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Rice (Oryza sativa L) paddies contribute approximately 7-17% to total global methane (CH4) emissions and are considered an important source of human-induced climate change. However, the interactive effects of rice roots and soil microbes on CH4 emissions in paddy fields are not clearly understood. We conducted two field experiments over three years. Soil CH4 fluxes and cumulative CH4 emissions, rice root traits, and microbial communities and activities in soil were measured using three mid-season japonica rice cultivars (Wuyujing 3, Zhendao 88, and Huaidao 5) that have the same growth durations and similar aboveground traits before heading. The CH4 emissions during the mid-growing period (from panicle initiation to heading) contributed 39.0-49.7% of the total emissions during the entire growing season and differed significantly among the rice cultivars. The root morphological and physiological traits (i.e. root dry weight, root length, root oxidation activity, and root radial oxygen loss) were negatively correlated with CH4 fluxes. Compared to the zero-N control, application rates of N fertilizer at 54 and 108 kg ha(-1) increased root biomass of cultivar Zhendao 88 by 10.1% and 17.3%, respectively, leading to corresponding decreases in CH4 emissions by 12.7% and 22.9%. The root exudates (malic acid, succinic acid, and citric acid) promoted the abundance and activity of methanotrophs, which was the primary factors underlying the low CH4 emissions in the paddy fields. Our findings suggested that stronger root systems, higher oxygen delivered by roots available for methanotrophs and suitable root exudates interacted in the rhizosphere, established a favourable habitat for microbial populations, and reduced CH4 emissions in paddy fields.