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Evolutionary analysis and functional characterization of BZR1 gene family in celery revealed their conserved roles in brassinosteroid signaling

BACKGROUND: Brassinosteroids (BRs) are a group of essential steroid hormones involved in diverse developmental and physiological processes in plants. The Brassinazole-resistant 1 (BZR1) transcription factors are key components of BR signaling and integrate a wide range of internal and environmental...

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Autores principales: Zuo, Chunliu, Zhang, Lan, Yan, Xinyue, Guo, Xinyue, Zhang, Qing, Li, Songyang, Li, Yanling, Xu, Wen, Song, Xiaoming, Wang, Jinpeng, Yuan, Min
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9361572/
https://www.ncbi.nlm.nih.gov/pubmed/35941544
http://dx.doi.org/10.1186/s12864-022-08810-3
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author Zuo, Chunliu
Zhang, Lan
Yan, Xinyue
Guo, Xinyue
Zhang, Qing
Li, Songyang
Li, Yanling
Xu, Wen
Song, Xiaoming
Wang, Jinpeng
Yuan, Min
author_facet Zuo, Chunliu
Zhang, Lan
Yan, Xinyue
Guo, Xinyue
Zhang, Qing
Li, Songyang
Li, Yanling
Xu, Wen
Song, Xiaoming
Wang, Jinpeng
Yuan, Min
author_sort Zuo, Chunliu
collection PubMed
description BACKGROUND: Brassinosteroids (BRs) are a group of essential steroid hormones involved in diverse developmental and physiological processes in plants. The Brassinazole-resistant 1 (BZR1) transcription factors are key components of BR signaling and integrate a wide range of internal and environmental signals to coordinate plant development, growth, and resistance to abiotic and biotic stresses. Although the BZR1 family has been fully studied in Arabidopsis, celery BZR1 family genes remain largely unknown. RESULTS: Nine BZR1 genes were identified in the celery genome, and categorized into four classes based on phylogenetic and gene structure analyses. All the BZR1 proteins shared a typical bHLH (basic helix-loop-helix) domain that is highly conserved across the whole family in Arabidopsis, grape, lettuce, ginseng, and three Apiaceae species. Both duplications and losses of the BZR1 gene family were detected during the shaping of the celery genome. Whole-genome duplication (WGD) or segmental duplication contributed 55.56% of the BZR1 genes expansion, and the γ as well as celery-ω polyploidization events made a considerable contribution to the production of the BZR1 paralogs in celery. Four AgBZR1 members (AgBZR1.1, AgBZR1.3, AgBZR1.5, and AgBZR1.9), which were localized both in the nucleus and cytoplasm, exhibit transcription activation activity in yeast. AgBZR1.5 overexpression transgenic plants in Arabidopsis showed curled leaves with bent, long petioles and constitutive BR-responsive phenotypes. Furthermore, the AgBZR1 genes possessed divergent expression patterns with some overlaps in roots, petioles, and leaves, suggesting an extensive involvement of AgBZR1s in the developmental processes in celery with both functional redundancy and divergence. CONCLUSIONS: Our results not only demonstrated that AgBZR1 played a conserved role in BR signaling but also suggested that AgBZR1 might be extensively involved in plant developmental processes in celery. The findings lay the foundation for further study on the molecular mechanism of the AgBZR1s in regulating the agronomic traits and environmental adaptation of celery, and provide insights for future BR-related genetic breeding of celery and other Apiaceae crops. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08810-3.
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spelling pubmed-93615722022-08-10 Evolutionary analysis and functional characterization of BZR1 gene family in celery revealed their conserved roles in brassinosteroid signaling Zuo, Chunliu Zhang, Lan Yan, Xinyue Guo, Xinyue Zhang, Qing Li, Songyang Li, Yanling Xu, Wen Song, Xiaoming Wang, Jinpeng Yuan, Min BMC Genomics Research BACKGROUND: Brassinosteroids (BRs) are a group of essential steroid hormones involved in diverse developmental and physiological processes in plants. The Brassinazole-resistant 1 (BZR1) transcription factors are key components of BR signaling and integrate a wide range of internal and environmental signals to coordinate plant development, growth, and resistance to abiotic and biotic stresses. Although the BZR1 family has been fully studied in Arabidopsis, celery BZR1 family genes remain largely unknown. RESULTS: Nine BZR1 genes were identified in the celery genome, and categorized into four classes based on phylogenetic and gene structure analyses. All the BZR1 proteins shared a typical bHLH (basic helix-loop-helix) domain that is highly conserved across the whole family in Arabidopsis, grape, lettuce, ginseng, and three Apiaceae species. Both duplications and losses of the BZR1 gene family were detected during the shaping of the celery genome. Whole-genome duplication (WGD) or segmental duplication contributed 55.56% of the BZR1 genes expansion, and the γ as well as celery-ω polyploidization events made a considerable contribution to the production of the BZR1 paralogs in celery. Four AgBZR1 members (AgBZR1.1, AgBZR1.3, AgBZR1.5, and AgBZR1.9), which were localized both in the nucleus and cytoplasm, exhibit transcription activation activity in yeast. AgBZR1.5 overexpression transgenic plants in Arabidopsis showed curled leaves with bent, long petioles and constitutive BR-responsive phenotypes. Furthermore, the AgBZR1 genes possessed divergent expression patterns with some overlaps in roots, petioles, and leaves, suggesting an extensive involvement of AgBZR1s in the developmental processes in celery with both functional redundancy and divergence. CONCLUSIONS: Our results not only demonstrated that AgBZR1 played a conserved role in BR signaling but also suggested that AgBZR1 might be extensively involved in plant developmental processes in celery. The findings lay the foundation for further study on the molecular mechanism of the AgBZR1s in regulating the agronomic traits and environmental adaptation of celery, and provide insights for future BR-related genetic breeding of celery and other Apiaceae crops. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08810-3. BioMed Central 2022-08-08 /pmc/articles/PMC9361572/ /pubmed/35941544 http://dx.doi.org/10.1186/s12864-022-08810-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zuo, Chunliu
Zhang, Lan
Yan, Xinyue
Guo, Xinyue
Zhang, Qing
Li, Songyang
Li, Yanling
Xu, Wen
Song, Xiaoming
Wang, Jinpeng
Yuan, Min
Evolutionary analysis and functional characterization of BZR1 gene family in celery revealed their conserved roles in brassinosteroid signaling
title Evolutionary analysis and functional characterization of BZR1 gene family in celery revealed their conserved roles in brassinosteroid signaling
title_full Evolutionary analysis and functional characterization of BZR1 gene family in celery revealed their conserved roles in brassinosteroid signaling
title_fullStr Evolutionary analysis and functional characterization of BZR1 gene family in celery revealed their conserved roles in brassinosteroid signaling
title_full_unstemmed Evolutionary analysis and functional characterization of BZR1 gene family in celery revealed their conserved roles in brassinosteroid signaling
title_short Evolutionary analysis and functional characterization of BZR1 gene family in celery revealed their conserved roles in brassinosteroid signaling
title_sort evolutionary analysis and functional characterization of bzr1 gene family in celery revealed their conserved roles in brassinosteroid signaling
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9361572/
https://www.ncbi.nlm.nih.gov/pubmed/35941544
http://dx.doi.org/10.1186/s12864-022-08810-3
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