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Journal of Integrative Agriculture  2025, Vol. 24 Issue (12): 4546-4560    DOI: 10.1016/j.jia.2024.03.041
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Integrated transcriptomics and metabolomics analysis provide insights into the alleviation of waterlogging stress in maize by exogenous spermidine application

Xiuling Wang1*, Li Niu2*, Huaipan Liu3, Xucun Jia1, Yulong Zhao4, Qun Wang1, Yali Zhao1, Pengfei Dong1, Moubiao Zhang1, Hongping Li1, Panpan An1, Zhi Li1, 5, Xiaohuan Mu1#, Yongen Zhang1, 5#, Chaohai Li1#

1 State Key Laboratory of High-Efficiency Production of Wheat–Maize Double Cropping/Collaborative Innovation Center of Henan Grain Crops/College of Agronomy, Henan Agricultural University, Zhengzhou 450046, China

2 Beijing Changping Agricultural Technology Extension Station, Beijing 102200, China

3 College of Life Science and Agronomy/Key Laboratory of Plant Genetics and Molecular Breeding, Zhoukou Normal University, Zhoukou 466001, China

4 College of Forestry, Henan Agricultural University, Zhengzhou 450046, China

5 Agricultural Information Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, China

 Highlights 
Under waterlogging stress, spermidine (Spd) application increased biomass accumulation by enhancing the expression of light-harvesting complex (LHC), photosynthesis, and starch-related genes, inhibiting chlorophyll degradation, and sustaining higher photosynthetic rates and thus increasing biomass accumulation.
Activation of trehalose and Spd biosynthetic genes elevated the accumulation of trehalose and enhanced endogenous Spd production which play a vital role in stress response.  
Increased auxin-related gene expression and indole acetic acid (IAA) levels promote cell elongation, and upregulation of lipid-related genes boosts lipid content to protect cell membranes under waterlogging conditions.
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摘要  
渍涝胁迫会影响植物的生发发育,进而降低作物产量。亚精胺(Spd)作为第二信使,在渍涝胁迫下对植物的生长有缓解作用。然而,外源施加Spd缓解渍涝胁迫的分子机制尚不清楚。本研究利用生理学分析和多组学联合分析以揭示施加Spd对渍涝胁迫的影响。施加Spd使参与捕光复合体(LHC)、光合作用和淀粉合成相关途径的基因上调表达,同时抑制了叶绿素降解,因此保持了较高的光合速率,从而增加了淹水胁迫下生物量的积累;海藻糖和Spd生物合成相关基因的上调表达引起海藻糖和内源性Spd的积累;抑制1-氨基环丙烷-1-羧酸氧化酶(ACO)基因的表达有助于减少乙烯排放。这些变化增加了玉米对渍涝的抗性。外源施加Spd后,生长素相关的基因发生上调表达,同时IAA含量增加,有利于玉米细胞伸长,能够使玉米在涝渍胁迫下保持相对正常的生产。在渍涝胁迫下施加外源Spd使大部分参与脂质合成相关的基因发生上调表达,引起脂质的积累,保护了细胞膜的完整性和稳定性。这些改变均有利于抵抗涝渍胁迫。本研究的发现扩宽了我们对外源施用Spd缓解渍涝损害机制的理解,并为培育耐涝玉米品种提供证据。


Abstract  

Waterlogging stress significantly impairs plant growth and reduces crop yields.  Spermidine (Spd), functioning as a second messenger, demonstrates positive effects on plant growth under waterlogging stress conditions.  However, the molecular mechanisms by which exogenous Spd application alleviates waterlogging stress remain unclear.  This study employed physiological analysis and multi-omics approaches to investigate the effect of Spd application on waterlogging stress.  The application of Spd enhanced the expression of genes related to light-harvesting complex (LHC), photosynthesis, and starch-related pathways, while inhibiting chlorophyll degradation and maintaining higher photosynthetic rates, thereby increasing biomass accumulation under waterlogging stress.  The activation of genes associated with trehalose and Spd biosynthesis resulted in elevated accumulation of trehalose and endogenous Spd.  The inhibition of 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase (ACO) expression contributed to reduced ethylene emission, enhancing maize resistance to waterlogging.  Following Spd application, auxin-related genes were up-regulated and indole acetic acid (IAA) content increased, promoting cell elongation in maize and maintaining normal growth under waterlogging stress.  Additionally, the upregulation of lipid-related genes led to increased lipid content, protecting cell membranes under waterlogging conditions.  These molecular and physiological modifications collectively enhanced resistance to waterlogging stress.  These findings advance our understanding of Spd’s regulatory roles in mitigating waterlogging damage and provide valuable insights for breeding waterlogging-tolerant maize varieties.

Keywords:  maize       spermidine        waterlogging stress        transcriptome        metabolome  
Received: 15 November 2023   Accepted: 17 January 2024 Online: 11 March 2024  
Fund: This research was supported by the China Agriculture Research System (CARS-02-20) and the Henan Province Agro-ecosystem Field Observation and Research Station, China (30602535).

About author:  Xiuling Wang, E-mail: 15038348221@163.com; Li Niu, E-mail: niulipipi@163.com; #Correspondence Chaohai Li, E-mail: lichaohai@henau.edu.cn; Xiaohuan Mu, E-mail: xiaohuanmu@henau.edu.cn; Yongen Zhang, Tel: +86-10-82109654, E-mail: zhangyongen@caas.cn * These authors contributed equally to this study.

Cite this article: 

Xiuling Wang, Li Niu, Huaipan Liu, Xucun Jia, Yulong Zhao, Qun Wang, Yali Zhao, Pengfei Dong, Moubiao Zhang, Hongping Li, Panpan An, Zhi Li, Xiaohuan Mu, Yongen Zhang, Chaohai Li. 2025. Integrated transcriptomics and metabolomics analysis provide insights into the alleviation of waterlogging stress in maize by exogenous spermidine application. Journal of Integrative Agriculture, 24(12): 4546-4560.

Chen D, Shao Q, Yin L, Younis A, Zheng B. 2019. Polyamine function in plants: Metabolism, regulation on development, and roles in abiotic stress responses. Frontiers in Plant Science9, 1945.

Chen X, Chen G, Guo S, Wang Y, Sun J. 2023. SlSAMS1 enhances salt tolerance through regulation DNA methylation of SlGI in tomato. Plant Science335, 111808.

Deng S, Ma J, Zhang L, Chen F, Sang Z, Jia Z, Ma L. 2019. De novo transcriptome sequencing and gene expression profiling of Magnolia wufengensis in response to cold stress. BMC Plant Biology19, 321.

Du H Y, Liu D X, Liu G T, Liu H P, Kurtenbach R. 2018. Relationship between polyamines and anaerobic respiration of wheat seedling root under water-logging stress. Russian Journal of Plant Physiology65, 874–881.

Fu Y, Gu Q, Dong Q, Zhang Z, Lin C, Hu W, Pan R, Guan Y, Hu J. 2019. Spermidine enhances heat tolerance of rice seeds by modulating endogenous starch and polyamine metabolism. Molecules24, 1395.

Gao J, Qian Z, Zhang Y, Zhuang S. 2022. Exogenous spermidine regulates the anaerobic enzyme system through hormone concentrations and related-gene expression in Phyllostachys praecox roots under flooding stress. Plant Physiology and Biochemistry186, 182–196.

Ge L F, Chao D Y, Shi M, Zhu M Z, Gao J P, Lin H X. 2008. Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta228, 191–201.

Hayashi K I, Arai K, Aoi Y, Tanaka Y, Hira H, Guo R, Hu Y, Ge C, Zhao Y, Kasahara H, Fukui K. 2021. The main oxidative inactivation pathway of the plant hormone auxin. Nature Communications12, 6752.

Hemati Matin N, Jalali M. 2016. The effect of waterlogging on electrochemical properties and soluble nutrients in paddy soils. Paddy and Water Environment15, 443–455.

Herzog M, Striker G G, Colmer T D, Pedersen O. 2016. Mechanisms of waterlogging tolerance in wheat – A review of root and shoot physiology. PlantCell and Environment39, 1068–1086.

Hou Y, Jiang F, Zheng X, Wu Z. 2019. Identification and analysis of oxygen responsive microRNAs in the root of wild tomato (Shabrochaites). BMC Plant Biology19, 100.

Jang I C, Oh S J, Seo J S, Choi W B, Song S I, Kim C H, Kim Y S, Seo H S, Choi Y D, Nahm B H, Kim J K. 2003. Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiology131, 516–524.

Ji M, Wang K, Wang L, Chen S, Li H, Ma C, Wang Y. 2019. Overexpression of a S-adenosylmethionine decarboxylase from sugar beet M14 increased Araidopsis salt tolerance. International Journal of Molecular Sciences20, 1990.

Jia Y X, Sun J, Guo S R, Li J, Hu X H, Wang S P. 2010. Effect of root-applied spermidine on growth and respiratory metabolism in roots of cucumber (Cucumis sativus) seedlings under hypoxia. Russian Journal of Plant Physiology57, 648–655.

Jiao P, Jin S, Chen N, Wang C, Liu S, Qu J, Guan S, Ma Y. 2022. Improvement of cold tolerance in maize (Zea mays L.) using Agrobacterium-mediated transformation of ZmSAMDC gene. GM Crops & Food13, 131–141.

Klecker M, Gasch P, Peisker H, Dormann P, Schlicke H, Grimm B, Mustroph A. 2014. A shoot-specific hypoxic response of Arabidopsis sheds light on the role of the phosphate-responsive transcription factor PHOSPHATE STARVATION RESPONSE1. Plant Physiology165, 774–790.

Li H, Peng T, Wang Q, Wu Y, Chang J, Zhang M, Tang G, Li C. 2017. Development of incompletely fused carpels in maize ovary revealed by miRNA, target gene and phytohormone analysis. Frontiers in Plant Science8, 463.

Li H W, Zang B S, Deng X W, Wang X P. 2011. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta234, 1007–1018.

Li J, Hu L, Zhang L, Pan X, Hu X. 2015. Exogenous spermidine is enhancing tomato tolerance to salinity–alkalinity stress by regulating chloroplast antioxidant system and chlorophyll metabolism. BMC Plant Biology15, 303.

Liu C, Lan C, Li C, Li C, Huang J. 2023. Exogenous spermidine and calcium alleviate waterlogging stress in cherry tomato at the seedling stage. Scientia Horticulturae307, 111504.

Liu Z, Kumari S, Zhang L, Zheng Y, Ware D. 2012. Characterization of miRNAs in response to short-term waterlogging in three inbred lines of Zea maysPLoS ONE7, e39786.

Lou Y, Guan R, Sun M, Han F, He W, Wang H, Song F, Cui X, Zhuge Y. 2018. Spermidine application alleviates salinity damage to antioxidant enzyme activity and gene expression in alfalfa. Ecotoxicology27, 1323–1330.

Nakazawa M, Yabe N, Ichikawa T, Yamamoto Y Y, Yoshizumi T, Hasunuma K, Matsui M. 2001. DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. The Plant Journal25, 213–221.

Okazaki Y, Saito K. 2014. Roles of lipids as signaling molecules and mitigators during stress response in plants. The Plant Journal79, 584–596.

Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K. 2008. Interplay of miR164CUP-SHAPED COTYLEDON genes and lateral suppressor controls axillary meristem formation in Arabidopsis thalianaThe Plant Journal55, 65–76.

Ren B Z, Zhang J W, Dong S T, Liu Peng, Zhao B. 2016. Effects of waterlogging on leaf mesophyll cell ultrastructure and photosynthetic characteristics of summer maize. PLoS ONE11, e0161424.

Salah A, Nwafor C C, Han Y, Liu L, Rashid M, Batool M, El-Badri A M, Cao C, Zhan M. 2022. Spermidine and brassinosteroid regulate root anatomical structure, photosynthetic traits and antioxidant defense systems to alleviate waterlogging stress in maize seedlings. South African Journal of Botany144, 389–402.

Takase T, Nakazawa M, Ishikawa A, Kawashima M, Ichikawa T, Takahashi N, Shimada H, Manabe K, Matsui M. 2004. ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyl and root elongation. The Plant Journal37, 471–483.

Tewari S. 2018. Flooding stress in plants and approaches to overcome. In: Plant Metabolites and Regulation under Environmental Stress. Elsevier Science & Technolog, USA.

Wang X, Wang Q, Zhang M, Zhao Y, Dong P, Zhao Y, Li H, Jia X, An P, Tang Y, Li C. 2022. Foliar application of spermidine alleviates waterlogging-induced damages to maize seedlings by enhancing antioxidative capacity, modulating polyamines and ethylene biosynthesis. Life12, 1921.

Wen X P, Ban Y, Inoue H, Matsuda N, Kita M, Moriguchi T. 2011. Antisense inhibition of a spermidine synthase gene highlights the role of polyamines for stress alleviation in pear shoots subjected to salinity and cadmium. Environmental and Experimental Botany72, 157–166.

Xie L J, Chen Q F, Chen M X, Yu L J, Huang L, Chen L, Wang F Z, Xia F N, Zhu T R, Wu J X, Yin J, Liao B, Shi J, Zhang J H, Aharoni A, Yao N, Shu W, Xiao S. 2015. Unsaturation of very-long-chain ceramides protects plant from hypoxia-induced damages by modulating ethylene signaling in ArabidopsisPLoS Genetics11, e1005143.

Xu Z Y, Ye L Z, Shen Q F, Zhang G P. 2024. Advances in studies on waterlogging tolerance in plants. Journal of Integrative Agriculture23, 2877–2897.

Yang C, Du P H, Shang Y W, Ji J H, Tan L Q, Zhang X, Xu J Z, Liang B W. 2024. Melatonin and dopamine alleviate waterlogging stress in apples by recruiting beneficial endophytes to enhance the physiological resilience. Journal of Integrative Agriculture, 23, 2270–2291.

Yiu J C, Liu C W, Fang D Y T, Lai Y S. 2009. Waterlogging tolerance of Welsh onion (Allium fistulosum L.) enhanced by exogenous spermidine and spermine. Plant Physiology and Biochemistry47, 710–716.

Zhang Q, Liu X, Zhang Z, Liu N, Li D, Hu L. 2019. Melatonin improved waterlogging tolerance in alfalfa (Medicago sativa) by reprogramming polyamine and ethylene metabolism. Frontiers in Plant Science10, 44.

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