Cold stress induces enhanced chromatin accessibility and bivalent histone modifications H3K4me3 and H3K27me3 of active genes in potato

Abstract

Background Cold stress can greatly affect plant growth and development. Plants have developed special systems to respond to and tolerate cold stress. While plant scientists have discovered numerous genes involved in responses to cold stress, few studies have been dedicated to investigation of genome-wide chromatin dynamics induced by cold or other abiotic stresses. Results Genomic regions containing active cis -regulatory DNA elements can be identified as DNase I hypersensitive sites (DHSs). We develop high-resolution DHS maps in potato ( Solanum tuberosum ) using chromatin isolated from tubers stored under room (22 °C) and cold (4 °C) conditions. We find that cold stress induces a large number of DHSs enriched in genic regions which are frequently associated with differential gene expression in response to temperature variation. Surprisingly, active genes show enhanced chromatin accessibility upon cold stress. A large number of active genes in cold-stored tubers are associated with the bivalent H3K4me3-H3K27me3 mark in gene body regions. Interestingly, upregulated genes associated with the bivalent mark are involved in stress response, whereas downregulated genes with the bivalent mark are involved in developmental processes. In addition, we observe that the bivalent mark-associated genes are more accessible than others upon cold stress. Conclusions Collectively, our results suggest that cold stress induces enhanced chromatin accessibility and bivalent histone modifications of active genes. We hypothesize that in cold-stored tubers, the bivalent H3K4me3-H3K27me3 mark represents a distinct chromatin environment with greater accessibility, which may facilitate the access of regulatory proteins required for gene upregulation or downregulation in response to cold stress. Electronic supplementary material The online version of this article (10.1186/s13059-019-1731-2) contains supplementary material, which is available to authorized users.

Transcriptional and post-transcriptional regulation and transcriptional memory of chromatin regulators in response to low temperature

“…In general, our analysis indicated that cold acclimation had a strong influence on the 437 expression of the selected epigenetics-related genes. This is in agreement with the finding 438 that cold stress enhanced the accessibility of chromatin and bivalent histone modifications of 439 active genes in potato (Zeng et al, 2019 It is interesting to note that several members of both families of demethylases displayed an 460 upregulation during cold acclimation before decreasing until 4 h Deacc followed by an 461 increase until 12 h Deacc before returning to the initial NA gene expression levels after 24 h 462…”

Defining chromatin state transitions predicts a network that modulates cell wall remodeling in phosphate-starved rice shoots

“…In contrast to H2A.Z, H3K4me3 is generally not recognized as playing a negative role in gene expression. Studies in a variety of plant species and tissues have examined the change in genic levels of H3K4me3 in response to environmental stressors (Tsuji et al, 2006, Sokol et al, 2007, Kim et al, 2008, Van Dijk et al, 2010, Jaskiewicz et al, 2011, Zeng et al, 2019). These studies generally reported increases in H3K4me3 at genes up-regulated by stress.…”

“…These studies generally reported increases in H3K4me3 at genes up-regulated by stress. However, most of the studies examined relatively small numbers of genes, and the genome-level studies that compared average H3K4me3 genic profiles between control and stressed samples actually found substantial decreases in 5’ localization of H3K4me3 in response to stress (Zong et al, 2013, Zeng et al, 2019). We observed a similar effect when comparing the H3K4me3 profiles for all PCG between control and Pi deficiency conditions (Figure S2).…”

“…First described in mouse embryonic stem cells were bivalent domains containing H3K4me3 and H3K27me3, in which H3K4me3 is proposed to poise genes for activation, whereas H3K27me3 maintains the genes in a repressed state (Bernstein et al, 2006). A recent study in potato tuber found an association between genes containing the bivalent H3K4me3 and H3K27me3 marks and differential expression in response to cold stress (Zeng et al, 2019). Interestingly, the bivalent mark was enriched among up-regulated genes linked to stress responses, as well as down-regulated genes linked to developmental processes.…”

Cold induced chromatin compaction and nuclear retention of clock mRNAs resets the circadian rhythm

“…At the heart of this regulation is the chaperone activity of the cold shock protein cspA and its 5'UTR that acts as a thermosensor (Giuliodori et al, 2010) and auto-regulates its own abundance in a temperature-dependent way . In plants, cold adaptation is more complex, involving temperature-induced adjustments of the chromatin (Zeng et al, 2019;Park et al, 2018), transcriptional (Nagano et al, 2019), pre-mRNA processing (Calixto et al, 2018), post-transcriptional and posttranslational landscapes (Zhu, 2016). The transcriptional response to cold acclimatization in plants is beginning to be unraveled and entire signaling networks such as the C-repeat binding transcription factor (CBFs) regulon have been exposed (Zhao et al, 2015).…”