The GhMAP3K62-GhMKK16-GhMPK32 kinase cascade regulates drought tolerance by activating GhEDT1-mediated ABA accumulation in cotton

Introduction: Drought is the principal abiotic stress that severely impacts cotton (Gossypium hirsutum) growth and productivity. Upon sensing drought, plants activate stress-related signal transduction pathways, including ABA signal and mitogen-activated protein kinase (MAPK) cascade. However, as th...

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Main Authors: Lin Chen, Bing Zhang, Linjie Xia, Dandan Yue, Bei Han, Weinan Sun, Fengjiao Wang, Keith Lindsey, Xianlong Zhang, Xiyan Yang
Format: Article
Language:English
Published: Elsevier 2023-09-01
Series:Journal of Advanced Research
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2090123222002491
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author Lin Chen
Bing Zhang
Linjie Xia
Dandan Yue
Bei Han
Weinan Sun
Fengjiao Wang
Keith Lindsey
Xianlong Zhang
Xiyan Yang
author_facet Lin Chen
Bing Zhang
Linjie Xia
Dandan Yue
Bei Han
Weinan Sun
Fengjiao Wang
Keith Lindsey
Xianlong Zhang
Xiyan Yang
author_sort Lin Chen
collection DOAJ
description Introduction: Drought is the principal abiotic stress that severely impacts cotton (Gossypium hirsutum) growth and productivity. Upon sensing drought, plants activate stress-related signal transduction pathways, including ABA signal and mitogen-activated protein kinase (MAPK) cascade. However, as the key components with the fewest members in the MAPK cascade, the function and regulation of GhMKKs need to be elucidated. In addition, the relationship between MAPK module and the ABA core signaling pathway remains incompletely understood. Objective: Here we aim to elucidate the molecular mechanism of cotton response to drought, with a focus on mitogen-activated protein kinase (MAPK) cascades activating ABA signaling. Methods: Biochemical, molecular and genetic analysis were used to study the GhMAP3K62-GhMKK16-GhMPK32-GhEDT1 pathway genes. Results: A nucleus- and membrane-localized MAPK cascade pathway GhMAP3K62-GhMKK16-GhMPK32, which targets and phosphorylates the nuclear-localized transcription factor GhEDT1, to activate downstream GhNCED3 to mediate ABA-induced stomatal closure and drought response was characterized in cotton. Overexpression of GhMKK16 promotes ABA accumulation, and enhances drought tolerance via regulating stomatal closure under drought stress. Conversely, RNAi-mediated knockdown of GhMKK16 expression inhibits ABA accumulation, and reduces drought tolerance. Virus-induced gene silencing (VIGS)-mediated knockdown of either GhMAP3K62, GhMPK32 or GhEDT1 expression represses ABA accumulation and reduces drought tolerance through inhibiting stomatal closure. Expression knockdown of GhMPK32 or GhEDT1 in GhMKK16-overexpressing cotton reinstates ABA content and stomatal opening-dependent drought sensitivity to wild type levels. GhEDT1 could bind to the HD boxes in the promoter of GhNCED3 to activate its expression, resulting in ABA accumulation. We propose that the MAPK cascade GhMAP3K62-GhMKK16-GhMPK32 pathway functions on drought response through ABA-dependent stomatal movement in cotton.
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spelling doaj.art-9014b018519e4d6c8db649022964f37e2023-09-01T05:01:02ZengElsevierJournal of Advanced Research2090-12322023-09-01511325The GhMAP3K62-GhMKK16-GhMPK32 kinase cascade regulates drought tolerance by activating GhEDT1-mediated ABA accumulation in cottonLin Chen0Bing Zhang1Linjie Xia2Dandan Yue3Bei Han4Weinan Sun5Fengjiao Wang6Keith Lindsey7Xianlong Zhang8Xiyan Yang9National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. ChinaNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. China; Hubei Hongshan Laboratory, Wuhan, ChinaNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. China; Hubei Hongshan Laboratory, Wuhan, ChinaNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. China; Hubei Hongshan Laboratory, Wuhan, ChinaNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. China; Hubei Hongshan Laboratory, Wuhan, ChinaNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. China; Hubei Hongshan Laboratory, Wuhan, ChinaNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. ChinaDepartment of Biosciences, Durham University, South Road, Durham DH1 3LE, UKNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. China; Hubei Hongshan Laboratory, Wuhan, ChinaNational Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. China; Hubei Hongshan Laboratory, Wuhan, China; Corresponding author.Introduction: Drought is the principal abiotic stress that severely impacts cotton (Gossypium hirsutum) growth and productivity. Upon sensing drought, plants activate stress-related signal transduction pathways, including ABA signal and mitogen-activated protein kinase (MAPK) cascade. However, as the key components with the fewest members in the MAPK cascade, the function and regulation of GhMKKs need to be elucidated. In addition, the relationship between MAPK module and the ABA core signaling pathway remains incompletely understood. Objective: Here we aim to elucidate the molecular mechanism of cotton response to drought, with a focus on mitogen-activated protein kinase (MAPK) cascades activating ABA signaling. Methods: Biochemical, molecular and genetic analysis were used to study the GhMAP3K62-GhMKK16-GhMPK32-GhEDT1 pathway genes. Results: A nucleus- and membrane-localized MAPK cascade pathway GhMAP3K62-GhMKK16-GhMPK32, which targets and phosphorylates the nuclear-localized transcription factor GhEDT1, to activate downstream GhNCED3 to mediate ABA-induced stomatal closure and drought response was characterized in cotton. Overexpression of GhMKK16 promotes ABA accumulation, and enhances drought tolerance via regulating stomatal closure under drought stress. Conversely, RNAi-mediated knockdown of GhMKK16 expression inhibits ABA accumulation, and reduces drought tolerance. Virus-induced gene silencing (VIGS)-mediated knockdown of either GhMAP3K62, GhMPK32 or GhEDT1 expression represses ABA accumulation and reduces drought tolerance through inhibiting stomatal closure. Expression knockdown of GhMPK32 or GhEDT1 in GhMKK16-overexpressing cotton reinstates ABA content and stomatal opening-dependent drought sensitivity to wild type levels. GhEDT1 could bind to the HD boxes in the promoter of GhNCED3 to activate its expression, resulting in ABA accumulation. We propose that the MAPK cascade GhMAP3K62-GhMKK16-GhMPK32 pathway functions on drought response through ABA-dependent stomatal movement in cotton.http://www.sciencedirect.com/science/article/pii/S2090123222002491ABACottonDroughtGhEDT1MAPK cascade pathwayStomatal movement
spellingShingle Lin Chen
Bing Zhang
Linjie Xia
Dandan Yue
Bei Han
Weinan Sun
Fengjiao Wang
Keith Lindsey
Xianlong Zhang
Xiyan Yang
The GhMAP3K62-GhMKK16-GhMPK32 kinase cascade regulates drought tolerance by activating GhEDT1-mediated ABA accumulation in cotton
Journal of Advanced Research
ABA
Cotton
Drought
GhEDT1
MAPK cascade pathway
Stomatal movement
title The GhMAP3K62-GhMKK16-GhMPK32 kinase cascade regulates drought tolerance by activating GhEDT1-mediated ABA accumulation in cotton
title_full The GhMAP3K62-GhMKK16-GhMPK32 kinase cascade regulates drought tolerance by activating GhEDT1-mediated ABA accumulation in cotton
title_fullStr The GhMAP3K62-GhMKK16-GhMPK32 kinase cascade regulates drought tolerance by activating GhEDT1-mediated ABA accumulation in cotton
title_full_unstemmed The GhMAP3K62-GhMKK16-GhMPK32 kinase cascade regulates drought tolerance by activating GhEDT1-mediated ABA accumulation in cotton
title_short The GhMAP3K62-GhMKK16-GhMPK32 kinase cascade regulates drought tolerance by activating GhEDT1-mediated ABA accumulation in cotton
title_sort ghmap3k62 ghmkk16 ghmpk32 kinase cascade regulates drought tolerance by activating ghedt1 mediated aba accumulation in cotton
topic ABA
Cotton
Drought
GhEDT1
MAPK cascade pathway
Stomatal movement
url http://www.sciencedirect.com/science/article/pii/S2090123222002491
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