Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses
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...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2021-01-01
|
| Series: | Plant Communications |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2590346220301152 |
| _version_ | 1818566513240571904 |
|---|---|
| author | Danlu Han Chen Chen Simin Xia Jun Liu Jie Shu Vi Nguyen Jianbin Lai Yuhai Cui Chengwei Yang |
| author_facet | Danlu Han Chen Chen Simin Xia Jun Liu Jie Shu Vi Nguyen Jianbin Lai Yuhai Cui Chengwei Yang |
| author_sort | Danlu Han |
| collection | DOAJ |
| 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 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. |
| first_indexed | 2024-12-14T01:54:39Z |
| format | Article |
| id | doaj.art-0e82dae938d14d9bb64405df2783fa50 |
| institution | Directory Open Access Journal |
| issn | 2590-3462 |
| language | English |
| last_indexed | 2024-12-14T01:54:39Z |
| publishDate | 2021-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Plant Communications |
| spelling | doaj.art-0e82dae938d14d9bb64405df2783fa502022-12-21T23:21:15ZengElsevierPlant Communications2590-34622021-01-0121100091Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responsesDanlu Han0Chen Chen1Simin Xia2Jun Liu3Jie Shu4Vi Nguyen5Jianbin Lai6Yuhai Cui7Chengwei Yang8Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Science, South China Normal University, 510631 Guangzhou, ChinaAgriculture and Agri-Food Canada, London Research and Development Centre, London, ON N5V 4T3, Canada; Department of Biology, Western University, London, ON N6A 5B7, CanadaGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Science, South China Normal University, 510631 Guangzhou, ChinaAgro-Biological Gene Research Center, Guangdong Academy of Agricultural Sciences, Guangzhou, ChinaAgriculture and Agri-Food Canada, London Research and Development Centre, London, ON N5V 4T3, Canada; Department of Biology, Western University, London, ON N6A 5B7, CanadaAgriculture and Agri-Food Canada, London Research and Development Centre, London, ON N5V 4T3, Canada; Department of Biology, Western University, London, ON N6A 5B7, CanadaGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Science, South China Normal University, 510631 Guangzhou, China; Corresponding authorAgriculture and Agri-Food Canada, London Research and Development Centre, London, ON N5V 4T3, Canada; Department of Biology, Western University, London, ON N6A 5B7, Canada; Corresponding authorGuangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Science, South China Normal University, 510631 Guangzhou, China; Corresponding authorThe 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.http://www.sciencedirect.com/science/article/pii/S2590346220301152chromatindevelopmentheat stressplant cellsSUMOylationtranscription |
| spellingShingle | Danlu Han Chen Chen Simin Xia Jun Liu Jie Shu Vi Nguyen Jianbin Lai Yuhai Cui Chengwei Yang Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses Plant Communications chromatin development heat stress plant cells SUMOylation transcription |
| title | Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses |
| title_full | Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses |
| title_fullStr | Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses |
| title_full_unstemmed | Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses |
| title_short | Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses |
| title_sort | chromatin associated sumoylation controls the transcriptional switch between plant development and heat stress responses |
| topic | chromatin development heat stress plant cells SUMOylation transcription |
| url | http://www.sciencedirect.com/science/article/pii/S2590346220301152 |
| work_keys_str_mv | AT danluhan chromatinassociatedsumoylationcontrolsthetranscriptionalswitchbetweenplantdevelopmentandheatstressresponses AT chenchen chromatinassociatedsumoylationcontrolsthetranscriptionalswitchbetweenplantdevelopmentandheatstressresponses AT siminxia chromatinassociatedsumoylationcontrolsthetranscriptionalswitchbetweenplantdevelopmentandheatstressresponses AT junliu chromatinassociatedsumoylationcontrolsthetranscriptionalswitchbetweenplantdevelopmentandheatstressresponses AT jieshu chromatinassociatedsumoylationcontrolsthetranscriptionalswitchbetweenplantdevelopmentandheatstressresponses AT vinguyen chromatinassociatedsumoylationcontrolsthetranscriptionalswitchbetweenplantdevelopmentandheatstressresponses AT jianbinlai chromatinassociatedsumoylationcontrolsthetranscriptionalswitchbetweenplantdevelopmentandheatstressresponses AT yuhaicui chromatinassociatedsumoylationcontrolsthetranscriptionalswitchbetweenplantdevelopmentandheatstressresponses AT chengweiyang chromatinassociatedsumoylationcontrolsthetranscriptionalswitchbetweenplantdevelopmentandheatstressresponses |