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Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice

Partial root-zone drying (PRD) is an effective water-saving irrigation strategy that improves stress tolerance and facilitates efficient water use in several crops. It has long been considered that abscisic acid (ABA)-dependent drought resistance may be involved during partial root-zone drying. Howe...

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Autores principales: Zhao, Minhua, Du, Canghao, Zeng, Jian, Gao, Zhihong, Zhu, Yongyong, Wang, Jinfei, Zhang, Yupeng, Zhu, Zetao, Wang, Yaqiong, Chen, Mingjie, Wang, Yuesheng, Chang, Junli, Yang, Guangxiao, He, Guangyuan, Li, Yin, Chen, Xiaoyuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10288491/
https://www.ncbi.nlm.nih.gov/pubmed/37360728
http://dx.doi.org/10.3389/fpls.2023.1156514
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author Zhao, Minhua
Du, Canghao
Zeng, Jian
Gao, Zhihong
Zhu, Yongyong
Wang, Jinfei
Zhang, Yupeng
Zhu, Zetao
Wang, Yaqiong
Chen, Mingjie
Wang, Yuesheng
Chang, Junli
Yang, Guangxiao
He, Guangyuan
Li, Yin
Chen, Xiaoyuan
author_facet Zhao, Minhua
Du, Canghao
Zeng, Jian
Gao, Zhihong
Zhu, Yongyong
Wang, Jinfei
Zhang, Yupeng
Zhu, Zetao
Wang, Yaqiong
Chen, Mingjie
Wang, Yuesheng
Chang, Junli
Yang, Guangxiao
He, Guangyuan
Li, Yin
Chen, Xiaoyuan
author_sort Zhao, Minhua
collection PubMed
description Partial root-zone drying (PRD) is an effective water-saving irrigation strategy that improves stress tolerance and facilitates efficient water use in several crops. It has long been considered that abscisic acid (ABA)-dependent drought resistance may be involved during partial root-zone drying. However, the molecular mechanisms underlying PRD-mediated stress tolerance remain unclear. It’s hypothesized that other mechanisms might contribute to PRD-mediated drought tolerance. Here, rice seedlings were used as a research model and the complex transcriptomic and metabolic reprogramming processes were revealed during PRD, with several key genes involved in osmotic stress tolerance identified by using a combination of physiological, transcriptome, and metabolome analyses. Our results demonstrated that PRD induces transcriptomic alteration mainly in the roots but not in the leaves and adjusts several amino-acid and phytohormone metabolic pathways to maintain the balance between growth and stress response compared to the polyethylene glycol (PEG)-treated roots. Integrated analysis of the transcriptome and metabolome associated the co-expression modules with PRD-induced metabolic reprogramming. Several genes encoding the key transcription factors (TFs) were identified in these co-expression modules, highlighting several key TFs, including TCP19, WRI1a, ABF1, ABF2, DERF1, and TZF7, involved in nitrogen metabolism, lipid metabolism, ABA signaling, ethylene signaling, and stress regulation. Thus, our work presents the first evidence that molecular mechanisms other than ABA-mediated drought resistance are involved in PRD-mediated stress tolerance. Overall, our results provide new insights into PRD-mediated osmotic stress tolerance, clarify the molecular regulation induced by PRD, and identify genes useful for further improving water-use efficiency and/or stress tolerance in rice.
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spelling pubmed-102884912023-06-24 Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice Zhao, Minhua Du, Canghao Zeng, Jian Gao, Zhihong Zhu, Yongyong Wang, Jinfei Zhang, Yupeng Zhu, Zetao Wang, Yaqiong Chen, Mingjie Wang, Yuesheng Chang, Junli Yang, Guangxiao He, Guangyuan Li, Yin Chen, Xiaoyuan Front Plant Sci Plant Science Partial root-zone drying (PRD) is an effective water-saving irrigation strategy that improves stress tolerance and facilitates efficient water use in several crops. It has long been considered that abscisic acid (ABA)-dependent drought resistance may be involved during partial root-zone drying. However, the molecular mechanisms underlying PRD-mediated stress tolerance remain unclear. It’s hypothesized that other mechanisms might contribute to PRD-mediated drought tolerance. Here, rice seedlings were used as a research model and the complex transcriptomic and metabolic reprogramming processes were revealed during PRD, with several key genes involved in osmotic stress tolerance identified by using a combination of physiological, transcriptome, and metabolome analyses. Our results demonstrated that PRD induces transcriptomic alteration mainly in the roots but not in the leaves and adjusts several amino-acid and phytohormone metabolic pathways to maintain the balance between growth and stress response compared to the polyethylene glycol (PEG)-treated roots. Integrated analysis of the transcriptome and metabolome associated the co-expression modules with PRD-induced metabolic reprogramming. Several genes encoding the key transcription factors (TFs) were identified in these co-expression modules, highlighting several key TFs, including TCP19, WRI1a, ABF1, ABF2, DERF1, and TZF7, involved in nitrogen metabolism, lipid metabolism, ABA signaling, ethylene signaling, and stress regulation. Thus, our work presents the first evidence that molecular mechanisms other than ABA-mediated drought resistance are involved in PRD-mediated stress tolerance. Overall, our results provide new insights into PRD-mediated osmotic stress tolerance, clarify the molecular regulation induced by PRD, and identify genes useful for further improving water-use efficiency and/or stress tolerance in rice. Frontiers Media S.A. 2023-06-09 /pmc/articles/PMC10288491/ /pubmed/37360728 http://dx.doi.org/10.3389/fpls.2023.1156514 Text en Copyright © 2023 Zhao, Du, Zeng, Gao, Zhu, Wang, Zhang, Zhu, Wang, Chen, Wang, Chang, Yang, He, Li and Chen 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
Zhao, Minhua
Du, Canghao
Zeng, Jian
Gao, Zhihong
Zhu, Yongyong
Wang, Jinfei
Zhang, Yupeng
Zhu, Zetao
Wang, Yaqiong
Chen, Mingjie
Wang, Yuesheng
Chang, Junli
Yang, Guangxiao
He, Guangyuan
Li, Yin
Chen, Xiaoyuan
Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice
title Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice
title_full Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice
title_fullStr Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice
title_full_unstemmed Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice
title_short Integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice
title_sort integrated omic analysis provides insights into the molecular regulation of stress tolerance by partial root-zone drying in rice
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10288491/
https://www.ncbi.nlm.nih.gov/pubmed/37360728
http://dx.doi.org/10.3389/fpls.2023.1156514
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