Priming‐induced alterations in histone modifications modulate transcriptional responses in soybean under salt stress

Abstract

Plants that have experienced certain abiotic stress may gain tolerance to a similar stress in subsequent exposure. This phenomenon, called priming, was observed here in soybean (Glycine max) seedlings exposed to salt stress. Time-course transcriptomic profiles revealed distinctively different transcriptional responses in the primed seedlings from those in the non-primed seedlings under high salinity stress, indicating a stress response strategy of repressing unhelpful biotic stress responses and focusing on the promotion of those responses important for salt tolerance. To identify histone marks altered by the priming salinity treatment, a genome-wide profiling of histone 3 lysine 4 dimethylation (H3K4me2), H3K4me3, and histone 3 lysine 9 acetylation (H3K9ac) was performed. Our integrative analyses revealed that priming induced drastic alterations in these histone marks, which coordinately modified the stress response, ion homeostasis, and cell wall modification. Furthermore, transcriptional network analyses unveiled epigenetically modified networks which mediate the strategic downregulation of defense responses. Altering the histone acetylation status using a chemical inhibitor could elicit the priming-like transcriptional responses in non-primed seedlings, confirming the importance of histone marks in forming the priming response.

Drought Stress Priming Improved the Drought Tolerance of Soybean

“…In a previous study, microarray analyses revealed higher transcript levels of all these genes during the second drought stress compared to the first stress in soybean [ 25 ], which is consistent with our qPCR analyses. The stronger response of the gene expression could potentially be explained by the chromatin remodeling and the global change in histone modification during the priming stress [ 23 ]. ABA is known to induce pathways that mediate the conversion of PP2C chromatins from a repressive to an active state that can create epigenetic memory [ 49 ].…”

“…Stress memory response has also been assessed in soybean. For example, salt-primed seedlings were found to have altered histone 3 lysine 4 dimethylations (H3K4me2), H3K4me3, and histone 3 lysine 9 acetylation (H3K9ac) marks throughout the genome to promote the response related to salt tolerance [ 23 ]. Soluble sugar and proline contents have been found to increase in the initial drought stress and then remain stable in the subsequent stresses to protect soybean plants from drought-induced osmotic stress [ 24 ].…”

Dynamic regulation of DNA methylation and histone modifications in response to abiotic stresses in plants

“…Besides DNA methylation, histone modifications are also involved in the salt stress response (Luo et al, 2012; Kim et al, 2015). In soybean plants under priming salinity treatment, histone marks, such as H3K4me2, H3K4me3, and H3K9ac were dramatically induced, which coordinately modified the stress response, cell wall modification, and ion homeostasis (Yung et al, 2022). Furthermore, inhibition of histone acetylation triggered priming‐like transcriptional responses in non‐primed plants, which verified the importance of histone marks in forming the priming response (Yung et al, 2022).…”

“…In soybean plants under priming salinity treatment, histone marks, such as H3K4me2, H3K4me3, and H3K9ac were dramatically induced, which coordinately modified the stress response, cell wall modification, and ion homeostasis (Yung et al, 2022). Furthermore, inhibition of histone acetylation triggered priming‐like transcriptional responses in non‐primed plants, which verified the importance of histone marks in forming the priming response (Yung et al, 2022). The H3K27me3 mark is highly enriched in the gene body of Arabidopsis HKT1 , and the activation of HKT1 expression under salinity stress is caused by the removal of H3K27me3 (Sani et al, 2013).…”

“…For instance, cold‐dependent vernalization was used as an example to demonstrate the link between environmental conditions and epigenetic markers (Bastow et al, 2004; Finnegan and Dennis, 2007; Schmitz et al, 2008; Luo and He, 2020; Sharma et al, 2020). Several studies showed that changes in global DNA methylation and histone modification levels are significantly synchronized with the expression levels of genes responsive to abiotic stresses including salinity, drought, heat, and cold (Wang et al, 2011; Pandey et al, 2016; Rajkumar et al, 2020; Yung et al, 2022). Moreover, several epigenetic modifications, such as histone H3 lysine 4 (H3K4) methylation and H3K27 methylation, have been implicated in the formation of stress memory after priming (Kim et al, 2012; Oberkofler et al, 2021).…”