Mechanosensing antagonizes ethylene signaling to promote root gravitropism in rice

• Published in: Nature communications Vol. 16; no. 1; pp. 3712 - 17
• Main Authors: Wang, Han-Qing, Zhao, Xing-Yu, Tang, Zhong, Huang, Xin-Yuan, Wang, Peng, Zhang, Wenhua, Zhang, Yunhui, Luan, Sheng, Zhao, Fang-Jie
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 19.04.2025; Nature Publishing Group; Nature Portfolio
• Subjects: 14/34; 38/15; 38/39; 38/70; 38/88; 631/449/1741; 631/449/1975; 631/449/2675; Auxins; Calcium; Calcium signalling; Coiling; Ethylene; Ethylenes - metabolism; F-box protein; Gene Expression Regulation, Plant; Gravitropism; Gravitropism - genetics; Gravitropism - physiology; Humanities and Social Sciences; Hydroponics; Indoleacetic Acids - metabolism; Localization; Mechanotransduction, Cellular - physiology; Modules; multidisciplinary; Mutants; Mutation; Oryza - genetics; Oryza - growth & development; Oryza - metabolism; Oryza - physiology; Phenotypes; Plant Growth Regulators - metabolism; Plant hormones; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Roots - genetics; Plant Roots - growth & development; Plant Roots - metabolism; Plant Roots - physiology; Reactive oxygen species; Reactive Oxygen Species - metabolism; Rice; Rice fields; Roots; Science; Science (multidisciplinary); Signal Transduction; Soil mechanics; Stability
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-025-59047-z

Root gravitropism relies on gravity perception by the root cap and requires tightly regulated phytohormone signaling. Here, we isolate a rice mutant that displays root coiling in hydroponics but normal gravitropic growth in soil. We identify COILING ROOT IN WATER 1 ( CRW1 ) encoding an ETHYLENE-INSENSITIVE3 (EIN3)-BINDING F-BOX PROTEIN (OsEBF1) as the causative gene for the mutant phenotype. We show that the OsCRW1-EIN3 LIKE 1 and 2 (OsEIL1/2)-ETHYLENE RESPONSE FACTOR 82 (OsERF82) module controls the production of reactive oxygen species in the root tip, subsequently impacting root cap stability, polar localization of PIN-FORMED 2 (OsPIN2), symmetric distribution of auxin, and ultimately gravitropic growth of roots. The OsEIL1/2-OsERF82 ethylene signaling module is effectively impeded by applying gentle mechanical resistance to root tips, including growing in water-saturated paddy soil. We further show that mechanosensing-induced calcium signaling is required and sufficient for antagonizing the ethylene signaling pathway. This study has revealed previously unanticipated interplay among ethylene, auxin, and mechanosensing in the control of plant gravitropism. This study demonstrated that amplified ethylene signaling impairs gravitropic growth of rice roots by affecting root cap stability and OsPIN2 polar localization, whereas mechanosensing-induced calcium signaling antagonizes ethylene signaling to safeguard gravitropism.