A conserved ethylene-triggered cell death mechanism may underlie hollow stem formation across plant species

Authors

• Mengxiao Yan, Shanghai Chenshan Botanical Garden
• Weijuan Fan, Shanghai Chenshan Botanical Garden
• Yinghui Meng, Shanghai Chenshan Botanical Garden
• Jiamin Zhao, Shanghai Chenshan Botanical Garden
• Wei Yang, Shanghai Chenshan Botanical Garden
• Ziyin Xu, Shanghai Chenshan Botanical Garden
• Yusen Gao, Shanghai Chenshan Botanical Garden
• Haiyan Zhuang, Chinese Academy of Sciences
• Wuyu Zhou, Shanghai Chenshan Botanical Garden
• Yuqin Wang, Shanghai Chenshan Botanical Garden
• Qingjun Huang, Shanghai Institute of Technology
• Ling Yuan, University of KentuckyFollow
• Hongxia Wang, Shanghai Chenshan Botanical GardenFollow
• Jun Yang, Shanghai Chenshan Botanical GardenFollow

Abstract

Hollow stems have independently evolved multiple times across the plant kingdom and play crucial roles in plant development and various environmental adaptations. However, the mechanisms underlying stem hollowness remain poorly understood. Water spinach (Ipomoea aquatica) is one of the few hollow-stemmed plants in the Convolvulaceae family (eudicot: asterid), and its hollow stems are essential for thriving in aquatic environments. Using histochemical staining and transcriptome analysis, we found that programmed cell death (PCD) is involved in cavity formation at water spinach shoot tips. Single-cell and spatial transcriptome analyses further revealed that ethylene and reactive oxygen species (ROS) likely drive and regulate this process by activating transcription factors IaNAC074, IaNAC087, IaNAC029, IaNTL9, and IaTGA9, which likely initiate PCD, senescence, and autophagy, collectively leading to pith cell death. These findings were validated through treatments with ethylene and ROS reagents in water spinach, as well as transient expression assays in tobacco. Additionally, transcriptomic data suggest that these mechanisms may also play a role in hollow stem formation in horsetail (fern), moso bamboo (monocot), and broad bean (eudicot: rosid), highlighting the conservation of PCD regulatory mechanisms in hollow stem formation. This study not only fills a major knowledge gap in the adaptive mechanisms of hollow stem formation but also opens broad avenues for agricultural and ecological applications, offering strategies to enhance crop tolerance to flooding and accelerate crop growth.

Document Type

Article

Publication Date

2026

Notes/Citation Information

Copyright © 2026 the Author(s). Published by PNAS. This article is distributed under Creative Commons Attribution-NonCommercial- NoDerivatives License 4.0 (CC BY- NC-ND).

Digital Object Identifier (DOI)

https://doi.org/10.1073/pnas.2530957123

Funding Information

This work was funded by the National Natural Science Foundation of China (32300207 to M.Y.) and the Shanghai Municipal Afforestation & City Appearance and Environmental Sanitation Administration (G262404 to M.Y. and G242407 to W.F.).

Repository Citation

Yan, Mengxiao; Fan, Weijuan; Meng, Yinghui; Zhao, Jiamin; Yang, Wei; Xu, Ziyin; Gao, Yusen; Zhuang, Haiyan; Zhou, Wuyu; Wang, Yuqin; Huang, Qingjun; Yuan, Ling; Wang, Hongxia; and Yang, Jun, "A conserved ethylene-triggered cell death mechanism may underlie hollow stem formation across plant species" (2026). Plant and Soil Sciences Faculty Publications. 183.
https://uknowledge.uky.edu/pss_facpub/183