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Primed histone demethylation regulates shoot regenerative competency

Ishihara, Hiroya and Sugimoto, Kaoru and Tarr, Paul T. and Temman, Haruka and Kadokura, Satoshi and Inui, Yayoi and Sakamoto, Takuya and Sasaki, Taku and Aida, Mitsuhiro and Suzuki, Takamasa and Inagaki, Soichi and Morohashi, Kengo and Seki, Motoaki and Kakutani, Tetsuji and Meyerowitz, Elliot M. and Matsunaga, Sachihiro (2019) Primed histone demethylation regulates shoot regenerative competency. Nature Communications, 10 . Art. No. 1786. ISSN 2041-1723. PMCID PMC6467990. doi:10.1038/s41467-019-09386-5. https://resolver.caltech.edu/CaltechAUTHORS:20190423-101937501

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Abstract

Acquisition of pluripotency by somatic cells is a striking process that enables multicellular organisms to regenerate organs. This process includes silencing of genes to erase original tissue memory and priming of additional cell type specification genes, which are then poised for activation by external signal inputs. Here, through analysis of genome-wide histone modifications and gene expression profiles, we show that a gene priming mechanism involving LYSINE-SPECIFIC DEMETHYLASE 1-LIKE 3 (LDL3) specifically eliminates H3K4me2 during formation of the intermediate pluripotent cell mass known as callus derived from Arabidopsis root cells. While LDL3-mediated H3K4me2 removal does not immediately affect gene expression, it does facilitate the later activation of genes that act to form shoot progenitors when external cues lead to shoot induction. These results give insights into the role of H3K4 methylation in plants, and into the primed state that provides plant cells with high regenerative competency.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41467-019-09386-5DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6467990/PubMed CentralArticle
ORCID:
AuthorORCID
Ishihara, Hiroya0000-0002-0536-1118
Suzuki, Takamasa0000-0002-1977-0510
Inagaki, Soichi0000-0003-4090-826X
Seki, Motoaki0000-0001-8288-0467
Meyerowitz, Elliot M.0000-0003-4798-5153
Matsunaga, Sachihiro0000-0003-3024-3559
Additional Information:© The Author(s) 2019. Open Access - This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 08 August 2018. Accepted 07 March 2019. Published 16 April 2019. We thank V. A. Grieneisen for pPIN1::PIN1-GFP seeds, the European Arabidopsis Stock Center (NASC) for ldl3-1 seeds, and the Salk Institute Genomic Analysis Laboratory Arabidopsis Biological Resource Center (ABRC) for ldl3-2, lsd1 (swp1-1), ldl2-2, cipk23, upl4, and glt1 seeds. We also thank Brian Ma and Edward Pursifull at the California Institute of Technology for technical assistance with initiating the project and screening the mutants, Keiko Yoda and Yukiko Kawaguchi at Tokyo University of Science for technical assistance, Adrienne Roeder for critical reading and comments on the manuscript, and Sarah Williams, PhD, from Edanz Group (www.edanzediting.com) for editing a draft of this manuscript. This research was supported by CREST grants from the Japan Science and Technology Agency (JPMJCR13B4) and MXT/JSPS KAKENHI (15H05955 and 15H05962) to S.M., MXT/JSPS KAKENHI (15H05963) to T.K. and by the Howard Hughes Medical Institute to E.M.M. These authors contributed equally: Hiroya Ishihara, Kaoru Sugimoto. Author Contributions K.S., H.I., and S.M.: Conception, design and interpretation of data; K.S. and E.M.M.: Project initiation and mutant screening; H.I.: Final mutant screening; H.I., H.T., and S.K.: Acquisition of data; K.S., H.I., H.T., and S.K.: Analysis and interpretation of data and drafting the article; K.S., P.T., E.M.M. and S.M.: Revising the article; P.T., Y.I., T.Sasaki., M.S., E.M.M. and S.M.: Generation of unpublished materials; S.K., Y.I., and H.T.: Observation of reporter lines; T.Sakamoto and M.A.: Technical support for microscopic observation, construction and western blotting analysis; S.I., H.T., M.K., and T.K.: Technical support for RNA-seq and ChiP-seq analysis; and T. Suzuki.: Sequencing. The manuscript was written based on inputs from all authors. Data availability: ChIP-seq and RNA-seq data associated with this study have been deposited in DDBJ Sequence Read Archive (DRA) under the accession number, DRA008014, and NCBI Sequence Read Archive (SRA) under the accession number, SRP187025. The source data underlying Figs. 4e, 7d, and Supplementary Figure 1a, b, c, 2b, 6b and d are provided as a Source Data file. The authors declare that any other data supporting the findings of this study are available within the manuscript and its supplementary files or are available from the corresponding authors upon request. Journal peer review information: Nature Communications thanks Xu lin, Célia Baroux, and the other anonymous reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available. Reporting summary: Further information on experimental design is available in the Nature Research Reporting Summary linked to this article. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Japan Science and Technology AgencyJPMJCR13B4
Ministry of Education, Culture, Sports, Science and Technology (MEXT)UNSPECIFIED
Japan Society for the Promotion of Science (JSPS)15H05955
Japan Society for the Promotion of Science (JSPS)15H05962
Japan Society for the Promotion of Science (JSPS)15H05963
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
PubMed Central ID:PMC6467990
DOI:10.1038/s41467-019-09386-5
Record Number:CaltechAUTHORS:20190423-101937501
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190423-101937501
Official Citation:Ishihara H, Sugimoto K, Tarr PT, Temman H, Kadokura S, Inui Y, Sakamoto T, Sasaki T, Aida M, Suzuki T, Inagaki S, Morohashi K, Seki M, Kakutani T, Meyerowitz EM, Matsunaga S. Primed histone demethylation regulates shoot regenerative competency. Nat Commun. 2019 Apr 16;10(1):1786. doi: 10.1038/s41467-019-09386-5.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:94891
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:23 Apr 2019 18:04
Last Modified:16 Nov 2021 17:08

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