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The Central Circadian Clock Protein TaCCA1 Regulates Seedling Growth and Spike Development in Wheat (Triticum aestivum L.)

The biological functions of the circadian clock on growth and development have been well elucidated in model plants, while its regulatory roles in crop species, especially the roles on yield-related traits, are poorly understood. In this study, we characterized the core clock gene CIRCADIAN CLOCK-AS...

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Autores principales: Gong, Jie, Tang, Yimiao, Liu, Yongjie, Sun, Renwei, Li, Yanhong, Ma, Jinxiu, Zhang, Shengquan, Zhang, Fengting, Chen, Zhaobo, Liao, Xiangzheng, Sun, Hui, Lu, Zefu, Zhao, Changping, Gao, Shiqing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340162/
https://www.ncbi.nlm.nih.gov/pubmed/35923880
http://dx.doi.org/10.3389/fpls.2022.946213
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author Gong, Jie
Tang, Yimiao
Liu, Yongjie
Sun, Renwei
Li, Yanhong
Ma, Jinxiu
Zhang, Shengquan
Zhang, Fengting
Chen, Zhaobo
Liao, Xiangzheng
Sun, Hui
Lu, Zefu
Zhao, Changping
Gao, Shiqing
author_facet Gong, Jie
Tang, Yimiao
Liu, Yongjie
Sun, Renwei
Li, Yanhong
Ma, Jinxiu
Zhang, Shengquan
Zhang, Fengting
Chen, Zhaobo
Liao, Xiangzheng
Sun, Hui
Lu, Zefu
Zhao, Changping
Gao, Shiqing
author_sort Gong, Jie
collection PubMed
description The biological functions of the circadian clock on growth and development have been well elucidated in model plants, while its regulatory roles in crop species, especially the roles on yield-related traits, are poorly understood. In this study, we characterized the core clock gene CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) homoeologs in wheat and studied their biological functions in seedling growth and spike development. TaCCA1 homoeologs exhibit typical diurnal expression patterns, which are positively regulated by rhythmic histone modifications including histone H3 lysine 4 trimethylation (H3K4me3), histone H3 lysine 9 acetylation (H3K9Ac), and histone H3 lysine 36 trimethylation (H3K36me3). TaCCA1s are preferentially located in the nucleus and tend to form both homo- and heterodimers. TaCCA1 overexpression (TaCCA1-OE) transgenic wheat plants show disrupted circadian rhythmicity coupling with reduced chlorophyll and starch content, as well as biomass at seedling stage, also decreased spike length, grain number per spike, and grain size at the ripening stage. Further studies using DNA affinity purification followed by deep sequencing [DNA affinity purification and sequencing (DAP-seq)] indicated that TaCCA1 preferentially binds to sequences similarly to “evening elements” (EE) motif in the wheat genome, particularly genes associated with photosynthesis, carbon utilization, and auxin homeostasis, and decreased transcriptional levels of these target genes are observed in TaCCA1-OE transgenic wheat plants. Collectively, our study provides novel insights into a circadian-mediated mechanism of gene regulation to coordinate photosynthetic and metabolic activities in wheat, which is important for optimal plant growth and crop yield formation.
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spelling pubmed-93401622022-08-02 The Central Circadian Clock Protein TaCCA1 Regulates Seedling Growth and Spike Development in Wheat (Triticum aestivum L.) Gong, Jie Tang, Yimiao Liu, Yongjie Sun, Renwei Li, Yanhong Ma, Jinxiu Zhang, Shengquan Zhang, Fengting Chen, Zhaobo Liao, Xiangzheng Sun, Hui Lu, Zefu Zhao, Changping Gao, Shiqing Front Plant Sci Plant Science The biological functions of the circadian clock on growth and development have been well elucidated in model plants, while its regulatory roles in crop species, especially the roles on yield-related traits, are poorly understood. In this study, we characterized the core clock gene CIRCADIAN CLOCK-ASSOCIATED 1 (CCA1) homoeologs in wheat and studied their biological functions in seedling growth and spike development. TaCCA1 homoeologs exhibit typical diurnal expression patterns, which are positively regulated by rhythmic histone modifications including histone H3 lysine 4 trimethylation (H3K4me3), histone H3 lysine 9 acetylation (H3K9Ac), and histone H3 lysine 36 trimethylation (H3K36me3). TaCCA1s are preferentially located in the nucleus and tend to form both homo- and heterodimers. TaCCA1 overexpression (TaCCA1-OE) transgenic wheat plants show disrupted circadian rhythmicity coupling with reduced chlorophyll and starch content, as well as biomass at seedling stage, also decreased spike length, grain number per spike, and grain size at the ripening stage. Further studies using DNA affinity purification followed by deep sequencing [DNA affinity purification and sequencing (DAP-seq)] indicated that TaCCA1 preferentially binds to sequences similarly to “evening elements” (EE) motif in the wheat genome, particularly genes associated with photosynthesis, carbon utilization, and auxin homeostasis, and decreased transcriptional levels of these target genes are observed in TaCCA1-OE transgenic wheat plants. Collectively, our study provides novel insights into a circadian-mediated mechanism of gene regulation to coordinate photosynthetic and metabolic activities in wheat, which is important for optimal plant growth and crop yield formation. Frontiers Media S.A. 2022-07-18 /pmc/articles/PMC9340162/ /pubmed/35923880 http://dx.doi.org/10.3389/fpls.2022.946213 Text en Copyright © 2022 Gong, Tang, Liu, Sun, Li, Ma, Zhang, Zhang, Chen, Liao, Sun, Lu, Zhao and Gao. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Gong, Jie
Tang, Yimiao
Liu, Yongjie
Sun, Renwei
Li, Yanhong
Ma, Jinxiu
Zhang, Shengquan
Zhang, Fengting
Chen, Zhaobo
Liao, Xiangzheng
Sun, Hui
Lu, Zefu
Zhao, Changping
Gao, Shiqing
The Central Circadian Clock Protein TaCCA1 Regulates Seedling Growth and Spike Development in Wheat (Triticum aestivum L.)
title The Central Circadian Clock Protein TaCCA1 Regulates Seedling Growth and Spike Development in Wheat (Triticum aestivum L.)
title_full The Central Circadian Clock Protein TaCCA1 Regulates Seedling Growth and Spike Development in Wheat (Triticum aestivum L.)
title_fullStr The Central Circadian Clock Protein TaCCA1 Regulates Seedling Growth and Spike Development in Wheat (Triticum aestivum L.)
title_full_unstemmed The Central Circadian Clock Protein TaCCA1 Regulates Seedling Growth and Spike Development in Wheat (Triticum aestivum L.)
title_short The Central Circadian Clock Protein TaCCA1 Regulates Seedling Growth and Spike Development in Wheat (Triticum aestivum L.)
title_sort central circadian clock protein tacca1 regulates seedling growth and spike development in wheat (triticum aestivum l.)
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9340162/
https://www.ncbi.nlm.nih.gov/pubmed/35923880
http://dx.doi.org/10.3389/fpls.2022.946213
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