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Low temperature-induced regulatory network rewiring via WRKY regulators during banana peel browning

Banana (Musa spp.) fruits, as typical tropical fruits, are cold sensitive, and lower temperatures can disrupt cellular compartmentalization and lead to severe browning. How tropical fruits respond to low temperature compared to the cold response mechanisms of model plants remains unknown. Here, we s...

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Autores principales: Zhu, Wenjun, Li, Hua, Dong, Pengfei, Ni, Xueting, Fan, Minlei, Yang, Yingjie, Xu, Shiyao, Xu, Yanbing, Qian, Yangwen, Chen, Zhuo, Lü, Peitao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469544/
https://www.ncbi.nlm.nih.gov/pubmed/37279567
http://dx.doi.org/10.1093/plphys/kiad322
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author Zhu, Wenjun
Li, Hua
Dong, Pengfei
Ni, Xueting
Fan, Minlei
Yang, Yingjie
Xu, Shiyao
Xu, Yanbing
Qian, Yangwen
Chen, Zhuo
Lü, Peitao
author_facet Zhu, Wenjun
Li, Hua
Dong, Pengfei
Ni, Xueting
Fan, Minlei
Yang, Yingjie
Xu, Shiyao
Xu, Yanbing
Qian, Yangwen
Chen, Zhuo
Lü, Peitao
author_sort Zhu, Wenjun
collection PubMed
description Banana (Musa spp.) fruits, as typical tropical fruits, are cold sensitive, and lower temperatures can disrupt cellular compartmentalization and lead to severe browning. How tropical fruits respond to low temperature compared to the cold response mechanisms of model plants remains unknown. Here, we systematically characterized the changes in chromatin accessibility, histone modifications, distal cis-regulatory elements, transcription factor binding, and gene expression levels in banana peels in response to low temperature. Dynamic patterns of cold-induced transcripts were generally accompanied by concordant chromatin accessibility and histone modification changes. These upregulated genes were enriched for WRKY binding sites in their promoters and/or active enhancers. Compared to banana peel at room temperature, large amounts of banana WRKYs were specifically induced by cold and mediated enhancer–promoter interactions regulating critical browning pathways, including phospholipid degradation, oxidation, and cold tolerance. This hypothesis was supported by DNA affinity purification sequencing, luciferase reporter assays, and transient expression assay. Together, our findings highlight widespread transcriptional reprogramming via WRKYs during banana peel browning at low temperature and provide an extensive resource for studying gene regulation in tropical plants in response to cold stress, as well as potential targets for improving cold tolerance and shelf life of tropical fruits.
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spelling pubmed-104695442023-09-01 Low temperature-induced regulatory network rewiring via WRKY regulators during banana peel browning Zhu, Wenjun Li, Hua Dong, Pengfei Ni, Xueting Fan, Minlei Yang, Yingjie Xu, Shiyao Xu, Yanbing Qian, Yangwen Chen, Zhuo Lü, Peitao Plant Physiol Research Article Banana (Musa spp.) fruits, as typical tropical fruits, are cold sensitive, and lower temperatures can disrupt cellular compartmentalization and lead to severe browning. How tropical fruits respond to low temperature compared to the cold response mechanisms of model plants remains unknown. Here, we systematically characterized the changes in chromatin accessibility, histone modifications, distal cis-regulatory elements, transcription factor binding, and gene expression levels in banana peels in response to low temperature. Dynamic patterns of cold-induced transcripts were generally accompanied by concordant chromatin accessibility and histone modification changes. These upregulated genes were enriched for WRKY binding sites in their promoters and/or active enhancers. Compared to banana peel at room temperature, large amounts of banana WRKYs were specifically induced by cold and mediated enhancer–promoter interactions regulating critical browning pathways, including phospholipid degradation, oxidation, and cold tolerance. This hypothesis was supported by DNA affinity purification sequencing, luciferase reporter assays, and transient expression assay. Together, our findings highlight widespread transcriptional reprogramming via WRKYs during banana peel browning at low temperature and provide an extensive resource for studying gene regulation in tropical plants in response to cold stress, as well as potential targets for improving cold tolerance and shelf life of tropical fruits. Oxford University Press 2023-06-04 /pmc/articles/PMC10469544/ /pubmed/37279567 http://dx.doi.org/10.1093/plphys/kiad322 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Zhu, Wenjun
Li, Hua
Dong, Pengfei
Ni, Xueting
Fan, Minlei
Yang, Yingjie
Xu, Shiyao
Xu, Yanbing
Qian, Yangwen
Chen, Zhuo
Lü, Peitao
Low temperature-induced regulatory network rewiring via WRKY regulators during banana peel browning
title Low temperature-induced regulatory network rewiring via WRKY regulators during banana peel browning
title_full Low temperature-induced regulatory network rewiring via WRKY regulators during banana peel browning
title_fullStr Low temperature-induced regulatory network rewiring via WRKY regulators during banana peel browning
title_full_unstemmed Low temperature-induced regulatory network rewiring via WRKY regulators during banana peel browning
title_short Low temperature-induced regulatory network rewiring via WRKY regulators during banana peel browning
title_sort low temperature-induced regulatory network rewiring via wrky regulators during banana peel browning
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10469544/
https://www.ncbi.nlm.nih.gov/pubmed/37279567
http://dx.doi.org/10.1093/plphys/kiad322
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