Root pre-adaptation: adventitious root plasticity from mild priming enhances hypoxia survival in wheat

doi:10.1016/j.jia.2026.01.029

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Yujie He¹^*, Yi Wang¹^*, Mei Huang¹, Ziru Zhang¹, Qing Li¹, Qin Zhou¹, Yingxin Zhong¹, Jian Cai¹, Stefania Masci², Xiao Wang¹^#, Dong Jiang¹

¹College of Agriculture, Nanjing Agricultural University/Key Laboratory of Crop Physiology and Ecology in Southern China, Nanjing 210095, China

²Department of Agriculture and Forest Sciences (DAFNE), University of Tuscia, Viterbo 01100, Italy

Highlights

Post-priming recovery is a critical window for waterlogging stress resilience.

Mild priming shifts adventitious root development toward a persistent, long-root-dominated architecture.

Primed roots co-optimize water transport and radial oxygen loss under hypoxia.

Anticipatory root priming model is proposed for pre-adaptation to recurrent waterlogging.

Abstract
References

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摘要

土壤渍水导致根系缺氧，严重制约全球小麦生产。尽管研究表明渍水锻炼可减轻胁迫造成的产量损失、提升植株耐渍性，但锻炼后耐渍性获得过程中不定根的发育规律及其生理机制尚不明晰。本研究证实，轻度渍水锻炼（MP）可显著增强小麦对后续渍水胁迫的耐受能力，且锻炼后的恢复阶段是植株进行根系形态与生理重编程的关键窗口。在此期间，经历轻度锻炼的小麦其不定根发育发生显著转变：从胁迫诱导产生的短小、暂时性不定根，转向形成以持久性长不定根为主导的根系构型。与新生不定根相比，这些经重编程的成熟不定根通过协同优化根系水力导度（Lpr）与径向氧损耗（ROL），表现出更优越的生理功能。机制上，Lpr的持续提升与水通道蛋白基因（TaTIP2-1、TaTIP2-2及TaPIP2-6）的稳定上调表达相一致，而ROL的增强则促进了根际氧环境的改善。结构方程模型进一步明确，恢复阶段长不定根的形成是驱动Lpr与ROL协同优化的核心性状。相比之下，重度锻炼导致根系不可逆损伤，未能诱发上述适应性响应。本研究提出“预适应型根系构建”模型，即轻度胁迫利用恢复窗口期，主动调控不定根发育，形成结构持久、功能高效的根系系统，从而将植物逆境应对策略从“被动应急反应”提升为“主动调控的韧性建立”。该研究为基于胁迫锻炼的作物抗逆性改良提供了重要的生理学框架与理论依据。

Abstract

Soil waterlogging threatens global wheat production by inducing root hypoxia. While stress priming can enhance plant resilience, the specific mechanisms underlying this pre-adaptation remain poorly understood. Here, we demonstrate that a single day of mild waterlogging priming (MP) induces a robust primed state in wheat, conferring superior recovery and tolerance to subsequent hypoxic stress. Crucially, we identify the post-priming recovery phase as a decisive window for physiological reprogramming, rather than a mere period of passive repair. During this window, MP plants developmentally reconstruct their adventitious roots (ARs) system, transitioning from transient, short ARs to a persistent architecture dominated by long ARs. This reprogrammed root system exhibits functionally superior through the synergistic co-optimization of root hydraulic conductivity (Lpr) and radial oxygen loss (ROL). Physiological and molecular analyses reveal that enhanced Lpr is accompanied by the sustained upregulation of aquaporin genes (TaTIP2-1, TaTIP2-2, and TaPIP2-6), while improved ROL facilitates superior root rhizosphere aeration. Structural equation modeling statistically validates that the formation of long ARs during recovery is the pivotal trait causally driving the optimization of Lpr and ROL. In contrast, severe priming causes irreversible damage and confers no adaptive benefit. Our findings propose a model of “anticipatory root priming”, wherein mild stress leverages the recovery window to pre-construct an energetically efficient root system. This fundamentally shifts the plant's strategy from a reactive emergency response to proactive, regulated resilience, providing a physiological framework for priming-based crop improvement.

Keywords: wheat waterlogging priming adventitious roots root hydraulic conductivity radial oxygen loss

Online: 20 January 2026

Fund:

This study was supported by the projects of the National Key Research and Development Program of China (2024YFD2301305), the National Natural Science Foundation of China (32272213), the Key Research and Development Project of Shandong Province, China (2024TZXD070), the China Agriculture Research System (CARS-03), and the Jiangsu Collaborative Innovation Center for Modern Crop Production, China (JCIC-MCP).

About author: #Correspondence Xiao Wang, E-mail: xiaowang@njau.edu.cn *These authors contributed equally.

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Yujie He, Yi Wang, Mei Huang, Ziru Zhang, Qing Li, Qin Zhou, Yingxin Zhong, Jian Cai, Stefania Masci, Xiao Wang, Dong Jiang . 2026. Root pre-adaptation: adventitious root plasticity from mild priming enhances hypoxia survival in wheat. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2026.01.029

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