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(Z)-3-Hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants

Cold and drought stresses severely limit crop production and can occur simultaneously. Although some transcription factors and hormones have been characterized in plants subjected each stress, the role of metabolites, especially volatiles, in response to cold and drought stress exposure is rarely st...

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Autores principales: Jin, Jieyang, Zhao, Mingyue, Jing, Tingting, Wang, Jingming, Lu, Mengqian, Pan, Yuting, Du, Wenkai, Zhao, Chenjie, Bao, Zhijie, Zhao, Wei, Tang, Xiaoyan, Schwab, Wilfried, Song, Chuankui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10517186/
https://www.ncbi.nlm.nih.gov/pubmed/37315209
http://dx.doi.org/10.1093/plphys/kiad346
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author Jin, Jieyang
Zhao, Mingyue
Jing, Tingting
Wang, Jingming
Lu, Mengqian
Pan, Yuting
Du, Wenkai
Zhao, Chenjie
Bao, Zhijie
Zhao, Wei
Tang, Xiaoyan
Schwab, Wilfried
Song, Chuankui
author_facet Jin, Jieyang
Zhao, Mingyue
Jing, Tingting
Wang, Jingming
Lu, Mengqian
Pan, Yuting
Du, Wenkai
Zhao, Chenjie
Bao, Zhijie
Zhao, Wei
Tang, Xiaoyan
Schwab, Wilfried
Song, Chuankui
author_sort Jin, Jieyang
collection PubMed
description Cold and drought stresses severely limit crop production and can occur simultaneously. Although some transcription factors and hormones have been characterized in plants subjected each stress, the role of metabolites, especially volatiles, in response to cold and drought stress exposure is rarely studied due to lack of suitable models. Here, we established a model for studying the role of volatiles in tea (Camellia sinensis) plants experiencing cold and drought stresses simultaneously. Using this model, we showed that volatiles induced by cold stress promote drought tolerance in tea plants by mediating reactive oxygen species and stomatal conductance. Needle trap microextraction combined with GC-MS identified the volatiles involved in the crosstalk and showed that cold-induced (Z)-3-hexenol improved the drought tolerance of tea plants. In addition, silencing C. sinensis alcohol dehydrogenase 2 (CsADH2) led to reduced (Z)-3-hexenol production and significantly reduced drought tolerance in response to simultaneous cold and drought stress. Transcriptome and metabolite analyses, together with plant hormone comparison and abscisic acid (ABA) biosynthesis pathway inhibition experiments, further confirmed the roles of ABA in (Z)-3-hexenol–induced drought tolerance of tea plants. (Z)-3-Hexenol application and gene silencing results supported the hypothesis that (Z)-3-hexenol plays a role in the integration of cold and drought tolerance by stimulating the dual-function glucosyltransferase UGT85A53, thereby altering ABA homeostasis in tea plants. Overall, we present a model for studying the roles of metabolites in plants under multiple stresses and reveal the roles of volatiles in integrating cold and drought stresses in plants.
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spelling pubmed-105171862023-09-24 (Z)-3-Hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants Jin, Jieyang Zhao, Mingyue Jing, Tingting Wang, Jingming Lu, Mengqian Pan, Yuting Du, Wenkai Zhao, Chenjie Bao, Zhijie Zhao, Wei Tang, Xiaoyan Schwab, Wilfried Song, Chuankui Plant Physiol Research Article Cold and drought stresses severely limit crop production and can occur simultaneously. Although some transcription factors and hormones have been characterized in plants subjected each stress, the role of metabolites, especially volatiles, in response to cold and drought stress exposure is rarely studied due to lack of suitable models. Here, we established a model for studying the role of volatiles in tea (Camellia sinensis) plants experiencing cold and drought stresses simultaneously. Using this model, we showed that volatiles induced by cold stress promote drought tolerance in tea plants by mediating reactive oxygen species and stomatal conductance. Needle trap microextraction combined with GC-MS identified the volatiles involved in the crosstalk and showed that cold-induced (Z)-3-hexenol improved the drought tolerance of tea plants. In addition, silencing C. sinensis alcohol dehydrogenase 2 (CsADH2) led to reduced (Z)-3-hexenol production and significantly reduced drought tolerance in response to simultaneous cold and drought stress. Transcriptome and metabolite analyses, together with plant hormone comparison and abscisic acid (ABA) biosynthesis pathway inhibition experiments, further confirmed the roles of ABA in (Z)-3-hexenol–induced drought tolerance of tea plants. (Z)-3-Hexenol application and gene silencing results supported the hypothesis that (Z)-3-hexenol plays a role in the integration of cold and drought tolerance by stimulating the dual-function glucosyltransferase UGT85A53, thereby altering ABA homeostasis in tea plants. Overall, we present a model for studying the roles of metabolites in plants under multiple stresses and reveal the roles of volatiles in integrating cold and drought stresses in plants. Oxford University Press 2023-06-14 /pmc/articles/PMC10517186/ /pubmed/37315209 http://dx.doi.org/10.1093/plphys/kiad346 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
Jin, Jieyang
Zhao, Mingyue
Jing, Tingting
Wang, Jingming
Lu, Mengqian
Pan, Yuting
Du, Wenkai
Zhao, Chenjie
Bao, Zhijie
Zhao, Wei
Tang, Xiaoyan
Schwab, Wilfried
Song, Chuankui
(Z)-3-Hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants
title (Z)-3-Hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants
title_full (Z)-3-Hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants
title_fullStr (Z)-3-Hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants
title_full_unstemmed (Z)-3-Hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants
title_short (Z)-3-Hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants
title_sort (z)-3-hexenol integrates drought and cold stress signaling by activating abscisic acid glucosylation in tea plants
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10517186/
https://www.ncbi.nlm.nih.gov/pubmed/37315209
http://dx.doi.org/10.1093/plphys/kiad346
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