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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KeAi Communications Co., Ltd.
2025-07-01
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| 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. |
| format | Article |
| id | doaj-art-0e913d69f44f4664a557a45aa9a6dee2 |
| institution | DOAJ |
| issn | 2468-2659 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | KeAi Communications Co., Ltd. |
| record_format | Article |
| series | Plant Diversity |
| 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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