The AREB1 Transcription Factor Influences Histone Acetylation to Regulate Drought Responses and Tolerance in Populus trichocarpa

Abstract

Plants develop tolerance to drought by activating genes with altered levels of epigenetic modifications. Specific transcription factors are involved in this activation, but the molecular connections within the regulatory system are unclear. Here, we analyzed genome-wide acetylated lysine residue 9 of histone H3 (H3K9ac) enrichment and examined its association with transcriptomes in Populus trichocarpa under drought stress. We revealed that abscisic acid-Responsive Element (ABRE) motifs in promoters of the drought-responsive genes PtrNAC006, PtrNAC007, and PtrNAC120 are involved in H3K9ac enhancement and activation of these genes. Overexpressing these PtrNAC genes in P. trichocarpa resulted in strong drought-tolerance phenotypes. We showed that the ABRE binding protein PtrAREB1-2 binds to ABRE motifs associated with these PtrNAC genes and recruits the histone acetyltransferase unit ADA2b-GCN5, forming AREB1-ADA2b-GCN5 ternary protein complexes. Moreover, this recruitment enables GCN5-mediated histone acetylation to enhance H3K9ac and enrich RNA polymerase II specifically at these PtrNAC genes for the development of drought tolerance. CRISPR editing or RNA interference-mediated downregulation of any of the ternary members results in highly drought-sensitive P. trichocarpa. Thus, the combinatorial function of the ternary proteins establishes a coordinated histone acetylation and transcription factormediated gene activation for drought response and tolerance in Populus species.

Synergistic regulation of drought‐responsive genes by transcription factor OsbZIP23 and histone modification in rice

“…On the other hand, OsbZIP23 overexpression in rice led to an increase in the binding levels of OsbZIP23 to the dehydrin gene promoters, but did not affect the H3K4me3 modification levels (Figure S9). This is consistent with a recent reported result that AREB1 overexpression alone in poplar protoplasts could not change histone H3K9 acetylation (H3K9ace) modification levels, but co‐overexpression of ADA2b and GCN5 together led to a significant increase in H3K9ace modification levels (Li et al 2019). OsbZIP23 may work together with an unknown H3K4 methyltransferase such as SDG723 to regulate the H3K4m3 modification levels in rice.…”

Epigenetic regulation in plant abiotic stress responses

“…This finding suggests that the PRC complex negatively regulates ABA‐dependent drought resistance via transcriptional repression of the ANAC019 and ANAC055 TFs. In Populus trichocarpa , Li et al (2019) reported that a number of drought‐responsive NAC TFs contain ABRE sequences in their promoters. AREB1 binds to the ABRE sequences of NAC genes and recruits the ADA2b‐GCN5 histone acetylation module to confer H3K9Ac, leading to activation of the PtrNAC genes and increasing drought resistance.…”

Epigenetic signatures of stress adaptation and flowering regulation in response to extended drought and recovery in Zea mays

“…For instance, acetylation of histone H3 at lysine 9 (H3K9ac) is a chromatin mark found around gene Transcription Start Sites (TSSs) and closely correlated with transcription activation during plant development and differentiation (Du et al, ; He et al, ; Wang et al, ). Moreover, time‐course analyses of histone modifications in plant tissues have shown dynamic changes of H3K9ac in response to environmental stimuli and stresses (Hu et al, ; Li et al, ; Zheng et al, ).…”