Please wait a minute...
Journal of Integrative Agriculture  2026, Vol. 25 Issue (9): 3609-3618    DOI: 10.1016/j.jia.2025.02.033
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Drought priming enhances young spike development in wheat under drought stress during stem elongation

Mengting He1, Hanxiao Li1, Zhuangzhuang Sun1, Xiangnan Li2, Qing Li1, Jian Cai1, Qin Zhou1, Yingxin Zhong1, Xiao Wang1#, Dong Jiang1

1 National Technique Innovation Center for Regional Wheat Production/Key Laboratory of Crop Ecophysiology, Ministry of Agriculture and Rural Affairs/College of Agriculture, Nanjing Agricultural University, Nanjing 210095, China

2 Key Laboratory of Mollisols AgroecologyNortheast Institute of Geography and AgroecologyChinese Academy of SciencesChangchun 130102China

 Highlight

Drought priming enhances photosynthesis and antioxidant defenses to improve drought tolerance.

Through priming, spike development is stabilized to promote floret differentiation and fertility under drought.

Optimized carbon metabolism and hormones support stress adaptation and yield improvement.

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

干旱胁迫是制约小麦产量的关键环境因子,其中拔节期干旱对穗分化的抑制作用尤为突出。本研究基于作物逆境胁迫记忆理论,系统解析了三叶期干旱锻炼对拔节期穗发育的生理调控机制。研究通过对三叶期小麦施加干旱锻炼与拔节期干旱胁迫试验,揭示了干旱锻炼通过碳代谢重编程稳定幼穗分化的生理机制。研究表明:干旱锻炼显著提升植株的生理适应能力。在拔节期干旱胁迫下,经过锻炼植株旗叶光合速率较未锻炼植株提25.7%,叶片水势增加17.4%,并有效缓解氧化损伤(过氧化氢和丙二醛含量分别降低30.6%和11.1%)叶片碳代谢关键酶活性分析发现,己糖激酶和果糖激酶的活性分别增加了170%和236%,驱动了碳代谢流稳态建立,从而增加了小穗和可育小花的形成,最终实现穗粒数13.8%的显著提升。本研究创新性地揭示了干旱锻炼通过“碳代谢稳态和穗器官建成”协同调控增强小麦耐逆性的生理机制,为作物抗逆栽培理论提供了重要补充,也为粮食安全生产提供了创新性解决方案。



Abstract  

Drought stress is a significant environmental stressor that can have detrimental effects on crop yields, especially during stem elongation.  Drought priming has emerged as a promising technique for enhancing plant drought tolerance.  However, the effects of drought priming on the spike differentiation process and its physiological basis in wheat are not clear.  In this study, we investigated the effects of drought priming on spike development under drought stress by applying drought priming at the three-leaf stage and drought stress during stem elongation.  This study demonstrated that drought priming significantly increased the photosynthetic rate of flag leaves by approximately 25.7% and improved leaf water potential by 17.4% during drought stress.  Moreover, it mitigated oxidative damage by reducing the hydrogen peroxide and malondialdehyde levels by 30.6 and 11.1%, respectively, during stem elongation.  Drought priming also markedly enhanced the activities of two key carbon metabolism enzymes, hexokinase and fructokinase, by 170.0 and 236.0%, respectively.  This improved carbon metabolism and stabilized spike differentiation, leading to increased spikelet and floret primordia formation.  Ultimately, drought priming achieved a 13.8% increase in kernel number per spike, demonstrating its potential for improving grain yield under drought conditions.  This study innovatively revealed the “carbon homeostasis-spike development” coordination mechanism underlying drought priming-enhanced reproductive stress tolerance.  The findings advance our understanding of stress memory as it relates to spatiotemporal regulation in crops and offer transformative solutions for stabilizing wheat production under climate change scenarios.

Keywords:  wheat       drought priming        spike differentiation       carbon metabolism  
Received: 31 October 2024   Accepted: 26 January 2025 Online: 19 February 2025  
Fund: This study was supported by projects of the National Natural Science Foundation of China (32272213 and 31771693), the National Key Research and Development Program of China (2024YFD2301305), the Jiangsu Innovation Support Program for International Science and Technology Cooperation Project, China (BZ2023049), 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, Tel/Fax: +86-25-84399627, E-mail: xiaowang@njau.edu.cn

Cite this article: 

Mengting He, Hanxiao Li, Zhuangzhuang Sun, Xiangnan Li, Qing Li, Jian Cai, Qin Zhou, Yingxin Zhong, Xiao Wang, Dong Jiang. 2026. Drought priming enhances young spike development in wheat under drought stress during stem elongation. Journal of Integrative Agriculture, 25(9): 3609-3618.

Ahmad K S, Shehzad M A, Javid H, Mehmood A, Akhtar G, Zafar S, Mahroof S, Mahmoud E A, Elansary H O, Ulfat A, Abid H. 2024. Transgenerational seed exposure to elevated CO involves stress memory regulation at metabolic levels to confer drought resistance in wheat. Acs Omega9, 20042–20055.

Ahmad Z, Waraich E A, Akhtar S, Anjum S, Ahmad T, Mahboob W, Hafeez O B, Tapera T, Labuschagne M, Rizwan M. 2018. Physiological responses of wheat to drought stress and its mitigation approaches. Acta Physiologiae Plantarum4080.

Bahuguna R N, Tamilselvan A, Muthurajan R, Solis C A, Jagadish S V K. 2018. Mild preflowering drought priming improves stress defences, assimilation and sink strength in rice under severe terminal drought. Functional Plant Biology45, 827–839.

Chen Z D, Wang J F, Dong D Q, Lou C, Zhang Y, Wang Y X, Yu B, Wang P F, Kang G Z. 2024. Comparative analysis of TaPHT1;9 function using CRISPR-edited mutants, ectopic transgenic plants and their wild types under soil conditions. Plant and Soil1, 1–12.

Daryanto S, Wang L, Jacinthe P A. 2016. Global synthesis of drought effects on maize and wheat production. PLoS ONE11, e0156362.

Ding Y, Fromm M, Avramova Z. 2012. Multiple exposures to drought ‘train’ transcriptional responses in ArabidopsisNature Communications3, 740.

Fan X, Jiang D, Dai T, Jing Q, Cao W. 2005. Effects of nitrogen supply on flag leaf photosynthesis and grain starch accumulation of wheat from its anthesis to maturity under drought or waterlogging. Chinese Journal of Applied Ecology16, 1883–1888.

Frank A B, Bauer A, Black A L. 1987. Effects of air-temperature and water-stress on apex development in spring wheat. Crop Science27, 113–116.

Frantová N, Rábek M, Elzner P, Streda T, Jovanovic I, Holková L, Martinek P, Smutná P, Prásil I T. 2022. Different drought tolerance strategy of wheat varieties in spike architecture. Agronomy-Basel12, 2328.

González F G, Slafer G A, Miralles D J. 2002. Vernalization and photoperiod responses in wheat pre-flowering reproductive phases. Field Crops Research, 74, 183–195.

Han Y J, Wang Y C, Zhang D M, Gao H, Sun Y, Tao B, Zhang F Y, Ma H, Liu X M, Ren H L. 2023. Planting models and deficit irrigation strategies to improve radiation use efficiency, dry matter translocation and winter wheat productivity under semi-arid regions. Journal of Plant Physiology280, 153864.

Hou M L, Li Y, Biswas A, Chen X G, Xie L L, Liu D L, Li L C, Feng H, Wu S F, Satoh Y, Pulatov A, Siddique K H M. 2024. Concurrent drought threaten wheat and maize production and widen crop yield gaps in the future. Agricultural Systems220, 104056.

Jammer A, Gasperl A, Luschin-Ebengreuth N, Heyneke E, Chu H, Cantero-Navarro E, Grosskinsky D K, Albacete A A, Stabentheiner E, Franzaring J, Fangmeier A, van der Graaff E, Roitsch T. 2015. Simple and robust determination of the activity signature of key carbohydrate metabolism enzymes for physiological phenotyping in model and crop plants. Journal of Experimental Botany66, 5531–5542.

Ji X M, Dong B D, Shiran B, Talbot M J, Edlington J E, Hughes T, White R G, Gubler F, Dolferus R. 2011. Control of abscisic acid catabolism and abscisic acid homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiology, 156, 647–662.

Ji X M, Shiran B, Wan J L, Lewis D C, Jenkins C L D, Condon A G, Richards R A, Dolferus R. 2010. Importance of pre-anthesis anther sink strength for maintenance of grain number during reproductive stage water stress in wheat. Plant Cell and Environment33, 926–942.

Jiang K, Asami T. 2018. Chemical regulators of plant hormones and their applications in basic research and agriculture. Bioscience Biotechnology and Biochemistry82, 1265–1300.

Kaur V, Madaan S, Behl R K. 2017. ADP-glucose pyrophosphorylase activity in relation to yield potential of wheat: Response to independent and combined high temperature and drought stress. Cereal Research Communications45, 181–191.

Kiba T, Takei K, Kojima M, Sakakibara H. 2013. Side-chain modification of cytokinins controls shoot growth in ArabidopsisDevelopmental Cell27, 452–461.

Lan Y Z, Chawade A, Kuktaite R, Johansson E. 2022. Climate change impact on wheat performance - Effects on vigour, plant traits and yield from early and late drought stress in diverse lines. International Journal of Molecular Sciences23, 3333.

Mittler R, Vanderauwera S, Gollery M, Van Breusegem F. 2004. Reactive oxygen gene network of plants. Trends in Plant Science9, 490–498.

Pan X, Welti R, Wang X. 2010. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nature Protocols5, 986–992.

Piedrahita V A, Roberts A P, Rohling E J, Heslop D, Zhao X, Galeotti S, Florindo F, Grant K M, Hu P X, Li J H. 2024. Dry hydroclimates in the late palaeocene-early eocene hothouse world. Nature Communications15, 7042.

Pradhan G P, Prasad P V V, Fritz A K, Kirkham M B, Gill B S. 2012. Effects of drought and high temperature stress on synthetic hexaploid wheat. Functional Plant Biology39, 190–198.

Prasad P V V, Boote K J, Allen L H, Sheehy J E, Thomas J M G. 2006. Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Research95, 398–411.

Shen S, Liang X G, Zhang L, Zhao X, Liu Y P, Lin S, Gao Z, Wang P, Wang Z M, Zhou S L. 2020. Intervening in sibling competition for assimilates by controlled pollination prevents seed abortion under postpollination drought in maize. Plant Cell Environment43, 903–919.

Shokat S, Grosskinsky D K, Liu F L. 2021. Impact of elevated CO on two contrasting wheat genotypes exposed to intermediate drought stress at anthesis. Journal of Agronomy and Crop Science207, 20–33.

Sohag A A, Tahjib-Ul-Arif M, Brestic M, Afrin S, Sakil M A, Hossain M T, Hossain M A, Hossain M A. 2020. Exogenous salicylic acid and hydrogen peroxide attenuate drought stress in rice. Plant Soil and Environment66, 7–13.

Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D. 2008. Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis water-logging. Photosynthetica46, 21–27.

Velikova V, Yordanov I, Edreva A. 2000. Oxidative stress and some antioxidant systems in acid rain-treated bean plants - Protective role of exogenous polyamines. Plant Science151, 59–66.

Wang X, Vignjevic M, Jiang D, Jacobsen S, Wollenweber B. 2014. Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. Journal of Experimental Botany65, 6441–6456.

Wang X, Vignjevic M, Liu F L, Jacobsen S, Jiang D, Wollenweber B. 2015. Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regulation75, 677–687.

Wang X, Zhang J, Song J, Huang M, Cai J, Zhou Q, Dai T, Jiang D. 2020. Abscisic acid and hydrogen peroxide are involved in drought priming-induced drought tolerance in wheat (Triticum aestivum L.). Plant Biology22, 1113–1122.

Whitechurch E, Slafer G, Miralles D. 2007. Variability in the duration of stem elongation in wheat and barley genotypes. Journal of Agronomy and Crop Science193, 138–145.

Wu X L, Liu M, Li C S, Mchugh A D, Li M, Xiong T, Liu Y B, Tang Y L. 2022. Source–sink relations and responses to sink–source manipulations during grain filling in wheat. Journal of Integrative Agriculture21, 1593–1605.

Xing X H, Fang C W, Li L, Jiang H Q, Zhou Q, Jiang H D, Wang S H. 2016. Improved drought tolerance by α-naphthaleneacetic acid-induced ROS accumulation in two soybean cultivars. Journal of Integrative Agriculture15, 1770–1784.

Ye F, Jiang M, Zhang P, Liu L, Liu S Q, Zhao C S, Li X N. 2022. Exogenous melatonin reprograms the rhizosphere microbial community to modulate the responses of barley to drought stress. International Journal of Molecular Sciences23, 9665.

Zhang Z, Li J, Hu N Y, Li W, Qin W L, Li J P, Gao Y M, Liu Y, Sun Z C, Yu K, Wang Z M, Zhang Y H. 2021. Spike growth affects spike fertility through the number of florets with green anthers before floret abortion in wheat. Field Crops Research260, 108007.

[1] Qian Liu, Qijing Xuan, Yuxin Lan, Xinlin Xie, Bin Chen, Jianing You, Longxing Su, Md Nahibuzzaman Lohani, Lei Wu, Xinrong Hu, Li Yin, Yanlin Liu, Tongzhu Wang, Qiantao Jiang, Yuming Wei, Youliang Zheng, Chunji Liu, Hongwei Geng, Jian Ma. Genetic identification and characterization of a novel locus for wheat kernel length[J]. >Journal of Integrative Agriculture, 2026, 25(9): 3548-3558.
[2] Shujuan Liu, Li Zhao, Chenyang Hao, Yuxue Pan, Mengjiao Guo, Yilin Huang, Haixia Liu, Jian Hou, Zaifeng Li, Tian Li, Xinhong Chen, Xueyong Zhang. TaRLK-1B: A novel wheat gene conferring resistance to leaf rust revealed by a genome-wide association study[J]. >Journal of Integrative Agriculture, 2026, 25(9): 3537-3547.
[3] Cong Li, Lei Wu, Xinyao He, Yi He, Peng Jiang, Jian Ma, Pawan K. Singh, Xu Zhang. Identification and validation of two QTLs associated with Fusarium head blight resistance in spring wheat (Triticum aestivum L.)[J]. >Journal of Integrative Agriculture, 2026, 25(8): 3126-3138.
[4] Linyi Qiao, Huifang Li, Jun Zheng, Xueyong Zhang. Towards a better understanding of auxin response factors for improving cereal crops[J]. >Journal of Integrative Agriculture, 2026, 25(8): 3103-3117.
[5] Jiajie He, Zhibin Xu, Bo Feng, Qiang Zhou, Xiaofeng Liu, Guangsi Ji, Shaodan Guo, Xiaoli Fan, Tao Wang. Genetic dissection and validation of a stable QTL for grain roundness on chromosome 5A in bread wheat (Triticum aestivum L.)[J]. >Journal of Integrative Agriculture, 2026, 25(7): 2714-2722.
[6] Yingpeng Wang, Yifan Hua, Lanxin Mei, Yixuan Meng, Yongtao Guo, Jian Cai, Mei Huang, Yingxin Zhong, Xiao Wang, Dong Jiang, Qin Zhou. An application strategy of combined controlled-release fertilizers can balance the yield and quality of soft wheat while meeting its nutrient requirements[J]. >Journal of Integrative Agriculture, 2026, 25(7): 2783-2795.
[7] Yunfeng Chen, Cheng Hu, Yufei Li, Xuemei Han, Donghai Liu, Yan Qiao, Min Xu. Long-term fertilization enriches soil food web mainly through bottom-up regulation in a rice–wheat cropping system[J]. >Journal of Integrative Agriculture, 2026, 25(7): 2982-2992.
[8] Luchen Zhang, Longqin Wang, Yongchao Tian, Liang Tang, Bing Liu, Yan Zhu, Weixing Cao, Liujun Xiao, Leilei Liu. Quantifying the effects of nitrogen and potassium interactions on wheat using a new development index[J]. >Journal of Integrative Agriculture, 2026, 25(6): 2374-2388.
[9] Zhipeng Shi, Guohao Han, Tiantian Gu, Hanwen Yan, Yujie Chang, Shiyu Zhuo, Lijun Cao, Lixian Xing, Yuping Liu, Xiaofang Li, Yelun Zhang, Diaoguo An. Multi-dimensional comprehensive evaluation reveals the quality trait characteristics of wheat cultivars in the Huang-Huai wheat region of China[J]. >Journal of Integrative Agriculture, 2026, 25(6): 2299-2313.
[10] Jingui Wei, Fang Yin, Yao Guo, Zhilong Fan, Falong Hu, Qiming Wang, Shoufa Mao, Qiang Chai, Wen Yin. Mixed cropping green manure can simultaneously improve the nutrient yield and quality of spring wheat grain under reduced chemical nitrogen supply[J]. >Journal of Integrative Agriculture, 2026, 25(5): 1887-1901.
[11] Ying Liu, Jiangyao Fu, Haotian Chen, Yajun Zhang, Siyu Li, Kuanyu Zhu, Yunji Xu, Weilu Wang, Junfei Gu, Hao Zhang, Zhiqin Wang, Lijun Liu, Jianhua Zhang, Weiyang Zhang, Jianchang Yang. Cytokinins redistributing drives nitrogen remobilization from source to sink in wheat under moderate water limitation during grain filling[J]. >Journal of Integrative Agriculture, 2026, 25(5): 1857-1870.
[12] Muhammad Fraz Ali, Lijuan Ma, Irsa Ejaz, Wanrui Han, Shengnan Wang, Xiang Lin, Dong Wang. Productivity and economic benefits of winter wheat in Northwest China by optimizing irrigation and planting density[J]. >Journal of Integrative Agriculture, 2026, 25(5): 1871-1886.
[13] Yufeng Wang, Zixuan Chang, Jiayu Wang, Tingliang Li, Zhiping Yang. Residual nitrogen exhibits lower stability and greater influence on wheat yield formation compared to phosphorus and potassium in drylands of the Loess Plateau[J]. >Journal of Integrative Agriculture, 2026, 25(5): 2063-2076.
[14] Yijun Wang, Jinhao Han, Tenglong Zhang, Mengjia Sun, Hongyu Ren, Cunyao Bo, Yuqing Diao, Xin Ma, Hongwei Wang, Xiaoqian Wang. Identification and fine mapping of a major QTL for grain protein content, qGPC4D, using wheat–Aegilops tauschii introgression lines[J]. >Journal of Integrative Agriculture, 2026, 25(5): 1813-1821.
[15] Guoming Li, Xiaotian Ren, Shengyan Pang, Changjie Feng, Yuxi Niu, Yanjie Qu, Changhong Liu, Xiang Lin, Dong Wang. Nitrogen redistribution during the grain-filling stage and its correlation with senescence and TaATG8 expression in leaves of winter wheat[J]. >Journal of Integrative Agriculture, 2026, 25(4): 1433-1442.
No Suggested Reading articles found!