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The Histone H3K27 Demethylase REF6 Is a Positive Regulator of Light-Initiated Seed Germination in Arabidopsis

Seed germination is the first step in initiating a new life cycle in seed plants. Light is a major environmental factor affecting seed germination. Phytochrome B (phyB) is the primary photoreceptor promoting germination during the initial phase of imbibition. Post-translational histone methylation o...

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Autores principales: Wang, Yahan, Gu, Dachuan, Deng, Ling, He, Chunmei, Zheng, Feng, Liu, Xuncheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9856397/
https://www.ncbi.nlm.nih.gov/pubmed/36672228
http://dx.doi.org/10.3390/cells12020295
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author Wang, Yahan
Gu, Dachuan
Deng, Ling
He, Chunmei
Zheng, Feng
Liu, Xuncheng
author_facet Wang, Yahan
Gu, Dachuan
Deng, Ling
He, Chunmei
Zheng, Feng
Liu, Xuncheng
author_sort Wang, Yahan
collection PubMed
description Seed germination is the first step in initiating a new life cycle in seed plants. Light is a major environmental factor affecting seed germination. Phytochrome B (phyB) is the primary photoreceptor promoting germination during the initial phase of imbibition. Post-translational histone methylation occurring at both lysine and arginine residues plays a crucial role in transcriptional regulation in plants. However, the role of histone lysine demethylation in light-initiated seed germination is not yet reported. Here, we identified that Relative of Early Flowering 6 (REF6)/Jumonji Domain-containing Protein 12 (JMJ12), a histone H3 lysine 27 (H3K27) demethylase, acts as a positive regulator of light-initiated seed germination. The loss of function of REF6 in Arabidopsis inhibits phyB-dependent seed germination. Genome-wide RNA-sequencing analysis revealed that REF6 regulates about half of the light-responsive transcriptome in imbibed seeds, including genes related to multiple hormonal signaling pathways and cellular processes. Phenotypic analyses indicated that REF6 not only regulates seed germination through GA (gibberellin) and ABA (abscisic acid) processes but also depends on the auxin signaling pathway. Furthermore, REF6 directly binds to and decreases the histone H3K27me3 levels of auxin-signaling- and cell-wall-loosening-related genes, leading to the activated expression of these genes in imbibed seeds. Taken together, our study identifies REF6 as the first histone lysine demethylase required for light-initiated seed germination. Our work also reveals the important role of REF6-mediated histone H3K27 demethylation in transcriptional reprogramming in the light-initiated seed germination process.
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spelling pubmed-98563972023-01-21 The Histone H3K27 Demethylase REF6 Is a Positive Regulator of Light-Initiated Seed Germination in Arabidopsis Wang, Yahan Gu, Dachuan Deng, Ling He, Chunmei Zheng, Feng Liu, Xuncheng Cells Article Seed germination is the first step in initiating a new life cycle in seed plants. Light is a major environmental factor affecting seed germination. Phytochrome B (phyB) is the primary photoreceptor promoting germination during the initial phase of imbibition. Post-translational histone methylation occurring at both lysine and arginine residues plays a crucial role in transcriptional regulation in plants. However, the role of histone lysine demethylation in light-initiated seed germination is not yet reported. Here, we identified that Relative of Early Flowering 6 (REF6)/Jumonji Domain-containing Protein 12 (JMJ12), a histone H3 lysine 27 (H3K27) demethylase, acts as a positive regulator of light-initiated seed germination. The loss of function of REF6 in Arabidopsis inhibits phyB-dependent seed germination. Genome-wide RNA-sequencing analysis revealed that REF6 regulates about half of the light-responsive transcriptome in imbibed seeds, including genes related to multiple hormonal signaling pathways and cellular processes. Phenotypic analyses indicated that REF6 not only regulates seed germination through GA (gibberellin) and ABA (abscisic acid) processes but also depends on the auxin signaling pathway. Furthermore, REF6 directly binds to and decreases the histone H3K27me3 levels of auxin-signaling- and cell-wall-loosening-related genes, leading to the activated expression of these genes in imbibed seeds. Taken together, our study identifies REF6 as the first histone lysine demethylase required for light-initiated seed germination. Our work also reveals the important role of REF6-mediated histone H3K27 demethylation in transcriptional reprogramming in the light-initiated seed germination process. MDPI 2023-01-12 /pmc/articles/PMC9856397/ /pubmed/36672228 http://dx.doi.org/10.3390/cells12020295 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Wang, Yahan
Gu, Dachuan
Deng, Ling
He, Chunmei
Zheng, Feng
Liu, Xuncheng
The Histone H3K27 Demethylase REF6 Is a Positive Regulator of Light-Initiated Seed Germination in Arabidopsis
title The Histone H3K27 Demethylase REF6 Is a Positive Regulator of Light-Initiated Seed Germination in Arabidopsis
title_full The Histone H3K27 Demethylase REF6 Is a Positive Regulator of Light-Initiated Seed Germination in Arabidopsis
title_fullStr The Histone H3K27 Demethylase REF6 Is a Positive Regulator of Light-Initiated Seed Germination in Arabidopsis
title_full_unstemmed The Histone H3K27 Demethylase REF6 Is a Positive Regulator of Light-Initiated Seed Germination in Arabidopsis
title_short The Histone H3K27 Demethylase REF6 Is a Positive Regulator of Light-Initiated Seed Germination in Arabidopsis
title_sort histone h3k27 demethylase ref6 is a positive regulator of light-initiated seed germination in arabidopsis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9856397/
https://www.ncbi.nlm.nih.gov/pubmed/36672228
http://dx.doi.org/10.3390/cells12020295
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