DEMETER DNA demethylase reshapes the global DNA methylation landscape and controls cell identity transition during plant regeneration
Abstract Background Plants possess a high potential for somatic cell reprogramming, enabling the transition from differentiated tissue to pluripotent callus, followed by the formation of de novo shoots during plant regeneration. Despite extensive studies on the molecular network and key genetic fact...
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2024-12-01
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| Series: | BMC Genomics |
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| Online Access: | https://doi.org/10.1186/s12864-024-11144-x |
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| author | Seunga Lee Soon Hyung Bae Yunji Jeon Pil Joon Seo Yeonhee Choi |
| author_facet | Seunga Lee Soon Hyung Bae Yunji Jeon Pil Joon Seo Yeonhee Choi |
| author_sort | Seunga Lee |
| collection | DOAJ |
| description | Abstract Background Plants possess a high potential for somatic cell reprogramming, enabling the transition from differentiated tissue to pluripotent callus, followed by the formation of de novo shoots during plant regeneration. Despite extensive studies on the molecular network and key genetic factors involved in this process, the underlying epigenetic landscape remains incompletely understood. Results Here, we explored the dynamics of the methylome and transcriptome during the two-step plant regeneration process. During the leaf-to-callus transition in Arabidopsis Ler, CG methylation shifted across genic regions, exhibiting a similar number of differentially methylated regions (DMRs) for both hypo- and hypermethylation. Pericentromeric regions underwent substantial CG and extensive CHH hypomethylation, alongside some CHG hypermethylation. Upon shoot regeneration from callus, genic regions displayed extensive reconfiguration of CG methylation, while pericentromeric methylation levels highly increased across all cytosine contexts, coinciding with the activation of the RNA-directed DNA methylation (RdDM) pathway. However, mutation in DEMETER (DME) DNA demethylase gene resulted in significant genic CG redistribution and global non-CG hypomethylation in pericentromeric regions, particularly during shoot regeneration. This non-CG hypomethylation observed in dme-2 mutants was, at least partly, due to RdDM downregulation. The dme-2 mutants affected gene expression involved in pluripotency and shoot meristem development, resulting in enhanced shoot regeneration through a reprogrammed state established by pericentromeric hypomethylation compared to wild type. Conclusion Our study demonstrates epigenetic changes, accompanied by transcriptome alterations, during pluripotency acquisition (leaf-to-callus) and regeneration (callus-to-de novo shoot). Additionally, it highlights the functions of the DME demethylase, particularly its close association with the RdDM pathway, which underlies pericentromeric non-CG methylation maintenance. These results provide important insights into the epigenetic reconfiguration associated with cell identity transition during somatic cell reprogramming. |
| format | Article |
| id | doaj-art-93bea381e89a40e9ba1a9170d7d85873 |
| institution | Kabale University |
| issn | 1471-2164 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj-art-93bea381e89a40e9ba1a9170d7d858732024-12-29T12:10:57ZengBMCBMC Genomics1471-21642024-12-0125111210.1186/s12864-024-11144-xDEMETER DNA demethylase reshapes the global DNA methylation landscape and controls cell identity transition during plant regenerationSeunga Lee0Soon Hyung Bae1Yunji Jeon2Pil Joon Seo3Yeonhee Choi4Department of Biological Sciences, Seoul National UniversityDepartment of Chemistry, Seoul National UniversityDepartment of Biological Sciences, Seoul National UniversityDepartment of Chemistry, Seoul National UniversityDepartment of Biological Sciences, Seoul National UniversityAbstract Background Plants possess a high potential for somatic cell reprogramming, enabling the transition from differentiated tissue to pluripotent callus, followed by the formation of de novo shoots during plant regeneration. Despite extensive studies on the molecular network and key genetic factors involved in this process, the underlying epigenetic landscape remains incompletely understood. Results Here, we explored the dynamics of the methylome and transcriptome during the two-step plant regeneration process. During the leaf-to-callus transition in Arabidopsis Ler, CG methylation shifted across genic regions, exhibiting a similar number of differentially methylated regions (DMRs) for both hypo- and hypermethylation. Pericentromeric regions underwent substantial CG and extensive CHH hypomethylation, alongside some CHG hypermethylation. Upon shoot regeneration from callus, genic regions displayed extensive reconfiguration of CG methylation, while pericentromeric methylation levels highly increased across all cytosine contexts, coinciding with the activation of the RNA-directed DNA methylation (RdDM) pathway. However, mutation in DEMETER (DME) DNA demethylase gene resulted in significant genic CG redistribution and global non-CG hypomethylation in pericentromeric regions, particularly during shoot regeneration. This non-CG hypomethylation observed in dme-2 mutants was, at least partly, due to RdDM downregulation. The dme-2 mutants affected gene expression involved in pluripotency and shoot meristem development, resulting in enhanced shoot regeneration through a reprogrammed state established by pericentromeric hypomethylation compared to wild type. Conclusion Our study demonstrates epigenetic changes, accompanied by transcriptome alterations, during pluripotency acquisition (leaf-to-callus) and regeneration (callus-to-de novo shoot). Additionally, it highlights the functions of the DME demethylase, particularly its close association with the RdDM pathway, which underlies pericentromeric non-CG methylation maintenance. These results provide important insights into the epigenetic reconfiguration associated with cell identity transition during somatic cell reprogramming.https://doi.org/10.1186/s12864-024-11144-xArabidopsisDNA methylationDEMETER (DME) DNA demethylaseSomatic cell reprogrammingIn vitro plant regenerationRNA-directed DNA methylation (RdDM) |
| spellingShingle | Seunga Lee Soon Hyung Bae Yunji Jeon Pil Joon Seo Yeonhee Choi DEMETER DNA demethylase reshapes the global DNA methylation landscape and controls cell identity transition during plant regeneration BMC Genomics Arabidopsis DNA methylation DEMETER (DME) DNA demethylase Somatic cell reprogramming In vitro plant regeneration RNA-directed DNA methylation (RdDM) |
| title | DEMETER DNA demethylase reshapes the global DNA methylation landscape and controls cell identity transition during plant regeneration |
| title_full | DEMETER DNA demethylase reshapes the global DNA methylation landscape and controls cell identity transition during plant regeneration |
| title_fullStr | DEMETER DNA demethylase reshapes the global DNA methylation landscape and controls cell identity transition during plant regeneration |
| title_full_unstemmed | DEMETER DNA demethylase reshapes the global DNA methylation landscape and controls cell identity transition during plant regeneration |
| title_short | DEMETER DNA demethylase reshapes the global DNA methylation landscape and controls cell identity transition during plant regeneration |
| title_sort | demeter dna demethylase reshapes the global dna methylation landscape and controls cell identity transition during plant regeneration |
| topic | Arabidopsis DNA methylation DEMETER (DME) DNA demethylase Somatic cell reprogramming In vitro plant regeneration RNA-directed DNA methylation (RdDM) |
| url | https://doi.org/10.1186/s12864-024-11144-x |
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