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Research paper | Open Access

Root-sourced H2O2 is essential for maintaining jasmonic acid and Na+/K+ homeostasis to delay leaf senescence during salt stress in Paspalum vaginatum

Ling Pana,b,c,1( )Tingchen Xua,1Jing WangbJunming ZhaodQuanquan SunaXu Hua,cXu TaoaJinlin Zhanga,eLi Liaoa,cZhiyong Wanga,c( )
Key Laboratory of Genetics and Germplasm Innovation of Tropical Special Forest Trees and Ornamental Plants, School of Breeding and Multiplication (Sanya Institute of Breeding and Multiplication), Hainan University, Sanya, Hainan 572000, China
College of Animal Science and Technology, Yangzhou University, Yangzhou, Jiangsu 225009, China
College of Tropical Agriculture and Forestry, Hainan University, Haikou, Hainan 570228, China
College of Grassland Science and Technology, Sichuan Agricultural University, Chengdu, Sichuan 611130, China
State Key Laboratory of Herbage Improvement and Grassland Agroecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Research Center of Grassland Industry, Ministry of Education, Center for Grassland Microbiome, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, Gansu 730000, China

1 These authors contributed equally to this work.

Peer review under responsibility of Chinese Society of Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS)

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Abstract

Improving salt tolerance and mitigating senescence in the presence of high salinity are crucial for sustaining agricultural productivity. Previous research has demonstrated that hydrogen peroxide (H2O2), specifically H2O2 derived from roots and mediated by the respiratory burst oxidase homolog (NADPH), plays a significant role in regulating ion and plant hormone homeostasis in glycophytic plants, such as Arabidopsis. However, the extent to which root-derived H2O2 fulfils similar functions in halophytic plants remains uncertain. Therefore, our study aimed to explore the potential contribution of root-sourced H2O2 in delaying leaf senescence induced by high salinity, utilizing seashore paspalum as a model halophytic plant. The application of the NADPH-oxidase inhibitor DPI, coupled with a series of leaf senescence analyses, we revealed that root-derived H2O2 significantly retards salt-induced leaf senescence. Furthermore, through the application of hormone analysis, lipidomics, ionomics, Non-invasive Micro-test Technology (NMT), and transcriptomics, we established that NADPH-dependent H2O2 induced by salt stress in the roots was indispensable for maintaining the balance of the aging hormone, jasmonic acid (JA), and sodium ion homeostasis within this halophytic plant. Finally, by utilizing AtrbohD Arabidopsis mutants and virus-induced gene silencing (VIGs) in Paspalum vaginatum, we demonstrated the pivotal role played by root-sourced H2O2 in upholding JA homeostasis and regulating JA-triggered leaf senescence in P. vaginatum. This study offers novel insights into the mechanisms that govern plant leaf senescence and its response to salinity-induced stress.

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Horticultural Plant Journal
Pages 1364-1376

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Cite this article:
Pan L, Xu T, Wang J, et al. Root-sourced H2O2 is essential for maintaining jasmonic acid and Na+/K+ homeostasis to delay leaf senescence during salt stress in Paspalum vaginatum. Horticultural Plant Journal, 2025, 11(3): 1364-1376. https://doi.org/10.1016/j.hpj.2024.04.009

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Received: 28 November 2023
Accepted: 16 April 2024
Published: 21 October 2024
© 2024 Chinese Society for Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS).

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).