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Heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (Triticum aestivum L.) and thermotolerance-regulation by TaHsfA2–10

BACKGROUND: Heat shock transcription factors (Hsfs) are present in majority of plants and play central roles in thermotolerance, transgenerational thermomemory, and many other stress responses. Our previous paper identified at least 82 Hsf members in a genome-wide study on wheat (Triticum aestivum L...

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Autores principales: Guo, Xiu-lin, Yuan, Sai-nan, Zhang, Hua-ning, Zhang, Yuan-yuan, Zhang, Yu-jie, Wang, Gui-yan, Li, Ya-qing, Li, Guo-liang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7397617/
https://www.ncbi.nlm.nih.gov/pubmed/32746866
http://dx.doi.org/10.1186/s12870-020-02555-5
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author Guo, Xiu-lin
Yuan, Sai-nan
Zhang, Hua-ning
Zhang, Yuan-yuan
Zhang, Yu-jie
Wang, Gui-yan
Li, Ya-qing
Li, Guo-liang
author_facet Guo, Xiu-lin
Yuan, Sai-nan
Zhang, Hua-ning
Zhang, Yuan-yuan
Zhang, Yu-jie
Wang, Gui-yan
Li, Ya-qing
Li, Guo-liang
author_sort Guo, Xiu-lin
collection PubMed
description BACKGROUND: Heat shock transcription factors (Hsfs) are present in majority of plants and play central roles in thermotolerance, transgenerational thermomemory, and many other stress responses. Our previous paper identified at least 82 Hsf members in a genome-wide study on wheat (Triticum aestivum L.). In this study, we analyzed the Hsf expression profiles in the advanced development stages of wheat, isolated the markedly heat-responsive gene TaHsfA2–10 (GenBank accession number MK922287), and characterized this gene and its role in thermotolerance regulation in seedlings of Arabidopsis thaliana (L. Heynh.). RESULTS: In the advanced development stages, wheat Hsf family transcription profiles exhibit different expression patterns and varying heat-responses in leaves and roots, and Hsfs are constitutively expressed to different degrees under the normal growth conditions. Overall, the majority of group A and B Hsfs are expressed in leaves while group C Hsfs are expressed at higher levels in roots. The expression of a few Hsf genes could not be detected. Heat shock (HS) caused upregulation about a quarter of genes in leaves and roots, while a number of genes were downregulated in response to HS. The highly heat-responsive gene TaHsfA2–10 was isolated through homeologous cloning. qRT-PCR revealed that TaHsfA2–10 is expressed in a wide range of tissues and organs of different development stages of wheat under the normal growth conditions. Compared to non-stress treatment, TaHsfA2–10 was highly upregulated in response to HS, H(2)O(2,) and salicylic acid (SA), and was downregulated by abscisic acid (ABA) treatment in two-leaf-old seedlings. Transient transfection of tobacco epidermal cells revealed subcellular localization of TaHsfA2–10 in the nucleus under the normal growth conditions. Phenotypic observation indicated that TaHsfA2–10 could improve both basal thermotolerance and acquired thermotolerance of transgenic Arabidopsis thaliana seedlings and rescue the thermotolerance defect of the T-DNA insertion mutant athsfa2 during HS. Compared to wild type (WT) seedlings, the TaHsfA2–10-overexpressing lines displayed both higher chlorophyll contents and higher survival rates. Yeast one-hybrid assay results revealed that TaHsfA2–10 had transactivation activity. The expression levels of thermotolerance-related AtHsps in the TaHsfA2–10 transgeinc Arabidopsis thaliana were higher than those in WT after HS. CONCLUSIONS: Wheat Hsf family members exhibit diversification and specificity of transcription expression patterns in advanced development stages under the normal conditions and after HS. As a markedly responsive transcriptional factor to HS, SA and H(2)O(2), TaHsfA2–10 involves in thermotolerance regulation of plants through binding to the HS responsive element in promoter domain of relative Hsps and upregulating the expression of Hsp genes.
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spelling pubmed-73976172020-08-06 Heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (Triticum aestivum L.) and thermotolerance-regulation by TaHsfA2–10 Guo, Xiu-lin Yuan, Sai-nan Zhang, Hua-ning Zhang, Yuan-yuan Zhang, Yu-jie Wang, Gui-yan Li, Ya-qing Li, Guo-liang BMC Plant Biol Research Article BACKGROUND: Heat shock transcription factors (Hsfs) are present in majority of plants and play central roles in thermotolerance, transgenerational thermomemory, and many other stress responses. Our previous paper identified at least 82 Hsf members in a genome-wide study on wheat (Triticum aestivum L.). In this study, we analyzed the Hsf expression profiles in the advanced development stages of wheat, isolated the markedly heat-responsive gene TaHsfA2–10 (GenBank accession number MK922287), and characterized this gene and its role in thermotolerance regulation in seedlings of Arabidopsis thaliana (L. Heynh.). RESULTS: In the advanced development stages, wheat Hsf family transcription profiles exhibit different expression patterns and varying heat-responses in leaves and roots, and Hsfs are constitutively expressed to different degrees under the normal growth conditions. Overall, the majority of group A and B Hsfs are expressed in leaves while group C Hsfs are expressed at higher levels in roots. The expression of a few Hsf genes could not be detected. Heat shock (HS) caused upregulation about a quarter of genes in leaves and roots, while a number of genes were downregulated in response to HS. The highly heat-responsive gene TaHsfA2–10 was isolated through homeologous cloning. qRT-PCR revealed that TaHsfA2–10 is expressed in a wide range of tissues and organs of different development stages of wheat under the normal growth conditions. Compared to non-stress treatment, TaHsfA2–10 was highly upregulated in response to HS, H(2)O(2,) and salicylic acid (SA), and was downregulated by abscisic acid (ABA) treatment in two-leaf-old seedlings. Transient transfection of tobacco epidermal cells revealed subcellular localization of TaHsfA2–10 in the nucleus under the normal growth conditions. Phenotypic observation indicated that TaHsfA2–10 could improve both basal thermotolerance and acquired thermotolerance of transgenic Arabidopsis thaliana seedlings and rescue the thermotolerance defect of the T-DNA insertion mutant athsfa2 during HS. Compared to wild type (WT) seedlings, the TaHsfA2–10-overexpressing lines displayed both higher chlorophyll contents and higher survival rates. Yeast one-hybrid assay results revealed that TaHsfA2–10 had transactivation activity. The expression levels of thermotolerance-related AtHsps in the TaHsfA2–10 transgeinc Arabidopsis thaliana were higher than those in WT after HS. CONCLUSIONS: Wheat Hsf family members exhibit diversification and specificity of transcription expression patterns in advanced development stages under the normal conditions and after HS. As a markedly responsive transcriptional factor to HS, SA and H(2)O(2), TaHsfA2–10 involves in thermotolerance regulation of plants through binding to the HS responsive element in promoter domain of relative Hsps and upregulating the expression of Hsp genes. BioMed Central 2020-08-03 /pmc/articles/PMC7397617/ /pubmed/32746866 http://dx.doi.org/10.1186/s12870-020-02555-5 Text en © The Author(s) 2020 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/. The Creative Commons Public Domain Dedication waiver (http://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 Article
Guo, Xiu-lin
Yuan, Sai-nan
Zhang, Hua-ning
Zhang, Yuan-yuan
Zhang, Yu-jie
Wang, Gui-yan
Li, Ya-qing
Li, Guo-liang
Heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (Triticum aestivum L.) and thermotolerance-regulation by TaHsfA2–10
title Heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (Triticum aestivum L.) and thermotolerance-regulation by TaHsfA2–10
title_full Heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (Triticum aestivum L.) and thermotolerance-regulation by TaHsfA2–10
title_fullStr Heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (Triticum aestivum L.) and thermotolerance-regulation by TaHsfA2–10
title_full_unstemmed Heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (Triticum aestivum L.) and thermotolerance-regulation by TaHsfA2–10
title_short Heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (Triticum aestivum L.) and thermotolerance-regulation by TaHsfA2–10
title_sort heat-response patterns of the heat shock transcription factor family in advanced development stages of wheat (triticum aestivum l.) and thermotolerance-regulation by tahsfa2–10
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7397617/
https://www.ncbi.nlm.nih.gov/pubmed/32746866
http://dx.doi.org/10.1186/s12870-020-02555-5
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