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Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses.

ABSTRACT: The post-translational protein modification known as SUMOylation has conserved roles in the heat stress responses of various species. The functional connection between the global regulation of gene expression and chromatin-associated SUMOylation in plant cells is unknown. Here, we uncovered a genome-wide relationship between chromatin-associated SUMOylation and transcriptional switches in Arabidopsis thaliana grown at room temperature, exposed to heat stress, and exposed to heat stress followed by recovery. The small ubiquitin-like modifier (SUMO)-associated chromatin sites, characterized by whole-genome ChIP-seq, were generally associated with active chromatin markers. In response to heat stress, chromatin-associated SUMO signals increased at promoter-transcriptional start site regions and decreased in gene bodies. RNA-seq analysis supported the role of chromatin-associated SUMOylation in transcriptional activation during rapid responses to high temperature. Changes in SUMO signals on chromatin were associated with the upregulation of heat-responsive genes and the downregulation of growth-related genes. Disruption of the SUMO ligase gene SIZ1 abolished SUMO signals on chromatin and attenuated rapid transcriptional responses to heat stress. The SUMO signal peaks were enriched in DNA elements recognized by distinct groups of transcription factors under different temperature conditions. These observations provide evidence that chromatin-associated SUMOylation regulates the transcriptional switch between development and heat stress response in plant cells.

SUBMITTER: Han D

PROVIDER: S-EPMC7816078 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Chromatin-Associated SUMOylation Controls the Transcriptional Switch between Plant Development and Heat Stress Responses

Project description:The post-translational protein modiﬁcation known as SUMOylation has conserved roles in the heat stress responses of various species. The functional connection between the global regulation of gene expression and chromatin-associated SUMOylation in plant cells isunknown. Here, we uncovereda genome-wide relationship between chromatin-associated SUMOylation and transcriptional switches in Arabidopsis thaliana grown at room temperature, exposed to heat stress, and exposed to heat stress followed by recovery. The small ubiquitin-like modiﬁer (SUMO)-associated chromatin sites, characterized by whole-genome ChIP-seq, were generally associated with active chromatin markers. In response to heat stress, chromatin-associated SUMO signals increased at promoter-transcriptional start site regions and decreased in gene bodies. RNAseqanalysissupportedthe role ofchromatin-associatedSUMOylationin transcriptionalactivation duringrapid responses to high temperature. Changes inSUMO signals on chromatinwere associated with the upregulation ofheat-responsivegenesandthedownregulationofgrowth-relatedgenes.DisruptionoftheSUMOligasegene SIZ1 abolished SUMO signals on chromatin and attenuated rapid transcriptional responses to heat stress. The SUMO signal peaks were enriched in DNA elements recognized by distinct groups of transcription factors under different temperature conditions. These observations provide evidence that chromatin-associated SUMOylation regulates the transcriptional switch between development and heat stress response in plant cells.

2020-08-04 | GSE140508 | GEO

Chromatin-Associated SUMOylation Controls the Transcriptional Switch between Plant Development and Heat Stress Responses

Project description:Chromatin-Associated SUMOylation Controls the Transcriptional Switch between Plant Development and Heat Stress Responses

| PRJNA590032 | ENA

SUMOylation on plant chromatin controls transcription switches between development and heat response [ChIP-Seq]

Project description:SUMOylation, a post-translational protein modification, is dramatically upregulated and critically involved in heat stress response conservatively among species. Previous studies in Arabidopsis indicated that numerous chromatin associated proteins are SUMOylation substrates and most of heat-enhancing SUMOylation reactions occur in nucleus. However, the global functional connection between gene expression regulation and SUMOylation on chromatin is completely unknown in plant cells. Here we show a genome-wide relationship of chromatin-associated SUMOylation and transcription switches under room temperature, heat stress, and recovering conditions in Arabidopsis. The SUMO-associated chromatin sites, characterized via whole-genome ChIP-seq assays, are generally correlated with active chromatin markers. In response to heat stress, we found chromatin-associated SUMO signals increased at promoter-transcriptional start site regions and decreased in the gene bodies. Further RNA-seq analysis supported the role of chromatin-associated SUMOylation in activation of transcription during rapid responses to high temperature. Changing of SUMO signals on chromatin is correlated with upregulation of heat-responsive genes and downregulation of growth-related genes. Disruption of the SUMO ligase gene SIZ1 abolishes SUMO signals on chromatin and attenuates the rapid transcriptional responses to heat stress. Interestingly, the SUMO signal peaks are enriched in DNA elements recognized by distinguished groups of transcription factors under different temperature conditions. Collectively, our data provide evidence that SUMOylation on chromatin regulates transcription switches during development and heat stress response, improving our understanding on the precise roles of SUMOylation in plant cells.

2020-08-04 | GSE140507 | GEO

SUMOylation on plant chromatin controls transcription switches between development and heat response [RNA-Seq]

2020-08-04 | GSE140506 | GEO

Pyrophosphate modulates plant stress responses via SUMOylation.

Project description:Pyrophosphate (PPi), a byproduct of macromolecule biosynthesis is maintained at low levels by soluble inorganic pyrophosphatases (sPPase) found in all eukaryotes. In plants, H+-pumping pyrophosphatases (H+-PPase) convert the substantial energy present in PPi into an electrochemical gradient. We show here, that both cold- and heat stress sensitivity of fugu5 mutants lacking the major H+-PPase isoform AVP1 is correlated with reduced SUMOylation. In addition, we show that increased PPi concentrations interfere with SUMOylation in yeast and we provide evidence that SUMO activating E1-enzymes are inhibited by micromolar concentrations of PPi in a non-competitive manner. Taken together, our results do not only provide a mechanistic explanation for the beneficial effects of AVP1 overexpression in plants but they also highlight PPi as an important integrator of metabolism and stress tolerance.

| S-EPMC6382351 | biostudies-literature

Global SUMOylation on active chromatin is an acute heat stress response restricting transcription.

Project description:BackgroundCells have developed many ways to cope with external stress. One distinctive feature in acute proteotoxic stresses, such as heat shock (HS), is rapid post-translational modification of proteins by SUMOs (small ubiquitin-like modifier proteins; SUMOylation). While many of the SUMO targets are chromatin proteins, there is scarce information on chromatin binding of SUMOylated proteins in HS and the role of chromatin SUMOylation in the regulation of transcription.ResultsWe mapped HS-induced genome-wide changes in chromatin occupancy of SUMO-2/3-modified proteins in K562 and VCaP cells using ChIP-seq. Chromatin SUMOylation was further correlated with HS-induced global changes in transcription using GRO-seq and RNA polymerase II (Pol2) ChIP-seq along with ENCODE data for K562 cells. HS induced a rapid and massive rearrangement of chromatin SUMOylation pattern: SUMOylation was gained at active promoters and enhancers associated with multiple transcription factors, including heat shock factor 1. Concomitant loss of SUMOylation occurred at inactive intergenic chromatin regions that were associated with CTCF-cohesin complex and SETDB1 methyltransferase complex. In addition, HS triggered a dynamic chromatin binding of SUMO ligase PIAS1, especially onto promoters. The HS-induced SUMOylation on chromatin was most notable at promoters of transcribed genes where it positively correlated with active transcription and Pol2 promoter-proximal pausing. Furthermore, silencing of SUMOylation machinery either by depletion of UBC9 or PIAS1 enhanced expression of HS-induced genes.ConclusionsHS-triggered SUMOylation targets promoters and enhancers of actively transcribed genes where it restricts the transcriptional activity of the HS-induced genes. PIAS1-mediated promoter SUMOylation is likely to regulate Pol2-associated factors in HS.

| S-EPMC4531811 | biostudies-literature

HSFA1a modulates plant heat stress responses and alters the 3D chromatin organization of enhancer-promoter interactions.

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| S-EPMC9884265 | biostudies-literature

Allyl-isothiocyanate treatment induces a complex transcriptional reprogramming including heat stress, oxidative stress and plant defence responses in Arabidopsis thaliana.

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SUMOylation on plant chromatin controls transcription switches between development and heat response [ChIP-Seq]

Project description:SUMOylation on plant chromatin controls transcription switches between development and heat response [ChIP-Seq]

| PRJNA590033 | ENA

SUMOylation on plant chromatin controls transcription switches between development and heat response [RNA-Seq]

Project description:SUMOylation on plant chromatin controls transcription switches between development and heat response [RNA-Seq]

| PRJNA590034 | ENA