Leaf senescence is an orderly and highly coordinated process, and finely regulated by ethylene and nitrogen (N), ultimately affecting grain yield and nitrogen-use efficiency (NUE). However, the underlying regulatory mechanisms on the crosstalk between ethylene- and N-regulated leaf senescence remain a mystery in maize. In this study, ethylene biosynthesis gene ZmACS7 overexpressing (OE-ZmACS7) plants were used to study the role of ethylene regulating leaf senescence in response to N deficiency, and they exhibited the premature leaf senescence accompanied by increased ethylene release, decreased chlorophyll content and Fv/Fm ratio, and accelerated chloroplast degradation. Then, we investigated the dynamics changes of transcriptome reprogramming underlying ethylene-accelerated leaf senescence in response to N deficiency. The differentially expressed genes (DEGs) involved in chlorophyll biosynthesis were significantly down-regulated, while DEGs involved in chlorophyll degradation and autophagy processes were significantly up-regulated, especially in OE-ZmACS7 plants in response to N deficiency. A gene regulatory network (GRN) was predicted during ethylene-accelerated leaf senescence in response to N deficiency. Three transcription factors (TFs) ZmHSF4, ZmbHLH106, and ZmEREB147 were identified as the key regulatory genes, which targeted chlorophyll biosynthesis gene ZmLES22, chlorophyll degradation gene ZmNYC1, and autophagy-related gene ZmATG5, respectively. Furthermore, ethylene signaling key genes might be located upstream of these TFs, generating the signaling cascade networks during ethylene-accelerated leaf senescence in response to N deficiency. Collectively, these findings improve our molecular knowledge of ethylene-accelerated maize leaf senescence in response to N deficiency, which is promising to improve NUE by manipulating the progress of leaf senescence in maize.
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