RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves

Ca2+ signaling plays crucial roles in plant stress responses, including defense against insects. To counteract insect feeding, different parts of a plant deploy systemic signaling to communicate and coordinate defense responses, but little is known about the underlying mechanisms. In this study, mic...

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Main Authors: Che Zhan, Na Xue, Zhongxiang Su, Tianyin Zheng, Jianqiang Wu
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2025-07-01
Series:Plant Diversity
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Online Access:http://www.sciencedirect.com/science/article/pii/S2468265925000903
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author Che Zhan
Na Xue
Zhongxiang Su
Tianyin Zheng
Jianqiang Wu
author_facet Che Zhan
Na Xue
Zhongxiang Su
Tianyin Zheng
Jianqiang Wu
author_sort Che Zhan
collection DOAJ
description Ca2+ signaling plays crucial roles in plant stress responses, including defense against insects. To counteract insect feeding, different parts of a plant deploy systemic signaling to communicate and coordinate defense responses, but little is known about the underlying mechanisms. In this study, micrografting, in vivo imaging of Ca2+ and reactive oxygen species (ROS), quantification of jasmonic acid (JA) and defensive metabolites, and bioassay were used to study how Arabidopsis seedlings regulate systemic responses in leaves after hypocotyls are wounded. We show that wounding hypocotyls rapidly activated both Ca2+ and ROS signals in leaves. RBOHD, which functions to produce ROS, along with two glutamate receptors GLR3.3 and GLR3.6, but not individually RBOHD or GLR3.3 and GLR3.6, in hypocotyls regulate the dynamics of systemic Ca2+ signals in leaves. In line with the systemic Ca2+ signals, after wounding hypocotyl, RBOHD, GLR3.3, and GLR3.6 in hypocotyl also cooperatively regulate the transcriptome, hormone jasmonic acid, and defensive secondary metabolites in leaves of Arabidopsis seedlings, thus controlling the systemic resistance to insects. Unlike leaf-to-leaf systemic signaling, this study reveals the unique regulation of wounding-induced hypocotyl-to-leaf systemic signaling and sheds new light on how different plant organs use complex signaling pathways to modulate defense responses.
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spelling doaj-art-0e913d69f44f4664a557a45aa9a6dee22025-08-20T03:12:36ZengKeAi Communications Co., Ltd.Plant Diversity2468-26592025-07-0147469070110.1016/j.pld.2025.05.004RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leavesChe Zhan0Na Xue1Zhongxiang Su2Tianyin Zheng3Jianqiang Wu4Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, ChinaDepartment of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, ChinaDepartment of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, ChinaDepartment of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, ChinaDepartment of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China; State Key Laboratory of Plant Diversity and Specialty Crops, Beijing 100093, China; Corresponding author. Department of Economic Plants and Biotechnology, Yunnan Key Laboratory for Wild Plant Resources, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China.Ca2+ signaling plays crucial roles in plant stress responses, including defense against insects. To counteract insect feeding, different parts of a plant deploy systemic signaling to communicate and coordinate defense responses, but little is known about the underlying mechanisms. In this study, micrografting, in vivo imaging of Ca2+ and reactive oxygen species (ROS), quantification of jasmonic acid (JA) and defensive metabolites, and bioassay were used to study how Arabidopsis seedlings regulate systemic responses in leaves after hypocotyls are wounded. We show that wounding hypocotyls rapidly activated both Ca2+ and ROS signals in leaves. RBOHD, which functions to produce ROS, along with two glutamate receptors GLR3.3 and GLR3.6, but not individually RBOHD or GLR3.3 and GLR3.6, in hypocotyls regulate the dynamics of systemic Ca2+ signals in leaves. In line with the systemic Ca2+ signals, after wounding hypocotyl, RBOHD, GLR3.3, and GLR3.6 in hypocotyl also cooperatively regulate the transcriptome, hormone jasmonic acid, and defensive secondary metabolites in leaves of Arabidopsis seedlings, thus controlling the systemic resistance to insects. Unlike leaf-to-leaf systemic signaling, this study reveals the unique regulation of wounding-induced hypocotyl-to-leaf systemic signaling and sheds new light on how different plant organs use complex signaling pathways to modulate defense responses.http://www.sciencedirect.com/science/article/pii/S2468265925000903Signal transductionGraftingReactive oxygen speciesCalcium signalingGlutamateJasmonic acid
spellingShingle Che Zhan
Na Xue
Zhongxiang Su
Tianyin Zheng
Jianqiang Wu
RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves
Plant Diversity
Signal transduction
Grafting
Reactive oxygen species
Calcium signaling
Glutamate
Jasmonic acid
title RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves
title_full RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves
title_fullStr RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves
title_full_unstemmed RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves
title_short RBOHD, GLR3.3, and GLR3.6 cooperatively control wounding hypocotyl-induced systemic Ca2+ signals, jasmonic acid, and glucosinolates in Arabidopsis leaves
title_sort rbohd glr3 3 and glr3 6 cooperatively control wounding hypocotyl induced systemic ca2 signals jasmonic acid and glucosinolates in arabidopsis leaves
topic Signal transduction
Grafting
Reactive oxygen species
Calcium signaling
Glutamate
Jasmonic acid
url http://www.sciencedirect.com/science/article/pii/S2468265925000903
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