Cold stress induces rapid gene-specific changes in the levels of H3K4me3 and H3K27me3 in Arabidopsis thaliana
When exposed to low temperatures, plants undergo a drastic reprogramming of their transcriptome in order to adapt to their new environmental conditions, which primes them for potential freezing temperatures. While the involvement of transcription factors in this process, termed cold acclimation, has...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2024-04-01
|
| Series: | Frontiers in Plant Science |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2024.1390144/full |
| _version_ | 1827283902256906240 |
|---|---|
| author | Léa Faivre Nathalie-Francesca Kinscher Ana Belén Kuhlmann Xiaocai Xu Kerstin Kaufmann Daniel Schubert |
| author_facet | Léa Faivre Nathalie-Francesca Kinscher Ana Belén Kuhlmann Xiaocai Xu Kerstin Kaufmann Daniel Schubert |
| author_sort | Léa Faivre |
| collection | DOAJ |
| description | When exposed to low temperatures, plants undergo a drastic reprogramming of their transcriptome in order to adapt to their new environmental conditions, which primes them for potential freezing temperatures. While the involvement of transcription factors in this process, termed cold acclimation, has been deeply investigated, the potential contribution of chromatin regulation remains largely unclear. A large proportion of cold-inducible genes carries the repressive mark histone 3 lysine 27 trimethylation (H3K27me3), which has been hypothesized as maintaining them in a silenced state in the absence of stress, but which would need to be removed or counteracted upon stress perception. However, the fate of H3K27me3 during cold exposure has not been studied genome-wide. In this study, we offer an epigenome profiling of H3K27me3 and its antagonistic active mark H3K4me3 during short-term cold exposure. Both chromatin marks undergo rapid redistribution upon cold exposure, however, the gene sets undergoing H3K4me3 or H3K27me3 differential methylation are distinct, refuting the simplistic idea that gene activation relies on a switch from an H3K27me3 repressed chromatin to an active form enriched in H3K4me3. Coupling the ChIP-seq experiments with transcriptome profiling reveals that differential histone methylation only weakly correlates with changes in expression. Interestingly, only a subset of cold-regulated genes lose H3K27me3 during their induction, indicating that H3K27me3 is not an obstacle to transcriptional activation. In the H3K27me3 methyltransferase curly leaf (clf) mutant, many cold regulated genes display reduced H3K27me3 levels but their transcriptional activity is not altered prior or during a cold exposure, suggesting that H3K27me3 may serve a more intricate role in the cold response than simply repressing the cold-inducible genes in naïve conditions. |
| first_indexed | 2024-04-24T09:44:54Z |
| format | Article |
| id | doaj.art-e4cf204ccc5b45fcb80d232aebbe4990 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-24T09:44:54Z |
| publishDate | 2024-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-e4cf204ccc5b45fcb80d232aebbe49902024-04-15T04:15:13ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-04-011510.3389/fpls.2024.13901441390144Cold stress induces rapid gene-specific changes in the levels of H3K4me3 and H3K27me3 in Arabidopsis thalianaLéa Faivre0Nathalie-Francesca Kinscher1Ana Belén Kuhlmann2Xiaocai Xu3Kerstin Kaufmann4Daniel Schubert5Epigenetics of Plants, Freie Universität Berlin, Berlin, GermanyEpigenetics of Plants, Freie Universität Berlin, Berlin, GermanyEpigenetics of Plants, Freie Universität Berlin, Berlin, GermanyDepartment for Plant Cell and Molecular Biology, Institute for Biology, Humboldt-Universität zu Berlin, Berlin, GermanyDepartment for Plant Cell and Molecular Biology, Institute for Biology, Humboldt-Universität zu Berlin, Berlin, GermanyEpigenetics of Plants, Freie Universität Berlin, Berlin, GermanyWhen exposed to low temperatures, plants undergo a drastic reprogramming of their transcriptome in order to adapt to their new environmental conditions, which primes them for potential freezing temperatures. While the involvement of transcription factors in this process, termed cold acclimation, has been deeply investigated, the potential contribution of chromatin regulation remains largely unclear. A large proportion of cold-inducible genes carries the repressive mark histone 3 lysine 27 trimethylation (H3K27me3), which has been hypothesized as maintaining them in a silenced state in the absence of stress, but which would need to be removed or counteracted upon stress perception. However, the fate of H3K27me3 during cold exposure has not been studied genome-wide. In this study, we offer an epigenome profiling of H3K27me3 and its antagonistic active mark H3K4me3 during short-term cold exposure. Both chromatin marks undergo rapid redistribution upon cold exposure, however, the gene sets undergoing H3K4me3 or H3K27me3 differential methylation are distinct, refuting the simplistic idea that gene activation relies on a switch from an H3K27me3 repressed chromatin to an active form enriched in H3K4me3. Coupling the ChIP-seq experiments with transcriptome profiling reveals that differential histone methylation only weakly correlates with changes in expression. Interestingly, only a subset of cold-regulated genes lose H3K27me3 during their induction, indicating that H3K27me3 is not an obstacle to transcriptional activation. In the H3K27me3 methyltransferase curly leaf (clf) mutant, many cold regulated genes display reduced H3K27me3 levels but their transcriptional activity is not altered prior or during a cold exposure, suggesting that H3K27me3 may serve a more intricate role in the cold response than simply repressing the cold-inducible genes in naïve conditions.https://www.frontiersin.org/articles/10.3389/fpls.2024.1390144/fullchromatinhistone methylationcold stresspolycombtrithoraxArabidopsis |
| spellingShingle | Léa Faivre Nathalie-Francesca Kinscher Ana Belén Kuhlmann Xiaocai Xu Kerstin Kaufmann Daniel Schubert Cold stress induces rapid gene-specific changes in the levels of H3K4me3 and H3K27me3 in Arabidopsis thaliana Frontiers in Plant Science chromatin histone methylation cold stress polycomb trithorax Arabidopsis |
| title | Cold stress induces rapid gene-specific changes in the levels of H3K4me3 and H3K27me3 in Arabidopsis thaliana |
| title_full | Cold stress induces rapid gene-specific changes in the levels of H3K4me3 and H3K27me3 in Arabidopsis thaliana |
| title_fullStr | Cold stress induces rapid gene-specific changes in the levels of H3K4me3 and H3K27me3 in Arabidopsis thaliana |
| title_full_unstemmed | Cold stress induces rapid gene-specific changes in the levels of H3K4me3 and H3K27me3 in Arabidopsis thaliana |
| title_short | Cold stress induces rapid gene-specific changes in the levels of H3K4me3 and H3K27me3 in Arabidopsis thaliana |
| title_sort | cold stress induces rapid gene specific changes in the levels of h3k4me3 and h3k27me3 in arabidopsis thaliana |
| topic | chromatin histone methylation cold stress polycomb trithorax Arabidopsis |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2024.1390144/full |
| work_keys_str_mv | AT leafaivre coldstressinducesrapidgenespecificchangesinthelevelsofh3k4me3andh3k27me3inarabidopsisthaliana AT nathaliefrancescakinscher coldstressinducesrapidgenespecificchangesinthelevelsofh3k4me3andh3k27me3inarabidopsisthaliana AT anabelenkuhlmann coldstressinducesrapidgenespecificchangesinthelevelsofh3k4me3andh3k27me3inarabidopsisthaliana AT xiaocaixu coldstressinducesrapidgenespecificchangesinthelevelsofh3k4me3andh3k27me3inarabidopsisthaliana AT kerstinkaufmann coldstressinducesrapidgenespecificchangesinthelevelsofh3k4me3andh3k27me3inarabidopsisthaliana AT danielschubert coldstressinducesrapidgenespecificchangesinthelevelsofh3k4me3andh3k27me3inarabidopsisthaliana |