Temporal modification of H3K9/14ac and H3K4me3 histone marks mediates mechano-responsive gene expression during the accommodation process in poplar

Abstract

Plants can attenuate their molecular response to repetitive mechanical stimulation as a function of their mechanical history. For instance, a single bending of stem is sufficient to attenuate the gene expression in poplar plants to the subsequent mechanical stimulation, and the state of desensitization can last for several days. The role of histone modifications in memory gene expression and modulating plant response to abiotic or biotic signals is well known. However, such information is still lacking to explain the attenuated expression pattern of mechano-responsive genes in plants under repetitive stimulation. Using poplar as a model plant in this study, we first measured the global level of H3K9/14ac and H3K4me3 marks in the bent stem. The result shows that a single mild bending of the stem for 6 seconds is sufficient to alter the global level of the H3K9/14ac mark in poplar, highlighting the fact that plants are extremely sensitive to mechanical signals. Next, we analyzed the temporal dynamics of these two active histone marks at attenuated (PtaZFP2, PtaXET6, and PtaACA13) and non-attenuated (PtaHRD) mechano-responsive loci during the desensitization and resensitization phases. Enrichment of H3K9/14ac and H3K4me3 in the regulatory region of attenuated genes correlates well with their transient expression pattern after the first bending. Moreover, the levels of H3K4me3 correlate well with their expression pattern after the second bending at desensitization (3 days after the first bending) as well as resensitization (5 days after the first bending) phases. On the other hand, H3K9/14ac status correlates only with their attenuated expression pattern at the desensitization phase. The expression efficiency of the attenuated genes was restored after the second bending in the histone deacetylase inhibitor-treated plants. While both histone modifications contribute to the expression of attenuated genes, mechanostimulated expression of the non-attenuated PtaHRD gene seems to be H3K4me3 dependent.

“Out of sight, out of mind”. The antagonistic role of the transcriptional memory associated with repeated acoustic stimuli on the priming of plant defense

“…Epigenetic regulation and the collaborative action of transcription factors constitute pivotal elements shaping transcriptional memory [27,29,43]. To explore the potential implication of epigenetic regulators in RAS-induced transcriptional memory, we examined known epigenetic regulators associated with defense and thermal memory [20,44] in conjunction with our expression data.…”

“…Moving across temporal spans ranging from hours to generations, transcriptional memory emerges as the most viable candidate. To comprehend the modulation of gene expression influenced by a plant's memory of stresses, the primary focus lies in the investigation of epigenetic regulation and transcription factors [27]. As an instance, tri-methylation of histone H3 at lysine 4 and 9 (H3K4, H3K9) constitutes notable epigenetic modifications associated with the acclimation of poplar trees to recurrent mechanical stimuli.…”