Up-regulation of stress-inducible genes in tobacco and Arabidopsis cells in response to abiotic stresses and ABA treatment correlates with dynamic changes in histone H3 and H4 modifications

Sokol, Agnieszka; Kwiatkowska, Aleksandra; Jerzmanowski, Andrzej; Prymakowska-Bosak, Marta

doi:10.1007/s00425-007-0612-1

Cited by 179 publications

(123 citation statements)

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“…A signature feature of the trained genes is the preservation of elevated H3K4me3 during their transcriptionally less active recovery periods. Changes in histone modifications, including H3K4me3, in response to environmental stresses have been reported for cold treatments, high salinity, hypoxia and drought-induced transcription from response genes in a variety of plant species and tissue cultures [30][31][32] . However, maintenance of these stress-induced chromatin changes after the removal of the initial signal has not been reported, except for some plant defence-response genes.…”

Section: Discussionmentioning

confidence: 99%

Multiple exposures to drought 'train' transcriptional responses in Arabidopsis

2012

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Pre-exposure to stress may alter plants' subsequent responses by producing faster and/or stronger reactions implying that plants exercise a form of 'stress memory'. The mechanisms of plants' stress memory responses are poorly understood leaving this fundamental biological question unanswered. Here we show that during recurring dehydration stresses Arabidopsis plants display transcriptional stress memory demonstrated by an increase in the rate of transcription and elevated transcript levels of a subset of the stress-response genes (trainable genes). During recovery (watered) states, trainable genes produce transcripts at basal (preinduced) levels, but remain associated with atypically high H3K4me3 and ser5P polymerase II levels, indicating that RnA polymerase II is stalled. This is the first example of a stalled RnA polymerase II and its involvement in transcriptional memory in plants. These newly discovered phenomena might be a general feature of plant stress-response systems and could lead to novel approaches for increasing the flexibility of a plant's ability to respond to the environment.

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Section: Discussionmentioning

confidence: 99%

Multiple exposures to drought 'train' transcriptional responses in Arabidopsis

2012

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“…Changes in DNA methylation, several posttranslational histone modifications, as well as a linker histone H1 variant have been implicated in plant responses to osmotic/salt stress (2,3,6,10,20,21,(42)(43)(44)(45), but in most cases the relationship among chromatin status, transcriptional responsiveness, and physiological outcomes is not clearly understood. Interestingly, in both metazoans and plants, histone phosphorylation appears to be involved in responses to osmotic/salt stress (3,17,(19)(20)(21).…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, in both metazoans and plants, histone phosphorylation appears to be involved in responses to osmotic/salt stress (3,17,(19)(20)(21). In Arabidopsis the expression of most histone genes is down-regulated by dehydration conditions (43) and exposure of tobacco BY-2 cells to sucrose or NaCl resulted in induction of H3T3 phosphorylation (21).…”

Section: Discussionmentioning

confidence: 99%

“…In metazoans, a variety of environmental stimuli can trigger histone H3 phosphorylation, both globally and at specific genes in interphase cells (11,14,(17)(18)(19). In plants, dynamic changes in histone H3 phosphorylation were also observed in cultured cells exposed to abiotic stress, such as high salt or low temperature, as well as to abscisic acid treatments (20,21). Thus, phosphorylation of histone H3 and alterations in chromatin structure are emerging as critical factors in organismal responses to environmental cues, although in many cases the specific molecular mechanisms are not clearly understood.…”

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confidence: 99%

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Osmotic stress induces phosphorylation of histone H3 at threonine 3 in pericentromeric regions of Arabidopsis thaliana

Wang

Casas-Mollano

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

132

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Histone phosphorylation plays key roles in stress-induced transcriptional reprogramming in metazoans but its function(s) in land plants has remained relatively unexplored. Here we report that an Arabidopsis mutant defective in At3g03940 and At5g18190, encoding closely related Ser/Thr protein kinases, shows pleiotropic phenotypes including dwarfism and hypersensitivity to osmotic/salt stress. The double mutant has reduced global levels of phosphorylated histone H3 threonine 3 (H3T3ph), which are not enhanced, unlike the response in the wild type, by drought-like treatments. Genome-wide analyses revealed increased H3T3ph, slight enhancement in trimethylated histone H3 lysine 4 (H3K4me3), and a modest decrease in histone H3 occupancy in pericentromeric/knob regions of wild-type plants under osmotic stress. However, despite these changes in heterochromatin, transposons and repeats remained transcriptionally repressed. In contrast, this reorganization of heterochromatin was mostly absent in the double mutant, which exhibited lower H3T3ph levels in pericentromeric regions even under normal environmental conditions. Interestingly, within actively transcribed protein-coding genes, H3T3ph density was minimal in 5′ genic regions, coincidental with a peak of H3K4me3 accumulation. This pattern was not affected in the double mutant, implying the existence of additional H3T3 protein kinases in Arabidopsis. Our results suggest that At3g03940 and At5g18190 are involved in the phosphorylation of H3T3 in pericentromeric/knob regions and that this repressive epigenetic mark may be important for maintaining proper heterochromatic organization and, possibly, chromosome function(s).epigenetics | heterochromatin | histone phosphorylation | abiotic stress | protein kinase

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“…In several plant species, similarly to metazoans, histone H3 is hyperphosphorylated at Ser-10/28 during mitosis and meiosis, and these modifications appear to be required for proper chromosome segregation and cell cycle progression (9,10,11). H3S10 phosphorylation (H3S10ph) is also involved in the transcriptional activation of genes responding to stress or mitogenstimulated signaling pathways in animals (10,12), and it has been found to increase transiently in plant cells subject to abiotic stresses (9,13). Indeed, H3S10ph facilitates RNA polymerase II release from promoter-proximal pausing in Drosophila (12) and binding of heterochromatin protein 1 (HP1), a polypeptide involved in heterochromatin formation, to H3K9me3 is disrupted by the presence of a phosphate group on Ser-10 (14, 15).…”

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confidence: 99%