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Wounding activates the HSFA1 transcription factors to promote cellular reprogramming in Arabidopsis.

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Title: Wounding activates the HSFA1 transcription factors to promote cellular reprogramming in Arabidopsis.
Authors: Coleman D; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan.; Department of Biological Sciences, Faculty of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan., Iwase A; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan.; JST, PRESTO, 7 Goban-cho, Chiyoda-ku, Tokyo 102-0076Japan., Kawamura A; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan., Takebayashi A; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan., Chen Y; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan., Minne M; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan., Jager KE; Leibniz-Institut für Gemüse- und Zierpflanzenbau, Theodor-Echtermeyer-Weg 1, Großbeeren 14979, Germany., Peng M; Leibniz-Institut für Gemüse- und Zierpflanzenbau, Theodor-Echtermeyer-Weg 1, Großbeeren 14979, Germany., Kodama Y; Center for Bioscience Research and Education, Utsunomiya University, 350 Mine-machi, Utsunomiya, Tochigi 331-8505, Japan., Favero DS; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan., Takahashi T; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan., Ikeuchi M; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan.; Division of Biological Sciences, Graduate School of Science and Technology, Nara Institute of Science and Technology, 8916-5, Takayama-cho, Ikoma, Nara 630-0192, Japan., Suzuki T; Department of Biological Chemistry, College of Bioscience and Biotechnology, Chubu University, 1200 Matsumoto-cho, Kasugai, Aichi 487-8501, Japan., Ohama N; Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan., Yamaguchi-Shinozaki K; Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan., Wigge PA; Leibniz-Institut für Gemüse- und Zierpflanzenbau, Theodor-Echtermeyer-Weg 1, Großbeeren 14979, Germany.; Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25 Haus 25, Raum B1.11-12, Potsdam 14476, Germany., De Veylder L; Department of Plant Biotechnology and Bioinformatics, Ghent University, Gent, Belgium.; Center for Plant Systems Biology, VIB, Gent, Belgium., Sugimoto K; RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi Ward, Yokohama, Kanagawa 230-0045, Japan.; Department of Biological Sciences, Faculty of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
Source: The Plant cell [Plant Cell] 2026 Jun 02; Vol. 38 (6).
Publication Type: Journal Article
Language: English
Journal Info: Publisher: Oxford University Press Country of Publication: England NLM ID: 9208688 Publication Model: Print Cited Medium: Internet ISSN: 1532-298X (Electronic) Linking ISSN: 10404651 NLM ISO Abbreviation: Plant Cell Subsets: MEDLINE
Imprint Name(s): Publication: 2021- : [Oxford] : Oxford University Press
Original Publication: Rockville, MD : American Society of Plant Physiologists, c1989-
MeSH Terms: Arabidopsis*/genetics , Arabidopsis*/metabolism , Arabidopsis*/physiology , Arabidopsis Proteins*/metabolism , Arabidopsis Proteins*/genetics , Cellular Reprogramming*/genetics , Cellular Reprogramming*/physiology , Heat Shock Transcription Factors*/metabolism , Heat Shock Transcription Factors*/genetics , Transcription Factors*/metabolism , Transcription Factors*/genetics, Gene Expression Regulation, Plant/genetics
Abstract: Mechanical injury is a primary trigger for cellular reprogramming during organ regeneration, yet the molecular mechanisms that link wounding to reprogramming remain poorly understood. In this study we identify the Arabidopsis HEAT SHOCK FACTOR A1 (HSFA1) class of transcription factors, which are key regulators of the heat stress response, as central players in wound-induced callus formation and shoot regeneration. Loss of HSFA1 function in the hsfa1abd triple or hsfa1abde quadruple mutants severely impairs cellular reprogramming, reducing callus formation from wounded hypocotyls, as well as shoot regeneration from explants. Conversely, overexpression of the HSFA1d gain-of-function variant markedly enhances regeneration. Time-series RNA-seq and ChIP-seq analyses revealed that HSFA1 directly activates the key reprogramming regulators WOUND-INDUCED DEDIFFERENTIATION 1 (WIND1), PLETHORA 3 (PLT3) and ZINC FINGER OF ARABIDOPSIS THALIANA 6 (ZAT6). Furthermore, we demonstrate that HSFA1d activity is attenuated by SAP AND MIZ1 DOMAIN-CONTAINING LIGASE1 (SIZ1)-mediated SMALL UBIQUITIN-LIKE MODIFIER (SUMO)ylation, linking post-translational modification to the regulation of wound responses. Our findings establish HSFA1 as an early transcriptional hub that integrates wound signals with the activation of a broad gene network that drives cellular reprogramming, thereby providing a mechanistic framework for understanding how stress-responsive transcription factors control regeneration.
(© The Author(s) 2026. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.)
Competing Interests: Conflicts of interest: The authors declare that they have no conflict of interest.
Grant Information: 22K15150 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 20H04893 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 22H05075 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 20H05905 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 20H05911 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 23KF0089 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 24K02051 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); JPMJPR20D2 Japan Science and Technology Agency; JPMJGXx23B Japan Science and Technology Agency; JPMJAP2306 Japan Science and Technology Agency; MEXT; JSPS; 101053972 European Union
Substance Nomenclature: 0 (Arabidopsis Proteins)
0 (Heat Shock Transcription Factors)
0 (Transcription Factors)
Entry Date(s): Date Created: 20260422 Date Completed: 20260624 Latest Revision: 20260630
Update Code: 20260701
DOI: 10.1093/plcell/koag124
PMID: 42019002
Database: MEDLINE
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  Data: Wounding activates the HSFA1 transcription factors to promote cellular reprogramming in Arabidopsis.
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  Data: <i>Publication</i>: 2021- : [Oxford] : Oxford University Press<br /><i>Original Publication</i>: Rockville, MD : American Society of Plant Physiologists, c1989-
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  Data: <searchLink fieldCode="MM" term="%22Arabidopsis%22">Arabidopsis*</searchLink>/<searchLink fieldCode="MM" term="%22Arabidopsis+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Arabidopsis%22">Arabidopsis*</searchLink>/<searchLink fieldCode="MM" term="%22Arabidopsis+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Arabidopsis%22">Arabidopsis*</searchLink>/<searchLink fieldCode="MM" term="%22Arabidopsis+physiology%22">physiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Arabidopsis+Proteins%22">Arabidopsis Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Arabidopsis+Proteins+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Arabidopsis+Proteins%22">Arabidopsis Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Arabidopsis+Proteins+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Cellular+Reprogramming%22">Cellular Reprogramming*</searchLink>/<searchLink fieldCode="MM" term="%22Cellular+Reprogramming+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Cellular+Reprogramming%22">Cellular Reprogramming*</searchLink>/<searchLink fieldCode="MM" term="%22Cellular+Reprogramming+physiology%22">physiology</searchLink> <br /><searchLink fieldCode="MM" term="%22Heat+Shock+Transcription+Factors%22">Heat Shock Transcription Factors*</searchLink>/<searchLink fieldCode="MM" term="%22Heat+Shock+Transcription+Factors+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Heat+Shock+Transcription+Factors%22">Heat Shock Transcription Factors*</searchLink>/<searchLink fieldCode="MM" term="%22Heat+Shock+Transcription+Factors+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Transcription+Factors%22">Transcription Factors*</searchLink>/<searchLink fieldCode="MM" term="%22Transcription+Factors+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Transcription+Factors%22">Transcription Factors*</searchLink>/<searchLink fieldCode="MM" term="%22Transcription+Factors+genetics%22">genetics</searchLink><br /><searchLink fieldCode="MH" term="%22Gene+Expression+Regulation%2C+Plant%22">Gene Expression Regulation, Plant</searchLink>/<searchLink fieldCode="MH" term="%22Gene+Expression+Regulation%2C+Plant+genetics%22">genetics</searchLink>
– Name: Abstract
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  Data: Mechanical injury is a primary trigger for cellular reprogramming during organ regeneration, yet the molecular mechanisms that link wounding to reprogramming remain poorly understood. In this study we identify the Arabidopsis HEAT SHOCK FACTOR A1 (HSFA1) class of transcription factors, which are key regulators of the heat stress response, as central players in wound-induced callus formation and shoot regeneration. Loss of HSFA1 function in the hsfa1abd triple or hsfa1abde quadruple mutants severely impairs cellular reprogramming, reducing callus formation from wounded hypocotyls, as well as shoot regeneration from explants. Conversely, overexpression of the HSFA1d gain-of-function variant markedly enhances regeneration. Time-series RNA-seq and ChIP-seq analyses revealed that HSFA1 directly activates the key reprogramming regulators WOUND-INDUCED DEDIFFERENTIATION 1 (WIND1), PLETHORA 3 (PLT3) and ZINC FINGER OF ARABIDOPSIS THALIANA 6 (ZAT6). Furthermore, we demonstrate that HSFA1d activity is attenuated by SAP AND MIZ1 DOMAIN-CONTAINING LIGASE1 (SIZ1)-mediated SMALL UBIQUITIN-LIKE MODIFIER (SUMO)ylation, linking post-translational modification to the regulation of wound responses. Our findings establish HSFA1 as an early transcriptional hub that integrates wound signals with the activation of a broad gene network that drives cellular reprogramming, thereby providing a mechanistic framework for understanding how stress-responsive transcription factors control regeneration.<br /> (© The Author(s) 2026. Published by Oxford University Press on behalf of American Society of Plant Biologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.)
– Name: Abstract
  Label: Competing Interests
  Group: Ab
  Data: Conflicts of interest: The authors declare that they have no conflict of interest.
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  Data: 22K15150 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 20H04893 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 22H05075 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 20H05905 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 20H05911 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 23KF0089 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); 24K02051 Ministry of Education, Culture, Sports, and Technology of Japan (MEXT); JPMJPR20D2 Japan Science and Technology Agency; JPMJGXx23B Japan Science and Technology Agency; JPMJAP2306 Japan Science and Technology Agency; MEXT; JSPS; 101053972 European Union
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        Value: 10.1093/plcell/koag124
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        Text: English
    Subjects:
      – SubjectFull: Gene Expression Regulation, Plant genetics
        Type: general
      – SubjectFull: Arabidopsis genetics
        Type: general
      – SubjectFull: Arabidopsis metabolism
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      – SubjectFull: Arabidopsis physiology
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      – SubjectFull: Cellular Reprogramming physiology
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      – SubjectFull: Heat Shock Transcription Factors metabolism
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      – SubjectFull: Heat Shock Transcription Factors genetics
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