CsWRKY51, a novel WRKY transcription factor of Camellia sinensis, participates in plant architecture and glutamine accumulation

• Overexpression of CsWRKY51 resulted in abnormal plant architectures by modulating hormone signaling pathways and key genes related to blade growth, branching, and flowering. • Activated nitrogen metabolism, amino acid metabolism, and the GS/GOGAT cycle contributed to the enhanced accumulation of glutamine in CsWRKY51 -overexpressing plants. • CsWRKY51 played a positive role in glutamine accumulation by influencing the GS/GOGAT cycle in the tea plants. The WRKY genes, belonging to one of the largest families of transcription factors (TFs) in plants, play critical roles in regulating diverse biological processes. In this study, we identified a novel gene from the WRKY IIc subfamily, designated as CsWRKY51 , in the tea plant, and confirmed its nuclear localization. Phenotypic analyses of CsWRKY51 -overexpressing (OE) plants revealed multiple abnormal traits, including dwarfism, curled leaves, and increased branching and flowering. Additionally, the accumulation levels of amino acids, such as glutamine, asparagine, arginine, and methionine, were significantly elevated in CsWRKY51 -OE plants, while chlorophyll content was greatly reduced. Transcriptional profiling indicated that several regulatory pathways, including phytohormone biosynthesis and signaling, photosynthesis, chlorophyll metabolism, carbon metabolism, amino acid metabolism, and nitrogen metabolism were significantly activated in the CsWRKY51 -OE plants. Furthermore, the silencing of CsWRKY51 in both green and etiolated tea shoots resulted in a significant reduction in glutamine accumulation, accompanied by a substantial decrease in the expression levels of genes encoding glutamine synthetase (GS), glutamate synthase (GOGAT), and glutamate dehydrogenase (GDH). Taken together, these comprehensive analyses demonstrated that CsWRKY51 significantly influenced plant aerial architecture, chlorophyll accumulation, and the GS/GOGAT cycle, all of which were implicated in the regulation of glutamine accumulation. This study provides new insights into the functional characterization of CsWRKY genes and the molecular mechanisms underlying plant architecture and glutamine metabolism.