Inhibition of histone deacetylase in Arabidopsis root calli promotes de novo shoot organogenesis
De novo organogenesis from somatic cells to the entire plant represents a remarkable biological phenomenon, but the underlying regulatory mechanism, particularly at the epigenetic level, remains obscure. In this work, we demonstrate the important role of histone deacetylases (HDACs) in shoot organog...
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Frontiers Media S.A.
2025-01-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2024.1500573/full |
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| author | Qinwei Pan Ruirui Huang Qiong Xiao Xuting Wu Baoxia Jian Yanan Xiang Lijun Gan Zongrang Liu Yi Li Tingting Gu Huawei Liu Huawei Liu |
| author_facet | Qinwei Pan Ruirui Huang Qiong Xiao Xuting Wu Baoxia Jian Yanan Xiang Lijun Gan Zongrang Liu Yi Li Tingting Gu Huawei Liu Huawei Liu |
| author_sort | Qinwei Pan |
| collection | DOAJ |
| description | De novo organogenesis from somatic cells to the entire plant represents a remarkable biological phenomenon, but the underlying regulatory mechanism, particularly at the epigenetic level, remains obscure. In this work, we demonstrate the important role of histone deacetylases (HDACs) in shoot organogenesis. HDAC inhibition by trichostatin A (an HDAC inhibitor) at the callus induction stage promotes shoot formation in wounded roots and circumvents tissue wounding to initiate shoot regeneration in unwounded roots. This HDAC inhibition-mediated promotion of shoot organogenesis in wounded roots is associated with the concomitant upregulation of the wound signaling pathway (WOUND INDUCED DEDIFFERENTIATION 4, ENHANCER OF SHOOT REGENERATION1, ISOPENTENYLTRANSFERASE 5, CUP-SHAPED COTYLEDON 2 etc.) and the ARF-LBD pathway (AUXIN RESPONSE FACTOR 19, LATERAL ORGAN BOUNDARIES-DOMAIN 29, etc.) and the downregulation of auxin biosynthesis and reduced auxin content. Furthermore, inhibiting HDACs enhances the local enrichment of histone 3 lysine 9/lysine 14 acetylation at ISOPENTENYLTRANSFERASE 5, supporting the role of histone acetylation in its transcriptional regulation. On the other hand, the HDAC inhibition-associated activation of shoot organogenesis from unwounded roots is coupled with increased expression of the ARF-LBD pathway gene LATERAL ORGAN BOUNDARIES-DOMAIN 29 while bypassing the wound signaling or auxin biosynthetic genes. These findings provide novel insights into the regulatory mechanisms underlying de novo shoot organogenesis and lay a foundation for the improvement of plant transformation technologies. |
| format | Article |
| id | doaj-art-148c4040946f4571ae5a2db8c13454cd |
| institution | Kabale University |
| issn | 1664-462X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj-art-148c4040946f4571ae5a2db8c13454cd2025-01-27T04:11:30ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-01-011510.3389/fpls.2024.15005731500573Inhibition of histone deacetylase in Arabidopsis root calli promotes de novo shoot organogenesisQinwei Pan0Ruirui Huang1Qiong Xiao2Xuting Wu3Baoxia Jian4Yanan Xiang5Lijun Gan6Zongrang Liu7Yi Li8Tingting Gu9Huawei Liu10Huawei Liu11State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing, ChinaLaboratory of Plant Hormone, College of Life Sciences, Nanjing Agricultural University, Nanjing, ChinaLaboratory of Plant Hormone, College of Life Sciences, Nanjing Agricultural University, Nanjing, ChinaUSDA-ARS, Appalachian Fruit Research Station, Kearneysville, WV, United StatesDepartment of Plant Science and Landscape Architecture, University of Connecticut, Storrs, CT, United StatesState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing, ChinaState Key Laboratory of Desert and Oasis Ecology, Key Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi, ChinaDe novo organogenesis from somatic cells to the entire plant represents a remarkable biological phenomenon, but the underlying regulatory mechanism, particularly at the epigenetic level, remains obscure. In this work, we demonstrate the important role of histone deacetylases (HDACs) in shoot organogenesis. HDAC inhibition by trichostatin A (an HDAC inhibitor) at the callus induction stage promotes shoot formation in wounded roots and circumvents tissue wounding to initiate shoot regeneration in unwounded roots. This HDAC inhibition-mediated promotion of shoot organogenesis in wounded roots is associated with the concomitant upregulation of the wound signaling pathway (WOUND INDUCED DEDIFFERENTIATION 4, ENHANCER OF SHOOT REGENERATION1, ISOPENTENYLTRANSFERASE 5, CUP-SHAPED COTYLEDON 2 etc.) and the ARF-LBD pathway (AUXIN RESPONSE FACTOR 19, LATERAL ORGAN BOUNDARIES-DOMAIN 29, etc.) and the downregulation of auxin biosynthesis and reduced auxin content. Furthermore, inhibiting HDACs enhances the local enrichment of histone 3 lysine 9/lysine 14 acetylation at ISOPENTENYLTRANSFERASE 5, supporting the role of histone acetylation in its transcriptional regulation. On the other hand, the HDAC inhibition-associated activation of shoot organogenesis from unwounded roots is coupled with increased expression of the ARF-LBD pathway gene LATERAL ORGAN BOUNDARIES-DOMAIN 29 while bypassing the wound signaling or auxin biosynthetic genes. These findings provide novel insights into the regulatory mechanisms underlying de novo shoot organogenesis and lay a foundation for the improvement of plant transformation technologies.https://www.frontiersin.org/articles/10.3389/fpls.2024.1500573/fullTSA applicationhistone deacetylase inhibitioncallus inductionshoot regenerationArabidopsis |
| spellingShingle | Qinwei Pan Ruirui Huang Qiong Xiao Xuting Wu Baoxia Jian Yanan Xiang Lijun Gan Zongrang Liu Yi Li Tingting Gu Huawei Liu Huawei Liu Inhibition of histone deacetylase in Arabidopsis root calli promotes de novo shoot organogenesis Frontiers in Plant Science TSA application histone deacetylase inhibition callus induction shoot regeneration Arabidopsis |
| title | Inhibition of histone deacetylase in Arabidopsis root calli promotes de novo shoot organogenesis |
| title_full | Inhibition of histone deacetylase in Arabidopsis root calli promotes de novo shoot organogenesis |
| title_fullStr | Inhibition of histone deacetylase in Arabidopsis root calli promotes de novo shoot organogenesis |
| title_full_unstemmed | Inhibition of histone deacetylase in Arabidopsis root calli promotes de novo shoot organogenesis |
| title_short | Inhibition of histone deacetylase in Arabidopsis root calli promotes de novo shoot organogenesis |
| title_sort | inhibition of histone deacetylase in arabidopsis root calli promotes de novo shoot organogenesis |
| topic | TSA application histone deacetylase inhibition callus induction shoot regeneration Arabidopsis |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2024.1500573/full |
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