Development stage-specific recovery of remedial nitrogen fertilizer application after waterlogging in maize through photosynthetic capacity and nitrogen allocation

doi:10.1016/j.jia.2025.11.015

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Yifei Sun^1*, Shancong Wang¹^*, Meiyu Chen¹, Xinru Hu¹, Reda M.M. Ahmed^{1, 3}, Fanzheng Meng¹, Yulou Tang^1#, Qinghua Yang¹, Shenjiao Yang^2#, Ruixin Shao^1#

¹ College of Agronomy/Key Laboratory of High-Efficiency Production of Wheat-Maize Double Cropping, Henan Agricultural University, Zhengzhou 450046, China

² Institute of Farmland Irrigation, Chinese Academy of Agricultural Sciences, Xinxiang 453002, China

³ Soil and Water Department, Faculty of Agriculture, Fayoum University, Fayoum 63514, Egypt

Highlights

Nitrogen (N) application at jointing stage (V6) led to significantly better recovery compared to that at blister stage (R2) under waterlogging stress (WS).

Under WS, N application restored photosynthetic capacity at V6 by enhancing photosynthetic enzyme activity, thereby increasing grains number.

Under WS, N application promoted N allocation to grain at R2 by activating protein synthesis of grain, which enhanced grain sink capacity.

Abstract
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摘要

淹水胁迫（WS）严重威胁夏玉米的产量，尽管补施氮（N）肥是常见的缓解策略，但不同发育阶段N调节途径的差异仍不清楚。以玉米杂交种“中玉505”为试验材料，在为期3年的田间定位试验中，研究了玉米在拔节期（V6）和灌浆期（R2）对WS的响应及N介导的恢复途径。在3年的试验中，与对照相比，WS在V6期和R2期分别使玉米产量平均降低27.6%和23.0%。结构方程模型表明，WS通过抑制叶片光合能力减少了V6期的穗粒数，并通过限制N向籽粒的分配降低了R2期的籽粒库容。然而，WS后补施N肥（WF）有效地减轻了产量损失，使V6期的穗粒数增加了19.1%，并使R2期的籽粒库容提高了23.4%。在V6期的恢复是由光合作用能力增强所驱动的，总叶绿素含量平均增加了23.6%，磷酸烯醇式丙酮酸羧化酶活性平均增加了36.3%，核酮糖-1,5-二磷酸羧化酶/加氧酶活性平均增加了24.8%。不同的是，R2期的恢复是由于氮素利用效率提高，籽粒中的氮素分配比例增加到73.1%，籽粒中的硝酸还原酶和谷氨酰胺合成酶活性分别平均增加了31.7% 和35.6%。转录组分析进一步证实了蛋白质加工基因（如hsp18a和hsp18c）的上调，促进了氮素分配和利用。总之，氮介导的恢复途径在玉米不同发育阶段有所不同，在V6期恢复了光合作用能力和籽粒数量，在R2期增加了氮素向籽粒的分配和库容。本研究将为提高玉米在V6和R2期对淹水胁迫的耐受性提供重要的理论和实践价值。

Abstract

Waterlogging stress (WS) significantly threatens summer maize production. Although supplemental nitrogen (N) fertilization is a common remediation strategy, the differences in N regulation pathways across developmental stages are still unclear. The maize hybrid ‘Zhongkeyu 505’ was used as the experimental material in a 3-year field localization experiment investigating the responses and N-mediated recovery pathway in maize at the jointing stage (V6) and blister stage (R2) to WS. Over three experimental years, compared to control, WS significantly decreased grain yield at V6 and R2 by an average of 27.6 and 23.0%, respectively. Structural equation modeling showed that WS decreased grain number at V6 by inhibiting leaf photosynthetic capacity, and reduced grain capacity at R2 by limiting N allocation to grains. However, post-waterlogging nitrogen application (WF) effectively mitigated these losses, increasing grain number by 19.1% at V6 and improving grain sink capacity by 23.4% at R2. The recovery at V6 was driven by enhanced photosynthetic capacity with average increases of 23.6% in total chlorophyll content, 36.3% in phosphoenolpyruvate carboxylase activity, and 24.8% in Rubisco activity. Differently, the recovery at R2 was due to improve N utilization, where N allocation in grains increased to 73.1%, and nitrate reductase and glutamine synthetase activities in grains increased by an average of 31.7 and 35.6%, respectively. Transcriptomic analysis further confirmed upregulation of protein-processing genes (e.g. hsp18a and hsp18c), facilitating N allocation and utilization. In conclusion, the N-mediated recovery pathway varied across maize development stages, with the photosynthetic capacity and grain number restored at V6 and N allocation to grains and sink capacity was increased at R2. This study will provide significant theoretical and practical value for enhancing tolerance in maize to WS at V6 and R2.

Keywords: summer maize waterlogging stress nitrogen fertilizer photosynthetic capacity nitrogen allocation

Online: 13 November 2025

Fund:

This work was supported by the Major Science and Technology Project of Henan Province, China (241100110300), the Scientific and Technological Innovation Team in Colleges and Universities in Henan Province (24IRTSTHN032), the Agricultural Science and Technology Innovation Program (ASTIP) of Chinese Academy of Agricultural Sciences, and the National Natural Science Foundation of China (51609246).

About author: Yifei Sun, E-mail: syf20020816@163.com; Shancong Wang, E-mail: wangshancong98@126.com; #Correspondence Ruixin Shao, E-mail: shao_rui_xin@126.com; Yulou Tang, E-mail: tyl134679@163.com; Shenjiao Yang, E-mail: yangshenjiao@caas.cn *These authors contributed equally to this work.

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Yifei Sun, Shancong Wang, Meiyu Chen, Xinru Hu, Reda M.M. Ahmed, Fanzheng Meng, Yulou Tang, Qinghua Yang, Shenjiao Yang, Ruixin Shao. 2025. Development stage-specific recovery of remedial nitrogen fertilizer application after waterlogging in maize through photosynthetic capacity and nitrogen allocation. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.11.015

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