Root-derived brassinosteroids coordinate high rice yield and methane mitigation under wetting alternating with mild drying management

doi:10.1016/j.jia.2026.03.037

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Weiyang Zhang^{1, 2}^#, Wei Cai^{1, 2}, Haotian Chen^{1, 2}, Meijie Jia^{1, 2}, Ying Liu^{1, 2}, Kuanyu Zhu^{1, 2}, Hao Zhang^{1, 2}, Junfei Gu^{1, 2}, Zhiqin Wang^{1, 2}, Zujian Zhang^{1, 2}, Lijun Liu^{1, 2}, Jianhua Zhang^{3, 4}

¹Jiangsu Key Laboratory of Crop Genetics Physiology/Jiangsu Key Laboratory of Crop Cultivation Physiology/Agricultural College, Yangzhou University, Yangzhou 225009, China

²Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, China

³Department of Biology, Hong Kong Baptist University, Hong Kong 999077, China

⁴The State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, Hong Kong 999077, China

Highlights

l Wetting alternating with mild drying (WMD) synergistically achieves high rice yield and mitigates CH₄ emissions.

l The WMD approach increases the level of root-derived brassinosteroids in rice.

l Root-derived brassinosteroids optimize critical processes at the rice root-soil interface.

Abstract
References

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摘要

本研究探讨了轻干湿交替灌溉(WMD)对水稻产量和甲烷(CH₄)排放的影响及其内在机制。以常规灌溉为对照，于大田条件下种植高产杂交稻，从移栽至成熟进行全生育期观察。结果表明，WMD处理显著提高了水稻产量，同时减少了CH₄排放。尽管与对照相比，WMD处理下氧化亚氮(N₂O)排放略有增加，但CH₄减排在降低全球增温潜势(GWP)和温室气体强度(GHGI)方面的效益，完全抵消了N₂O增加带来的不利影响。WMD处理下，根系内源油菜素甾醇(BRs)水平升高，通过抗坏血酸-谷胱甘肽循环途径增强了抗氧化防御能力，降低了活性氧积累，从而在维持根系活力的同时抑制了通气组织形成，最终限制了CH₄的传输通道。此外，根系内源BRs水平升高通过直接或间接抑制mcrA基因丰度来抑制CH₄产生，同时通过富含特定有机酸的根际分泌物刺激pmoA基因丰度，促进了水稻土中CH₄的氧化。在WMD处理下，BR诱导的根系活力提升显著增强了光合能力，形成促进同化物积累的正反馈；同时，WMD促进了同化物从营养器官向籽粒的分配，共同提高了水稻产量。综上，WMD措施通过刺激根系BRs的生物合成，能够在保持水稻高产的同时，有效减少稻田CH₄排放、GWP和GHGI。

Abstract

This study explored the effects of a wetting alternating with mild drying (WMD) management strategy, on rice productivity and methane (CH₄) emissions, and its underlying mechanisms. A high-yielding hybrid rice cultivar was grown in field trials under either conventional irrigation (CI) or the WMD regimen from transplanting to maturity. Results revealed that the WMD approach significantly boosted grain yield while simultaneously reducing CH₄ emissions. It was accompanied by a slight increase in nitrous oxide (N₂O) emissions versus CI. However, the mitigation benefits of decreased CH₄ emissions in lowering global warming potential (GWP) and greenhouse-gas intensity (GHGI) outweighed the adverse contributions of elevated N₂O emissions. Elevated BR levels in roots enhanced antioxidant defense through the ascorbate-glutathione cycle pathway, which reduced ROS accumulation, thereby not only maintaining root activity but also suppressing root aerenchyma formation—ultimately restricting CH₄ transport pathways under WMD regime. Furthermore, the increased root BR levels suppressed CH₄ production by directly or indirectly inhibiting the mcrA gene abundance, while promoting CH₄ oxidation through rhizosphere exudates enriched with specific organic acids that stimulated the pmoA gene abundance in paddy soil. Under the WMD regime, BR-induced enhancement of root activity significantly boosted photosynthetic capacity, establishing a positive feedback loop that promoted assimilate accumulation. Concurrently, WMD facilitated photosynthate allocation from vegetative tissues to grains, collectively improving rice yield. Collectively, our data suggest that the WMD practices can effectively reduce CH₄ emissions, GWP, and GHGI in rice paddies while maintaining high grain yield by stimulating root-derived BR biosynthesis.

Keywords: greenhouse gas emission paddy field water-saving irrigation root

Online: 18 March 2026

Fund:

This work was supported by the National Natural Science Foundation of China (32372214 and 31901445), the National Key Research Development Program (2022YFD2300304), the Jiangsu Agriculture Science Technology Innovation Fund, China (CX(23)1035), the Priority Academic Program Development of Jiangsu Higher Education Institutions, China (PAPD-2020-01), the Top Talent Supporting Program of Yangzhou University (YZU-2028-01), China, and the Hong Kong Research Grants Council, China (GRF 12101722, 12102423, and 12105824).

About author: #Correspondence Weiyang Zhang, E-mail: wyz@yzu.edu.cn

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Weiyang Zhang, Wei Cai, Haotian Chen, Meijie Jia, Ying Liu, Kuanyu Zhu, Hao Zhang, Junfei Gu, Zhiqin Wang, Zujian Zhang, Lijun Liu, Jianhua Zhang. 2026. Root-derived brassinosteroids coordinate high rice yield and methane mitigation under wetting alternating with mild drying management. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2026.03.037

Aulakh M S, Wassmann R, Bueno C, Kreuzwieser J, Rennenberg H. 2001. Characterization of root exudates at different growth stages of ten rice (Oryza sativa L.) cultivars. Plant Biology, 3, 139–148.

Bandumula N. 2017. Rice production in Asia: Key to global food security. Proceedings of the National Academy of Sciences, India Section (B: Biological Sciences), 88, 1323–1328.

Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld J. 2010. Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. The Plant Cell, 22, 376–391.

Brennan T, Frenkel C. 1977. Involvement of hydrogen peroxide in the regulation of senescence in pear. Plant Physiology, 59, 411–416.

Bwire D, Saito H, Sidle R C, Nishiwaki J. 2024. Water management hydrological characteristics of paddy-rice fields under alternate wetting and drying irrigation practice as climate smart practice: A review. Agronomy, 14, 1421.

Carrijo D R, Lundy M E, Linquist B A. 2017. Rice yields and water use under alternate wetting and drying irrigation: A meta-analysis. Field Crops Research, 203, 173–180.

Chen H T, Qin Y, Zhong X H, Lin C Y, Qin J H, Yang J C, Zhang W Y. 2024. Research progress on the relationship between rice root, soil properties and methane emissions in paddy fields. Chinese Journal of Rice Science, 38, 233–245.

Chen M, Lu Y, Ma Q, Guo L, Feng Y Q. 2009. Boronate affinity monolith for highly selective enrichment of glycopeptides and glycoproteins. Analyst, 134, 2158–2164.

Chen Y, Li S Y, Zhang Y J, Li T T, Ge H M, Xia S M, Gu J F, Zhang H, Lü B, Wu X X, Wang Z Q, Yang J C, Zhang J H, Liu L J. 2019. Rice root morphological and physiological traits interaction with rhizosphere soil and its effect on methane emissions in paddy fields. Soil Biology and Biochemistry, 129, 191–200.

Ding J, Mao L J, Yuan B F, Feng Y Q. 2013. A selective pretreatment method for determination of endogenous active brassinosteroids in plant tissues: Double layered solid phase extraction combined with boronate affinity polymer monolith microextraction. Plant Methods, 9, 1–9.

Dutilleul C, Driscoll S, Cornic G, De P R, Foyer C H, Noctor G. 2003. Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions during transients. Plant Physiology, 131, 264–275.

Foyer C H, Noctor G. 2005. Oxidant antioxidant signalling in plants: Are-evaluation of the concept of oxidative stress in a physiological context. Plant, Cell and Environment, 28, 1056-1071.

Girkin N T, Turner B L, Ostle N, Craigon J, Sjögersten S. 2018. Root exudate analogues accelerate CO₂ and CH₄ production in tropical peat. Soil Biology and Biochemistry, 117, 48–55.

Iqbal M F, Liu S H, Zhu J W, Zhao L M, Qi T T, Liang J, Luo J, Xiao X, Fan X R. 2021. Limited aerenchyma reduces oxygen diffusion and methane emission in paddy. Journal of Environmental Management, 279, 111583.

Krüger M, Frenzel P, Conrad R. 2001. Microbial processes influencing methane emission from rice fields. Global Change Biology, 7, 49–63.

Li S Y, Zhang Y J, Zhao J M, van Groenigen K J, Shen X Y, Zhang H, Gu J F, Zhang W Y, Hui D F, Chen Y, Liu L J. 2025. Water-saving irrigation practices in rice paddies reverse the impact of root aerenchyma on methane emissions. Agriculture, Ecosystems & Environment, 378, 109309.

Li Z K, Shen Y, Zhang W Y, Wang Z Q, Gu J F, Yang J C, Zhang J H. 2023. A moderate wetting and drying regime produces more and healthier rice food with less environmental risk. Field Crops Research, 298, 108954.

Ma Y C, Kong X W, Yang B, Zhang X L, Yan X Y, Yang J C, Xiong Z Q. 2013. Net global warming potential and greenhouse gas intensity of annual rice-wheat rotations with integrated soil-crop system management. Agriculture, Ecosystems & Environment, 164, 209–219.

Nolan T M, Vukašinović N, Liu D R, Russinova E, Yin Y H. 2020. Brassinosteroids: Multidimensional regulators of plant growth, development, and stress responses. The Plant Cell, 32, 295–318.

Norton G J, Shafaei M, Travis A J, Deacon C M, Danku J, Pond D, Cochrane Ni, Lockhart K, Salt D, Zhang H, Dodd I C, Hossain M, Islam M R, Price A H. 2017. Impact of alternate wetting and drying on rice physiology, grain production, and grain quality. Field Crops Research, 205, 1–13.

Porcher A, Guérin V, Leduc N, Lebrec A, Lothier J, Vian A. 2021. Ascorbate-glutathione pathways mediated by cytokinin regulate H₂O₂ levels in light-controlled rose bud burst. Plant Physiology, 186, 910–928.

Rahman M T, Crombie A, Chen Y, Stralis-Pavese N, Bodrossy L, Meir P, McNamara N P, Colin Murrell J. 2011. Environmental distribution and abundance of the facultative methanotroph Methylocella. The ISME Journal, 5, 1061–1066.

Steffens B, Geske T, Sauter M. 2011. Aerenchyma formation in the rice stem and its promotion by H₂O₂. New Phytologist, 190, 369–378.

Sun J, Ma Z, Zhou G, Liang T, Liu R, Chang D, Liu H, Liu J, Zou C, Cao W. 2025. Ethylene stimulates methane oxidation inhibits and methane production in green manure-rice systems. Journal of Environmental Management, 383, 125461.

Suzuki N, Miller G, Morales J, Shulaev V, Torres M A, Mittler R. 2011. Respiratory burst oxidases: The engines of ROS signaling. Current Opinion in Plant Biology, 14, 691–699.

Tang L, Risalat H, Cao R, Hu Q N, Pan X Y, Hu Y X, Zhang G Y. 2022. Food security in China: A brief view of rice production in recent 20 years. Foods, 11, 3324.

Theint E E, Suzuki S, Ono E, Bellingrath-Kimura S D. 2015. Influence of different rates of gypsum application on methane emission from saline soil related with rice growth and rhizosphere exudation. Catena, 133, 467–473.

Upadhyay S K, Srivastava A K, Rajput V D, Chauhan P K, Bhojiya A A, Jain D, Chaubey G, Dwivedi P, Sharma B, Minkina T. 2022. Root exudates: Mechanistic insight of plant growth promoting rhizobacteria for sustainable crop production. Frontiers in Microbiology, 13, 916488.

Vukašinović N, Wang Y, Vanhoutte I, Fendrych M, Guo B, Kvasnica M, Jiroutová P, Oklestkova J, Strnad M, Russinova E. 2021. Local brassinosteroid biosynthesis enables optimal root growth. Nature Plants, 7, 619–632.

Wang X J, Tang C X, Severi J, Butterly C R, Baldock J A. 2016. Rhizosphere priming effect on soil organic carbon decomposition under plant species differing in soil acidification and root exudation. New Phytologist, 211, 864–873.

Wei Z Y, Li J. 2016. Brassinosteroids regulate root growth, development, and symbiosis. Molecular Plant, 9, 86–100.

Xu Y J, Weng X L, Tang S P, Zhang W Y, Zhu K Y, Zhu G L, Zhang H, Wang Z Q, Yang J C. 2025. Untargeted lipidomic analysis of milled rice under different alternate wetting and soil drying irrigation regimes. Journal of Integrative Agriculture, 24, 3351–3367.

Yamauchi T, Shimamura S, Nakazono M, Mochizuki T. 2013. Aerenchyma formation in crop species: A review. Field Crops Research, 152, 8–16.

Yamauchi T, Yoshioka M, Fukazawa A, Mori H, Nishizawa N K, Tsutsumi N, Yoshioka H, Nakazono M. 2017. An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions. The Plant Cell, 29, 775–790.

Yang Y, Tilman D, Jin Z, Smith P, Barrett C B, Zhu Y G, Burney J, D’Odorico P, Fantke P, Fargione J, Finlay J C, Rulli M C, Sloat L, van Groenigen K J, West P C, Ziska L, Michalak A M, Lobell D B, Clark M, Colquhoun J, et al. 2024. Climate change exacerbates the environmental impacts of agriculture. Science, 385, eadn3747.

Yang Y Z, Chu C C, Qian Q, Tong H N. 2024. Leveraging brassinosteroids towards the next Green Revolution. Trends in Plant Science, 29, 86–98.

Yoshida S, Forno D, Cock J, Gomez K. 1976. Laboratory Manual for Physiological Studies of Rice. International Rice Research Institute, The Philippines.

Zang Y G, Wu G Z, Li Q Q, Xu Y W, Xue M M, Chen X Y, Wei H Y, Zhang W Y, Zhang H, Liu L J, Wang Z Q, Gu J F, Yang J C. 2024. Irrigation regimes modulate non-structural carbohydrate remobilization and improve grain filling in rice (Oryza sativa L.) by regulating starch metabolism. Journal of Integrative Agriculture, 23, 1507–1522.

Zhang W Y, Huang H H, Zhou Y J, Zhu K Y, Wu Y F, Xu Y J, Wang W L, Gu J F, Xiong F, Wang Z Q, Liu L J, Yang J C. 2023. Brassinosteroids mediate moderate soil-drying to alleviate spikelet degeneration under high temperature during meiosis of rice. Plant Cell & Environment, 46, 1340–1362.

Zhang W Y, Wu M Y, Zhong X H, Liu Y, Yang X X, Cai W, Zhu K Y, Zhang H, Gu J F, Wang Z Q, Liu L J, Zhang J H, Yang J C. 2024. Involvement of brassinosteroids and abscisic acid in spikelet degeneration in rice under soil drying during meiosis. Journal of Experimental Botany, 75, 1580–1600.

Zhang W Y, Yu J X, Xu Y J, Wang Z Q, Liu L J, Zhang H, Gu J F, Zhang J H, Yang J C. 2021. Alternate wetting and drying irrigation combined with the proportion of polymer-coated urea and conventional urea rates increases grain yield, water and nitrogen use efficiencies in rice. Field Crops Research, 268, 108165.

Zhang W Y, Zhu K Y, Wang Z Q, Zhang H, Gu J F, Liu L J, Yang J C, Zhang J H, 2019. Brassinosteroids function in spikelet differentiation and degeneration in rice. Journal of Integrative Plant Biology, 61, 943–963.

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