar genetic features to regular TSSs and their activation is strongly associated with the ectopic recruitment of RNAPII machinery. The activation of cryptic TSSs significantly alters transcription of nearby TSSs, including those of genes important for development and stress responses. Our study, therefore, sheds light on the role of epigenetic regulation in maintaining proper gene functions in plants by suppressing transcription from cryptic TSSs.

Natural temperature fluctuations promote COOLAIR regulation of FLC

“…All the independent transgenes analyzed produce new antisense transcripts initiating in the first intron. Consistent with this, recent genome-wide measurements of TSSs showed that extensive alternative intragenic transcriptional initiation occurs in Arabidopsis, and this can be affected by cold (Kindgren et al 2018), cotranscriptional RNA degradation (Thieffry et al 2020;Thomas et al 2020), or mutants disrupted in chromatin signaling (Nielsen et al 2019;Le et al 2020). The activation of alternative TSSs significantly influences transcription from nearby TSSs, and thus is important for plant development and adaptation to environmental changes (Kindgren et al 2018;Nielsen et al 2019;Le et al 2020;Thieffry et al 2020;Thomas et al 2020).…”

Repression of CHROMOMETHYLASE 3 prevents epigenetic collateral damage in Arabidopsis

“…However, errors in restricting CMT3 to heterochromatin are inevitable on an evolutionary timescale ( Zhang et al, 2020 ) and recent studies indicate that CMT3-induced methylation of genes precedes gbM ( Wendte et al, 2019 ). Because gbM can be stably maintained over many generations by MET1 and its functional significance is debatable ( Bewick et al, 2016 ; Bewick et al, 2019 ; Choi et al, 2020 ; Coleman-Derr and Zilberman, 2012 ; Le et al, 2020 ; Picard and Gehring, 2017 ; Shahzad et al, 2021 ; Takuno and Gaut, 2013 ; Wendte et al, 2019 ; Williams et al, 2021 ; Zilberman, 2017 ), it cannot be excluded that gbM is merely an evolutionary record of epigenetic collateral damage events that occurred in the past ( Bewick and Schmitz, 2017 ; Bewick et al, 2017 ). Our results suggest that derepressed CMT3 and MET1 both prefer genic regions characterized by increased nucleosome stability ( Figure 4 ).…”

Repression of CHROMOMETHYLASE 3 Prevents Epigenetic Collateral Damage in Arabidopsis

“…However, errors in restricting CMT3 to heterochromatin are inevitable on an evolutionary timescale (Zhang et al, 2020) and recent studies indicate that CMT3-induced methylation of genes precedes gbM (Wendte et al, 2019). Because gbM can be stably maintained over many generations by MET1 and its functional significance is debatable (Bewick et al, 2016(Bewick et al, , 2019Choi et al, 2019;Coleman-Derr and Zilberman, 2012;Le et al, 2020;Picard and Gehring, 2017;Shahzad et al, 2021;Takuno and Gaut, 2013;Wendte et al, 2019;Williams et al, 2021;Zilberman, 2017), it cannot be excluded that gbM is merely an evolutionary record of epigenetic collateral damage events that occurred in the past . Our results suggest that…”